Oceanography and Marine Biology: An Annual Review: Volume 39

OCEANOGRAPHY and MARINE BIOLOGY AN ANNUAL REVIEW Volume 39

OCEANOGRAPHY and MARINE BIOLOGY AN ANNUAL REVIEW Volume 39

Editors R.N.Gibson and Margaret Barnes The Dunstaffnage Marine Laboratory Oban, Argyll, Scotland

R.J.A.Atkinson University Marine Biological Station Millport, Isle of Cumbrae, Scotland

Founded by Harold Barnes

First published 2001 by Taylor & Francis 11 New Fetter Lane, London EC4P 4EE Simultaneously published in the USA and Canada by Taylor & Francis Inc, 29 West 35th Street, New York, NY 10001 Taylor & Francis is an imprint of the Taylor & Francis Group This edition published in the Taylor & Francis e-Library, 2004. © 2001 R.N.Gibson, Margaret Barnes & R.J.A.Atkinson All rights reserved. No part of this book may be reprinted or reproduced or utilised in any form or by any electronic, mechanical, or other means, now known or hereafter invented, including photocopying and recording, or in any information storage or retrieval system, without permission in writing from the publishers. Every effort has been made to ensure that the advice and information in this book is true and accurate at the time of going to press. However, neither the publisher, editors nor the authors can accept any legal responsibility or liability for any errors or omissions that may be made. In the case of drug administration, any medical procedure or the use of technical equipment mentioned within this book, you are strongly advised to consult the manufacturer’s guidelines. British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging in Publication Data A catalog record for this book has been requested ISBN 0-203-24719-1 Master e-book ISBN

ISBN 0-203-22896-0 (Adobe eReader Format) ISBN 0-415-23874-9 (Print Edition)

CONTENTS Preface

vii

Life-history patterns in serpulimorph polychaetes: ecological and evolutionary perspectives Elena K.Kupriyanova, Eijiroh Nishi, Harry A.ten Hove & Alexander V.Rzhavsky

1

Molluscs as archives of environmental change C.A.Richardson

103

The evolution of eyes in the Bivalvia Brian Morton

165

Practical measures of marine biodiversity based on relatedness of species R.M.Warwick & K.R.Clarke

207

Functional group ecology in soft-sediment marine benthos: the role of bioturbation T.H.Pearson

233

The importance of seagrass beds as a habitat for fishery species Emma L.Jackson, Ashley A.Rowden, Martin J.Attrill, Simon J.Bossey & Malcolm B.Jones

269

Selective tidal-stream transport of marine animals Richard B.Forward Jr & Richard A.Tankersley

305

Territorial damselfishes as determinants of the structure of benthic communities on coral reefs Daniela M.Ceccarelli, Geoffrey P.Jones & Laurence J.McCook

355

Author index

391

Systematic index

418

Subject index

431

v

PREFACE

The thirty-ninth volume of this series contains eight reviews written by an international array of authors. As usual, the reviews range widely in subject and taxonomic and geographic coverage. The majority of articles were solicited but the editors always welcome suggestions from potential authors for topics they consider could form the basis of appropriate contributions. Because an annual publication schedule necessarily places constraints on the timetable for submission, evaluation and acceptance of manuscripts, potential contributors are advised to make contact at an early stage of preparation so that the delay between submission and publication is minimised. The editors again gratefully acknowledge the willingness and speed with which authors complied with the editors’ suggestions, requests and questions and the efficiency of the copy editor and publishers in ensuring the regular annual appearance of each volume. This year has seen a further change in the editorial team and it is a pleasure to welcome Dr R.J.A. Atkinson as a co-editor for the series.

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Oceanography and Marine Biology: an Annual Review 2001, 39, 1–101 © R.N.Gibson, Margaret Barnes and R.J.A.Atkinson, Editors Taylor & Francis

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES: ECOLOGICAL AND EVOLUTIONARY PERSPECTIVES ELENA K.KUPRIYANOVA1, EIJIROH NISHI 2, HARRY A.TEN HOVE3 & ALEXANDER V.RZHAVSKY 4 1

School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide 5001, Australia e-mail: [email protected] (the corresponding author) 2 Manazuru Marine Laboratory for Science Education, Yokohama National University, Iwa, Manazuru, Kanagawa 259–0202, Japan 3 Instituut voor Biodiversiteit en Ecosysteem Dynamica/Zoölogisch Museum, Universiteit van Amsterdam, Mauritskade 61, NL-1090 GT Amsterdam, The Netherlands 4 A.N.Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Leninskij Prospekt 33, Moscow, 117071, Russia

Abstract The paper summarises information on the life history of tubeworms (Serpulidae and Spirorbidae). Topics reviewed are sexuality patterns, asexual reproduction, gamete attributes, fecundity, spawning and fertilisation, larval development and morphology, larval ecology and behaviour (including larval swimming, feeding, photoresponse, and defences), brooding, settlement and metamorphosis, longevity and mortality. Gonochorism, simultaneous and sequential hermaphroditism are found in the group, the last pattern being apparently under-reported. Asexual reproduction commonly leads to the formation of colonies. The egg size range is 40–200 µm in serpulids and 80–230 µm in spirorbids. The sperms with spherical and with elongated heads correspond, respectively, to broadcasting and brooding. Variability of brooding methods in serpulids has been grossly under-reported and even exceeds that of spirorbids. Development is similar in feeding and non-feeding larvae and the developmental events are easily reproducible in the laboratory until the onset of competency, after which larvae require specific cues to proceed with settlement and metamorphosis. Settlement is affected by both non-specific and substratum-specific cues (conspecifics, microbial film, other organisms). Initial rapid juvenile growth slows down at later life stages. The growth rates are affected both by factors acting after the settlement and those experienced during the larval stage. Maturation is reached at a certain body size and depends on the factors controlling growth. Longevity varies from several months in small serpulids and spirorbids to 35 yr in the largest serpulids. Mortality is highest during the early embryonic and juvenile stages. The egg-size distribution in serpulimorph polychaetes is bimodal but the modes do not correspond to feeding and non-feeding development and egg sizes of species with feeding and non-feeding larvae partially overlap. This pattern may be explained by high interspecific variability in the organic content of eggs and/or facultative larval feeding of some serpulids. Planktonic development is strongly correlated with larval feeding, and planktonic lecitotrophy is rare. The potential selective advantage of larval feeding is in the flexibility of the duration of the competent stage that increases the possibility to locate suitable substrata. As in other groups, small body size correlates with simultaneous hermaphroditism, brooding, and non-feeding development.

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Broader generalisations require better knowledge of the life history of a greater number of species. Integration of phylogenetic analyses into life-history studies should help to clarify the direction of life-history transitions in this group and determine whether phylogenetic constraints can account for the observed life-history patterns.

Introduction

Phylogenetic position and taxonomic problems in the group The serpulimorph polychaetes constitute a discrete group of sedentary worms, which secrete calcareous tubes. Traditionally, they constituted the family Serpulidae and have been divided into three subfamilies: Spirorbinae, Serpulinae and Filograninae (e.g. Fauvel 1927, Rioja 1931). Pillai (1970) elevated the Spirorbinae to family status. Ten Hove (1984) and Fitzhugh (1989) questioned this division of serpulimorph polychaetes into Serpulidae (with subfamilies Serpulinae and Filograninae) and Spirorbidae. They suggested, based on cladistic analyses, that the Spirorbidae are more closely related to the Serpulinae than to the Filograninae and assigning a rank of family to this group makes the Serpulidae sensu stricto a paraphyletic group. Smith (1991) also concludes that family rank of the Spirorbidae is not justified. It is also not clear if Filograninae are monophyletic (ten Hove 1984, Kupriyanova & Jirkov 1997). Being aware of these phylogenetic considerations, we maintain here the separation of the serpulimorph polychaetes into the families Serpulidae and Spirorbidae for practical reasons. First, confusion may exist whether the family Serpulidae includes Spirorbinae or not, since some authors (e.g. A.Rzhavsky, P.Knight-Jones and E.W.Knight-Jones, pers. comm.) continue to use family rank for spirorbids. Second, an elaborated taxonomic system below the family level in the Spirorbidae needs to be revisited if the rank of the group is to be lowered to subfamily and such a revision is clearly out of scope of the current review. A major problem in writing a literature survey of experimental and ecological studies in serpulimorph polychaetes is their confused taxonomy. For example, many earlier fouling studies from all over the world mention Hydroides norvegicus. However, this is a strictly boreal species, extending into deeper waters in the Mediterranean. In (sub)tropical waters the fouling species is generally H. elegans (Zibrowius 1973, ten Hove 1974), although in tropical waters a few similar species may also occur incidentally. Frequently used in earlier experimental studies is “H. uncinatus”, which was shown to be a “dustbin” of about 13 species (Zibrowius 1971). The often quoted work of Sentz-Braconnot (1964) on “Hydroides norvegica” with an operculum in the shape of a double funnel and “Serpula concharum” with a single funnel most probably only dealt with the single species Hydroides elegans. Studies on the regeneration of opercula in H. elegans by Cresp (1964) have shown that if the peduncle (opercular stalk) is cut proximally, the regenerating operculum will form a single funnel only; a distal caesura will regenerate the normal double funnel. Even the well known Pomatoceros triqueter should be regarded with some suspicion: Zibrowius (1968) demonstrated that the “P. triqueter” of earlier authors contains two valid species, P. triqueter and P. lamarckii; this was confirmed by electrophoretic studies by Ekaratne et al. (1982). Most, but maybe not all, of Straughan’s (1972a,b) studies on the ecology of Ficopomatus 2

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

were not based upon F. enigmaticus, but on the related tropical form F. uschakovi. “Spirorbis spirillum” reported in numerous ecological studies more likely refers to Circeis armoricana, whereas the data on “Spirorbis granulata” may refer to Bushiella (Jugaria) granulatus, B. (Jugaria) similis, B. (Jugaria) quadrangularis or some other Bushiella species. In many cases it is still unclear which species were studied. This review takes advantage of the taxonomic research on the group that has been conducted in the past few decades. Only the taxonomic names that are currently considered valid are used in the review. We have compiled an addendum (p. 72) that contains all species names appearing in the text as well as their correspondence to invalid names or misidentifications that appear in original publications.

Importance of life-history research in serpulimorph polychaetes Secretion of calcareous tubes make serpulimorph polychaetes important and troublesome members of fouling communities (e.g. Mohan & Aruna 1994). Studies of larval development and settlement therefore have practical importance and constitute a major part of serpulimorph life-history research. Spirorbid larvae with very short planktonic stage are especially convenient subjects of settlement studies. Planktotrophic larvae of serpulids, in contrast with larvae of most polychaetes, can be easily obtained and reared in the laboratory. “Nothing is easier than the rearing of Serpulids in the laboratory and especially is this the case with regard to Pomatoceros” (Fuchs 1911, most probably referring to P. lamarckii). Consequently, serpulids have served as objects of classical descriptive studies of embryology and early development since the mid-nineteenth century (see review in Segrove 1941). Also, their larvae have often been used as “typical polychaete larvae” in various recent questionorientated ecological, ultrastructural, life-history and evolutionary studies. As a result, life history of serpulimorph polychaetes has been studied very unevenly. Reproduction, development and settlement of a few common and fouling species are fairly well known but information on the life history of most species is lacking. The objective of this paper is to put together available up-to-date information derived from various studies in order to elucidate the diversity of life-history patterns in this group. We also consider this information in the light of current hypotheses of life-history evolution in marine invertebrates and discuss possible evolutionary mechanisms shaping life history in the group.

Sexuality patterns

Gonochorism and sequential hermaphroditism The sexes were traditionally considered to be almost exclusively separate in the Serpulidae, Johnson (1908) for instance lists, with some Spirorbidae, only the genus Salmacina as hermaphroditic. However, studies on the biology of the most common and commercially important fouling species eventually revealed protandric hermaphroditism with a very short intermediate stage in some species (Hydroides elegans: Ranzoli 1962; Pomatoceros triqueter.

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E.K.KUPRIYANOVA, E.NISHI, H.A.TEN HOVE & A.V.RZHAVSKY

Føyn & Gjøen 1950, 1954; Ficopomatus uschakovi: Straughan 1968, 1972a,b; F. enigmaticus: Dixon 1981). Individuals producing both eggs and sperm can be found also in populations of Galeolaria caespitosa and G. hystrix (Kupriyanova unpubl.), suggesting sequential hermaphroditism in these species. Sequential hermaphroditism causes biased sex ratios and difference in size between sexes (Straughan 1972a, Dixon 1981, Castric-Fey 1984). In Ficopomatus uschakovi about 40% of worms were males during the peak of the reproductive season (Straughan 1972a). The male : female sex ratio was 1:5 in Pomatoceros triqueter (Cragg 1939). Although the overall sex ratio was reported to be 1:1 in both P. triqueter and P. lamarckii, very young worms were male and old worms were female (Castric-Fey 1984). The male to female ratio of juvenile Hydroides elegans varied from 1:4 to 3:1 (Qiu & Qian 1998). However, in the apparently gonochoristic Pomatoleios kraussi the sex ratio was 1:2 in the peak of the reproductive season and even during other months (Nishi 1996). There is a growing perception among polychaete biologists that hermaphroditism is significantly under-reported in the family and that sequential hermaphroditism may be the rule rather than an exception for serpulids. The difficulty arises from the fact that simple examination is sufficient to determine simultaneous hermaphroditism but special populationlevel studies are required to distinguish between true gonochorism and sequential hermaphroditism.

Simultaneous hermaphroditism Simultaneous hermaphroditism is less common in serpulids and it seems to develop as a result of slower protandrous transition in small species such as Rhodopsis pusilla and species of the Filograna/Salmacina complex. In Salmacina dysteri colonies, simultaneous hermaphrodite specimens coexist with male and female specimens (Japan: Nishi & Nishihira 1993, 1994) (Fig. 1B-D). In Salmacina and Filograna, male segments are usually or mainly in anterior segments and female ones are usually or mainly in posterior ones (UK, Italy, Salmacina dysteri: Huxley 1855, Vannini 1965). However, Claparède (1870) explicitly states the reverse for S. aedificatrix from Naples but this trend does not apply for all individuals. Few segments contained both male and female gametes in S. dysteri (Japan: Nishi & Yamasu 1992b, Nishi & Nishihira 1993). Protandrous S. incrustans retains the capacity to produce male gametes after emergence of female gametes (Vannini 1950). Spirobranchus polycerus sensu stricto is also a simultaneous hermaphrodite (Marsden 1992), although the two-horned sympatric form (var. augeneri, ten Hove 1970), of supposedly the same species, is apparently gonochoristic. In contrast to serpulids, all known spirorbids are simultaneous hermaphrodites. Their anterior abdominal segments contain eggs and the posterior segments contain male gametes (e.g. Bergan 1953, Potswald 1967a,b, King et al. 1969) (Fig. 1B). However, because sperm appear to develop faster than oocytes, juvenile worms may function as males before they can also function as females (Potswald 1981). The number of female and male chaetigerous segments varied between 2–4 and 6–31, respectively (e.g. Circeis cf. armoricana, Spirorbis spirorbis, and Bushiella sp.: Bergan 1953; Simplaria potswaldi: Potswald 1967a,b; Spirorbis spirorbis: King et al. 1969; Neodexiospira brasiliensis: Rzhavsky & Britayev 1984) (Fig. 1). Stagni (1959, 1961) also reported the presence of female germ cells in the achaetigerous region of Janua pagenstecheri. 4

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

Figure 1 Simultaneous hermaphroditism in serpulids and spirorbids. A: Spirorbis spirorbis, schematic representation of female and male segments (after King et al. 1969 with permission of Cambridge University Press), e—eggs in female segments, s—sperm in male segments; B: Salmacina dysteri, histological section, hermaphrodite segment; C: S. dysteri, histological section, female segments; D: S. dysteri, histological section, male segments (after Nishi & Nishihira 1993). B-D, no scale given in original publications.

Bergan (1953) found that in most specimens of Circeis cf. armoricana there were one or two segments where the right (concave) half was female, while the left (convex) half was male. These segments were situated between the completely female segments and the completely male ones. Similar lateral asymmetry in sex differentiation was found in one specimen of Simplaria potswaldi (Potswald 1967b). According to Bergan (1953), with exception of this asymmetry, spirorbid segments never contain both mature eggs and sperm, although Potswald (1967b) found two individuals of S. potswaldi that had oocytes and sperm developing together in the second abdominal segment, between a purely female and male segment.

Asexual reproduction Asexual reproduction has been most extensively studied in the genera Filograna and Salmacina. In these taxa the parental animal divides into two, a process that leads to the 5

E.K.KUPRIYANOVA, E.NISHI, H.A.TEN HOVE & A.V.RZHAVSKY

Figure 2 Asexual reproduction of Salmacina dysteri (scanning electron microphotograph). The asexual bud (bu) and parental worm (st) both have extended branchial crowns (br) (Nishi unpubl.). Scale: 1 mm.

formation of colonies. Before the real separation takes place, the new cephalic region forms in the middle part of the parental specimen by transformation of abdominal segments into thoracic ones (morphallaxis) (e.g. Malaquin 1895, 1911, Benham 1927, Faulkner 1929, Vannini 1950, 1965, Ranzoli 1955, Vannini & Ranzoli 1962, Nishi & Yamasu 1992b, Nishi & Nishihira 1994) (Fig. 2). Filogranula gracilis reproduces asexually by transverse fission in the middle of the abdomen (ten Hove 1979b). Scissiparity results in chains of individuals with the greater part of each tube growing along the substratum. However, its youngest part is generally free and erect, causing the mouth to lie at some distance from the substratum. Very thin tubes of new individuals bud at the mouths of established tubes and descend to the substratum, where they gradually attain the appearance and dimensions of mature tubes. In Josephella marenzelleri asexual reproduction leads to a network of branching tubes (George 1974). The same holds for Rhodopsis pusilla (Ben-Eliahu & ten Hove 1989, Nishi & Yamasu 1992a). Scissiparity was inferred from a few branching tubes in at least three species of Spiraserpula. In S. snellii one tube revealed two specimens: a parent and a schizont closely pressed to its posterior end (Pillai & ten Hove 1994), which proves asexual reproduction. Ben-Eliahu & Dafni (1979) give no evidence of asexual reproduction in Filogranella, but ten Hove (pers. comm.) found three very evidently branching tubes of Filogranella elatensis from the Seychelles, which is indicative of asexual reproduction. 6

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

Gametes

Gamete production and development

Gonads and other gamete-producing organs True gonads are absent in some serpulids (e.g. Hydroides dianthus, Ficopomatus enigmaticus) in either sex and the germ cells are produced by a germinal epithelium associated with the ring blood vessels in the intersegmental septa (Schenk 1875, Vuillemin 1965, Dixon 1981). Rullier (1955) described these gonadial tissues as zones of proliferation. Di Grande & Sabelli (1973) described their structure and the connections with blood vessels. Similar structures are present in other species of the Serpulidae (Clark & Olive 1973). Genital organs other than ovaries or testes in the Polychaeta have been reviewed by Westheide (1988). Distinct gonads have been described in Salmacina/Filograna complex (Malaquin 1925, Faulkner 1929) and in Pomatoceros triqueter (Thomas 1940, Jyssum 1957). Developing gametes are released into the coelom. In both sexes there is a lack of synchrony in the way gametes are produced, with all but the pre-spawning mature and recently spawned individuals containing gametocytes in different stages of development. If spawning is artificially induced in laboratory conditions, a mixture of mature and immature oocytes is sometimes expelled (Kupriyanova unpubl.). It is unknown, however, whether immature oocytes are also released during natural spawning events. Stagni (1961) reported that the female germ cells of the spirorbid Janua pagenstecheri are localised around the walls of the ventral blood vessel in the achaetigerous region and around ring vessels and the ventral vessel in abdominal segments 1 and 2. Oocytes are released into the coelom only at the beginning of vitellogenesis. Male germ cells are connected with the same vessels in other abdominal segments. They may separate from the vessel walls and float into the coelom where they actively multiply. In several species of spirorbids (Simplaria potswaldi, Protolaeospira eximia, Circeis spirillum and Paradexiospira (Spirorbides) vitrea), Potswald (1967b) described the gonad as a discrete organ composed of clumps of primordial germ cells. These cells are arranged in two retroperitoneal rows along the middle of the ventral nerve cord and running the length of the abdominal segments. Both female and male gametes differentiate simultaneously in the same individual (Potswald 1967b). Chromosome numbers, including those known in the Serpulidae and Spirorbidae have been reviewed by Christensen (1980) and Vitturi et al. (1984). The diploid chromosome numbers in serpulids normally range from 20 to 28, although there are two records of 14 in Serpula vermicularis as opposed to one record of 28 (Vitturi et al. 1984). Spirorbids have a diploid chromosome count of 20 (Dasgupta & Austin 1960, Table 1).

Oogenesis and spermatogenesis Cytological events and ultrastructural details of oogenesis have been studied in Pomatoceros (Jyssum 1957), Hydroides norvegicus (Nordback 1956), Spirorbis spirorbis (King et al. 1969, Potswald 1969, 1972), Simplaria potswaldi, Paradexiospira (Spirorbides) vitrea, Circeis spirillum and Protolaeospira eximia (Potswald 1967b). Spermatogenesis has been studied in 7

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Table 1 Chromosome numbers of serpulids and spirorbids.

Chitinopoma serrula (Franzén 1982, Franzén & Rice 1988), Hydroides norvegicus, Placostegus tridentatus, Protula globifera and Serpula vermicularis (Franzén 1956), Hydroides diramphus (Mona et al. 1994), Simplaria potswaldi (Potswald 1966, 1967a,b), Paradexiospira (Spirorbides) vitrea, Circeis spirillum and Protolaeospira eximia (Potswald 1967b), Janua pagenstecheri (Stagni 1959, 1961), and Spirorbis spirorbis (Picard 1980). These details are not considered here. Both oogenesis and spermatogenesis of the Polychaeta are discussed in a broader context by Eckelbarger (1983, 1988) and Franzén & Rice (1988). In the spirorbid Circeis armoricana from the Sea of Japan two to three generations of oocytes develop simultaneously. The gonads of a specimen that has just started incubation of a brood usually contain oocytes up to 50 µm in diameter. These oocytes mature by the time the development of the brood is completed. The specimen starts a new brood soon after the previous brood is released from the brooding structure (Ivin et al. 1990).

Fecundity Little information is available on the number of gametes produced by free-spawning serpulids (Table 2). The available data indicate that female fecundity may vary by an order of magnitude within a species. The average number of mature ova expelled by a female of Hydroides dianthus is reported to vary from 3600 (Toonen & Pawlik 1994) to 30000 (Leone 1970), 8

Table 2 Descriptive table of literature on reproduction and development of serpulimorph polychaetes. PR—protandric hermaphrodite, SM—simultaneous hermaphrodite, GH—gonochoristic, FS—free spawning, BR—brooding (type of brooding is specified in the text), F—feeding (planktotrophic) larva, NF— non-feeding (lecithotrophic) larva, EL—sperm with elongated head, SPH—sperm with spherical head.

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

9

Table 2 continued

E.K.KUPRIYANOVA, E.NISHI, H.A.TEN HOVE & A.V.RZHAVSKY

10

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

11

Table 2 continued

E.K.KUPRIYANOVA, E.NISHI, H.A.TEN HOVE & A.V.RZHAVSKY

12

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

13

Table 2 continued

E.K.KUPRIYANOVA, E.NISHI, H.A.TEN HOVE & A.V.RZHAVSKY

14

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

15

16

‡Estimated from figure.

*Note that in serpulids the body length without a tube is reported, while in spirorbids it is the coil diameter of the tube that is used as a measure of body size, unless indicated otherwise. †Since all known spirorbids are simultaneous hermaphrodites and characterised by non-feeding development, data in parentheses (SM), (NF) are used when sexual pattern and larval feeding were not explicitly stated in cited publications.

Table 2 continued

E.K.KUPRIYANOVA, E.NISHI, H.A.TEN HOVE & A.V.RZHAVSKY

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

whereas Zuraw & Leone (1968) report a range of 600–180000. Average female fecundity of Pseudochitinopoma occidentalis was reported to be about 2500 (Hess 1993) and that of Hydroides elegans ranged from 1100 to 9050 oocytes per female (Qiu & Qian 1998). Similarly, the fecundity of Ficopomatus enigmaticus is reported to vary between 1000– 10000 (Kinoshita & Hirano 1977). Fecundity of brooding serpulid species may be as low as one embryo per brood chamber in Rhodopsis pusilla (Nishi & Yamasu 1992a) and does not exceed 50 embryos in Paraprotis dendrova (Nishi & Yamasu 1992c) (Table 2). The maximum number of eggs per segment in Salmacina dysteri was six and it was on average 26 in a whole worm (Japan: Nishi & Nishihira 1993). In contrast to the fecundity of serpulids, the fecundity of brooding spirorbids is well documented (Table 2). It is slightly higher than that of brooding serpulids but also shows significant variability among species. The lowest fecundity (not more than five embryos per brood) was reported for Nidificaria nidica, Spirorbis infundibulum, Bushiella (Jugaria) atlantica, Pileolaria dakarensis and the highest (>200 embryos per brood) was reported for Romanchella pustulata, Metalaeospira pixelli, and Protolaeospira (Dextralia) stalagmia. Even less is known about male fecundity in both spirorbids and serpulids. The estimated number of sperm released by Hydroides dianthus is 62 millions (Leone 1970). The maximum number of 7600 sperms per segment was reported for Salmacina dysteri (Japan: Nishi & Nishihira 1993).

Factors affecting gamete maturation and fecundity Temperature Later stages of gametogenesis in Ficopomatus enigmaticus require an increase in water temperature (Dixon 1981). The rate of gamete maturation in Spirorbis rupestris was slow at 5°C but was more rapid at higher temperatures (Gee 1967). Hydroides dianthus responds to artificially elevated temperatures in the winter by developing gametes out of season. Worms subjected to a temperature approximating that of the natural environment during the normal reproductive period developed normal ripe gametes in 10 days (Turner & Hanks 1960). On the other hand, according to Leone (1970), gamete production (fecundity) in this species decreased at temperatures abnormally high for this species (26–30°C). Average fecundity of H. elegans was unaffected by temperature within the range of 15–30°C (Qiu & Qian 1998). Salinity Low salinity reduces gamete production in serpulids. The average fecundity in H. dianthus decreased from 34000 at a salinity of 35 to 28000 at 25 and to 13000 at 15. Average fecundity of H. dianthus and H. elegans was similar at salinities ⭓25 but was lower at the lowest survival salinity of 15–20 (Leone 1970, Qiu & Qian 1998). Food The type of food affects the number of sperm released in H. dianthus: more sperm were obtained in the worms fed an algal mixture than in those fed a single species (Leone 1970) but the number of eggs did not appear to be significantly affected by the different food types. Chemical stimulation of gamete maturation Certain chemicals affect gamete maturation. Hörstadius (1923) found that increased concentrations of CaCl2 in calcium-free sea water 17

E.K.KUPRIYANOVA, E.NISHI, H.A.TEN HOVE & A.V.RZHAVSKY

promoted maturation of Pomatoceros. Maturation of oocytes in this species was also promoted by the absence of potassium in artificial sea water and the addition of increasing levels of potassium chloride had an increasingly inhibitory effect. Ashton (1959) found that oocytes of Hydroides could be activated by trypsin or chymotrypsin in the absence of calcium. Body size Adult body size is the major factor determining fecundity in many invertebrates, including serpulimorph polychaetes. Larger maximum body size correlates with higher maximum fecundity in spirorbids, where such data are available (see Fig. 14, p. 69). Observed significant intraspecific variability is determined by the environmental conditions during the reproductive season, individual age, nutritional status, or a combination of factors. Daly (1978a) showed that the number of eggs per brood of a Northumberland population of Spirorbis spirorbis positively correlated with individual size (and age) and, for a given size, declined steadily during the breeding season. Fecundity of Neodexiospira brasiliensis from the Sea of Japan also correlates with the size of animals but does not change during the reproductive season (Rzhavsky & Britayev 1984). The average fecundity of Circeis armoricana increased from 79 in January to 160.8 in June, but only the maximum fecundity observed in April—May positively correlated with body size (Ivin 1998).

Gamete morphology and composition

The eggs Mature egg sizes show a wide range of variation (Table 2, Fig. 3). Egg size in serpulids range from 45–50 µm in Ficopomatus miamiensis (Lacalli 1976) and Hydroides ezoensis (Miura & Kajihara 1981, 1984) to 180–200 µm in Chitinopoma serrula (Dons 1933). Egg size in spirorbids ranges from 80 µm in Neodexiospira foraminosa (Nishi & Yamasu 1992d) to 230 µm in Pileolaria militaris (Kiseleva 1957, see also Table 2). Many authors report some range for serpulid egg sizes which, at least partly, may be due to measuring at different moments in the cycle (see below). No detailed studies on natural intraspecific variability of egg size are available. The unfertilised oocytes of free-spawners are negatively buoyant. When released, they are lens-shaped (double-concave) in Serpula columbiana (Strathmann 1987), biconvex in Pomatoceros triqueter (von Drasche 1884, Kuhl 1941), cup shaped to irregular in Ficopomatus enigmaticus (Fischer-Piette 1937, Vuillemin 1965) or somewhat polygonal and crumpled in appearance in Galeolaria caespitosa and Hydroides ezoensis (Andrews & Anderson 1962, Grant 1981, Miura & Kajihara 1981). All become spherical after contact with sea water. The colour of oocytes ranges from pale pink or yellowish (Pomatoleios kraussi: Crisp 1977; Galeolaria caespitosa: Marsden & Anderson 1981) to deep red-violet in Pomatoceros triqueter (Segrove 1941, Kuhl 1941). The egg coat (chorion) is approximately 2 µm thick and sometimes has a reticulate patterned surface (Spirobranchus corniculatus: Smith 1984a; Galeolaria caespitosa: Grant 1981; G. hystrix: Kupriyanova unpubl.; Spirobranchus polycerus: Lacalli 1976). The development of an extracellular coat in oocytes of Galeolaria caespitosa is described by Grant & Crossley (1980). There are few reliable observations on shape and size of freshly spawned unfertilised eggs of spirorbids. Quite often the eggs (=unfertilised oocytes) are confused with embryos at early developmental stages or, more often, developing embryos in brooding structures 18

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

Figure 3 Eggs of serpulids and spirorbids. A: Hydroides elegans 50 µm (after Wisely 1958 by permission of CSIRO Australia); B: Galeolaria hystrix, 60 µm (Kupriyanova unpubl.); C: Pomatoceros triqueter, 75 µm (after Segrove 1941); D: Rhodopsis pusilla, 90 µm (after Nishi & Yamasu 1992a); E: Salmacina dysteri, 150 µm (after Nishi & Yamasu 1992b); F: Spirobranchus giganteus, 80 µm after Smith 1984a); G: Dexiospira foraminosa, 80 µm (after Nishi & Yamasu 1992d); H: Protula sp. 80 µm (after Tampi 1960).

19

E.K.KUPRIYANOVA, E.NISHI, H.A.TEN HOVE & A.V.RZHAVSKY

Figure 4 Sperm morphology of serpulimorph polychaetes. Broadcasting species, A: Serpula sp. (after Jamieson & Rouse 1989 with permission of Cambridge University Press); B: Pomatoleios kraussi (after Jamieson & Rouse 1989); C: Spirobranchus giganteus corniculatus (after Nishi 1992b); D: Galeolaria caespitosa (after Grant 1981 with permission of Springer-Verlag, redrawn from SEM photo); E: Hydroides elegans (after Nishi 1992b). Brooding species, F: Paraprotis dendrova (from Nishi & Yamasu 1992b); G: Salmacina sp. (after Rouse 1996 with permission of Springer-Verlag); H: Chitinopoma serrula (after Franzén 1982 with permission of Balaban Publishers); I: Spirorbis spirorbis (after Franzén 1956 with permission); J: Bushiella sp. (after Franzén 1956); K: Pileolaria militaris (after Franzén 1958 with permission); L: Janua pagenstecheri (after Franzén 1958). A, B, G, H redrawn from TEM photograph. Scale, A-C and E: 2 µm; D and F: 1 µm; G and H: 2 µm; I-L: 5 µm.

20

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

are mistakenly termed “eggs” (e.g. Sveshnikov 1978). Eggs and embryos of spirorbids are brown, green, yellow, red, or pale. Knight-Jones & Knight-Jones (1977) mentioned various colours (brownish orange, orange brown, reddish brown, salmon pink, etc.) of ovaries but most likely they referred to the colour of ripe oocytes in the coelomic cavity of genital segments. There are almost no data on the biochemical composition and energetic content of serpulid and spirorbid eggs. One published estimate of egg energy content in a serpulid is that of Strathmann & Vedder (1977) for Serpula columbiana from Friday Harbor, WA, USA. Based on significant overlap in egg size of species with feeding and non-feeding larvae (see Table 2), one should expect a significant variation in energetic content for eggs of similar size from distantly related species.

The sperm Sperms that are characterised by a spherical to conical head were already described in 1870 for Hydroides elegans (Claparède 1870). Such sperm, with a midpiece containing spherical mitochondria and a flagellum, are known for Pomatoleios kraussi, Spirobranchus corniculatus (Nishi 1992b), Protula globifera, Placostegus tridentatus, Serpula vermicularis, Hydroides norvegicus (Franzén 1956), H. dianthus (Colwin & Colwin 1961a), H. ezoensis, H. fusicola and H. elegans (Matsuo & Yoshioshi 1983, Nishi 1992b), Floriprotis sabiuraensis (Uchida 1978) and Galeolaria caespitosa (Grant 1981) (Fig. 4A-E). Sperm with an an elongated head and midpiece are known for brooding species, such as Salmacina dysteri (Sweden) and Chitinopoma serrula (Franzén 1956, 1958, 1982), Rhodopsis pusilla and Paraprotis dendrova (Nishi & Yamasu 1992a,c) (Fig. 4F-L). Spirorbidae also (Table 2) have elongated sperm, although Franzén (1958) recognises three and Potswald (1967b) two different morphological types within the general elongated sperm type. Differences in sperm morphology are considered to reflect different modes of fertilisation or sperm transfer (Franzén 1956, 1982, Sawada 1984). Jamieson & Rouse (1989) distinguished ect-aquasperm for broadcast spawning species and ent-aquasperm that is released into water at some stage but is stored by the female prior to fertilisation (see p. 000).

Spawning and fertilisation

Morphological changes accompanying spawning According to Vuillemin (1965), in Ficopomatus enigmaticus and Hydroides elegans, maturation is accompanied by “epitoky”, significant morphological changes (mainly an increase in pigmentation) in the abdomen. Such a phenomenon has not been reported since 1965. It is strange that she found many regenerating abdomens both in Hydroides and Ficopomatus, indicative of autotomy. However, she explicitly states that she never observed autotomised abdominal parts being passed out of the tube, which one would expect of real epitoky (concurrent with swarming). Nevertheless, her photographs indeed are very suggestive for regeneration and thus autotomy. 21

E.K.KUPRIYANOVA, E.NISHI, H.A.TEN HOVE & A.V.RZHAVSKY

Dixon (1977) states: “Following spawning the gonadial tissues undergo a short resting phase during which the spent adults resemble juvenile worms, except for their larger size.” He, however, does not mention a sharp contrast between unspent and spent segments, which could be an alternative explanation for Vuillemin’s regenerating specimens. One wonders if spawning may result in such a damage that the animal sheds part of the spent abdomen.

Frequency of spawning and length of the breeding seasons Serpulimorph polychaetes are referred to as iteroparous, polytelic, or multiannual with respect to the frequency of reproduction. All these terms are used to describe species that spawn several times in a lifetime. Serpulids spawn more or less continuously during an extended reproductive season. For example, the reproductive period of Spirobranchus giganteus in Puerto Rico lasted from March through October (Allen 1957). Spawning of S. polycerus from the West Indies was also observed during the summer months (Lewis 1960, Marsden 1960) but Lacalli (1976) found ripe gametes in this species from mid-October to late May in Barbados. The greatest proportion of ripe adults of S. corniculatus was found in Australia in summer between October and January (Smith 1984a). Crucigera irregularis, C. zygophora and Serpula columbiana spawn from April to September in Puget Sound, Washington State, USA (Strathmann 1987). Spawning of Ficopomatus enigmaticus in southeastern England commences in June and continues through October (Dixon 1981). The breeding season of Japanese Hydroides ezoensis lasts from late May to September and is longer than that of sympatric Pomatoleios kraussi (Miura & Kajihara 1984). Nishi (1996) reported that the reproductive season of P. kraussi in Japan lasts from April to December, although worms with eggs can be found all year around (Nishi unpubl.). It was possible to find a few ripe individuals of Galeolaria caespitosa at any time of the year but the most successful fertilisations were achieved with worms collected in spring (from early September) and summer (M.A.O’Donnell pers. comm.). Tropical populations of Ficopomatus uschakovi have a longer breeding season than populations of their temperate relative F. enigmaticus (Dixon 1981). The data on spawning of spirorbids exist only for populations from the Northern Hemisphere and mainly for arctic and/or boreal species. Commencement of spawning is inferred from the presence of brooded embryos. Some spirorbids (Spirorbis spirorbis, S. tridentatus, S. rupestris, Janua pagenstecheri) spawn between April-May and OctoberNovember (Garbarini 1933, 1936a, Bergan 1953, de Silva 1967, Gee 1967, Daly 1978a), except for Spirorbis corallinae, which stop spawning by the end of July (de Silva 1967). The breeding season of the spirorbid Circeis paguri in southern UK lasts from February to August (AlOgily & Knight-Jones 1981). Other spirorbids spawn all year round, although the proportion of spawning individuals decreases significantly during the winter. These are Simplaria potswaldi (Potswald 1967b), Spirorbis rothlisbergi (Rothlisberg 1974), Circeis spirillum (Potswald 1967b), Neodexiospira cf. brasiliensis (Abe 1943), Bushiella sp. (Bergan 1953), Neodexiospira alveolata (Rzhavsky & Britayev 1984, Radashevsky pers. comm.) and Pileolaria berkeleyana sensu lato (Thorp 1991). The proportion of Circeis armoricana with broods increased from 9.4% in February to 96.7% in June then gradually decreased to 2.5% in December (Ivin 1997). 22

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

While special studies on breeding periods for tropical, subantarctic and Antarctic spirorbids are lacking, occasional observations (Rzhavsky unpubl.) and data in faunistic papers (e.g. Vine 1977) suggest that tropical and subtropical species spawn continuously all year round, whereas the peak of breeding of antarctic/austral species occurs during austral summer (December-March). The breeding periods for a species may vary geographically. For example, Circeis armoricana from the Kamchatka coast probably stops breeding by the end of September (Rzhavsky & Britayev 1988), whereas it breeds throughout the year in the Sea of Japan (Ivin et al. 1990, Ivin 1998) and possibly on the Norwegian coast (Bergan 1953). Paradexiospira (Spirorbides) vitrea from the Pacific coast of USA (Potswald 1967b) and from Kamchatka (Rzhavsky unpubl.) brood throughout the entire year. However, Bergan (1953) states that the Norwegian population of this species only broods from October to November and never in the summer months, which seems quite unlikely.

Factors affecting spawning

Environmental physical factors Spawning in polychaetes is influenced by environmental factors such as temperature, day length and lunar cycles (Clark 1979). Temperature seems to be one of the major exogenous factors controlling the timing of reproduction of serpulids and spirorbids because the peaks of the reproductive seasons generally coincide with warmer months. Spirorbis spirorbis spawned in Roscoff every 14 days throughout the whole year as long as water temperature remained at 11–18°C (Garbarini 1936a). However, this is not always the case for some spirorbids. De Silva (1967) observed that the sea temperature was higher when breeding of S. spirorbis ceased than it was when brooding commenced. Probably, change in temperature may be more important than the absolute level, or the decline in breeding during autumn is related more to a reduction in food supply (de Silva 1967). The time when breeding begins in a S. spirorbis population in Northumberland, England varies little from year to year but is apparently not triggered by an environmental temperature rise (Daly 1978a). Abe (1943) found that Neodexiospira cf. brasiliensis in Japan breeds throughout the year at temperatures as low as 5–6°C in winter and as high as 32°C in summer.

Spawning synchronisation Given the semi-continuous or continuous nature of their spawning, serpulids apparently synchronise gamete release with their closest neighbours and pheromones probably coordinate gamete release, as has been demonstrated for other polychaetes (Hardege & Bentley 1997, Hardege et al. 1998). However, the degree of this synchronisation and its mechanisms are not known. Since spawning events are very difficult to observe in brooding species, synchronisation of spawning in spirorbids is often inferred from the synchronous release of competent larvae. Distinct synchronisation of spawning was reported for Spirorbis spirorbis (Garbarini 1933, 1936a, Knight-Jones 1951, de Silva 1967, Gee 1967), S. rothlisbergi (Rothlisberg 1974) and not so obviously for S. corallinae (de Silva 1967). These species have 2-wk periods of 23

E.K.KUPRIYANOVA, E.NISHI, H.A.TEN HOVE & A.V.RZHAVSKY

larval development that correlate with lunar cycles. Daly (1978b) also found synchronisation in spawning and release of embryos of S. spirorbis from Northumberland, England but it cannot be synchronised with lunar or tidal cycles since the larval development takes about 20–23 days. The synchrony within the population in both spawning and larval release increases later in the breeding season, even though the events are not synchronised with any obvious environmental variable (Daly 1978b). Such synchrony of spawning and larval release may be under an endogenous control. Daly (1978b) suggested that a factor causing epidemic spawning might also improve the synchrony of spawning within the population. For populations of S. spirorbis from Norway synchronisation of spawning is very local, that is, specimens from the same Fucus breed synchronously but synchronisation with breeding of specimens from the neighbouring tidal pool is absent (Bergan 1953). Complete lack of spawning synchronisation has been demonstrated for some species (Bergan 1953, Gee 1967, Potswald 1967b).

Ecology of fertilisation

External fertilisation in broadcast spawning species The gametes of broadcast-spawners (e.g. genera Hydroides, Serpula, Crucigera, Galeolaria, Pomatoceros and Spirobranchus, see Table 2, p. 9) are released through nephridiopores and are delivered to the tube orifice with the help of ciliary beating in the faecal groove. In Spirobranchus corniculatus gametes are released via the right side of the branchial crown and are ejected in a stream extending several centimetres above the worm (Smith 1985). Natural spawning events are rarely observed in serpulids but gamete release is stimulated by breaking the tubes and artificial fertilisation is easy to achieve in the laboratory. The rates of gamete transport and mixing, as well as fertilisation success and factors affecting it, have not been studied in natural populations nor in the laboratory. In free-spawning invertebrates contact of gametes is highly dependent on the proximity of conspecifics, the hydrological conditions at the time of spawning and the quantity of gametes released (a function of the size of adults and the overall population density). Successful fertilisation may be further influenced by the egg-sperm contact time, the age of gametes and sperm swimming velocity (Chia & Barker 1996). Qian & Pechenik (1998) state that fertilisation is successful over a remarkably broad range of sperm concentration in Hydroides elegans and usually more than 95% of eggs were fertilised within 15 min after the eggs and the sperm were mixed.

Fertilisation in brooding species Little is known about the fertilisation biology in small-bodied brooding serpulids and spirorbids. In spirorbids artificial fertilisation is difficult to achieve: none of the attempts to fertilise eggs of Simplaria potswaldi (Potswald 1968) artificially was successful. No data are available on fertilisation success and the assumption that the fertilisation rate for brooding species is high may not be correct and evidence for this is needed. Gee & Williams (1965) reported that in Spirorbis spirorbis eggs and sperm are shed through the nephridioducts and fertilisation occurs externally to the body but inside the 24

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

tube. Broadcasting of sperm was previously assumed to be a common fertilisation mechanism for all brooding tube-dwellers. However, discovery of a spermatheca in spirorbids (Daly & Golding 1977, Picard 1980) and one serpulid (Rouse 1996, see below) suggests that fertilisation is more complex in some, if not most, brooding species. S. spirorbis stores sperm in single spermatheca located at the base of the branchial crown (Daly & Golding 1977, Picard 1980). It has been proposed that sperm is released into the sea, collected by other individuals and stored in the spermatheca. Sperm leaves the spermatheca at the time of spawning and fertilises eggs within the animal tube. Fertilisation probably also takes place in the tube of the operculum-brooding spirorbids and fertilised embryos are transferred later to the opercular incubating chamber. Picard (1980) states that among spirorbids spermathecae were found in S. spirorbis, S. inornatus, S. rupestris, S. tridentatus, Janua pagenstecheri, Paradexiospira vitrea, Circeis armoricana, Protolaeospira striata, and Paralaeospira malardi, but he does not give any details. Spermathecae of Salmacina, the only serpulid species so far known to store sperm, are different from those of spirorbids. Females of Salmacina sp. store sperm in paired spermathecae situated in the base of the branchial crown (Belize: Rouse 1996).

Self-fertilisation Electrophoretic evidence and laboratory experiments with isolated individuals showed that spirorbids are capable of self-fertilisation (Simplaria potswaldi: Potswald 1964; Spirorbis spirorbis and Janua pagenstecheri: Gee & Williams 1965; Neodexiospira brasiliensis and Simplaria pseudomilitaris: Beckwitt 1982). Self-fertilisation in the laboratory does not occur as readily as cross-fertilisation and it is believed to be facultative and not obligatory in spirorbids (Potswald 1964, 1968, Gee & Williams 1965, Beckwitt 1982). Many embryos of Spirorbis borealis and Janua pagenstecheri resulting from self-fertilisation develop slowly or are not viable; some, however, are capable of hatching and metamorphosing (Gee & Williams 1965). Self-fertilisation could not be demonstrated in the hermaphrodite serpulid Salmacina (Japan: Nishi & Nishihara 1993).

Cytological aspects of fertilisation The ultrastructural details of cytological processes taking place during fertilisation in serpulids and spirorbids have been addressed by a number of authors and were placed in a wider context by Franklin (1970). A classic series of studies on the ultrastructure of sperm-egg interaction in Hydroides dianthus by Colwin & Colwin (1961a,b,c) addressed the functional significance of the acrosome reaction, and the sequence of events during the fusion of the gamete membrane. The fertilisation reaction has been studied in Pomatoceros triqueter (Cragg 1939, Kuhl 1941, Monroy 1948, 1954, Ap Gwynn & Jones 1971, 1972, Ap Gwynn et al. 1971), Hydroides elegans and H. norvegicus (Monroy 1954, Nordback 1956), Ficopomatus enigmaticus (Rullier 1955, Sichel 1965), Galeolaria caespitosa (Grant & Dwarte 1980) and Spirorbis spirorbis (Babbage & King 1970). In most polychaetes the oocytes are arrested in the prophase of the first meiotic division and fertilisation is a physiological trigger that activates the oocyte maturation. The egg starts precleavage development and resumes meiosis. In some tube dwellers, the oocytes resume meiosis 25

E.K.KUPRIYANOVA, E.NISHI, H.A.TEN HOVE & A.V.RZHAVSKY

before fertilisation. The oocytes in these species undergo “prematuration”, that is, they progress from prophase I to metaphase I after release from the female. Apparently, serpulid eggs that are spawned when the female is removed from the tube, undergo spontaneous prematuration, similar to that reported for the sabellariid Sabellaria alveolata (Peaucellier 1997).

Development

Overview of embryological and developmental studies The embryonic development of serpulids has been studied extensively, especially at the turn of the century. Shearer (1911) summarised early embryological data from the literature published mostly prior to 1910 and provided a detailed description of development of Hydroides dianthus through the early trochophore stage (see Rouse 1999 for a (re)definition of the trochophore concept). More recent studies on serpulid embryonic development include the work of Vuillemin (1965, 1968) on Ficopomatus enigmaticus and Groepler (1984, 1985) on Pomatoceros triqueter. Most of the accounts that have followed serpulid larval development from fertilisation to settlement include a brief description of pre-trochophore development, including some description of cleavage and gastrulation (P. triqueter. Segrove 1941; Hydroides elegans: Wisely 1958, Sentz-Braconnot 1964; Spirobranchus polycerus: Marsden 1960; Galeolaria caespitosa: Andrews & Anderson 1962, Grant 1981; Marifugia cavatica: Matjasic & Sket 1966; Pomatoleios kraussi: Crisp 1977; Hydroides ezoensis: Miura & Kajihara 1981; Spirobranchus corniculatus: Smith 1984a; Pomatoceros triqueter: Dorresteijn & Luetjens 1994). Tampi (1960) gave a brief description of development of Protula sp. up to the threechaetiger stage. Very short accounts of larval development in Spirobranchus corniculatus were given by White (1976) and in S. giganteus by Allen (1957) and Lewis (1960). Formation of larval segments is described in Protula tubularia by Soulier (1917) and in Hydroides dianthus by Ivanoff (1928). An overview of early development in polychaetes, including Pomatoceros triqueter, is given by Dorresteijn & Fischer (1988). A number of studies addressed various aspects of ultrastructural larval morphology. Lacalli (1984) provided a very detailed study of the nervous system in Spirobranchus polycerus trochophore (48-h old to metatrochopohore). Structure and development of the apical organ in this species on the basis of ultrastructural surveys and three-dimensional reconstructions was described by Lacalli (1981). The ultrastructure of the eyespot in S. corniculatus was described by Smith (1984b) and in Serpula columbiana and Spirobranchus giganteus by Marsden & Hsieh (1987). Pemerl (1965) and Wessing & Polenz (1974) studied the ultrastructure of protonephridia in Serpula columbiana and Pomatoceros triqueter, respectively. Uschakova (1989) described the nervous system of some unidentified spirorbid larva (probably Spirorbis spirorbis) from the White Sea.

Development of feeding larvae Developmental events in genera such as Ficopomatus, Galeolaria, Hydroides, Pomatoceros, Pomatoleios, Serpula and Spirobranchus, which have small eggs and planktotrophic larvae, 26

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

Figure 5 Development of serpulids with planktotrophic larvae. Hydroides elegans (after Wisely 1958 by permission of CSIRO Australia). A: egg, B: 2-cell stage; C: 4-cell stage; D: 8-cell stage; E: early trochophore, apical view; F: the same, lateral view; G: later metatrochophore, lateral view; H: 3chaetiger competent stage, dorsal view; I: larva starting to metamorphose. Scale, A-I: 50 µm.

are very similar (Fig. 5). After fertilisation, the negatively buoyant eggs sink to the bottom, where they undergo cleavage up to the blastula stage. The first cleavage occurs after 1–1.5 h after fertilisation at 20–25°C (Wisely 1958, Andrews & Anderson 1962, Smith 1984a) but it takes 2.5 h at 15°C and almost 4 h at 10–11°C (Strathmann 1987). See Table 2, p. 9 for the comparative timing of planktotrophic development. All cleavages of the blastomeres up to the morula stage are synchronous, holoblastic, and equal. Blastulae are uniformly ciliated and move about the culture dish (Smith 1984a). The blastula develops into a larva with a prototroch consisting of a single ring of cilia. The prototroch separates a rounded episphere from conical hyposphere. The simple gut opens with the mouth below the prototroch and the anus exiting on the opposite side above the anal vesicle. The anal vesicle is a large transparent functionally enigmatic sac located posteriorly in feeding serpulid larvae. The apical plate and the apical tuft of long rigid cilia become distinct. Cilia on the hyposphere are organised into the neurotroch, which runs from the ventral posterior surface to the mouth. 27

E.K.KUPRIYANOVA, E.NISHI, H.A.TEN HOVE & A.V.RZHAVSKY

Later, the prototroch develops three main ciliary bands: the upper and lower with shorter cilia and the middle with much longer cilia (Smith 1984a, Grant 1981). A metatroch is developed at this stage. Between the prototroch and metatroch is a band of short feeding cilia. On the right side of the episphere, a cluster of red pigment cells forms an ocellus. The ventral longitudinal muscle and metatroch circular muscle form and protonephridia become visible. The trochophore continues to grow but does not undergo any significant changes. Next, the larva develops the left ocellus identical to the right one. After this stage the growth is mostly confined to the hyposphere and the larva elongates and develops three chaetigerous segments. Before the settlement a small fourth trunk segment is delineated and paired branchial rudiments appear posterior to the metatroch.

Development of non-feeding larvae

Serpulid larvae The only non-feeding planktonic development reported for the Serpulidae is that of Protula sp. by Tampi (1960). The early stages of development are characterised by the presence of a large number of oil globules. The development is very similar to that of feeding larvae but the active gut is still not formed by the 3-chaetiger stage. Non-feeding development in Protula sp. from Florida observed by Pernet (pers. comm.) was similar to that described by Tampi (1960). Development of non-feeding serpulid embryos that takes place within a brooding structure has been less well studied than that of planktotrophic larvae. Short accounts of development of non-feeding larvae of serpulids are given for Salmacina dysteri (Nishi & Yamasu 1992b), Paraprotis dendrova (Nishi & Yamasu 1992c), and Rhodopsis pusilla (Nishi & Yamasu 1992a). Apparently, the developmental events and general larval morphology are very similar for brooded and planktonic serpulid larvae (Fig. 6). R. pusilla develops to a trochophore with a prototroch consisting of three rows of ciliary bands that at first lacks the apical tuft. The trochophore develops into a one-chaetiger larva and then into a three-chaetiger larva with neurotroch, metatroch and two ocelli. Paraprotis dendrova eggs develop into slowly rotating trochophores with a long apical tuft. The early trochophore of Salmacina dysteri bears a prototroch, a short apical tuft and a pair of brownish red ocelli. The later trochophore stage has a well-developed neurotroch and the prototroch differentiates into three separate ciliary rings: a middle ring with longer cilia and anterior and posterior rings with short cilia. Hatching and settlement in all three species take place at the three-chaetiger stage, when larvae possess an apical tuft, a neurotroch and two ocelli.

Spirorbid larvae The description of developmental events inside the spirorbid brooding structures is very fragmentary (e.g. Schively 1897, Abe 1943, Kiseleva 1957). Early embryology has been described only by Salensky (1883) for Pileolaria cf. militaris. Development from the early trochophore to swimming competent larvae (Fig. 7) was described in more or less detail for P. cf. militaris by Salensky (1883), for Spirorbis sp. by Fewkes (1885), for Circeis cf. armoricana and Neodexiospira alveolata by Okuda (1946), for N. pseudocorrugata by 28

LIFE-HISTORY PATTERNS IN SERPULIMORPH POLYCHAETES

Figure 6 Development of serpulids with lecithotrophic larvae. Brooded larvae: Salmacina dysteri, development inside the adult tube, A: egg; B: 2-cell stage; C: late stage of cleavage; D and E: early trochophore; F: 3-chaetigerous competent larva (after Nishi & Yamasu 1992d). Planktonic larvae: Protula sp., G: egg; H: 2-cell stage; I: 4-cell stage; J: 16-cell stage; K: spherical ciliated larva; L: early trochophore; M: later trochophore; N: 3-chaetiger competent stage; O: larva starting to metamorphose (after Tampi 1960). Scale, A-C: 0.15 mm; D-F: 0.1 mm; G-O: 50 µm.

Casanova (1954), and for Neodexiospira sp., Circeis cf. armoricana and Spirorbis spirorbis by Sveshnikov (1967, 1978). The most detailed description is given by Okuda (1946). Like serpulid trochophores, early spirorbid trochophores are subdivided into a small episphere and a large hyposphere by a prototroch. The prototroch of the early spirorbid consists of two bands of cilia (the upper from long and the lower from short cilia). Apical cilia and ocelli may be present or absent at the early stage. A functional mouth and anus are always absent, although the future location of the mouth can be recognised by an oval depression (Okuda 1946). In metatrochophores the collar forms ventrally under the prototroch; the apical cilia and eyes spots are always present. A neurotroch consisting of transverse rows of cilia appears mid-ventrally. At this stage the prototroch may consist of two rows (the upper long and the lower short cilia), or three rows (the upper short, middle long, and lower short cilia), as in serpulids. In the late stages of metatrochophore development the mouth opens, and branchial and opercular buds develop. The terminal part of the anal segment is covered with short cilia and may bear, in addition, two very long stiff cilia. Some species develop very distinct white primary shell glands (see below). A competent spirorbid larva released from the brooding chamber has three chaetigers and a terminal segment, bands of locomotory cilia (prototroch, metatroch and neurotroch), apical cilia, eyespots, branchial and opercular buds and a large collar which is wider ventrally than dorsally. 29

E.K.KUPRIYANOVA, E.NISHI, H.A.TEN HOVE & A.V.RZHAVSKY

Figure 7 Development of spirorbid larvae. Circeis cf. armoricana, A: trochophores, ventral view; B and C: early metatrochophores, lateral and ventral views; D-F: late metatrochophores, dorsal, lateral, and ventral views; G: pre-release larva ventral view; H: swimming larva (no primary shell glands) lateral view (after Okuda 1946). Janua pagenstecheri, I and J: swimming larva with two primary shell glands, ventral and lateral views (after Höglund 1951). Spirorbis tridentatus, K and L: swimming larva with a single shell gland, ventral and lateral views; psg—primary shell glands (after Höglund 1951); M: sagittal section of competent larvae, midgut and hindgut are not connected (after Nott 1973). Scale, A-F: 50 µm; G-H: 100 µm; I-M: no scale was given in the original publication.

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The mouth (stomodeum) is open ventrally, between prototroch and collar, but the stomach is not functional and is filled with yolk. The anus is also open and surrounded by cilia; some species also have two additional stiff long cilia. Stiff long cilia may also be present apically on the head, on the branchial rudiments and collar. Species differ in the number of larval eyespots (1–5 pairs) whose size and shape can change during development from trochophores to competent larvae. Based on illustrations presented in various publications, the neurotroch, as a rule, contains four ciliary rows but this number may vary slightly among species.

Comparative morphology of feeding and non-feeding larvae The morphology and development of feeding and non-feeding serpulid larvae are extremely similar. The latter contain more yolk, and as a result, are opaque and have under-developed stomachs. However, some features apparently distinguish serpulid and spirorbid larvae. The prominent collar that develops by the early metatrochophore stage and unfolds during spirorbid metamorphosis is such a feature. Another striking feature is the presence of various larval glands. Nott (1973) and Potswald (1978) describe a complex of thoracic gland cells that do not persist after metamorphosis. A pair of ventral subcollar glands secretes the adult tube. Dorsal collar glands are unicellular glands on either side of the mid-dorsal line. In some larvae the hindgut serves as a large white sac known as the “attachment gland” (KnightJones 1951) or the “primary shell gland” (Höglund 1951). The latter author recognised three morphological types of spirorbid larvae: (a) lacking a primary shell gland (Circeinae, Romanchellinae and Paralaeospirinae), (b) with one abdominal shell gland (Spirorbinae, Pileolariinae) and (c) with two primary shell glands (Januinae) (Fig. 7H, I, J, K, L). The structure of the last type is not well understood. The glands are located on the ventral side of the thorax and are retained in juveniles for a short time. Finally, serpulid larvae have a pair of large eyes, whereas spirorbid larvae may have several pairs of eyes that are similar to each other or differ significantly in size and shape. The order of some developmental events also differs for serpulid and spirorbid larvae. In serpulids the collar and branchial buds develop in late demersal larvae after the collapse of the prototroch and before tube construction starts, whereas development of the operculum begins later, at the juvenile stage. In contrast, competent spirorbid larvae with branchial and opercular buds retain the prototroch that serves as a means of locomotion during their short planktonic stage. The anal vesicle is large and unpaired in the feeding larvae of Hydroides, Pomatoceros, and Spirobranchus (e.g. Hatschek 1885, Shearer 1911, Segrove 1941, Lacalli 1984): it is small and paired in the non-feeding larvae of Protula and spirorbids (Salensky 1883, Meyer 1888). In the latter aspect non-feeding larvae resemble those of sabellids (Wilson 1936).

Factors affecting larval development The development time of the pelagic feeding stage in serpulids and that of the brooded stage in spirorbids is, like most other reproductive and developmental processes, profoundly affected by temperature (Table 2, p. 9). The duration and success of planktotrophic development also depends on salinity, food availability and external metabolites of other invertebrates. 31

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Temperature Generally, development time increases with decreasing temperatures, e.g. 7 h at 30°C, and 15 h at 20°C for Ficopomatus enigmaticus (Vuillemin 1958). Although the planktonic stage in Pomatoceros lamarckii is 3 wk in laboratory conditions at 18°C, it varies from about 2 months in early spring to 8–15 days in June and 20 days in August (South Brittanny: Castric-Fey 1984). Larval development of Serpula columbiana takes up to 50 days (the longest developmental period recorded in the laboratory) at 12°C at Friday Harbor, Washington State, USA (Young & Chia 1982, Strathmann 1987); Hydroides dianthus and H. elegans develop to metamorphosis in only 5 days at 24–35°C (Scheltema et al. 1981, Carpizo-Ituarte & Hadfield 1998). The brooding period of Pileolaria berkeleyana sensu lato increases with decreasing temperature from about 10 days at 25°C to about 37 days at 10°C (Thorp 1991). The reported variation in the time of brooding in Spirorbis spirorbis from 14 to 23 days (Garbarini 1933, 1936a, Knight-Jones 1951, de Silva 1967, Gee 1967, Daly 1978b) apparently results from different temperature conditions. Although low temperature (15°C) led to longer duration of development of Hydroides elegans, it did not affect survival from newly-released oocyte to trochophore stages and temperature does not seem to be a limiting factor for early development of this species (Qiu & Qian 1997). On the other hand, Crisp (1977) demonstrated that suboptimal temperatures had a significant effect on both duration of development and survival in Pomatoleios kraussi. At low temperatures of 15–21°C the development to metamorphosis was not completed and at 15°C it did not proceed beyond the gastrula stage. At 23–25°C P. kraussi developed to metamorphosis in 17–18 days, while it took only 7–13 days to reach that stage at 27°C. At 30°C, the development was even faster, the advanced trochophore stage being reached in 4 days but metamorphosis was never observed.

Salinity Salinity is another important factor affecting larval survival and development. Although Galeolaria caespitosa is able to survive dilutions down to 60% sea water, its reproduction is inhibited at concentrations below 80% sea water. Early development proceeded regularly in normal and 80% sea water but no development occurred in oocytes released into 60% sea water (Tait et al. 1984). Lyster (1965) showed that Pomatoceros triqueter larvae survive well in a salinity of 20, can tolerate salinities down to only 10 but can survive in such media for only a few hours. Lowered salinity lengthened the duration of development of Hydroides elegans and reduced its survival (Qiu & Qian 1997). Resistance to salinity stress is reduced when the larvae are simultaneously exposed to temperature stress. The temperature at which the maximum salinity tolerance was displayed for Pomatoceros larvae was 14°C (Lyster 1965).

Food Both food concentration and diet composition affect larval planktotrophic development. Low food concentration lengthened the duration of development from trochophore to newlysettled juvenile and reduced survival and settlement of Hydroides elegans (Qiu & Qian 1997). Paulay et al. (1985) demonstrated that larvae of Serpula columbiana grew significantly 32

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faster with enhanced rations than in natural sea water and suggested that natural food supplies may commonly limit growth and development of larvae. A diet of cultured algae gave less variability through the metatrochophore stage of Spirobranchus but poor success at settlement, whereas a diet of wild algae from the field resulted in a more variable development but more robust larvae (Lacalli 1984).

Other invertebrates External metabolites released by some marine animals can make the surrounding environment either suitable or unsuitable for other organisms. Conditioning of water by adult Hydroides elegans promotes normal development of larvae and is more beneficial than natural sea water. Conditioning by Mytilus delays development and that by Balanus accelerates the development to such an extent that abnormalities may result (Srinivasagam 1966). The early development of Hydroides elegans can be affected if the eggs and sperms are treated with the extract of hemichordate Ptychodera flava (Whitin & Azariah 1982).

Pollutants Effects of pollutants vary with the type of pollution. Larval development in Pomatoceros triqueter was significantly suppressed in trial water from the titanium dioxide dump site in the North Sea: only about 33–34% of larvae developed normally in the polluted water (Klöckner et al. 1985). However, larval development of Galeolaria caespitosa was not greatly affected by exposure to the polluted water from Port Kembla Harbour, Australia (Moran & Grant 1993).

Light Although light does not affect larval development itself, it may serve as a cue for timing of larval release. The only observation of this type is given by Knight-Jones (1953), who observed that Spirorbis spirorbis released larvae in the early morning. Larval release could be induced by exposure to light following a period of darkness.

Larval ecology and behaviour

Larval swimming

Swimming behaviour Swimming behaviour of larvae has been described for Spirobranchus spinosus, S. polycerus (Lacalli 1984) and S. corniculatus (Smith 1985). The larvae are propelled by the strong and continuous beat of the prototroch cilia and normally swim in a clockwise spiral with the apical tuft directed forward. As they swim, the trochophore also rotate on their axis, their 33

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axis of rotation precessing with a period matching that of the rotation. They swim in tight spirals when the angle of precession is small and tumble in broad arcs when it is large. At younger stages (e.g. the 24-h stage in S. polycerus) contact with obstacles results in immediate rebound without change to the prototrochal beat. In older trochophores (48 h and older in S. polycerus), collisions are followed by a brief pause accompanied by an apparent alteration to the ciliary beat but only rarely do the cilia stop altogether. The metatrochophore exhibits somewhat more effective and frequent arrests, and its swimming is more erratic as a consequence. The metatroch beats with variable speed, exhibiting periodic and sudden arrests. After an arrest, its cilia usually resume beating after a few seconds but longer periods of quiescence were observed. Metatrochal arrests were not correlated with any of the other ciliary or muscular activities of the oral apparatus. Cilia of the food groove and neurotroch beat continuously and at a constant speed. Food groove cilia beat towards the mouth and neurotroch cilia away from it (Lacalli 1984). The body of swimming competent spirorbid larvae (Knight-Jones 1951: Spirorbis spirorbis) rotates clockwise on its axis. Sveshnikov (1978) reported that larvae of Circeis cf. armoricana swim in a straight line, not in spirals, like serpulid larvae. Höglund (1951) observed that spirorbid larvae typically swam forward in a long winding course, all the time turning on their longitudinal axis. Sometimes larvae even turn somersaults with the abdomen bent towards the ventral side. After turning several times in this way larvae then proceed on their winding course. It should be noted that planktonic spirorbid larvae correspond to the pre-settlement stage of serpulid larvae, therefore, serpulid and spirorbid swimming should be compared with caution. Swimming mechanism Marsden & Hassessian (1986) found that swimming cilia of Spirobranchus giganteus arrest on exposure to EDTA, Ba(OH)2, lanthanum chloride, trifluoperazine and Ca2+-free sea water, i.e. under conditions that interfere with the supply of external Ca2+. They concluded that there is a Ca2+-dependent, catecholaminergic excitation of the swimming cilia of the S. giganteus larva, involving ␤ receptors and probably neurally mediated. This conclusion agrees well with the description of basal neurite-like processes in the prototroch and neurotroch that serve as a nervous system of Galeolaria caespitosa larvae (Marsden 1982). Other cilia on the larval body are insensitive to agents affecting the activity of swimming cilia. Swimming velocity Swimming speeds in serpulids increase with increasing size of trochophores. A 1-day-old trochophore of Spirobranchus giganteus can attain the speed of at least 1.7 m h-1. By its second day the trochophore has doubled its speed to 3.4 m h-1. A 5-day metatrochophore swims at about 5 m h-1and some late metatrochophores can achieve speeds in excess of 7 m h1 (Smith 1985). Marsden (1984) reports that 1–4-day larvae of S. polycerus had horizontal swimming speeds of 0.4–3.5 mm s-1 (1.44–12.6 m h-1). Competent larvae of Spirorbis spirorbis show comparable swimming speeds of about 3 mm s-1 (10.8 m h-1, Knight-Jones 1951). The typical swimming speeds seem to be sufficient to enable serpulid larvae to control their vertical position in the coastal water column whereas horizontally, the larvae of most serpulids are distributed by sea currents. Even a short planktonic stage of about 10 min may result in dispersal up to 270 m in larvae of Circeis cf. armoricanus (Dirnberger 1993). 34

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Factors affecting larval swimming Hydrostatic pressure Marsden (1994a) documented the effect of changes in hydrostatic pressure on the vertical swimming of larvae of Spirobranchus polycerus and demonstrated a cyclical change in geotactic response mediated by changes in hydrostatic pressure. Oneday larvae usually swim up or down more frequently than horizontally. They respond to an increase in hydrostatic pressure with an increase in the percentage of larvae moving downward and to a decrease in pressure with an increase in the percentage moving upward. S. polycerus larvae move downward not by sinking passively but by swimming actively. Temperature Bolton & Havenhand (1997) investigated the relative physiological and viscosity-induced effects of water temperature at 25°C and 15°C on the swimming and sinking velocity of larvae of Galeolaria caespitosa. Both physiological and viscosity components of water temperature influenced the swimming velocity of the larvae but the influence of water viscosity did not change significantly over the course of larval development. The sinking velocity of G. caespitosa larvae was proportionally reduced with a temperature-induced increase in water viscosity. The metabolic costs of swimming required to counteract this sinking were similar at 25°C and 15°C but the metabolic costs of swimming a given distance were slightly higher at 15°C (Bolton & Havenhand 1997).

Photoresponse

Variability of photoresponses Serpulid larvae show a wide range of interspecific variations of light responses that can change during the course of development. Trochophores of Serpula columbiana (Young & Chia 1982), Hydroides ezoensis and Pomatoleios kraussi (Miura & Kajihara 1984) show a strong positive photoresponse, whereas later metatrochophores become photonegative. Spirobranchus corniculatus and S. giganteus display only positive photoresponses (Marsden 1984, 1986, Smith 1985). The non-ocellate trochophores of S. corniculatus swim randomly until they develop the first ocellus (Smith 1985) and after that become positively phototactic for the rest of the planktonic stage. A positive photoresponse was reported for the demersal larvae of Galeolaria caespitosa but responses at other stages of this species were not described except for a tendency for settling larvae to congregate on light coloured surfaces (Marsden & Andersen 1981). Pomatoceros lamarckii (Segrove 1941), Hydroides dianthus (Zeleny 1905), and H. elegans (Wisely 1958) are reported to settle in the most illuminated regions of the culturing containers. Crisp (1977) found no consistent photoresponse for swimming larvae of Pomatoleios kraussi. Settling larvae of Pomatoceros triqueter were found to be negatively phototactic (Klöckner 1976). Planktotrophic larvae of Spirobranchus polycerus were photonegative or photoneutral at the age of 16 h to 22 h and photopositive or photoneutral at 72 h to 350 h. During the 22- to 72-h interval, larvae may be photonegative, photoneutral or photopositive. Some spirorbid larvae are able to change their photoresponse during their short planktonic life, which probably may explain some confusion existing in the literature. Newly released Spirorbis spirorbis larvae are photopositive, then become alternatively photopositive and photonegative, until finally entering the completely photonegative stage (Knight-Jones 1953, 35

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Williams 1964). However, according to Doyle (1974), larvae of this species are photonegative from the beginning of their planktonic life, whereas de Silva (1962) claimed that they are photopositive when settling. Larvae of Circeis cf. armoricana are photopositive upon release but turn photonegative within minutes (Dirnberger 1993). Larvae of Spirorbis rupestris and S. tridentatus are photonegative from release (de Silva 1962, Gee & Knight-Jones 1962), whereas larvae of Neodexiospira alveolata are photopositive (Okuda 1946). Correlates of photorespouse Photoresponse is reported to be structurally correlated with the pigment cup orientation of larval ocelli. For example, in Spirobranchus polycerus (Lacalli 1984) and Serpula columbiana (Marsden 1984) the eyecup is directed anteriorly, whereas in Spirobranchus giganteus the direction is posterodorsal (Marsden 1984). The receptor cell of larval ocelli in photonegative S. polycerus larvae is shaded from below (Lacalli 1988). In S. giganteus direct movement towards a light source takes place when the microvilli of the eyespot are largely shaded by the pigmented cup (Marsden 1984, Marsden & Hsieh 1987). Level of irradiance and duration of exposure influence the strength of the photopositive response. Larvae of S. polycerus were indifferent to wavelengths longer than 590 nm (Marsden 1990). Spirobranchus trochophores respond positively to white light at levels of illumination from 1 to 2168×1014 quanta cm-2 s-1 and this response is increased by dark adaptation (Marsden 1986). The photoresponse also depends on the origin of the population. Doyle (1974) showed that larvae of Spirorbis spirorbis from specimens taken from a tidal pool were more photonegative than those obtained outside the pool. Larval feeding Distribution of larval feeding in the group Feeding pelagic larvae are common in serpulid species such as Crucigera zygophora, Ficopomatus enigmaticus, F. miamiensis, Galeolaria caespitosa, Hydroides dianthus, H. elegans, H. ezoensis, H. norvegicus, Pomatoceros triqueter, Pomatoleios kraussi, Serpula columbiana, Spirobranchus giganteus, S. polycerus. Larvae commence feeding from within 10–14 h after fertilisation in H. elegans (Finley 1971) to 48 h in Protula palliata (Kupriyanova unpubl.). The difference probably correlates with egg size. Non-feeding planktonic larvae have only been reported for Protula spp. (Tampi 1960, Pernet pers. comm.). According to Salensky (1882) and LoBianco (1888) larvae of P. tubularia develop (apparently without feeding) in a gelatinous mass outside the tube mouth (see also p. 43). Most small bodied species of serpulids (Chitinopoma serrula, Filograna salmacina spp., Microprotula ovicellata, Paraprotis dendrova, Rhodopsis pusilla) and all the Spirorbidae have non-feeding lecithotrophic development concurrent with some form of brooding.

Larval feeding mechanism Suspension feeding by serpulid larvae is achieved by use of the opposed band system of the trochophore (Strathmann et al. 1972). The long cilia of the preoral band (prototroch) generate 36

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the major current used in feeding and locomotion, whereas the postoral band (metatroch) is used in feeding and rejection and the food groove in transport of particles. Both preoral and postoral bands are essential for clearance. The opposed beat of cilia of the preoral and postoral bands results in increased movement of the preoral cilia relative to the water in the latter half of their effective stroke. Most of the clearance of particles from water occurs at this point. Trochophores are able to continue swimming without feeding. If the metatroch and cilia of the food groove stop beating, particles are not collected behind the prototroch but are carried posteriorly with water (Strathmann et al. 1972).

Feeding rates The feeding rates of serpulid trochophores have not been studied in much detail. Bolton & Havenhand (1998) fed 3- and 10-µm diameter polymer spheres to 1-day-old larvae of Galeolaria caespitosa. The overall rate of ingestion per 20 min varied from 4 to 20 for 3µm spheres and from 2 to 11 for 10-µm spheres. Reduction by 10°C in the water temperature resulted in a 60% decline in the number of microspheres ingested.

Preferred type of food Normally unicellular planktonic algae serve as food for both serpulid larvae and adults. There are no special field or laboratory studies documenting either the composition of the natural diet or examining the preferential selection of algal species by trochophores. Larval serpulid cultures have been successfully raised on naked flagellages Isochrysis galbana (Crisp 1977, Marsden 1987, Connaugton et al. 1994, Qiu & Qian 1997), diatoms Chaetoceros sp. (Connaugton et al. 1994), flagellates Dunaliella salina (Lacalli 1984), D. primolecta and D. tertiolecta (Marsden & Anderson 1981), Nannochloris atomus (Andrews & Anderson 1962), Tetraselmis suecica (Crisp 1977) or a mixture of flagellates Dunaliella tertiolecta and Isochrysis galbana and diatoms Thalassiosira pseudonana (Scheltema et al. 1981).

Bacterivory Some invertebrate larvae can meet part of their metabolic needs through bacterivory (e.g. Rivkin et al. 1986 for asteroids). In laboratory experiments, Hydroides elegans larvae from Hong Kong were able to survive, grow, develop to competence and metamorphose into healthy early juveniles solely on a diet of bacteria. Recruitment of H. elegans occurs throughout the year, suggesting that spawning and successful larval development may be independent of phytoplankton availability, and that larvae largely rely on alternate food sources such as bacteria (Gosselin & Qian 1997a). Larvae of Ficopomatus miamiensis, unlike typical serpulid trochophores normally feeding on phytoplankton, lack a metatroch, which is attributed to their ability to use a bacterial surface film as a food source (Lacalli 1976).

Larval defences Defence mechanisms of larvae can be classified as morphological, behavioural or chemical (Young & Chia 1987). Some polychaete larvae have chaetae that can be erected to a larger 37

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or lesser degree and might serve as a potential mechanical defence against predation. Pennington & Chia (1984) suggested that larval chaetae increase the effective size of the larvae, reduce the chances that predators will contact the larval tissues, and possibly pierce the predator. However, trochophores of the sabellariid Neosabellaria cementarium, whose larvae have large chaetae with many teeth, are not preyed upon by the “suction feeding” ascidian Styela gibbsii any less than trochophores of Serpula columbiana, a species with no apparent structural defences (Cowden et al. 1984, Young & Chia 1987). While nothing is known about the potential behavioural mechanisms of serpulid larvae, chemical defence has been shown for trochophores of Hydroides dianthus that release a water-soluble compound that inhibits feeding in weakfish (Cynoscion regalis) larvae (Connaughton et al. 1994).

Parental care of eggs and young

Spirorbid brooding methods All spirorbids incubate their embryos (Fig. 8). Two major types of incubation are in the opercular brood-chamber or in their tube. However, tube incubation methods vary markedly according to the methods of embryo anchorage within the tube (Knight-Jones et al. 1972, Knight-Jones & Fordy 1978, Rzhavsky 1991, Knight-Jones & Knight-Jones 1994).

Figure 8 (opposite) Brooding methods in Spirorbidae. Tube incubation, A: Paralaeospira levinseni, Paralaeospirinae. Embryo string is free in the tube (after Knight-Jones & Walker 1972 with permission of British Antarctic Society); B: Spirorbis spirorbis, Spirorbinae. Egg string is attached to the tube by a posterior filament (after Knight-Jones et al. 1972 with permission of Springer-Verlag); C: Paradexiospira (Spirorbides) vitrea, Circeinae. Embryos adhere to each other and directly to the tube wall (after Knight-Jones et al. 1972); D: Romanchella scoresbyi, Romanchellinae. Embryo sac attached anteriorly to thoracic funnel-like stalk (after Knight-Jones et al. 1972); E: Metalaeospira tennis, Romanchellinae. Embryo sac attached anteriorly to epithelial oviducal funnel, fully developed eggstring attached to the thorax; F: Metalaeospira tenuis, Romanchellinae. Embryo sac attached anteriorly to epithelial oviducal funnel, forming smaller egg-string attached to the abdominal faecal groove (after Knight-Jones 1973 with permission). Opercular incubation, Pileolariinae. Embryo brooded inside the brood chamber formed by invagination of an opercular ampula; G: Nidificaria palliata, brood chamber resembles an open cup (after Knight-Jones & Knight-Jones 1991 with permission); H: Pileolaria spinifer, brood chamber is a completely closed ampula, the primary opercular plate is shed (after Knight-Jones 1978 with permission of Academic Press); I: Bushiella (Jugaria) kofiadii, brood chamber is a completely closed ampula fused with primary opercular plate (after Rzhavsky 1988 with permission); Januinae—cuticular brood chambers are formed distally by the calcified opercular plate outside the opercular ampula; J: Neodexiospira brasiliensis, specimen in a process of separation of the primary brood chamber (distal, empty) with talon from the secondary brood chamber without talon (proximal, with embryos); K: primary mature brood chamber with a talon (after Knight-Jones et al. 1979); L: secondary brood chamber without a talon (after Knight-Jones et al. 1975 with permission of Academic Press). Scale, A: 0.25 mm, B-J: 0.5 mm, K and L: 0.2 mm.

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Tube brooding In the Paralaeospirinae (genus Paralaeospira) embryos are not attached to the body or the tube (Fig. 8A). In the Spirorbinae (genus Spirorbis) embryos form an egg string attached to the tube by a posterior filament (Fig. 8B). Embryos adhere to each other and directly to the tube wall in the Circeinae (Circeis and Paradexiospira, Fig. 8C). They are attached anteriorly to a specialised thoracic funnel-like stalk or epithelial oviducal funnel in the Romanchellinae (Protolaeospira, Helicosiphon, Romanchella, Metalaeospira and Eulaeospira, Fig. 8D-F).

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The last brooding method has also been reported as “embryos directly attached to the body” (e.g. Knight-Jones et al. 1972).

Opercular brooding Opercular incubation is found in more than a half of approximately 140 known species of the Spirorbidae. About one-fifth of opercular brooders belong to the Januinae and the remainder to the Pileolariinae (Bailey 1969, Knight-Jones & Fordy 1978, Knight-Jones & Thorp 1984, Rzhavsky 1991). How embryos enter the brood chamber has never been observed and this problem has caused numerous discussions (Vuillemin 1965, Potswald 1968, 1977, Bailey 1969, Thorp 1975, Thorp & Segrove 1975, Knight-Jones & Thorp 1984). The brood chambers of the Pileolariinae (genera Amplicaria, Pileolaria, Nidificaria, Vinearia, Simplaria, Protoleodora and Bushiella) are very different but all of them are formed by invagination of the opercular ampulla (Thorp 1975, Thorp & Segrove 1975, Knight-Jones & Thorp 1984). The chamber may look like an open cup (e.g. Vinearia and Nidificaria, Fig. 8G) or a completely closed ampulla (e.g. Pileolaria or Bushiella) with an opercular pore that is used for the entry of embryos (eggs?) and the exit of larvae (Potswald 1968, 1977, Thorp 1975). Such a brood chamber may be used for a number of broods. The primary calcified non-brooding operculum is usually shed after the brood chamber is formed (e.g. Pileolaria, Fig. 8H). Alternatively, it may be fused to the brooding chamber and serve as additional protection for the embryos (Bushiella, Fig. 8I). Formation of the brooding operculum is initiated as animals approach maturity. When breeding activity ceases, the brooding organ may again be replaced by a non-brooding operculum, which may also be replaced later by a new brood chamber (Thorp 1989, Rzhavsky & Knight-Jones 2000). Brood chambers in the Januinae (genera Neodexiospira, Janua, Pillaiospira, Leodora) are formed distally by the calcified opercular plate outside of the opercular ampula (Fig. 8J-L). The distal part of the first brooding chamber is the distal plate of the primary non-brooding operculum. In the next generations of brood chambers, the distal part of a new brood chamber is the basal part of the previous brood chamber. Every brood chamber is used for only one brood and it has to be shed to liberate larvae (KnightJones & Thorp 1984). How embryos enter the brood chamber is still unclear, because the Januinae with mature brood chambers do not have any pores similar to those of the Pileolariinae. Numerous perforations in brood chambers are too small for the embryos and apparently serve to facilitate embryonic respiration (Knight-Jones & Thorp 1984). Vuillemin (1965) observed in Neodexiospira pseudocorrugata what she calls an egg canal within the opercular stalk and suggested that eggs (embryos?) reach the brood chamber via the stalk route. Thorp & Segrove (1975) initially reported that at some stage of the opercular moult Janua pagenstecheri develops an apparently temporary pore through which the eggs enter the brood chamber. Later Knight-Jones & Thorp (1984) proposed that the embryos enter through a split between the base and the lateral wall of the brood chamber that closes to retain the embryos in the chamber. They also considered as a plausible possibility Vuillemin’s suggestion that embryos enter the chamber through the opercular stalk, although such a route implies fertilisation inside the body cavity in the Januinae, which seems to be quite unlikely in our opinion. 40

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Serpulid brooding methods Although brooding was previously considered an exception among serpulids, several new brooding taxa have been recently reported for serpulids and it has become obvious that the variety of brooding methods even exceeds that of spirorbids. Tube brooding Tube incubation, probably, the simplest and most primitive type of incubation is well known for species of Filograna/Salmacina complex (Fig. 9A). These animals brood embryos on the compressed abdomen (Faulkner 1929, Nishi & Nishihira 1993, Nishi et al. 1996). According to ten Hove (unpubl. obs.), Semivermilia aff. uchidai from the Seychelles produced eggs and at least two swimming trochophores when its tube broke open. Uchida (1978) mentions that Paraprotula apomatoides spawns inside the tube and that hatched larvae are spherical trochophores approximately 90 µm in diameter but he does not say how long the larvae stay inside the tube or whether when released they are early trochophores or competent three-chaetiger larvae. Brooding in tube ovicells This type of brooding is more common in serpulids but the number of embryos incubated, the shape and the position of these ovicells vary among species. Chitinopoma serrula, C. arndti and C. rzhavskii produce pouches with twin chambers at the orifice of the tube, each containing 10–20 larvae (Fig. 9B) (Dons 1933, Thorson 1946, Zibrowius 1969, 1983, Rzhavsky unpubl.). Ovicells of Microprotula ovicellata start as tube peristomes and then narrow down to a diameter barely wider than that of the usual tube. Thus, the ovicells resemble swellings encircling the distal part of the tube (Uchida 1978) (Fig. 9C). After the worm completes building the upper narrow part of the ovicell, it spawns about 10–15 eggs and covers the space between the upper margin of the ovicell and the inner tube with the collar. The tube stops growing during incubation. After the larvae are released, the worm continues growing the inner tube up over the distal margin of the ovicell. Brooding in ovicells by Rhodopsis pusilla was originally proposed by Ben-Eliahu & ten Hove (1989) and then later described by Nishi & Yamasu (1992a) (Fig. 9D). The ovicells in this species do not encircle the tube but rather resemble wide inverted pouches arranged one by one along the length of the tube. Each ovicell contains a single egg. At least 3 out of 17 specimens of Filogranula sp. from the Seychelles showed 1–3 ovicells near the tube mouth. These are balloon-shaped, slightly oval, and associated with one of the keels of the tube. Pseudovermilia cf. occidentalis from Bonaire broods larvae in a scalloped tube peristome; one of the spoon-shaped leaflets in a three-leafed orifice was filled with developing embryos. Another specimen with large spoon-shaped leaflets near the orifice was found on Curaçao (Fig. 9E). P. conchata has been named after these cupped leaflets (ten Hove 1975: plate VIIIe) and similar structures are found on tubes of Pseudochitinopoma occidentalis (ten Hove unpubl.), although it is unclear if they are also used for brooding. Such scooped tube parts might indicate retention of early embryos for a short time. A tube of Pseudovermilia cf. pacifica from the Seychelles shows a beautiful cup- to dome-shaped ovicell over the entrance of the tube, deeper than that figured for Pseudovermilia cf. occidentalis (ten Hove unpubl.). 41

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Brooding inside the branchial crown Paraprotis dendrova embryos are brooded inside the branchial crown on a long and slightly spiral appendage with branches growing from the mouth parts (Nishi 1992a, 1993, Nishi & Yamasu 1992c) (Fig 9F). Metavermilia cf. ovata from the Seychelles has developing embryos inside the base of its branchiae (ten Hove unpubl.) (Fig. 9G). Brooding in pockets of the thoracic membranes Such incubation of eggs is only known for Floriprotis sabiuraensis (Uchida 1978, BaileyBrock 1985). A pair of pockets, one on each side of the inner surface of the thoracic membrane, is located between the second and the third thoracic segments. The pockets are rectangular with the opening directed forward. Brooding in gelatinous masses It is strange that the explicit record of Protula tubularia brooding eggs until the threechaetiger stage in a gelatinous mass near the tube mouth (Salensky 1882, LoBianco 1888, 1909)—a common method in sabellids and other tubicolous or burrowing polychaetes (Strathmann 1987)—is not mentioned in the subsequent extensive literature on this common species. However, this type of brooding in Protula has recently also been observed independently by R.Sanfilippo (material from the BIOICE project on benthic fauna around Iceland, deposited at the Marine Invertebrate Icelandic Institute and Museum of Natural History of Reykjavik) and D.Martin (pers. comm.) (Fig. 9H). Erroneous records of serpulid brooding The presumed brooding by Serpula vasifera, as mentioned by Schroeder & Hermans (1975), is an erroneous quote from Augener (1914). He stated that he, contrary to Haswell (1884, 1885), had not been able to find embryos of a commensal or parasitic isopod in the tube of S. vasifera. The record of opercular brooding in Ficopomatus enigmaticus by McIntosh (1924) was demonstrated to be erroneous by McIntosh (1926). The single, but very explicit record by Fischer-Piette (1937) of F. enigmaticus brooding its larvae in the tube is uncorroborated in the subsequent very extensive literature on this species (over 300 records) and refuted by

Figure 9 (opposite) Brooding methods in serpulids. Brooding inside the tube, A: Salmacina dysteri, two larvae in the tube near the parental abdomen. Histological section, la—larvae, ab—abdomen, t—tube (after Nishi & Yamasu 1992d with permission of Shokabu Publishing). Brooding in ovicells outside the tube, B: Chitinopoma serrula, paired ovicells at the tube orifice (after Dons 1930); C: Microprotula ovicellata, ovicells encircling the distal part of the tube (after Uchida 1978); D: Rhodopsis pusilla, single ovicells located along the tube, SEM photographs (after Nishi & Yamasu 1992a); E: Pseudovermilia occidentalis, spoon-shaped leaflets (ten Hove unpubl.). Brooding inside the branchial crown, F: Paraprotis dendrova, eggs and embryos on spiral branchial rudiment, SEM photographs (after Nishi & Yamasu 1992b); G: Metavermilia cf. ovata, embryos inside the base of branchia (ten Hove unpubl.). Brooding in gelatinous masses outside the tube, H: Protula tubularia (Sanfilippo unpubl.). Scale, A: no scale was given in the original publication; B and C: 1 mm; D and E: 0.5 mm; F: 0.2 mm; H: 5 mm; G: 1 mm.

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Dixon (1977). Hoagland & Robertson (1988) give Gravier (1923, cited by Thorson 1936) as the primary source for the observation of ovovipiparity (a form of brooding) in Pomatoceros triqueter. However, Gravier refers to Saint-Joseph (1894:359) who claims to have found embryos without any organisation except an eyespot in the abdomen of the female. This observation has not been confirmed in the very extensive literature (over 500 records) on P. triqueter.

Length of metamorphic competence stage and delaying of metamorphosis The three-chaetiger stage in serpulimorph polychaetes marks the onset of metamorphic competence in larvae. In planktonic serpulid larvae the competence coincides with the transition to the demersal stage and with changes in larval behaviour, while in brooded larvae it is marked by the release from the brooding structure and the beginning of a short pelagic swimming stage. The easy repeatability of serpulid larval development up to a three-chaetiger (competent) stage in laboratory cultures indicates that the developmental events up to this stage are predetermined genetically (Marsden & Anderson 1981). However, after the onset of competency, larvae require a cue (or cues) to proceed with further development. If such cues are temporarily unavailable, the competence period can be significantly protracted and metamorphosis delayed. For example, competent larvae of Hydroides elegans will remain swimming in clean water for several weeks if they do not receive an appropriate cue (Bryan et al. 1997, Qian & Pechenik 1998). Exposure to metamorphic cues curtails the competency period, thus resulting in a shorter overall developmental period: larvae of this species can complete development in 5 days. Settlement and metamorphosis of lecithotrophic spirorbids are similarly affected by the absence of appropriate cues. Under laboratory conditions, larvae of Spirorbis spirorbis normally settle after 15 min to 3 h of swimming if suitable substrata are present. Later they become less discriminating in their choice of the substratum. After swimming for about 8 h many larvae fail to settle (Knight-Jones 1951, 1953). Given that the pelagic stage in spirorbids roughly corresponds to the competence stage, one should expect that the swimming periods would be shortened by availability of suitable settlement cues. Interestingly, the length of the pelagic stage is reported to depend both on the availability of suitable substrata and the degree of permanence of these substrata (Gee 1963a): lack of suitable substrata prolonged the pelagic stage and their presence reduced the pelagic life to differing degrees in four spirorbid species. S. rupestris, which inhabits permanent and widely distributed substrata such as bedrock encrusted by Lithothamnion, lacks the pelagic stage, whereas Spirorbis borealis, which occupies Fucus serratus, a comparatively ephemeral and discontinuous substratum, has a pelagic stage. A pelagic stage may also be eliminated in Spirorbis inornatus from populations found on the turf alga Chondrus (Al-Ogily 1985).

Settlement and metamorphosis Settlement and metamorphosis are terms that are often used interchangeably and clarification is necessary. For the purpose of the current review, settlement is defined as the ecological 44

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transition from a pelagic swimming to an obligate sessile life style. Metamorphosis is a set of morphogenetic events accompanying this transition and making it possible. The metamorphosis in serpulimorph polychaetes begins with the disappearance of the prototroch and is further characterised by differentiation of the branchial crown in the head region the collar and thoracic membrane in the thoracic region, and the pygidium at the tip of the abdomen. Successful attachment and construction of the calcareous tube marks the completion of normal metamorphosis. In planktonic serpulid larvae, the onset of metamorphosis generally coincides with the shift into demersal life but it is not completed until after settlement. Some initial events of metamorphosis, such as collapse of prototroch, development of branchial buds, pygidial appendages and thoracic membrane rudiments, can be observed even in the absence of settlement (Galeolaria caespitosa: Marsden & Andersen 1981). Other events of metamorphosis, especially tube formation, depend on successful settlement, which itself depends on a number of cues. Lack of such cues may result in failure to complete normal metamorphosis. Bryan et al. (1997) observed several types of abnormal metamorphosis in Hydroides elegans: (a) attached, production of branchia but no tube, (b) not attached, production of branchia but no tube, and (c) deformed development involving elongation of larvae and crawling behaviour but no tube or branchia production. Carpizo-Ituarte & Hadfield (1998) reported that some metamorphosed H. elegans larvae (i.e. with branchia buds) were unable to secrete primary and secondary tubes but survived up to 2 months in cultures when fed single-celled algae. In the absence of any substrata in clean Petri dishes lacking a microbial film, spirorbid larvae start metamorphosis, settle and build tubes underneath the water surface film but die very soon after (Britayev pers. comm.). In subsequent sections of the review only the events of normal settlement and metamorphosis will be considered.

Settlement behaviour

Settlement behaviour of planktotrophic larvae Settlement behaviour has been described for planktotrophic larvae of H. dianthus (Zeleny 1905), H. elegans (Wisely 1958, Ghobashy & Selim 1979a), Ficopomatus enigmaticus (Straughan 1968), Pomatoceros triqueter (Segrove 1941), Pomatoleios kraussi (Crisp 1977) and Spirobranchus corniculatus (Smith 1984a). As metamorphosis starts, the behaviour of planktotrophic serpulid larvae changes from pelagic swimming to a slow exploration of the bottom of the dish. From time to time, metamorphosing larvae of Pomatoleios stop their forward crawling and quiver on the spot. Larvae which had been quivering in the same position for many minutes sometime attach to the substratum by mucous threads but this attachment may be temporary (Crisp 1977). The searching demersal larvae of Spirobranchus swim over the bottom with the abdomen usually in close contact with the surface. They pause and flex the abdomen from side to side across the substratum. Settlement behaviour is more variable in Hydroides elegans (Wisely 1958). Larvae begin to secrete an adhesive substance that trails from the posterior end of their bodies before they reach the fully developed metatrochophore stage. Larvae were seen towing small pieces of bacterial film, detritus, or even smaller larvae through the cultures, often some distance behind them. Apparently, larval feeding is not adversely affected by this temporary attachment 45

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relatively early in development. No evidence of pre-settling searching was observed in this species and the larvae apparently settled at random (Wisely 1958). However, Hadfield et al. (1994) observed that pre-settlement larvae of H. elegans spent much time swimming across submerged surfaces, repeatedly contacting these surfaces with their apical tufts. After the demersal stage, the larvae settle by secreting an abdominal posterior mucous bag. Juveniles originally secrete a mucous tube, covering it later with calcareous matter secreted by the ventral collar surface. During this stage the juvenile Spirobranchus partially emerges from its tube and partially rotates within it. The rotation allows the ventral secretory area to produce a complete tube (Smith 1985). The further process of tube-formation in Pomatoceros triqueter has been described by Hedley (1958).

Settlement behaviour of lecithotrophic larvae In spirorbids, settlement behaviour has been described for Spirorbis spirorbis by KnightJones (1951, 1953), Wisely (1960), Williams (1964), and Nott (1973) and for S. corallinae by de Silva & Knight-Jones (1962). Spirorbid larvae are competent to settle when they are liberated from the brood chamber and the length of the pelagic swimming stage may last up to several hours (Knight-Jones 1951). After the short pelagic stage, S. spirorbis larvae enter a searching stage when swimming alternates with slow (about 1 mm s-1) crawling on the ventral side (Knight-Jones 1951). Wisely (1960) rarely observed the alternating swimming-crawling behaviour in S. spirorbis; the movements of settling larvae mostly consisted of crawling. Most larvae of S. spirorbis arrive at the substratum in a head-on collision but remain attached for <1 s. During this initial attachment, properties of the substratum determine whether larvae will investigate the surface further or resume swimming in search of another substratum. The exploring larvae move on the substratum and, if dislodged by a jet of water, remain attached at some distance by a thread, originating from the terminal segment (Nott 1973). When the larva has selected a settlement site, it remains stationary on the substratum (Nott 1973) or frequently changes the direction of crawling (Knight-Jones 1951, Wisely 1960). In Simplaria potswaldi the contents of the primary shell gland are extruded via the anus in an explosive fashion and the calcareous secretion is moulded by the movements of the larva into a tube capable of housing the entire settled larvae in <5 min (Potswald 1978). In Spirorbis spirorbis the initial tube is transparent. The larva rolls from side to side and vigorously moves the extended chaetae so that the secretion is spread to form a transparent covering over the posterior half of the body. Within a minute of the release of secretion from the attachment gland, the animal rolls 180°, together with the mucoid covering, to assume the adult position—i.e. the ventral surface facing upwards and the dorsal one facing the substratum (Nott 1973). Simplaria potswaldi does not rotate a full 180° until about 2 h after discharge of the primary shell gland (Potswald 1978). After initial attachment of the Spirorbis spirorbis larvae, the secretion from the ventral collar gland is released onto the uppermost ventral surface and moved posteriorly by the neurotroch action forming a primary mucoid tube. The secretion of the ventral gland does not persist beyond this stage. The collar unfolds revealing the dorsal collar gland, which remains active after metamorphosis and cements the tube to the substratum. Within an hour of settlement calcification starts and 4 h after settlement a calcareous tube encloses the whole animal (Nott 1973). 46

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The initial tube of Neodexiospira alveolata is transparent and soft and it covers only the thoracic region of settled larva. A pair of shell glands is now used to form a tube. A day later the tube hardens and elongates covering the juvenile completely (Okuda 1946)

Morphological changes at metamorphosis

Metamorphosis in planktotrophic larvae The morphological stages of metamorphosis in planktotrophic larvae have been described for Hydroides elegans (Wisely 1958, Sentz-Braconnot 1964), Spirobranchus corniculatus (Smith 1985), Pomatoceros triqueter (Segrove 1941) (Fig. 10A-F) and Galeolaria caespitosa (Grant 1981, Marsden & Anderson 1981). The onset of metamorphosis is preceded by increased contraction of the circular muscles, especially the anterior band, which contracts just below the eyes to constrict a definite head region. The contraction of the prototroch circular muscle decreases the larval diameter whilst increasing its length. The ventral collar rudiment evaginates, forming a ventral fold and at first two separate dorsoventral folds develop behind the metatroch. Usually ventral and lateral collar folds fuse to form the adult collar. The formation of collar folds is described by Meyer (1888), Segrove (1941), Wisely (1958), Grant (1981) and Marsden & Anderson (1981). The chaetal sacs enlarge and the most anterior pair begins to turn upwards. Uncini appear on the second chaetiger and later on the third. During settlement the head is reduced and the mouth and anus move to occupy their terminal positions. The prototroch, metatroch, and feeding band disappear. The collar folds evaginate completely to form the adult configuration and the anterior pair of chaetae becomes collar chaetae. Stiff ciliary tufts are formed on the branchial rudiments and all subsequently develop pinnules (Smith 1985). The intraepithelial system of nerves supplying the larval pharynx in trochophores of Spirobranchus spinosus is retained through metamorphosis and, with minimal alteration, provides the source of nerves in the juvenile foregut (Lacalli & West 1988). Post-settlement development of the branchial crown and the operculum, as well as the formation of additional thoracic segments have been described in Ficopomatus enigmaticus (Vuillemin 1962a,b), Pomatoceros triqueter (Segrove 1941), Hydroides elegans (Wisely 1958, Sentz-Braconnot 1964) and Pomatoleios kraussi (Crisp 1977).

Metamorphosis in lecithotrophic larvae Post-metamorphic development of the non-feeding larvae of Protula tubularia described by Meyer (1888) and Salmacina dysteri described by (Nishi & Yamasu 1992d) (Fig. 10) do not differ significantly from that of planktotrophic larvae. Morphological events associated with settlement and metamorphosis in spirorbids (Fig. 11) have been described by Agassiz (1866), Fewkes (1885), Abe (1943), Okuda (1946), Höglund (1951), Casanova (1954), Nott (1973) and Nott & Parker (1975). A detailed comparative study of metamorphosis, including internal changes, in spirorbids Simplaria potswaldi, Paradexiospira (S.) vitrea and Circeis cf. armoricana was provided by Potswald (1978). The opercular and branchial rudiments start to develop at a rapid rate only after formation of the initial tube. The cells producing trochal cilia, the trochoblasts, become detached and 47

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Figure 10 Serpulid metamorphosis. Pomatoceros triqueter, A: ventral view of a larva with branchial rudiments; B: dorsal view of a metamorphosed juvenile; C and D: ventral view of a juvenile removed from the tube; E: juvenile in the tube, pinnules form on 4th right filament; F: dorsal view of young worm, pinnules form on second right filament (after Segrove 1941). Salmacina dysteri, G: recently settled worm with branchial rudiments; H: juvenile with thin tube; I: juveniles with branchial crowns; J: juvenile with collar setae and 10 chaetigerous segments (after Nishi & Yamasu 1992d). Scale, A-C: 0.1 mm; D: 0.25 mm; E and F: 2 mm; G, H and J: 0.1 mm; I: 0.15 mm.

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Figure 11 Spirorbid metamorphosis. Spirorbis spirorbis, A: recently settled larva secreting the tube; B: early juvenile (after Fewkes 1885). Neodexiospira alveolata, C: Metamorphosing juvenile in soft transparent tube, the abdomen is naked; D: one day after settlement, the tube covers entire body of the juvenile; E: juvenile completed the metamorphosis (removed from the tube); F: the same, inside the tube. Circeis aff. armoricana; G: recently metamorphosed juvenile in the tube, adhesive processes are extended (after Okuda 1946). Scale, B: 200 µm; A, C-F: no scale was given in the original publication; G: 320 µm.

are completely sloughed off. Simplaria potswaldi larvae do not ingest prototrochal cells (Potswald 1978), as it is thought to be the case in Spirorbis spirorbis (Nott 1973). Apical tuft cilia are lost at the time of settlement but the apical cells are retained and apparently incorporated into the brain. Two hours after formation of the initial tube, the branchial and opercular rudiments in Simplaria potswaldi grow to about twice the length they were in fully formed larva and the opercular rudiment is much larger than any of the simple branchial rudiments. The pigmented eyecups migrate to the midline and remain there for a day or two before they disappear. In the midline, ventral to the rapidly developing branchial crown, shrinking of the head results in the appearance of a “proboscis” or snout-like structure. The post-settlement larval abdomen becomes shorter and broader and therefore is not clearly delimited from the thorax as in the free-swimming larvae. 49

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The initial tube is chalky white and opaque in S. potswaldi but it is transparent in Circeis cf. armoricana and Paradexiospira (Spirorbides) vitrea (Potswald 1978). In species of Januinae these tubes are transparent, soft and cover only the thorax (Abe 1943, Okuda 1946). The part of the tube adjacent to the substratum is secreted by the ventral thoracic glands prior to the turning over of the larva to assume the adult position (with the dorsum towards the substratum). Soon after the collar has folded back to enclose the lip of the primary tube, deposition of the secondary tube begins. Calcium secretions originating from the major subcollar glands, as demonstrated by Swan (1950), Medley (1956a,b), and Nott & Parker (1975), are added to the anterior lip of the tube and moulded into place by the encompassing collar fold. Twenty-four hours after settlement, the anterior end of the tube starts to turn in a direction typical for each species (Potswald 1978). During further development, the yolk of the midgut breaks down and is absorbed, the anus takes the terminal position, the abdominal shell gland becomes the hindgut, the partition between the midgut and hindgut opens, the “proboscis” is cast off and the branchial rudiments develop into the branchial crown. The ventral prostomial glands, the apical tuft, and various trochs are lost during metamorphosis. By the eleventh day of post-larval development the major features of the adult, with the exception of abdominal or secondary segments, are either present or starting to form in Simplaria potswaldi. The gross asymmetry, characteristic of spirorbids, develops as a result of differential growth in the achaetous zone, which corresponds to the larval abdomen. This change from an essentially symmetrical larva to an asymmetrical pre-adult is considered to constitute spirorbid metamorphosis (Potswald 1978). Interesting changes of the posterior body region during the settlement were observed for Circeis cf. armoricana by Okuda (1946). According to his observations, the posterior lateral portions of the body are protruded backwards to form a pair of massive foot-like appendages. Each of them terminates posteriorly in a digit-shaped adhesive process, which is attached to the inner wall of the tube and supports the body. When the body is withdrawn into the tube, these foot-like appendages are contracted to the level of the anal region. Such processes are absent in adults and it is unclear for how long they function in juveniles. Okuda (1946) also reports that juveniles of Neodexiospira alveolata certainly lack these processes.

Factors affecting settlement and metamorphosis There is a vast amount of literature on settlement cues for larvae of sessile fouling invertebrates, including serpulids and spirorbids. Settlement and recruitment are complex processes, determined by the interaction of biotic and abiotic factors. These factors can serve as positive or negative cues, which are physical or chemical in nature and they operate at different temporal and spatial scales and various levels of organisation (i.e. ecologicalphysiological-molecular, see Rodriguez et al. 1993 and Slattery 1997 for reviews). One of the ways to deal with such a complexity of factors is to separate all factors into generic precondition factors and specific settlement cues. The former factors affect a wide range of larvae and act at various stages of development. An optimal combination of such factors ensures that larvae are in condition to respond to specific cues. The settlement cues are species-specific, they act during the settlement periods and affect only the larvae preconditioned to respond to them. 50

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Generic precondition settlement factors Seasonal settlement Settlement in serpulids and spirorbids living in temperate climates is seasonal and generally the length of the settlement period coincides with the length of reproductive period. In tropical species that reproduce throughout the entire year, settlement also takes place throughout the entire year. However, the intensity of settlement may vary significantly within the reproductive period and may show one or more peaks. The intensity of settlement in the field is usually inferred from the intensity of recruitment on various submerged panels. Larvae of Pomatoleios kraussi settle in Kuwait from March to December with the maximum of abundance in August (Mohammad 1975). In many places (Australia and New Zealand, California, Japan, China) peaks of Hydroides elegans settlement occur in summer and autumn but in Hong Kong settlement of this species peaks in early spring to early summer (Qiu & Qian 1997). Ficopomatus enigmaticus shows two distinct settling peaks, March/April and November/December in Argentina (Schwindt & Iribarne 1998), June/ July and September in the North Adriatic (Bianchi & Morri 1996), May and October in Japan (Okamoto & Watanabe 1997). Sentz-Braconnot (1968) mentions a variable settling pattern in Mediterranean Pomatoceros triqueter over a period of 10 yr, mostly between July and October, often in two peaks. However, she may have been working with two species, P. triqueter and P. lamarckii, and thus the observations are not conclusive. The same holds for Alvariño’s (1951) observations on “P. triqueter” from Atlantic Spain, settling in three peaks between May and December. While P. triqueter in northern Helgoland shows a single period of maximal settlement in August/September (Klöckner 1976), Castric-Fey (1983), who distinguished between the two species, mentions settlement all year round but with maxima in April, June, August and October (South Brittany, France). The settling season for seven serpulid taxa in the harbour of Civitavecchia (Mediterranean) is generally 4 months per species (Chimenz Gusso & Rivosecchi Taramelli 1973). Filograna implexa settles throughout the entire year except for May in the northern Adriatic (Igic 1969). General abiotic factors: temperature, salinity, dissolved oxygen, sedimentation During the settlement season, abiotic factors such as ambient temperature, salinity, dissolved oxygen and light intensity that generally have measurable affects on larval development, behaviour, and survival also affect the intensity of settlement. Settlement of Hydroides elegans occurred when the water temperature was above 20°C and more intensive settlement occurred at stations having a greater concentration of dissolved oxygen (Reish 1961). Dew & Wood (1954) present non-conclusive evidence of the settlement periodicity of H. elegans, which may be related to tides, while Daniel (1958) showed that larvae of this species could not settle in water currents exceeding 0.9–1.2 knots. Settlement of Ficopomatus uschakovi (Hill 1967) took place in a range of salinities from 1 to 33 but the most abundant settlement occured in salinity above 30. Hydroides dianthus settled only when the high tide salinity was above 30 and the low tide salinity was 20 or over (Hill 1967). Soldatova & Turpaeva (1960) assumed settlement of Pomatoceros triqueter to be a compromise between photopositive attraction to surface waters and a negative reaction to brackish water, resulting in settling intertidally in normal sea water, at depths of 15–20 m under brackish conditions. Increased sedimentation reduced recruitment of Pseudochitinopoma occidentalis (Duggins et al. 1990) and other serpulimorph polychaetes (Vine & Bailey-Brock 1984). Photoresponse The larval photoresponse at the time of settlement can affect settlement 51

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preferences. A general approach to this phenomenon was given by Thorson (1950). Reduced light intensity negatively affected recruitment of Pseudochitinopoma occidentalis (Duggins et al. 1990). Larvae of Spirorbis tridentatus tend to be photonegative when settling, which apparently reflects the natural occurrence of this species in dimly lit places (de Silva 1962). Substratum Physical properties associated with the abiotic substratum, such as its colour and its roughness may be important for settlement preferences (e.g. Wisely 1959, Sentz-Braconnot 1968, Straughan 1969). Spirorbids recruit in greater numbers to bare, dark grey shale boulders than to bare, light yellow sandstone boulders on the same shore (James & Underwood 1994). Spirorbis rupestris prefer to settle on rough surfaces rather than on smooth ones (Gee & Knight-Jones 1962, Gee 1965), whereas larvae of S. spirorbis clearly avoid roughened surfaces (Crisp & Ryland 1960). Although settling larvae of Pomatoleios kraussi adhere much better on artificial substrata with higher surface tension than on those with low tension, colonisation patterns under natural conditions were not influenced by surface tension (Becker 1993).

Specific settlement factors Larvae of many invertebrates often settle in response to highly specific stimuli. Although some serpulimorphs are notorious opportunistic foulers and are apparently able to colonise any available substratum, many spirorbids and serpulids have very specific habitat requirements. Such substratum-specific settlement usually results from active substratum selection by settling larvae. In the majority of cases the substratum is biogenic and the settlement cues are believed to be chemical in nature. Pawlik (1992) distinguishes three main categories of substratum-specific settlement: associative settlement, settlement on microbial films and gregarious settlement. Associative settlement According to (Crisp 1974), associative settlement is the specific or enhanced settlement of one species on another. The degree of substratum specificity varies significantly within serpulimorph polychaetes. Members of the Spirobranchus giganteus complex are obligate associates of corals and their successful settlement with tube construction occurs only on live corals (Marsden 1987, Hunte et al. 1990, Marsden et al. 1990). Adults of S. corniculatus occur commonly on Acropora prolifera and much less frequently on Porites ramosa (Marsden 1987). The pre-settlement larvae respond positively to water-borne exudates of corals commonly colonised by the worm and are indifferent to exudates of rarely colonised corals (Marsden & Meeuwig 1990). Spirorbids are commonly found in specific epiphytic associations with various macrophytes and their larvae show remarkable discrimination among algal substrata. Settlement of such organisms can be stimulated by algal extracts. Spirorbis rupestris larvae seem reluctant to settle on clean smooth surfaces but settle abundantly if slates are soaked in aqueous extracts of Lithothamnion polymorphum (Gee 1965). Larvae of Spirorbis spirorbis settle in significantly greater numbers on surfaces treated with extracts of Fucus serratus, the typical host alga, than on untreated surfaces (Williams 1964). Photopositive behaviour is curtailed and the duration of the crawling behaviour preceding settlement is shortened as a result of contact with this alga (Williams 1964). Spirorbids not only select particular algal species for settlement but also tend to differentiate between younger and older parts of the alga. Larvae of Spirorbis cf. inornatus and Janua pagenstecheri prefer to settle on younger parts of fronds of Laminaria digitata. 52

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The youngest part is probably a more stable substratum because the growth of Laminaria occurs near the base of the frond and the old tissue is shed distally (Stebbing 1972). Similarly, Neodexiospira brasiliensis and Circeis cf. armoricana that co-occur on Zostera marina, Z. asiatica and Phyllospadix iwatensis were observed to be more abundant on younger leaves of all three seagrass species. They were distributed evenly along entire young leaves of all three species but were restricted to the basal portion of old leaves (Hamamoto et al. 1996). Larvae of Circeis cf. armoricana tended to settle near the base of growing seagrass blades of Thalassia testudinum (Dirnberger 1990, 1993, 1994), apparently searching efficiently for space produced rapidly by the blade growth (Dirnberger 1990). In contrast, Nelson (1979) reports that Neodexiospira brasiliensis tends to be more abundant on older portions of Zostera blades, probably because it requires a diatom mat for settling. These data totally contradict the data of Hamamoto et al. (1996, see above) that Neodexiospira brasilensis prefer settling on younger parts of Zostera. This discrepancy is strange if both authors did study the same spirorbid species. Algae serve as negative or positive settlement cues for serpulid larvae. Settlement of Hydroides elegans larvae was affected by waters conditioned by 12 species of macroalgae. Compounds released by 4 of 12 macroalgae tested immediately killed larvae of H. elegans or inhibited their settlement; the remaining eight algal species prevented settlement, had no effect or even stimulated settlement (Walters et al. 1996). Larval settlement of H. elegans was also inhibited by brown algal phlorotannins (Lau & Qian 1997). Many serpulids and spirorbids form epizoic associations with other invertebrates, mostly molluscs, crustaceans, and some bryozoans and hydrozoans (e.g. Stebbing 1972, Stachowitsch 1980, ten Hove 1994a). For spirorbids such relations can be quite specific. For example, Circeis spirillum is usually found only on hydrozoans and bryozoans (KnightJones & Knight-Jones 1977, Knight-Jones et al. 1979), Protoleodora uschakovi settles only on the shells of molluscs and large crustaceans (Rzhavsky unpubl.). Circeis paguri is associated with the hermit crab Eupagurus bernhardus (Al-Ogily & Knight-Jones 1981) and Bushiella (B.) evoluta is found only on the inner surface of gastropod shells inhabited by hermit crabs. However, it is not known whether active larval habitat selection takes place nor whether extracts from the host species also stimulate settlement in these organisms. Epizoic relations of serpulids with their hosts are apparently less specific than those of spirorbids. The only example of settlement stimulation of serpulid larvae by an invertebrate host is that demonstrated for Hydroides elegans. This species, which inhabits a wide variety of substrata, is also found living on the arboresent bryozoan Bugula neritina in Hong Kong and the samples derived from this bryozoan induce metamorphosis in the laboratory (Bryan et al. 1998). When several hosts are used by a species, preference for specific hosts may vary for different populations within one species and appears to be genetically determined. Larvae of Spirorbis inornatus favoured the algal species to which their parents were attached (KnightJones et al. 1975). Similarly, larvae of S. spirorbis from a tidepool population prefered Ascophyllum, while those from an embayment settled much more readily on Fucus (Mackay & Doyle 1978). Animals collected from an environmental cline ranging from tidepool-like to embayment-like conditions exhibit a corresponding range in behaviour. Bio-organic film The presence of a bio-organic film has been long recognised as a prerequisite for larval settlement in many fouling marine invertebrates (e.g. Scheltema 1974). Microorganisms have been reported to promote settlement of Spirorbis spirorbis (Meadows & 53

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Williams 1963), Hydroides elegans (Hadfield et al. 1994, Harder & Qian 1999), Serpula sp. (Keough & Raimondi 1995) and Neodexiospira brasiliensis (Kirchman et al. 1982a). Bacterial films of different age and composition have different effects on larval settlement. Clean surfaces exposed to sea water go through a succession of changes advancing to the development of a complex microbial community (Mitchell & Kirchman 1984) and it is not surprising, therefore, that recruitment of serpulids and spirorbids is affected by the film age and immersion time (Keough & Raimondi 1995). Larvae of Hydroides elegans distinguish among the films ranging in age from 1 to 3 days. Larval settlement curves closely parallel population growth curves for bacteria, suggesting that settlement is quantitatively dictated by bacterial density (Hadfield et al. 1994). Different film-forming species and strains vary in their ability to promote settlement in serpulid and spirorbid larvae. Spirorbis spirorbis larvae settle more readily on films developed in the presence of diatoms and their associates than on those developed in the presence of a green flagellate (Meadows & Williams 1963). Larvae of Neodexiospira brasiliensis prefer to settle on pure culture films of bacteria isolated from Ulva lobata (Kirchman et al. 1982a). Larvae of Hydroides elegans settle differentially on different species of bacteria (Lau & Qian 1997). Of a series of bacterial strains isolated from marine biofilms, 13 induced larval settlement, 11 gave moderate or mixed results and 10 others did not stimulate the settlement of H. elegans (Unabia & Hadfield 1999). Changes in the ratio of species in multispecies bacterial films also affected larval settlement. The amount of settlement induced by monospecific strains is usually less than that induced with natural, multispecies films (Unabia & Hadfield 1999). Most of the isolated bacteria that induce settlement in H. elegans were motile Gram-negative rods but Grampositive strains were also present. Biofilms killed by treatment with heat, ultraviolet radiation or chemical fixatives were no longer inductive. Soluble, dialysable, heat-stable bacterial products induced settlement and metamorphosis more slowly (Unabia & Hadfield 1999). Gregarious settlement Many serpulid and spirorbid larvae settle in response to the members of their own species to form conspecific aggregations (Spirorbis spirorbis, Janua pagenstecheri: Knight-Jones 1951; Spirorbis tridentatus and S. corallinae: de Silva 962; Galeolaria caespitosa: Andrews & Anderson 1962; Spirorbis corallinae and Janua pagenstecheri: Stebbing 1972, Ryland 1972; Neodexiospira pseudocorrugata: Ghobashy & Selim 1979b; N. brasiliensis: Nelson 1979; Hydroides dianthus: Scheltema et al. 1981, Toonen & Pawlik 1996; Pomatoceros triqueter: Klöckner 1976; Pomatoleios kraussi: Crisp 1977). Such gregarious settlement is thought to rely on chemical cues associated with adults and could not be demonstrated between members of a single cohort of settling larvae of Hydroides dianthus (Mullineaux & Garland 1993). Gregarious response is well pronounced at the pre-settlement period but Marsden (1991) observed preference for adult tubes by planktonic metatrochophores of Spirobranchus polycerus. Still-water laboratory assays demonstrated that the settlement cue was soluble in water and was associated with the body of live adults in Hydroides dianthus and H. elegans (Toonen & Pawlik 1996, Bryan et al. 1997). Live worms removed from their tubes and amputated tentacular crowns of live worms resulted in a greater settlement response than dead worms, empty tubes or slides with biofilms. A single adult was equally capable of eliciting a gregarious response as were five or 25 conspecifics and newly settled juveniles began to elicit gregarious settlement after approximately 96 h (Toonen & Pawlik 1994, 1996). However, Carpizo-Ituarte & Hadfield (1998) contradict Bryan et al. (1997), hypothesising 54

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that the latent response of H. elegans to extracts of adult worms is a result of the build-up of bacteria in their test vessels. Toonen & Pawlik (1994) found that females of H. dianthus produced larvae that settled in two different ways: one type colonised uninhabited substrata (founders), whereas the other settled only in response to cues associated with conspecifics (aggregators). There was a distinct subordination of larvae that responded to a biofilmed substratum; once these individuals were removed, the remaining aggregators delayed settlement in the absence of acceptable conspecific-associated clues. Some authors argue that aggregations may also arise as a result of passive deposition of larvae. Walters et al. (1997) demonstrated that larvae of H. elegans did not settle faster or in greater numbers on surfaces already occupied by adults or their tubes. However, in the field in moving water there was significantly more settlement in tube crevices than expected by chance, which probably results from hydrodynamics. The authors concluded that dense aggregations of H. elegans found on hard surfaces in bays and estuaries probably result from passive deposition of larvae in crevices beside tubes of conspecific individuals, followed by selective attachment in these locations if the bio-organic film is acceptable (Walters et al. 1997).

Chemical nature of inducers

Conspecific inducers A new monoacyl glycerol isolated from the methyl alcohol extract of adults acts as a metamorphosisinducing substance in H. ezoensis larvae. However, since acyl glycerols are common primary metabolites, they have been hypothesised to act as the second messengers, not as a primary cue of metamorphosis (Watanabe et al. 1998). Isolation of larval metamorphic inducers from adults of H. elegans showed that biologically active fractions were composed of free amino acids. The entire free amino acid composition was found to comprise aspartic acid, glutamic acid, serine, histidine, glycine, arginine, alanine, asparagine, glutamine and taurine. The larval metamorphic response to an artificially prepared sample in identical concentrations of these amino acids was very similar to the response to the natural isolates (Harder & Qian 1999). Beckmann et al. (1999) tested whether the metamorphic response was caused by direct dissolved free amino acids (DFAA) perception or by induction of DFAA-utilising bacteria. The results of the experiment suggested that the larval response had been exclusively triggered by an inductive bacterial film rather than by direct larval perception of DFAA. If putative signalling compounds serve as a nutrition source for settlement-inducing bacteria, an explicit investigation of the efficacy of chemical metamorphic cues is unreliable (Beckmann et al. 1999).

Artificial induction or inhibition of settlement Inductors The metamorphic response in H. elegans larvae can be induced by ions Cs+ or K+ but such a response is much slower than the response to biofilms (Carpizo-Ituarte & Hadfield 1998). Lectines have been shown to mediate the settlement and metamorphosis of Neodexiospira brasiliensis larvae (Kirchman et al. 1982b). Settlement by larvae of this species was blocked if the biofilms were first exposed to certain lectines, indicating that larvae settled in response to particular surface polysaccharides or glucoproteins in the bacterial films. 55

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The cyclic nucleotide phosphodiesterase inhibitor isobutyl methylxanthine (IBMX) and non-specific phosphodiesterase inhibitors theophylline and papaverine induced a high percentage of normal metamorphosis in Hydroides elegans (Bryan et al. 1997, Holm et al. 1998, Pechenik & Qian 1998, Qian & Pechenik 1998). Gamma-aminobutyric acid (GABA), choline chloride, dihydroxyphenyl L-alanine (L-DOPA), and potassium chloride evoked a low percentage of settlement but abnormal metamorphosis in this species (Bryan et al. 1997). L-DOPA and D-DOPA were shown to induce larval metamorphosis in Hydroides ezoensis, Pomatoleios kraussi, and Ficopomatus enigmaticus. Other neuroactive molecules, epinephrine and norepinephrine, also induced larval metamorphosis in Hydroides ezoensis and Pomatoleios kraussi (Okamoto et al. 1995, 1998). Inhibitors Polyaromatic hydrocarbons (PAHs), the main toxic components of crude oil polluting the marine environment, have an adverse effect on the settlement of Hydroides elegans larvae (Paul et al. 1998). Six cuporous oxide antifouling paints resulted in both post-attachment mortality and pre-attachment mortality of larva of Neodexiospira lamellosa and Eulaeospira convexis (Wisely 1964). Glucose blocks the settlement and metamorphosis of Neodexiospira brasiliensis larvae (Kirchman et al. 1982b). Larval settlement may be inhibited directly, or through compounds that regulate the growth of bacteria, which in turn affects larval settlement. Settlement of Hydroides elegans is inhibited by brown algal phlorotannins and two related compounds, tannic acid and phloroglucinol. Phlorotannins, tannic acid and phloroglucinol were inhibitory to H. elegans larval settlement and to the growth of certain marine bacteria that induced high levels of H. elegans larval settlement. However, some of the bacteria that induced low levels of larval settlement were resistant to these compounds (Lau & Qian 1997). Adenylate cyclase activator forskolin inhibited responses of larvae of H. elegans to inductive bacterial biofilms (Holm et al. 1998).

Signalling pathways involved in metamorphosis Studies of the response of H. elegans larvae to neuropharmacological agents demonstrated that neither the G-protein activator Gpp [NH]p nor the inhibitor GDP-P-S affected metamorphosis. Therefore, neither G protein-coupled receptors nor their associated signal-transduction pathways regulate induction of metamorphosis by bacterial cues (Holm et al. 1998). In conclusion, Wilson’s remark that “All the explanations so far advanced, effect of light, texture of surface, grade of bottom soil, metamorphosis-inducing substances, etc…, are at best partial answers to that problem” still summarises the complexity of settlement (Wilson 1952 in Thorson 1957). Juvenile growth and maturation Growth The rate of post-settlement growth of juvenile serpulids has been well studied for fouling species (e.g. Ficopomatus enigmaticus: Rullier 1946, Soldatova & Turpaeva 1960, Vuillemin 1965; F. uschakovi: Hill 1967, Straughan 1972 a,b; Hydroides dianthus: Grave 1933; H. elegans: Grave 1933, Paul 1937, 1942, Dew 1958, Behrens 1968, Sentz-Braconnot 1968; H. ezoensis: Miura & Kajihara 1981; Pomatoceros triqueter: Føyn & Gjøen 1954, Sentz56

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Braconnot 1968; Pseudochitinopoma occidentalis: Smith & Haderlie 1969) and the growth rate of spirorbids is known for Spirorbis spirorbis, S. corallinae, S. tridentatus and Janua pagenstecheri (de Silva 1967), Spirorbis rupestris (Gee 1967), Neodexiospira sp. (Bagaveeva 1975) and N. brasiliensis (Rzhavsky & Britayev 1984).

Ontogenetic changes of growth rates Tubes of juvenile worms grow rapidly but the growth slows down in later life (ten Hove & van der Hurk 1993). Settled Spirobranchus juveniles put down at least a body length of tube (0.5– 1 mm) per day when first settled (Smith 1985). Paul (1937) reports a growth rate of 14 mm in 9 days for Hydroides elegans. In H. dianthus the first three months increases in length by 54 mm but in the next 9 months only 12 mm are added (Grave 1933). Pomatoleios kraussi grows 130 µm day-1 for the first 2 months, slowing to 50 µm day-1 in the third month (Crisp 1977).

Seasonal changes in growth rates Under natural conditions the growth of Spirorbis spirorbis is much slower in winter (0.17 mm month-1) than in summer (0.66 mm month-1) (de Silva 1967). The same holds true for Pomatoceros triqueter (20–30 mm month-1 in spring, 2–10 mm month-1 in winter) and Hydroides elegans (12 mm month-1 in spring, 4 mm month-1 in winter) (Sentz-Braconnot 1968). Monthly increments in coil diameter of tubes of Spirorbis rupestris were about 0.5 mm to 0.7 mm between September and January, but only about 0.2 mm between January and March (Gee 1967). The median summer growth rate in coil diameter of Neodexiospira brasiliensis for 2 months after settlement was about 0.82–0.88 mm month-1 (Rzhavsky & Britayev 1984). Calculated summer growth of juveniles under natural conditions is in the same range in Neodexiospira sp. (Bagaveeva 1975) and is about 0.66 mm month-1 in Spirorbis spirorbis (de Silva 1967). The growth of the latter species is slightly faster than calculated growth of S. spirorbis, S. corallinae and Janua pagenstecheri in the laboratory (0.55–0.58 mm month-1, de Silva 1967) and is markedly faster than that of Spirorbis tridentatus (0.36 mm month-1) reported by de Silva (1967). Estimates of juvenile growth for Pomatoceros triqueter and Hydroides elegans range from 7 (Norway)-12 mm (Mediterranean) in the first month to 0.2–12 mm in winter, depending on the natural conditions (Sentz-Braconnot 1968). Klöckner (1976) found the growth rate ranging from 0.6 mm month-1 in winter to 11.4 mm month-1 in summer for tubes of Pomatoceros triqueter at Helgoland (North Sea). Klöckner (1976) found the tube regeneration by tubeless worms to be a function of body weight (the larger the worm, the slower growth) and temperature (the growth increasing between 6°C and 22°C and decreasing above 25°C).

Factors affecting juvenile growth In addition to the above-mentioned ontogenetic and/or seasonal changes, the growth rate in serpulimorphs varies according to temperature and/or population density (e.g. Ficopomatus uschakovi: Straughan 1972b; Hydroides dianthus: Leone 1970; Pomatoleios kraussi: Crisp 1977), flow speed (Pseudochitinopoma occidentalis: Eckman & Duggins 1993), salinity (Ficopomatus enigmaticus: Soldatova & Turpaeva 1960, Turpaeva 1961; Hydroides dianthus: Leone 1970; H. elegans: Qiu & Qian 1998), the pollution (H. elegans: Moran & Grant 57

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1984) and availability of food (Pomatoceros triqueter: Føyn & Gjøen 1954; Hydroides. dianthus: Leone 1970). Castric-Fey (1983) also mentions high density as a factor affecting growth; in closely spaced Pomatoceros the touch of neighbouring branchial crowns apparently decreases growth. Bianchi & Morri (1996) noted an inverse relation between settlement and growth in Ficopomatus enigmaticus, arguing that the alternating phases of heavy gregarious settlement and rapid vertical growth are an expression of the species’ ability to shift from an r to a K strategy during the annual cycle. Juvenile growth after the metamorphosis may be determined not only by the factors acting during the post-settlement period but also to a larger degree by factors experienced during the larval stage. In particular, juvenile growth rates have been shown to be affected in Hydroides elegans (Qian & Pechenik 1998) as a result of food limitation during development or delayed metamorphosis. Treatment of larvae with excess K+ also has adverse effects on juvenile growth (Qian & Pechenik 1998).

Maturation (size and age at first reproduction) Serpulids and spirorbids reach sexual maturity after they achieve a certain body size. That is, maturation correlates with growth rate and depends on the factors controlling it. Animals living under conditions suboptimal for growth reach maturity slowly and some never reach it. For instance, Ficopomatus uschakovi juveniles growing in optimum salinity become mature in 4 wk, those that grew slowly at salinities either below 5 or above 30 never matured (Hill 1967). At salinity⭓25 and temperature⭓20°C, the first spawning of Hydroides elegans occurred on day 16 after settlement. Both low temperature and low salinity led to slower growth and subsequently to a longer time to maturation (Qiu & Qian 1998). Spawning of H. elegans reared in the laboratory was observed on average 40 days after fertilisation at 23°C (Matsuo & Ko 1981). However, according to Paul (1937, 1942) H. elegans reaches maturity within 9 days after settlement in Madras, India at 25.5–29.5°C. Vuillemin (1965) mentions maturation in 6 wk for Ficopomatus enigmaticus, within 4 wk for Hydroides elegans (Lake of Tunis). H. dianthus matured within 7–8 wk at Woods Hole (Grave 1933), and within 6 wk after settlement in Lagos, Nigeria (Hill 1967). The first macroscopic signs of sexuality appear 1.5–3 months after settlement in Pomatoceros triqueter and P. lamarckii (Castric-Fey 1984). Size at maturation of Ficopomatus uschakovi at Lagos, Nigeria started from 6 mm but not all worms of this size were mature (Hill 1967). In Japan, mature eggs or sperm in F. enigmaticus were first observed in individuals 6–8 mm long, 3–4 wk after settlement (Okamoto & Watanabe 1997), whereas in France F. enigmaticus becomes mature at 9–10 mm (Fischer-Piette 1937). The smallest mature worm of Hydroides dianthus was 13 mm long (Hill 1967). Tubes of reproductive individuals of H. elegans were usually longer than 1.2 cm (Qui & Qian 1998). Neodexiospira brasiliensis (Rzhavsky & Britayev 1984) may start brooding when 5 wk old. Large broods were found in the tubes of 2–3 month old Circeis armoricana with coil diameters of at least 1.9 mm (Ivin 1997). In Simplaria potswaldi gametes start to differentiate when 10–12 abdominal segments are formed (Potswald 1981). Breeding begins at a coil diameter of 1.5 mm in Spirorbis spirorbis, 2.0 mm in S. rupestris, 1 mm in S. rothlisbergi, 1.2 mm in Neodexiospira brasiliensis (Gee 1967, Rothlisberg 1974, Daly 1978a, Rzhavsky & Britayev 1984). These coil diameters constitute about a half of the maximum coil diameter known for each species. 58

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Longevity The longevity of all organisms, including serpulimorph polychaetes, correlates with body size. The life span of small Serpulidae and Spirorbidae rarely exceeds 1 yr. For example, N. brasiliensis live only several months (Rzhavsky & Britayev 1984). Maximum length of tubes (1.4mm) of N. pseudocorrugata was attained 25 days after settlement (Ghobashy & Selim 1979b). The maximum life span of fouling polychaetes that mainly aggregate on crustacean carapaces apparently does not exceed the intermoult period (6–7 months) of their crustacean hosts (Gili et al. 1993). Large specimens of Janua pagenstecheri are often found on the common lobster (Astacus gammarus) that moults its carapace once a year, which suggests that Janua pagenstecheri attain their full size in one year. Similarly, Circeis cf. armoricana of maximum size are found on the thallus of Laminaria that is renewed every year (Bergan 1953). Spirorbis spirorbis and S. corallinae do not reach sexual maturity until the spring of the following year (Thorson 1946, de Silva 1967, Daly 1978a), which implies a life span of at least a year. Filograna implexa, a small form (up to 5 mm), can possibly live two seasons (Plymouth, UK, Faulkner 1929), although asexual reproduction probably makes estimates of longevity in this species difficult. The life span of the aquarium-reared specimens of Hydroides elegans and Pseudochitinopoma occidentalis was 1 yr (Grave 1933, Smith & Haderlie 1969). The freeliving Ditrupa arietina shows a strictly linear growth-curve during its first year but growth is asymptotic in the second and final year (Medernach & Grémare 1999). Pomatoceros triqueter has a life span of 4 yr according to Dons (1927), but estimates of the longevity for this species in northern Europe vary from 1.5 (Føyn & Gjøen 1954) to 2.5 yr (Castric-Fey 1983). Larger species, such as Spirobranchus polycerus and Ficopomatus enigmaticus, can live for 10–12 yr (Fox 1963, Marsden 1994b). The even larger forms of the Spirobranchus giganteus complex can live for 18–35 yr (Smith 1985, Nishi & Nishihira 1996, 1999, Nishi 1997).

Mortality

Age-specific mortality Mortality rates may vary for different stages of the life cycle but quantitative estimates of embryonic, larval, juvenile and adult mortality are too rare for serpulimorph polychaetes to make reliable comparisons. Generally, at least two peaks of increased vulnerability and probably associated mortality have been reported for serpulids with planktonic larvae; in the early embryonic and early juvenile stages. Gray (1976) showed that 4-day-old larvae of Serpula columbiana were more resistant to reduced salinity at low temperatures than were gastrula and 1-day-old larvae. Qiu & Qian (1997) studied tolerances to various experimental salinities among various developmental stages of Hydroides elegans. Among four stages (newly-released oocyte to 2-cell stage, 2-cell to blastula, blastula to trochophore, trochophore to newly-settled juvenile) development failed at salinities of <20, 20, 25 and 15, respectively. That is, the trochophore stage seems to be slightly more tolerant to salinity stress than the embryonic and early juvenile stages. Juveniles of H. elegans were more vulnerable to low salinity (20) within 1 day of settlement than when older. Apparently, the early developmental stages are more sensitive to environmental stress than late juveniles and adults and the 59

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juveniles are most vulnerable at the onset of benthic life (Qiu & Qian 1998). High natural mortality is also reported for juveniles of Pomatoceros triqueter (Klöckner 1976). Extreme vulnerability at the onset of juvenile life and very high juvenile mortality (>90%) are widespread among benthic marine invertebrates (see Gosselin & Qian 1997b for review). Mortality of brooded embryos due to failure of fertilisation or any other causes acting before the time of larval release is reported to be very low (e.g. Daly 1978a,b for Spirorbis spirorbis) but increases in the post-settlement period. Rzhavsky & Britayev (1984) report that mortality of Neodexiospira brasiliensis is highest during the first week after the settlement and may reach 79.5% of the newly settled juveniles. Hamamoto et al. (1996) found two peaks of mortality in spirorbids; early post-settlement mortality and mortality of individuals with tube diameters over 1.5mm. The second peak probably corresponds to the natural mortality of adults.

Mortality factors Natural variation in mortality rate at any given stage is apparently due to variation in the intensity of mortality factors. Documented sources of serpulid and spirorbid mortality include the above-mentioned factors affecting development, settlement and growth, such as inadequate food conditions, physical environmental factors, pollution, lack of adequate larval settlement sites and delaying of metamorphosis. For example, survival of Hydroides elegans trochophores increased with increasing algal concentrations from 0 to 106 cells ml-1. No settlement occurred at concentrations <103 cells ml-1. Larvae that were allowed to resume feeding after 10 days starvation did not settle. Such a period of food limitation exceeds the point at which H. elegans retain the ability to develop to competence (Qiu & Qian 1997). Brooding success (survival of embryos) of Pileolaria berkeleyana sensu lato appears to be dependent on temperature (Harris 1972, Thorp 1991). Natural mortality of juveniles of Pomatoceros triqueter reached a maximum in late autumn, when the phytoplankton supply was approaching a minimum and water temperatures were decreasing (Klöckner 1976). Low salinity increased mortality during both the larval and early juvenile periods of Hydroides elegans (Qui & Qian 1997, 1998). High sedimentation contributes to juvenile and adult mortality in some spirorbids settling on rocks (Rzhavsky unpubl.) and in Pseudochitinopoma occidentalis (Duggins et al. 1990). Two-day-old larvae of Serpula columbiana died after 3 h in 0.5% of diesel oil (Chia 1973). Delaying of metamorphosis had significant adverse effects on juvenile survival of Hydroides elegans (Qiu & Qian 1998).

Biotic factors: predation, competition and parasitism Natural predators Predation is an important source of mortality at all stages of the life history. However, predation on serpulid larvae is difficult to document probably because small transparent larvae are digested very fast and cannot be detected in predators’ stomachs. Cowden et al. (1984) mention that suction-feeding bivalves are capable of catching serpulid larvae. Gastropod molluscs are the most commonly reported predators on juvenile and adult serpulids and spirorbids (Moran et al. 1984, O’Donnell 1984, Tan & Morton 1998, Hoisaeter 1989, Ward 1989, ten Hove 1994a, Rzhavsky unpubl.). Okadaia elegans, a dorid nudibranch of the family Vayssiereidae (Opistobranchia, Gastropoda) feeds on spirorbids and serpulids (Baba 1937, Young 1969). In penetrating the tubes, 60

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specimens of O. elegans bore smooth round holes presumably by chemical activity and mechanical rasping (Young 1967, 1969). Other reported predators of serpulids include crabs (Pomatoleios kraussi: Straughan 1969; Ficopomatus uschakovi: Straughan 1972a), fishes (e.g. Vinogradov 1948, Wesenberg-Lund 1951, Hiatt & Strasburg 1960, Randall 1967, Bosence 1973, KnightJones et al. 1973, Bailey-Brock 1976: Families Chaetodontidae, Acanthuridae, Balistidae, Labridae), Asteroidea (Christensen 1970, Bosence 1973) and Echinoidea (Chadwick 1900, Hunt 1925, Vine & Bailey-Brock 1984). However, according to ten Hove (1979a) predation by fishes generally only affects the (extended) branchial crowns, which may regenerate after removal within a couple of days. Spirorbids are occasionally found in stomachs of the sea urchin Strongylocentrotus polyacanthus that indiscriminately scrapes hard substrata. Small or juvenile sea stars also sometimes consume spirorbids (Feder 1970, Rzhavsky unpubl.). There is a single record of a nereid polychaete eating Ficopomatus (Margalef 1962). The high frequency of occurrence of rhabdocoels and mites in tubes of spirorbids led Knight-Jones et al. (1975) to the conclusion that those animals were important predators of spirorbids. Competition Competition for space is an important determinant of mortality in many sessile organisms. The outcome of such competition depends on the serpulid species and the composition of the fouling community (e.g. Straughan 1972a). For example, Pomatoceros triqueter successfully competed for space with bryozoans (Rubin 1985), whereas Pseudochitinopoma occidentalis was completely smothered by encrusting bryozoans after several months following settlement (Haderlie 1974). Overgrowth by bryozoans and tunicates (Castric 1977) and by the soft coral Xenia (Vine & Bailey-Brock 1984) has been reported as a source of serpulid mortality. Mortality and competitive abilities of juveniles of Pomatoleios kraussi varies according to tidal height and the intensity of settlement. At low level exposure sites, encrusting ectoprocts, sponges and filamentous algae cause heavy mortality among low density populations of P. kraussi. At the mid-tidal level, where the most abundant larval settlement occurs, P. kraussi almost completely smothers Balanus amphitrite, whereas at the highest level the competition for space is almost completely eliminated because the intensity of larval settlement is low (Mohammad 1975). Spirorbids are often overgrown by encrusting species (Stebbing 1973, O’Connor & Lamont 1978) and whereas some redirection of growth in an attempt to elevate the tube orifice above the competing species is possible, most individuals are ultimately smothered. Such observations thus confirm Jackson’s (1977) assertion that colonial species can generally outcompete solitary species. Parasites Parasitism may also control populations to some extent but there is no overview of parasites and/or commensals occurring in or on serpulids. Host specificity of parasites can be used as a tool in resolving evolutionary pathways in different host groups although a complete evaluation requires a profound knowledge of the various parasitic or commensal groups, and even then the precise nature of the symbiosis will not always be clear. This difficulty may be illustrated by a remark by Gotto (1993) regarding the copepod Acaenomolgus protulae (Stock 1979), reported from Protula intestinum and P. tubularia: “Unlike Sabelliphilus, it is probably a commensal rather than a parasite.” Host specificity is difficult to prove: 61

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Despite the fact that previous authors have reported many different, most probably only occasional hosts of Pseudanthessius gracilis, the true natural host (Gotto 1993), still remains unknown. Our study has identified the polychaete Hydroides elegans as at least one of the true hosts of this species, since we have managed to rear all copepodids up to the adult stage in its presence. (Costanzo et al. 1996) However, this copepod is not a true parasite but is a kleptoparasite stealing slime and particles from ciliary ducts (Stock pers. comm.). It is thus not relevant to the present discussion. A number of older references mention infestations of serpulids by protists like the Gregarinidae (known as endoparasites in various invertebrates). The nature of these infestations is not always clear, nor is their effect on the well-being of the hosts. Species mentioned include Pomatoceros triqueter, Protula tubularia, Salmacina dysteri, Serpula vermicularis, Spirobranchus latiscapus and Janua pagenstecheri and the nominal infesting taxa are Anoplophyra spirorbis, Haplosporidium marchouxi, Monocystis serpulae, Polyrhabdina serpulae, Selenidium caulleryi, Selenidium sp. (Lankester 1863, McIntosh 1885, Mingazzini 1893, Caullery & Mesnil 1899, 1905, Brasil 1907, Lee 1912, Hempelmann 1930). There is just one remark about the frequency of occurrence: “there is no individual of Protula tubularia from the coast of Calvados [France] of which the alimentary canal does not contain a great number [of Selenidium]” (Brasil 1907). Margolis (1971) reviews the role of polychaetes as intermediate hosts of helminth parasites of vertebrates, of which only trematodes are known from serpulids. The sporocysts of one species, Cercaria loossi, develop in the coelom of Hydroides dianthus as first intermediate host, in the Woods Hole area, USA (see also Stunkard 1970). It is apparently a specific parasite for H. dianthus. Whether or not it castrates its host, like in the comparable situation of Aporocotyle simplex in the terebellid polychaete Arctacama proboscidea (Køie 1982) is unknown. The sporocysts (with cercariae) leave the polychaete through its genital pores on the way to their definitive fish host (Martin 1944) but this may be an artefact (Køie 1982). Another digenetic trematode, Proctoeces maculatus uses Hydroides elegans as a secondary host in the Mediterranean (Prévot 1965). It is not an obligatory parasite of the serpulid because it is known from the errant polychaete Nereis and even also from molluscs. It is a matter of semantics whether the Pyramidellidae (Gastropoda), which suck fluids from various invertebrates with their long proboscis, should be regarded as ectoparasites or as micro-predators. Their occurrence in serpulids has been reviewed by ten Hove (1994a). On the one hand, species of the genus Fargoa seem to be genus-specific ectoparasites of the genus Hydroides, while on the other hand, members of the genus Boonea are generalists that also occur on various molluscan hosts (Robertson & MauLastovicka 1979). In the genus Odostomia one species is reported to be specific to Pomatoceros triqueter, another to the mussel Mytilus edulis and a third is associated with many bivalve molluscs (Baer 1971). The small size of the gastropod, however, makes field observations difficult. The question of host-specificity is further obscured by the fact that their most frequently mentioned serpulid hosts (Pomatoceros triqueter, Galeolaria caespitosa and Hydroides dianthus) occur in dense masses with a diverse accompanying fauna. The statement “found on H. dianthus” is thus no guarantee that the host was indeed the serpulid (ten Hove 1994a). Several other gastropods are known as kleptoparasites. Trichotropis cancellata, (Family Capulidae) inserts its proboscis into the mouth of Serpula columbiana (as well as sabellids and sabellariids) and removes food from the worm (Pernet & Kohn 1998). Unpublished 62

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results of experiments (Pernet & Iyengar pers. comm) show that parasitic snails substantially reduce growth rates (measured as tube extension) of S. columbiana in the field. There is a single record of a polychaete endoparasite in a serpulid, that of Drilonereis sp. in Serpula vermicularis (Pérès 1949, Paris 1955). The parasitic worm penetrates its host in the 6th abdominal chaetiger, makes a loop almost throughout the entire abdomen in such a way that its prostomium is situated in the first abdominal chaetiger; the posterior 4 cm of the parasite remain outside its host. The literature on parasitic copepods is vast. One of the first records of copepods on serpulids may be that on Hyalopomatus claparedii by von Marenzeller (1878), without further taxonomic details of the copepods involved. Other old records include those by McIntosh (1885, 1919, 1923) and Gravier (1912, 1913). In her review of the association of copepods with marine invertebrates, Gotto (1979) concludes: “few hard and fast rules can be applied to the incidence of host specificity.” She also states: “If older records could be relied on, the genus occurs in quite an array of ascidian hosts; but this is almost certainly erroneous and stems from the confusing synonymies which have accreted over the years for ascidians and copepods alike.” This statement also holds true for the situation in serpulids. For instance, Faulkner (1929) ascribes differences in size between colonies of Filograna implexa (Plymouth, UK) to the presence of the endoparasitic monstrillid Haemocera in some colonies but it is not clear if the author distinguished between the operculate Filograna implexa and the non-operculate Salmacina dysteri. Nelson-Smith & Gee (1966) explicitly state: “At Plymouth, Cymbasoma filogranarum [senior synonym of Haemocera] is said to infect Filograna implexa but not Salmacina dysteri…, which reinforces the proposal of Gee (1963b) that these two species should remain distinct.” However, this is in contradiction to the drawing by Malaquin (1901; copied by e.g. Baer 1952, 1971, Davies 1984), clearly showing the non-operculate Salmacina as host of the monstrillid. Isaac (1974) attributes the monstrillid to yet another taxon, Thoumaleus rigidus. Ectoparasitic (or commensal) copepods have been recorded from abdomens, inside the tube (e.g. Southward 1964: Salmacina setosa, Filogranula stellata and Placostegus tridentatus) and from branchial crowns in serpulids. Our knowledge is far from complete, as is shown by the high proportion of new genera and species described by Stock (1979, 1988, 1989, 1995a,b) based on accidental collections by one of us (tH). In one case, a single serpulid (Spirobranchus corniculatus) even yielded two different genera of ectoparasitic copepods (Stock 1995a), suggestive either of different microniches or of different food sources utilised by the copepods (cf. Gotto 1979). Humes & Stock (1973) revised the Lichomolgidae, of which a number of taxa are associated with various serpulids (Filograna, Pomatoceros triqueter, Pomatostegus stellatus, Protula tubularia, P. intestinum, Serpula vermicularis and Spirobranchus giganteus). Later records include those by Humes & Grassle (1979, Josephella sp.), Bailey-Brock (1985, Spirobranchus tetraceros), ten Hove (1994b, Hydroides tuberculatus, Serpula hartmanae, Spirobranchus corniculatus, S. gardineri). Although the overall pattern suggests that copepod taxa are specific to certain genera of serpulids rather than to species, a complete evaluation should be done in a joint effort by serpulid and copepod taxonomists. Haswell (1884, 1885 cited by Augener 1914, McIntosh 1923) reported a new genus Eisothistos (=“invader”) of parasitic isopod inhabiting tubes of Serpula vasifera. These isopods prey on serpulids and rear broods in their tubes (Haswell 1884). Wägele (1979, 1981) found two more Eisothistos species in serpulid tubes and studied their growth, 63

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maturation, brooding, and adaptation to the occupied niche. Finally, Knight-Jones & KnightJones (in prep., pers. comm.) described five new species of the genus Eisothistos inhabiting tubes of various spirorbid species. From all these scattered records, the general impression is that parasitism does not play a major role in the population dynamics of serpulids.

Discussion While many polychaetes show extremely high overall diversity and flexibility of life histories, such diversity varies significantly among families (Wilson 1991, Giangrande 1997). For example, the families Capitellidae and Spionidae show the highest variability and flexibility in their life cycles, whereas the Sabellariidae, Spirorbidae and Nepthyidae show the least variability. The question is whether ecology and morphology of various polychaete groups impose constraints on the evolutionary diversity of their life-history and reproductive traits. Such constraints may be related to the morphological design, ecology, and habitats used by a group (McHugh 1993, Giangrande 1997). Phylogenetic constraints (defined as a result of the phylogenetic history of a lineage that prevents anticipated course of evolution) might be tested only within a phylogenetic framework. Variability of life histories may also be limited because life-history traits are known to covary and co-evolve. Some constraints on the reproductive biology of serpulimorph polychaetes are apparently imposed by their obligatory sessile life style. The features typical for mobile and some sedentary polychaetes (e.g. spionids, cirratulids) such as swarming, epitoky, hypodermic insemination, mating by direct copulation and some active forms of parental care are not found in serpulimorph polychaetes. Other constraints and life-history patterns are not so obvious. For example, sessile life style has been proposed to explain the evolution of hermaphroditism in some groups. Ghiselin (1969, 1974) suggests that simultaneous hermaphroditism is advantageous in sessile species or in low-density populations because each contact of adults can lead to reproduction. However, his hypothesis fails to account for the observed gonochorism and/or protandric hermaphroditism in serpulimorphs. Moreover, some simultaneous hermaphrodites (e.g. species of the Filograna/Salmacina complex) are found in high-density colonies. Below we consider the patterns in serpulid egg size, larval feeding modes, parental care, planktonic and benthic developmental habitats and investigate if the hypotheses proposed to explain evolution of these life-history traits can be applied to serpulimorphs.

Trends in egg size and larval feeding modes The egg size, an indicator of energy investment per offspring, is one of the most important life-history traits. The evolution of egg size has been of considerable interest to evolutionary biologists. The original fecundity-time Vance model and its modifications (Vance 1973a,b, Christiansen & Fenchel 1979, Perron & Carrier 1981, Grant 1983) predict that reproductive success for planktonic larvae is maximised in species with the smallest eggs that require larval feeding or in the largest eggs associated with non-feeding development. Therefore, bimodal egg size distribution with modes corresponding to feeding and non-feeding development is expected. 64

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The pattern of egg size distribution in serpulimorph polychaetes shows some expected and unexpected trends. Egg sizes in serpulimorphs vary from 45 µm to 230 µm. As expected, smaller eggs (<80 µm) correlate with feeding larval development and larger eggs (>80 µm) correlate with non-feeding development. The egg size distribution is visually bimodal if data for serpulids and spirorbids are pooled (Fig. 12A) but the observed modes do not correspond to feeding and non-feeding development, as predicted by the Vance model. Rather, they reflect taxonomic differences. If distributions of serpulid and spirorbid eggs are considered separately, the egg size distributions are clearly unimodal (Fig. 12B, C). Moreover, the egg sizes of feeding and nonfeeding larvae partially overlap; intermediate egg sizes (80–90 µm) are found both in species with feeding larvae and non-feeding larvae. One explanation of this pattern is that egg diameters are not reliable indicators of parental investment in serpulimorph polychaetes, especially because the overall differences in egg size are relatively small. Both total organic content and organic content per volume may vary significantly among species. Another explanation of this pattern is that larvae of some planktotrophic species with larger eggs are facultative feeders, that is, they are capable of completing metamorphosis without feeding. Incorporation of facultative feeding into the fecundity-time model showed that reproductive success can be maximised at intermediate egg sizes depending on larval food availability and the intensity of planktonic mortality (McEdward 1997). The facultative feeding model predicts that a continuum of nutritional strategies exist between planktotrophy and lecitotrophy and that planktotrophic species should differ in parental investment, susceptibility to food limitation, development rate, growth and size at metamorphosis. At present there is insufficient information and additional studies are needed to determine whether facultative feeding is common in serpulids and in other polychaetes and whether it can account for egg size variability and distribution. An alternative hypothesis that explains continuous variation in egg size between species from the perspective of fertilisation kinetics was proposed by Levitan (1993). He suggested that larger eggs present a larger target for sperm and will be fertilised at higher rates. Therefore, for broadcast-spawning species there is a trade-off between the production of many small eggs with low probability of fertilisation and fewer large eggs with higher probability of fertilisation. Although there is some variation in egg size of free-spawning serpulids, it is unknown whether such a difference is translated into differences in fertilisation rates. More important, the model does not explain the predominance of relatively small eggs corresponding to planktotrophy and almost total lack of larger eggs corresponding to planktonic lecithotrophy in serpulids. Two related questions here are how broadcasting serpulids overcome the potential problem of sperm limitation and why planktonic lecithotrophy is so rare.

Why not planktonic lecithotrophy? The dominance of larval feeding in serpulids is intriguing because the closely related Sabellidae have exclusively non-feeding larval development. The question arises whether serpulids are constrained in their mode of larval nutrition or whether larval feeding is selectively advantageous for this group.

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Figure 12 Egg size distribution in serpulimorph polychaetes. Above, serpulids and spirorbids combined. Centre, serpulids only. Below, spirorbids only.

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Figure 13 Relationship between maximum adult size and maximum egg size in planktotrophic serpulids.

Since larval feeding usually corresponds to smaller eggs, it offers the advantage of higher fecundity than lecithotrophy. However, serpulids with planktotrophic larvae show a significant positive correlation between the maximum adult size and maximum egg size (Fig. 13), suggesting that fecundity is not necessarily maximised with increased body size. The duration of non-feeding larval development depends primarily on temperature, whereas the duration of feeding development is also affected by food availability. Low food levels may lead to longer development and increased mortality due to predation and other factors. Apparently, any adaptation to decrease development time should increase overall fitness. Havenhand (1993) developed a model that considers the effect of the development time on the evolution of egg size and larval type. According to the model, there are selective pressures that reduce the egg-to-juvenile period. Since species with non-feeding larvae tend to have a shorter development time, this means selective pressure towards non-feeding development. Interestingly, because this effect is more pronounced at shorter life cycle durations (Havenhand 1993), the model probably better explains the selective pressures towards lecitotrophy connected with small body size and brooding (see below) than towards planktonic lecitotrophy of larger species with longer life cycles. Increased dispersal distance is a consequence of the longer planktonic life of feeding larvae. However, an increased scale of dispersal offers little if any advantage for feeding larvae (Palmer & Strathmann 1981). The evolutionary importance of a planktonic stage in serpulids is likely to be in small-scale habitat selection rather than in long-distance dispersal because serpulid larvae require specific cues for settlement and suitable habitats are commonly patchy in their distribution. The question is whether larval feeding improves habitat selection relative to non-feeding larvae. Consequences of larval feeding for habitat selection and postmetamorphic growth and survival have not been well studied. It is obvious from the literature that successful settlement 67

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in serpulids is dependent both on how well larvae are preconditioned to respond to metamorphic cues and whether the required cues are available (see pp. 44–56). Larval feeding allows extension of the period when larvae remain competent to metamorphose thus increasing the possibility of locating a suitable substratum, although such an extension is not without a cost (see pp. 44–56). It appears that there is a trade-off between mortality due to the lack of suitable substrata and mortality due to postponed settlement. Further studies could show whether better habitat selection by planktotrophic larvae does make serpulid larval feeding selectively advantageous.

Fertilisation success It has been suggested that low fertilisation rates resulting from gamete dilution may constrain reproductive success in free-spawning organisms (Levitan 1995). The nature of the adaptations to decrease the effects of sperm dilution is not clear. It is likely, for example, that high fecundity of large serpulids and high population density of species that settle gregariously offset these factors to some extent, yet some relatively small-bodied freespawning serpulids are common in low-density populations. Therefore, further studies of fertilisation success in serpulids should address gamete longevity, concentration, and postspawning behaviour, as well as the size of adults and their distribution in the field.

Planktonic and non-planktonic development Egg size and corresponding larval feeding modes (planktotrophy and lecitotrophy) are so closely connected to the habitat where the larval development takes place (benthos or plankton) that they are not always distinguished. Thorson’s classification of reproductive modes into planktotrophy, lecithotrophy and brooding (Thorson 1950) stressed that invertebrate larvae developing in the plankton can be either feeding or non-feeding but during brooding (or any encapsulated benthic development) larvae are usually lecithotrophic. However, an initial benthic stage in the form of encapsulation or brooding is followed by later release of feeding larvae in “mixed” development in some molluscs and crustaceans (Pechenik 1979). In serpulimorph polychaetes, planktonic development correlates with larval feeding (see above) and benthic development in the form of brooding is associated with lecithotrophy. This association is especially true for spirorbids that have only brooded lecithotrophic larvae with a short habitat-selecting stage. Whether the association of brooding with non-feeding development in serpulids is universal or some brooding species can release feeding larvae is not known because the frequency and variability of brooding methods has been significantly under-reported. Observations by one of us (ten Hove, see p. 41) suggest that a short period of initial brooding may be present in Pseudochitinopoma occidentalis, a species with typical planktotrophic larvae but confirmatory studies are needed. Factors influencing the evolutionary maintenance or loss of planktonic dispersive stages may be closely interconnected with those affecting evolution of feeding and non-feeding development (see above). Some factors include the nature of habitats used and effects of the body size. Obrebski (1979) developed a model of colonising strategy in planktonic larvae that links the availability of adult habitats with energy allocation to habitat search and larval 68

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metamorphosis. The model predicts that benthic organisms that colonise abundant habitats, such as coastal sandy and muddy sediments, will lose dispersive larval stages more often than species inhabiting rocky shores or highly specific habitats. From this perspective, planktonic larvae of serpulimorph polychaetes, even short-swimming spirorbid larvae, should be retained. Bhaud & Duchene (1996), on the contrary, suggested that for species inhabiting highly specialised and restricted habitats (such as bays, lagoons, and fissured hard bottoms) the reduction of larval dispersal is a prerequisite for the maintenance of populations. However, reduction of a planktonic stage does not always reduce dispersal. Drifting and rafting may serve as efficient means of long-distance dispersal (Highsmith 1985, Johannesson 1988, Martel & Chia 1991), especially if adults are small, as in spirorbids inhabiting algae.

Covariates of body size Body size is an important determinant of life history in many marine invertebrates but it seems to be of paramount importance in the life history of polychaetes (Giangrande 1997). Large body size is almost universally correlated with higher longevity and fecundity (see Fig. 14 and p. 18 for spirorbids). Increased longevity allows an adult to produce offspring over a longer period of time and the onset of sexual maturation is delayed. In such cases generation time and number of reproductive events are increased. In contrast, small adult size is associated with lower longevity and fecundity, earlier sexual maturation, and shorter generation time. Other very important life-history covariates of body size include sexuality patterns and developmental habitats (planktonic or benthic).

Figure 14 Relationship between tube coil diameter and maximum fecundity in spirorbids.

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Body size and sexuality patterns Evolution of protandric hermaphroditism as observed in serpulids is well explained by the sizeadvantage hypothesis (Ghiselin 1969, 1974, Warner 1988). According to the hypothesis, sequential hermaphroditism is favoured when an individual can reproduce most efficiently as a member of one sex when small but as a member of the other sex when it gets older and larger. Since larger body size usually increases female fecundity more than male fecundity, small individuals are expected to be males and larger individuals to become female, providing that cost of sex reversal is not too high. The observed pattern of serpulid protandric hermaphroditism (e.g. Pomatoceros triqueter: Føyn & Gjøen 1954) fits well into the size-advantage hypothesis. Simultaneous hermaphroditism correlates not only with small body size but also with brooding (see below), the trend exemplified by all spirorbids as well as by small serpulids. According to Heath’s (1979) hypothesis, given that brooding is internal, hermaphroditism may evolve if the resources a female can allocate to ova production are limited by lack of brooding space. In this case, spare resources then could be allocated to produce male gametes in a hermaphrodite.

Correlation of small body size and brooding The correlation of small size with brooding has been observed in many marine invertebrates (e.g. Chia 1974, Menge 1975, Knight-Jones & Bowden 1979). In serpulimorph polychaetes brooding is typical for all spirorbids and small serpulids (usually <10 mm in length), whereas large serpulids with a body size of >20 mm tend to be broadcasters (see Table 2, pp. 9–16). Several hypotheses have been proposed to explain such a correlation. The most intuitive hypothesis, that of Chia (1974), states that brooding should be advantageous in small organisms with low energy reserves for gamete production because planktonic mortality is high. Low fecundity (of small species) means there is a high probability that no embryos will survive because they are exposed to the hazards of planktonic life. According to the recruitment hypothesis (Strathmann & Strathmann 1982), predictable recruitment typical for brooding species is more important for small than for large species. If recruitment is unpredictable, and larval or juvenile survival is more variable than survival of adults (which is apparently the case for serpulids), selection may favour greater adult longevity with ensuring higher fecundity. Thus, varying survival may link absence of brooding to higher longevity and therefore, larger body size. The dispersal hypothesis (Strathmann & Strathmann 1982) states that the advantages of brooding for smaller species exceed potential advantages provided by greater dispersal. Given that small spirorbids can disperse considerable distances using rafting, drifting and floating, any disadvantages of limited larval dispersal in brooders may be compensated. Long-term dispersal may be disadvantageous and Bhaud & Duchene (1996) even suggested that brooding evolved as an adaptation for reduced dispersal to ensure fertilisation in a dispersive environment. However, their hypothesis does not suggest that brooding is more beneficial for small species than for large. The allometry hypothesis (Strathmann & Strathmann 1982) states that with increased body size, the capacity for egg production may increase faster than space for brooding. Hess (1993) found no evidence that scaling limits brood size in spirorbids. However, her test may not be decisive because she compared four spirorbid species with 70

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Pseudochitinopoma occidentalis, the small-bodied serpulid species that probably provides early embryos with short-term parental care (see pp. 41–4). Because the validity of the allometry hypothesis depends on the type and geometry of the brood space provided, it may be only applicable to certain methods of internal brooding. For example, it probably is not applicable to brooding in gelatinous masses outside the tube as found in Protula and inside the branchial crown as in Paraprotis. While the allometry hypothesis explains why brooding is not a beneficial strategy for larger organisms, it does not necessarily imply that brooding should be a preferred mode for small species. The model of Havenhand (1993, see p. 67), which stresses the selective pressures toward reduction of development time to metamorphosis, indirectly emphasises the importance of brooding in small organisms, because brooders are commonly lecithotrophic and tend to have shorter development time than planktotrophs. All the hypotheses outlined here are not mutually exclusive and some of them emphasise the association of large body size with absence of brooding more than the association of small size with brooding. While in serpulimorph polychaetes the association of brooding and broadcasting with extreme body sizes is well expressed, there is a range of intermediate body sizes (approximately 10–20 mm) where both brooding and broadcasting species can be found.

Direction of evolution of life history traits In marine invertebrates in general, planktotrophic larvae are often assumed to be primitive, while lecithotrophic development with or without brood care is thought to be advanced (e.g. Jägersten 1972, Strathmann 1985). One of the arguments in favour of the evolution of nonfeeding from feeding planktonic development involves loss of complex ciliary feeding bands. According to Strathmann (1985), if such structures are lost, their “re-evolution” seems so improbable that a biased unidirectional transition has been hypothesised. The transitional bias argument is well supported by comparative morphology data for echinoderms. However, the two major ciliary bands used for both swimming and feeding in polychaete trochophores can hardly be classified as complex structures. In serpulids there is no significant difference in morphology of feeding and non-feeding larvae: both the metatroch and the prototroch are present in lecithotrophic larvae which have guts filled with yolk. The assumptions about the direction of evolutionary transitions from feeding to nonfeeding development in life-history traits were developed in the absence of rigorous phylogenetic methods (McHugh & Rouse 1998). Recent phylogenetic evidence suggests multiple origins of planktonic larvae and plesiomorphy of benthic development for some spiralian taxa (Reid 1989, for molluscs; Rouse & Fitzhugh 1994, for sabellid polychaetes). Further integration of phylogenetic analyses into life-history evolution studies is essential to infer accurately the original condition of reproductive traits for serpulimorph polychaetes and other groups.

Conclusions The reviewed literature data indicate that, like many other groups of marine invertebrates, serpulimorph polychaetes show correlation of smaller eggs with feeding and larger eggs with non-feeding larval development, as well as correlation of small body size with simultaneous hermaphroditism, lecithotrophy and brooding. Less common features include 71

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overlap in egg sizes of species with feeding and non-feeding development and rarity of planktonic lecithotrophy. Many aspects of serpulimorph life histories are still poorly known and because of this lack of knowledge, any generalisations about the observed patterns may be biased. Nothing is known about the energetic content of serpulid and spirorbid eggs, the ecology of external fertilisation or any adaptations that increase fertilisation success. Knowledge of reproduction and development of many more species is required to determine the real distribution of brooding and non-feeding planktonic development in the group. Broader generalisations also require better information on egg sizes, larval and juvenile mortality and growth, development rates, size at metamorphosis, larval feeding and susceptibility to food limitation. Finally, robust hypotheses of phylogenetic relationships in serpulimorph polychaetes are necessary to determine whether phylogenetic constraints may explain some life-history features of this group.

Acknowledgements We thank J.Havenhand and Bruno Pernet who read and criticised the manuscript; R. Sanfilippo and D.Martin kindly shared their observations on extratubular brooding in Protula tubularia and P. and E.W.Knight-Jones provided information from their unpublished paper on spirorbid parasitism. We thank T.Britayev, M.A.O’Donnell, V.Radashevsky, B.Pernet, and the late J.H.Stock who provided their unpublished observations on various aspects of serpulimorph life history. Part of this research was carried out whilst EK was an IPR Scholarship holder at Flinders University.

Taxonomic addendum

Serpulidae Apomatolos simplex Uchida, 1978 see Rhodopsis pusilla: Uchida 1978 Apomatus globifer Willey, 1905 see Protula globifera Chitinopoma occidentalis Bush, 1905 see Pseudochitinopoma occidentalis: Smith & Haderlie 1969 Chitinopoma arndti Zibrowius, 1983 Chitinopoma rzhavskii (Kupriyanova, 1993), new combination, originally described as Filogranula rzhavskii. However, thoracic uncini with single row of teeth all over (in Filogranula with multiple rows above fang) and presence of brood-chambers as in Chitinopoma serrula (Rzhavsky unpubl.) rather place the taxon in Chitinopoma, Chitinopoma serrula (Stimpson, 1853) Crucigera irregularis Bush, 1905 Crucigera zygophora (Johnson, 1901) Ditrupa arietina (Müller, 1776) Ficopomatus enigmaticus (Fauvel, 1923) Ficopomatus miamiensis (Treadwell, 1934) Ficopomatus uschakovi (Pillai, 1960) Filograna implexa M.Berkeley, 1835: the Filograna/Salmacina complex needs revision; some authors regard the genera as synonymous, even synonymise operculate and non-operculate forms (e.g. Faulkner 1929), others maintain a generic distinction. We quoted various names at face value, but added localities (if known to us).

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Filograna tribranchiata Moore, 1923 Filogranella elatensis Ben-Eliahu & Dafni, 1979 Filogranula gracilis Langerhans, 1884 Filogranula rzhavskii Kupriyanova, 1993 see Chitinopoma rzhavskii Filogranula stellata (Southward, 1963) Floriprotis sabiuraensis Uchida, 1978 Galeolaria caespitosa Lamarck, 1818 Galeolaria hystrix Mörch, 1863 Hyalopomatus claparedii von Marenzeller, 1878 Hydroides dianthus (Verrill, 1873) Hydroides diramphus Mörch, 1863 Hydroides elegans (Haswell, 1883) Hydroides ezoensis Okuda, 1934 Hydroides fusicola Mörch, 1863 Hydroides hexagonis/us (Bosc, 1802) see H. dianthus: Colwin & Colwin 1961a,b,c Hydroides norvegica/us see H. elegans: Monroy 1954, Wisely 1958, Reish 1961, Ranzoli 1962, SentzBraconnot 1964, Prévot 1965, Srinivasagam 1966, Margolis 1971, Ghobashy & Selim 1979a Hydroides norvegicus Gunnerus, 1768; (sub)tropical records most probably belong to H. elegans Hydroides pectinatus (Philippi, 1844) see H. elegans: Zeleny 1905 Hydroides tuberculatus Imajima, 1976 Hydroides uncinatus (Philippi, 1844) see H. dianthus: Shearer 1911, Ivanoff 1928, Hill 1967 (probably) Josephella marenzelleri Caullery & Mesnil, 1896 Josephella spec. Humes & Grassle, 1979; the genus Josephella is known only from shelf depths, this bathyal (2500 m) record should be checked Marifugia cavatica Absolon & Hrabe, 1930 Mercierella enigmatica Fauvel, 1923, see Ficopomatus enigmaticus: Fischer-Piette 1937, Vuillemin 1954, 1962a,b, 1965, 1968, Dixon 1977 Mercierella enigmatica: see Ficopomatus uschakovi: Hill 1967, Straughan 1968 (in part, Victorian material is enigmaticus), Straughan 1972 a,b Metavermilia cf. ovata Imajima, 1978 Microprotula ovicellata Uchida, 1978 Mi(c)roserpula inflata Dons, 1930 see Chitinopoma serrula Neosabellaria cementarium (Moore, 1906) N.B.Sabellariidae, not serpulid Omphalopoma stellata Southward, 1963 see Filogranula stellata Paraprotis dendrova Uchida, 1978 Paraprotula apomatoides Uchida, 1978 Placostegus tridentatus (Fabricius, 1779) Pomatoceros lamarckii (Quatrefages, 1865), in shallow Mediterranean/Atlantic waters often confused with P. triqueter Pomatoceros strigiceps Mörch, 1863 see Spirobranchus latiscapus: McIntosh 1885 Pomatoceros terranovae Benham, 1927 Pomatoceros triqueter (Linnaeus, 1758) Pomatoleios kraussi (Baird, 1865) Pomatostegus actinoceras Mörch, 1863 Pomatostegus stellatus (Abildgaard, 1789): a Caribbean taxon; Indo-Pacific records belong to P. actinoceras: Nishi 1993 Protula globifera (Théel, 1878); although the species is classified in the genus Protula here, it should be noted that ten Hove & Pantus (1985) are of the opinion that Apomatus is a valid genus. Protula intestinum (Lamarck, 1818) Protula meilhaci Marion, 1875 see Protula tubularia: Soulier 1917 Protula palliata (Willey, 1905)

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Protula tubularia (Montagu, 1803) Protula tubularia: Pérès’ (1949) Figure 1 (also in Paris 1955) clearly shows two club-like pseudopercula, referring his specimen to Serpula vermicularis Pseudochitinopoma occidentalis (Bush, 1905) Pseudovermilia conchata ten Hove, 1975 Pseudovermilia occidentalis (McIntosh, 1885) Psygmobranchus protensus Philippi, 1844 see Protula tubularia: LoBianco 1888, 1909, Meyer 1888 Rhodopsis pusilla Bush, 1905 Sabellaria alveolata (Linnaeus, 1767); N.B. Sabellariidae, not serpulid Sabellaria cementarium Moore, 1906 see Neosabellaria cementarium: Cowden et al. 1984 N.B. Sabellariidae, not serpulid Salmacina aedificatrix Claparède, 1870 Salmacina amphidentata Jones, 1962 Salmacina aedificatrix Claparède, 1870: generally synonymised with S. dysteri. Salmacina dysteri Huxley, 1855; see remark under Filograna implexa Salmacina dysteri var. tribranchiata (Moore, 1923) see Filograna tribranchiata: MacGinitie & MacGinitie 1949 Salmacina setosa Langerhans, 1884 Semivermilia aff. uchidai Imajima & ten Hove, 1986 Serpula columbiana Johnson, 1901 Serpula concharum Langerhans, 1880 Serpula concharum see Hydroides elegans: Sentz-Braconnot 1964 Serpula contortuplicata Linnaeus, 1767: confused, in the sense as used by Lankester (1863) probably see S. vermicularis Serpula hartmanae Reish, 1968 Serpula sp. Serpula uncinata see Hydroides dianthus: Schenk 1875 Serpula vasifera Haswell, 1885 Serpula vermicularis Linnaeus, 1767; this name has been used for all larger representatives of the genus from all over the world. Recent work has shown that S. vermicularis sensu auctores is a complex of species (ten Hove & Jansen-Jacobs 1984, Kupriyanova 1999), and the species S. vermicularis sensu stricto most probably only occurs in the North Atlantic and Mediterranean (Pillai, pers. comm.) Serpula vermicularis see S. columbiana: Gray 1976, Young & Chia 1982, Paulay et al. 1985, Strathmann 1987 Serpula uschakovi Kupriyanova, 1999 Sphaeropomatus miamiensis Treadwell, 1934 see Ficopomatus miamiensis Spiraserpula snellii Pillai & ten Hove, 1984 Spirobranchus corniculatus (Grube, 1862) Spirobranchus corniculatus complex, essentially three morphologically close species occurring in the Indo-Pacific: S. corniculatus sensu stricto, S. cruciger and S. gaymardi (Quatrefages, 1865) Spirobranchus cruciger (Grube, 1862) Spirobranchus gardineri Pixell, 1913 Spirobranchus gaymardi (Quatrefages, 1865) Spirobranchus giganteus (Pallas, 1766); has long been regarded as a circumtropical species but was split by ten Hove (1970) into two, possibly three subspecies: S. giganteus giganteus from the Caribbean, S. g. corniculatus from the Indo-Pacific and possibly S. g. incrassatus (Krøyer) Mörch, 1863 from the tropical Pacific Americas. Recent work has shown that this was an over-simplification, and that ten Hove’s subspecies are species-complexes (see Fiege & ten Hove 1999 for a full survey). Where possible we attribute the literature records to their proper species, sometimes we have to refer to the next level, that of a geographically defined complex.

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Spirobranchus giganteus: see Spirobranchus corniculatus complex White 1976 Spirobranchus giganteus corniculatus: see Spirobranchus corniculatus complex Smith 1984a,b, Nishi 1992b Spirobranchus latiscapus (Marenzeller, 1885) Spirobranchus polycerus sensu stricto (Schmarda, 1861) Spirobranchus spinosus Moore, 1923, Californian representative of the S. giganteus complex Spirobranchus tetraceros (Schmarda, 1861) Spirobranchus tricornis Ehlers, 1887: see S. giganteus: Allen 1957 Vermiliopsis infundibulum (Philippi, 1844) see Vermiliopsis infundibulum-glandigera complex: Nishi 1993 Spirorbidae Bushiella (B.) abnormis (Bush, 1905) Bushiella (Jugaria) granulata (L., 1767) Bushiella (Jugaria) kofiadii (Rzhavsky, 1988) often recorded as “Spirorbis granulatus” Bushiella (Jugaria) quadrangularis (Stimpson, 1854) often recorded as “Spirorbis granulatus” Bushiella (Jugaria) similis (Bush, 1905) often recorded as “Spirorbis granulatus” Bushiella (Jugaria) atlantica (Knight-Jones, 1978) Bushiella sp. True species identity of some “Spirorbis granulatus” records cannot be recognised. It could be Bushiella (Jugaria) quadrangularis, Bushiella (Jugaria) similis, Bushiella (Jugaria) kofiadii, Bushiella (Jugaria) granulata sensu stricto or any other Bushiella species Circeis armoricana Saint-Joseph, 1894. Often recorded as “Spirorbis spirillum”. This species is found on algae, stones, crustaceans, and molluscs and is distinct from C. spirillum, which is found on hydrozoans and bryozoans. Circeis cf. armoricana most records of “Spirorbis spirillum” from algae, stones, crustaceans and mollusc shells apparently belong to Circeis armoricana. Circeis oshurkovi Rzhavsky, 1998 Circeis paguri Knight-Jones & Knight-Jones, 1977 Circeis spirillum (L., 1758). This species inhabits mostly branching bryozoans and hydrozoans, whereas most records from algae, stones, crustaceans and molluscs refer to Circeis armoricana. Dexiospira foraminosa see Neodexiospira foraminosa: Nishi & Yamasu 1992d Eulaeospira convexis (Wisely, 1963) Helicosiphon biscoeensis Gravier, 1907 Helicosiphon platyspira Knight-Jones, 1978 Janua (Dexiospira) alveolata see Neodexiospira alveolata: Rzhavsky & Britayev 1984 Janua (Dexiospira) brasiliensis see Neodexiospira brasiliensis: Nelson 1979, Kirchman et al. 1982a,b Janua (Dexiospira) formosa see Neodexiospira formosa: Knight-Jones 1972, Knight-Jones et al. 1974 Janua (Dexiospira) lamellosa see Neodexiospira lamellosa: Knight-Jones et al. 1974 Janua (Dexiospira) nipponica see Neodexiospira brasiliensis: Rzhavsky & Britayev 1984 Janua (Dexiospira) steuri see Neodexiospira steueri: Knight-Jones 1972; Knight-Jones et al. 1974 Janua (Fauveledora) kayi see Neodexiospira kayi: Knight-Jones 1972 Janua (Pillaiospira) trifurcata see Pillaiospira trifurcata: Knight-Jones 1973 Janua pagenstecheri (Quatrefages, 1865) Metalaeospira clasmani Vine, 1977 Metalaeospira pixelli (Harris, 1969) Metalaeospira tenuis Knight-Jones, 1973 Neodexiospira alveolata (Zachs, 1933) Neodexiospira brasiliensis (Grube, 1872) Neodexiospira foraminosa (Moore & Bush, 1904) Neodexiospira formosa (Bush, 1905) Neodexiospira kayi (Knight-Jones, 1972)

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Neodexiospira lamellosa (Lamarck, 1818) Neodexiospira pseudocorrugata (Bush, 1905) Neodexiospira sp. The material identified by Sveshnikov (1967) and Bagaveeva (1975) as “Spirorbis alveolatus” may belong to Neodexiospira alveolata or N. brasiliensis Neodexiospira steueri (Sterzinger, 1909) Nidificaria nidica (Knight-Jones, 1978) Paradexiospira (Spirorbides) vitrea (Fabricius, 1780) Paradexiospira nakamurai see Paradexiospira (Spirorbides) vitrea: Uchida 1971 Paralaeospira levinseni Caullery & Mesnil, 1897 Paralaeospira malardi Caullery & Mesnil, 1897 Paralaeospira parallela Vine, 1977 Pileaolaria spinifer Knight-Jones, 1978 Pileolaria (Duplicaria) zibrowii see Vinearia zibrowii: Knight-Jones 1978 Pileolaria (Jugaria) atlantica see Bushiella (Jugaria) atlantica: Knight-Jones 1978 Pileolaria (Nidularia) nidica see Nidificaria nidica: Knight-Jones 1978 Pileolaria (Nidularia) palliata see Nidificaria palliata: Knight-Jones 1978 Pileolaria (P.) granulata see Bushiella (Jugaria) granulata: Thorp 1975 Pileolaria berkeleyana (Rioja, 1942) sensu lato—This species currently considered as cosmopolitan, is probably a complex of sibling species that includes Pileolaria berkeleyana sensu stricto, Pileolaria rosepigmentata Uchida, 1971 and some others. This problem has been studied (Rzhavsky unpubl.) Pileolaria cf. militaris—The species of Pileolaria described by Salensky (1882) is probably Pileolaria militaris Pileolaria daijonesi Knight-Jones, 1972 Pileolaria dakarensis Knight-Jones, 1978 Pileolaria lateralis Knight-Jones, 1978 Pileolaria marginata Knight-Jones, 1978 Pileolaria militaris Claparède, 1868 Pileolaria moerchi (Levinsen, 1883) Pileolaria pseudoclavus Vine, 1972 Pileolaria pseudomilitaris, Pileolaria (Simplicaria) pseudomilitaris see Simplaria pseudomilitaris: Beckwitt 1982, Knight-Jones et al. 1974 Pileolaria rosepigmentata Uchida, 1971 is currently synonymised with Pileolaria berkeleyana (Rioja, 1942) by Thorp et al. 1986. However, the validity of this species is currently being re-examined (Rzhavsky unpubl.) Pileolaria sp. 1 (connexa) Rzhavsky & Knight-Jones, 2000 Pileolaria sp. 2 (invultuosa) Rzhavsky & Knight-Jones, 2000 Pileolaria sp. see Pileolaria cf. militaris: Salensky 1882 Pileolaria tiarata Knight-Jones, 1978 Pillaiospira trifurcata (Knight-Jones, 1973) Protolaeospira (Dextralia) stalagmia Knight-Jones & Walker, 1972 Protolaeospira (P.) canina see Protolaeospira (P.) tricostalis: Knight-Jones 1973 Protolaeospira (P.) pedalis Knight-Jones & Knight-Jones, 1994 Protolaeospira (P.) striata Quievreux, 1963 Protolaeospira (P.) tricostalis (Lamarck, 1818) Protolaeospira (P.) triflabellis Knight-Jones, 1973 Protolaeospira (P.) eximia (Bush, 1905) Protoleodora uschakovi Knight-Jones, 1984 Romanchella quadricostalis Knight-Jones, 1973 Romanchella scoresbyi (Harris, 1969) Romanchella solea Vine, 1977 Romanchella pustulata Knight-Jones, 1978

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Simplaria potswaldi (Knight-Jones, 1978) Simplaria pseudomilitaris (Thiriot-Quievreux, 1965) Spirorbis (S.) strigatus Knight-Jones, 1978 Spirorbis (S.) bifurcatus Knight-Jones, 1978 Spirorbis (S.) corallinae de Silva & Knight-Jones, 1962 see S. inornatus: Ryland 1972, Stebbing 1972. Since S. corallinae settle almost exclusively on calcareous alga Corallina officinalis, the above records of this species from Laminaria probably refer to Spirorbis inornatus. Spirorbis (S.) cuneatus Gee, 1964 Spirorbis (S.) infundibulum Harris & Knight-Jones, 1964 Spirorbis (S.) inornatus L’Hardy & Quievreux, 1962. This species is usually found on Laminaria Spirorbis (S.) rothlisbergi Knight-Jones, 1978 Spirorbis (S.) rupestris Gee & Knight-Jones, 1962 Spirorbis (S.) spatulatus Knight-Jones, 1978 Spirorbis (S.) spirorbis (L, 1758) is often recorded as S. borealis. All records of “spirorbis” or “borealis” from Fucus in the intertidal zone of the Atlantic and Arctic European coast certainly belong to S. (S.) spirorbis. Spirorbis (S.) tridentatus Levinsen, 1883. Some earlier workers considered “tridentatus” as an operculum-incubating variety of “Spirorbis granulatus”, but later the name started to refer to the tube-incubating form. Spirorbis (Spirorbella) marioni see Spirorbis (S.) rothlisbergi: Rothlisberg 1974 Spirorbis (Velorbis) gesae Knight-Jones & Knight-Jones, 1995 Spirorbis alveolatus see Neodexiospira sp.: Sveshnikov 1967, Bagaveeva 1975 Spirorbis ambilateralis see Protolaeospira (P.) eximia: Potswald 1967b. Spirorbis argutus see Neodexiospira cf. brasiliensis: Abe 1943. This species name is a nomen dubium that was assigned to one of Eulaeospira species. Spirorbis borealis or Spirorbis (Laeospira) borealis see Spirorbis (S.) spirorbis: Babbage & King 1970, Bergan 1953, Crisp & Ryland 1960, Dasgupta & Austin 1960, Doyle 1974, Fewkes 1885, Franzén 1956, 1970, Garbarini 1933, 1936a,b, Gee 1963a, 1964, 1965, 1967, Gee & Williams 1965, Knight-Jones 1951, 1953, King et al. 1969, Mackay & Doyle 1978, Meadows & Williams 1963, Nott 1973, Potswald 1969, 1972, de Silva 1962, 1967, Thorson 1946, Williams 1964, Wisely 1960 Spirorbis borealis var. tridentatus see Spirorbis (S.) tridentatus: Franzén 1956, 1970 Spirorbis convexis see Eulaeospira convexis: Wisely 1964 Spirorbis corrugatus see Neodexiospira pseudocorrugata: Casanova 1954, Vuillemin 1965, Ghobashy & Selim 1979b Spirorbis granulatus see Bushiella sp.: Bergan 1953, Franzén 1956, 1970 Spirorbis lamellosa see Neodexiospira lamellosa: Wisely 1964 Spirorbis malardi see Paralaeospira malardi: Quievreux 1962 Spirorbis militaris see Pileolaria militaris: Franzén 1958, 1970, Kiseleva 1957 Spirorbis moerchi, Spirorbis (Laeospira) moerchi see Simplaria potswaldi: Potswald 1964, 1966, 1967a,b, 1968, 1969, 1977, 1978, 1981. The taxonomic status of some similar species, including Pileolaria moerchi, Pileolaria berkeleyana, and Pileolaria rosepigmentata have been recently studied (Rzhavsky unpubl.) Spirorbis nipponicus see Neodexiospira alveolata: Okuda 1946. Neodexiospira brasiliensis or any other Neodexiospira species can be also mis-identified as “Spirorbis nipponicus” Spirorbis pagenstecheri, Spirorbis (Janua) pagenstecheri see Janua pagenstecheri: Bergan 1953, Dasgupta & Austin 1960, Franzén 1958, 1970, Gee & Williams 1965, de Silva 1967, Stagni 1959, 1961, Stebbing 1972 Spirorbis pusill/a(us) see Janua pagenstecheri: Kiseleva 1957, Hempelmann 1930 Spirorbis pusilloides see Janua pagenstecheri: Thorp & Segrove 1975 Spirorbis scoresbyi see Romanchella scoresbyi: Harris 1969

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Spirorbis spirillum, Spirorbis (Dexiospira) spirillum see Circeis spirillum: Potswald 1967b, see Circeis cf. armoricana: Bergan 1953, Dasgupta & Austin 1960, Dirnberger 1990, 1993, 1994, Okuda 1946, Potswald 1978, Sveshnikov 1967 Spirorbis vitreus or Spirorbis (Paradexiospira) vitreus see Paradexiospira (Spirorbides) vitrea: Bergan 1953, Franzén 1956, 1970, Potswald 1967b, 1978. Vinearia zibrowii (Knight-Jones, 1978)

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MOLLUSCS AS ARCHIVES OF ENVIRONMENTAL CHANGE C.A.RICHARDSON School of Ocean Sciences, University of Wales—Bangor, Menai Bridge, Anglesey, LL59 5EY e-mail: [email protected]

Abstract External surface rings, internal growth lines and microgrowth bands in bivalve shells have been used to estimate age and to investigate the effects of environmental factors such as seawater and air temperatures, spawning, the spring neap lunar cycle and anthropogenic disturbance. Life-history information, including longevity, hatching times and migration patterns have been obtained from growth patterns in the statoliths of gastropods and cephalopods. Ontogenetic changes in bivalve and gastropod shells and the skeletal parts of cephalopods have been revealed using stable oxygen and carbon isotopes and radioisotopes. These techniques have allowed the reconstruction of the physical and chemical environment of growth and estimates of the water depth in which these organisms were living, the temperature of the water which they inhabited, and the effect of upwelling and other perturbations on shell growth to be ascertained. Elemental records contained within the hard parts of molluscs can provide detailed information about the mechanisms and chemical environment of shell growth. Such information has been used to assess the effects of anthropogenic inputs into coastal waters with the considerable potential for reconstructing historical changes in the chemistry of the marine environment.

Introduction In 1975 and 1980 two major publications appeared which contributed considerably to our knowledge and understanding of the skeletal growth of aquatic organisms (Rosenberg & Runcorn 1975, Rhoads & Lutz 1980). Both recognised that invertebrate skeletons, particularly of molluscs, could provide a continuous record of growth and furnish life-history information as well as records of environmental change within the marine environment. Since the publication of those papers, further developments have occurred, most notably in chemical analytical techniques such as stable isotope and trace element chemistry. These developments have enabled both the mechanisms of growth line formation and skeletal deposition to be more fully understood and have assisted in unravelling the environmental conditions under which they were formed. With the arrival of a new millennium it is timely to review recent developments against a background of the previous 20 years of growth line research. This review is selective in its focus and concentrates on the literature relating to the skeletal and hard parts of the three major classes of molluscs, the Bivalvia, Gastropoda and Cephalopoda. The review considers how the skeletal parts of living molluscs and their fossil relatives can be studied to reveal an ontogenetic record of their life. Such information can provide details about the prevailing marine environment, as well as historical records of environmental and

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climatic change during the last century and past geological epochs, details that are difficult or impossible to obtain by other means.

Surface rings and internal shell growth patterns

Bivalves

Growth rings Traditionally growth rings or annuli on the shell surface have been employed as a means of establishing age in molluscs, e.g. cockles Cerastoderma edule (Craig & Hallam 1963, Farrow 1971, 1972, Boyden 1972, Jones 1979), hard-shelled clams Mercenaria mercenaria (Ansell et al. 1964, Coughlan & Holmes 1972), soft-shelled clams Mya arenaria (Feder & Paul 1974, MacDonald & Thomas 1980), scallops Placopecten magellanicus (Stevenson & Dickie 1954, Merrill et al. 1961, Ropes & Jearld 1987), Pecten maximus (Mason 1957), Chlamys opercularis (Taylor & Venn 1978), C. varia (Conan & Shafee 1978), mussels Mytilus edulis (Seed 1969), M. galloprovincialis (Hosomi 1983), Geukensia (=Modiolus) demissa (Dillwyn) (Brousseau 1984), Scrobicularia plana (Green 1957), Macoma balthica (Lammens 1967, Bachelet 1980) and Donax vittatus (Rámon et al. 1995). Surface rings represent annual periods of growth cessation and are associated generally with the colder (winter) months (Merrill et al. 1961, Farrow 1971, Jones 1979, Bachelet 1980, Richardson et al. 1980c) or warmer (summer) months of the year (e.g. Lammens 1967, Rámon et al. 1995). During these periods the shell-secreting mantle edges are withdrawn from the shell margins and shell deposition slows down or ceases. When conditions are again suitable for shell growth the mantle margins are extended so that old and new regions of the shell are no longer continuous and an obvious growth ring results. The rings can be enhanced by illuminating the inner shell surface with a bright light to produce a pattern of dark narrow rings, through which light cannot penetrate, alternating with wider white translucent areas in the shells, e.g. Mytilus galloprovincialis (Hosomi 1983) and Donax vittatus (Rámon et al. 1995). Annual invasions of boring organisms, which infest the upper shell valves of sea scallops Placopecten magellanicus (Merrill et al. 1961) aid in ring location, as the heaviest areas of infestation occur during the summer between the annual rings. Scallops from shallow water where seawater temperatures are low during the winter have more prominent growth rings than individuals from deeper water where temperatures vary less (Merrill et al. 1961). Ansell et al. (1964) showed that growth rings corresponded with age during the early life of Mercenaria mercenaria, although difficulty was encountered in identifying the first ring. Clams which settled late in the season over-wintered at a small size and often achieved considerable shell growth early in the following year, a factor that tended to push the ring onto the umbone where it was difficult to discern (Ansell et al. 1964, Coughlan & Holmes 1972). In older cockles, Cerastoderma edule and C. glaucum, the umbo of the shell may be worn and the ring laid down during the first winter may be obliterated (Boyden 1972). Also, shell deposition in C. edule may continue during the first winter, albeit at a slower rate than during the summer, owing to the partitioning of energy reserves for shell growth rather than for reproduction. Only in the second year of growth, when cockles become sexually mature, 104

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is energy diverted away from shell growth to reproduction and a prominent second growth ring is formed (Richardson et al. 1980c).

Disturbance rings The principal difficulty encountered in employing growth rings on shells to estimate their age and growth arises from an inability to distinguish between disturbance rings and those of annual origin. Disturbance rings are produced by various environmental irregularities such as storms, gales, spawning, displacement or anthropogenic disturbance. They are generally less prominent than annual rings and usually do not completely encircle the shell, tending to fade away at the posterior and anterior shell margins. In addition to the annual rings on Placopecten magellanicus, most shells displayed disturbance rings (Merrill et al. 1961). Scallops inhabiting shallow water possessed “shock rings” arising from disturbance during severe storms, whereas those from deeper water were probably caused by damage from fishing gears; lightly fished areas yielding unmarked scallops, while shells from heavily fished areas were a confusion of “shock rings” (Merrill et al. 1961). In Pecten maximus disturbance rings can be distinguished from annual rings (Mason 1957). The shell surface of P. maximus is covered with prominent striae and Mason (1957) observed that the annual growth rings (~<0.5 mm wide) were composed of less well defined and narrowly spaced striae (~50 µm apart). A disturbance ring is distinguished from an annual ring in that there are no small crowded striae and the striae on either side of the disturbance ring are equally spaced (Mason 1957). The problem of separating disturbance rings from growth rings has been tackled statistically by growth-ring analysis (Craig & Hallam 1963). Thus, upon the picture of annual rings are superimposed additional rings unrelated to the annual growth of the organism.

Growth ridges and spines Ridges and spines adorn the shell surface of several molluscs and these may aid in stabilising the organism within or on the sediment surface. Small striae cover the shell surface of adult and juvenile P. diegensis and Argopecten gibbus (Clark 1968, 1975), Pecten maximus (Antoine 1978) and Chlamys opercularis (Broom & Mason 1978, Gruffydd 1981) and small ridges are a characteristic of the surface of mussel, Mytilus edulis shells (Bérard et al. 1992). Clark (1968, 1975) suggested that the deposition of striae in Pecten diegensis and Argopecten gibbus maintained under different regimes of illumination and darkness were formed with a daily periodicity, even though his data suggested that the number of striae did not coincide exactly with the number of days over which the experiment was conducted. Similarly, Broom & Mason (1978) and Helm & Malouf (1983) suggested that striae deposition was a daily process in Chlamys opercularis and Argopecten irradians, respectively, but only when shell growth was rapid; during less favourable growing conditions few or no striae were deposited. Hurley et al. (1987) and Parsons et al. (1993) reported daily deposition of striae in both larval and juvenile Placopecten magellanicus, respectively, whereas Joll (1988) demonstrated a close correlation between the number of pigmented rings on the shell surface of tagged juvenile saucer scallops, Amusium balloti, and the number of days since release. Controlled laboratory experiments undertaken by Gruffydd (1981) refuted the idea of a daily periodicity of striae formation in Pecten maximus by demonstrating that formation in 105

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juveniles was controlled by water temperature, striae forming at less than half the rate at 10°C than at 14.5°C. Striae deposition also varied around the shell margin, with maximum numbers deposited along the anterior/posterior mid-line of the shell where growth rates were maximal. Inter-striae distance varies seasonally in P. maximus, with the deposition of widely spaced striae during the warmer summer months and narrowly spaced striae during the winter when seawater temperatures are at their lowest. The close spacing of the striae produces a surface ring (Dare 1991, Dare & Deith 1991). Variation in striae abundance across the shell surface is now routinely used to identify periods of slow shell growth and estimate the age of scallops (Dare 1991). By contrast, external ridge production in Mytilus edulis held in field and laboratory experiments was found to be independent of the environment; each mussel producing its own pattern of external ridges (Bérard et al. 1992.)

Growth lines The difficulties associated with distinguishing between disturbance rings and annual rings has been reduced considerably by analysing the patterns of microgrowth bands and growth lines present in the internal structure of many mollusc shells. To reveal these bands and lines the shell valves are either sectioned whole or embedded in resin and then sectioned from umbone to shell margin (Fig. 1A). The sectioned surfaces are ground on progressively

Figure 1 Diagrammatic representation of, A: the shell of Arctica islandica with prominent external surface growth rings, X-Y line of cross section, B: radial shell section taken along axis X-Y to reveal the internal annual growth lines (L) in the outer shell layers and umbone (U). Position of drilled spot samples (S) and trough samples (T) removed for stable isotope analysis, R; surface growth rings, C: inner surface of a scallop, Pecten maximus shell to show the position of the ligament scar (LS) and adductor muscle scar (AMS) and, D: growth lines (L) on the inner surface of the ligament scar. Scale bars=1 cm.

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finer abrasive papers or powders, polished with diamond paste or metal polish (e.g. Brasso), and the surfaces etched with acids for various periods of time (e.g. 15–30min in 0.01M HCl, 0.1M EDTA or the formic based decalcifying agent “Decal”) (see Rosenberg & Runcorn 1975, Richardson et al. 1979, 1980c, Rhoads & Lutz 1980, Ropes 1987, Ropes & Jearld 1987, Richardson 1988b, 1989). The period exposed to the etching reagent is critical, for example 3 min in 0.1M HCl for the umbones of Glycymeris glycymeris (Ramsay et al. 2000) and 30 min etch in 0.01M HCl for the prismatic layer of Mytilus edulis (Richardson 1989). The cut surfaces are either viewed directly, or more commonly acetate peel replicas (referred to as peels) of the polished and etched shell sections are prepared (see Richardson et al. 1979, Rhoads & Lutz 1980). Different regions of the shell have been examined in the light microscope to study the position of the internal growth lines and bands, including the resilium of the ligament (Figs 1C and 2A), the chondrophore or umbone (referred to as umbone) (Figs 1B, 2B, C), the inner nacreous shell layer (Fig. 2D) and the middle homogeneous and outer shell layers (Fig. 2E, F) (for shell structures of the different bivalve genera see Taylor et al. 1969, 1973). Examination of Pecten maximus shell sections under cathodoluminescence provides a novel alternative method for studying the position of the internal growth lines. Narrow lines are marked by orange luminescent stripes whereas the rest of the shell has a weak blue luminescence (Barbin et al. 1991). Various terms have been used to describe the observed patterns in the bivalve shell. In Spisula solidissima and Arctica islandica an alteration of two repeating growth layers (laminations or increments) occurs (Jones et al. 1978, Thompson et al. 1980). The relatively thin, dark laminations have been termed “growth lines” while the wider bands between have been termed “growth bands”. According to Jones (1980) this choice of terminology is inappropriate because the alternating structures are microstructurally distinct, neither increment formed in a short period of time as the term “growth line” implies and the term “growth line” could be confused with the thin small-scale growth lines of other workers. These growth lines, described by among others Pannella & MacClintock (1968) and Rhoads & Pannella (1970), were termed growth bands by Richardson et al. (1979, 1980a). Descriptive terms for the two types of increments such as wide and narrow or light and dark are also unsuitable (Jones 1980). The wide growth increments thin progressively throughout ontogeny so that in later life there is often no width distinction between the two growth increments. Also, the increment that appears dark in the cut and polished shell section is actually translucent in thin section (compare Fig. 3B, C) so that when peels are being investigated the descriptions are reversed (Jones 1980). To avoid ambiguity in this review, the following terminology is used to describe the growth patterns observed in peels of shell sections. Growth band refers to the small-scale (daily, tidal and sub-daily) patterns and growth increment, the distance separating adjacent growth bands (Fig. 3C). Growth line refers to an annually deposited line and annual increment the distance separating adjacent growth lines (Fig. 3D, E). A disturbance line is formed as a result of a perturbation in shell growth (Fig. 3F). Confirmation that the growth lines are formed annually has been demonstrated in bivalves using mark-recapture experiments (Peterson et al. 1983, 1985, Ropes et al. 1983, Ropes 1986, Richardson & Walker 1991). In several bivalve species growth line formation in the outer shell layers has been attributed to low winter seawater temperatures, e.g. Modiolus modiolus (Anwar et al. 1990), Arctica islandica (Jones 1980, Weidman & Jones 1994), Mercenaria mercenaria (Grizzle & Lutz 1988, Richardson & Walker 1991), Mya arenaria 107

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Figure 2 Photomicrographs of acetate peel replicas of shell sections of, A: Ostrea edulis ligament scar, R; resilium, arrows indicate positions of annual growth lines; B and C: umbones of Modiolus modiolus and Glycymeris glycymeris, respectively, to show the annual growth lines (arrows); D: inner nacreous layer of Modiolus modiolus and annual growth lines (arrows); E: strongly defined growth bands (arrows) alternating with weakly defined bands in the crossed lamellar layer of Cerastoderma edule; F: weakly defined endogenous bands in the prismatic layer of Tapes philippinarum. Scale bars=100 µm except D and E where scale bars=0.5 mm.

(MacDonald & Thomas 1980); to maximum summer sea temperatures, e.g. Callista chione (Linnaeus, 1758) from the Adriatic (Hall et al. 1974); to declining water temperatures in the summer late-fall in Mercenaria mercenaria (Peterson et al. 1983) and to late spring in the inner nacreous layer of Mytilus edulis (Lutz 1976). Growth lines in Geukensia demissa (Brousseau 1984), Mya arenaria (MacDonald & Thomas 1980) and Crenomytilus grayanus (Zolotarev 1974) have generally proved to be more sensitive age indicators than the surface growth rings. The number of internal lines in Arctica islandica apparently correlate in number and position with the external growth rings (Murawski et al. 1982). 108

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Figure 3 Photomicrographs of acetate peel replicas of shell sections of, A: Pecten maximus with surface striae (S). B: thin section of Cerastoderma edule; B, growth band, I, growth increment. C: Cerastoderma edule; B, growth band, I, Growth increment. D: Mercenaria mercenaria to show a growth line (arrow) in the prismatic shell layer. E: Glycymeris glycymeris, two growth lines are arrowed. F: Ensis ensis shell break resulting from a disturbance to shell growth. Scale bars in B, C and D=100 µm those in A, E and F=0.5 mm.

The season of growth line formation also varies with latitude. Near the northern limit of the geographic range of the Californian surf clam, Tivela stultorum, (Mawe, 1823), growth lines are deposited in November, whereas at the southern most limit deposition is in January or February (Hall et al. 1974, Hall 1975). In Mercenaria mercenaria from the east coast of North America growth lines are produced in winter in northern populations (Kennish & Olsson 1975, Kennish 1980, Jones et al. 1989, 1990, Jones & Quitmyer 1996) and during the summer in southern populations (Jones et al. 1990, Jones & Quitmyer 1996). This observed dichotomy in the season of growth line formation in modern Mercenaria mercenaria would make it difficult to ascertain the season in which growth line deposition occurred in 109

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fossil material without the use of other methods of analysis such as stable isotopes for reconstructing the temperature at the time of growth line deposition (p. 133). Latitudinal variations have been observed in the clarity of the growth lines in Phacosoma japonicum (Tanabe & Oba 1988). Lutz (1976) and Lutz & Rhoads (1977) demonstrated in mussels a seasonal alternation of wide increments of nacre with narrower prismatic and homogeneous structures. Nacre deposition occurred during the warmer months of the year (April to November) and was often interrupted during the hottest months (mid to late summer) by the deposition of irregular prismatic structures. With increasing age the percentage of nacre within a given region of the sectioned inner shell layer generally decreased and often only two types of sub-layer (nacre and irregular prismatic, plus homogeneous) were observed in the outer (older) regions of the shell sections. Lutz & Castagna (1980) noticed almost identical patterns of seasonality in the growth of the inner layer in four geographically separated populations of Geukensia demissa. However, dissimilarities in the structural patterns in the inner shell layer exist between the northern (Gulf of Maine, USA) and southern (Virginia and Maryland, USA) populations. Structural changes took place (mid to late summer) in shells from Virginia and Maryland which did not appear in those from the Gulf of Maine (Lutz & Rhoads 1977). Further work on geographically separated populations of G. demissa led Lutz & Clark (1984) to propose that the percentage area of the various microstructures in the inner nacreous layer might prove useful in predicting mean annual seawater temperature; information that could be useful in temporal temperature gradient reconstruction in fossil and modern mussel shell material. Growth lines are formed seasonally on the resilium of the ligament of the scallops Placopecten magellanicus (Merrill et al. 1961) and the oysters Ostrea edulis (Richardson et al. 1993a) (Figs 1D and 2A), Tiostrea edulis (Richardson et al. 1993b) and Crassostrea gigas (Kirby et al. 1998). As new material is deposited along the shell margins, material is also added to the ligament. When shell growth slows or ceases, ligament growth also slows or ceases, producing a line. These lines can be counted and used to estimate the age of scallops or oysters, particularly where there are no clearly obvious surface rings. An added advantage is that the resilium and the epithelial cells which produce it are protected within the shell valves and are less exposed to shock and injury than the shell margins and epithelial cells of the mantle. Umbone lines have been used to estimate the age of several bivalve species, including Mya arenaria (MacDonald & Thomas 1980, Ropes & Crawford 1986, Brousseau & Baglivo 1987), M. truncata (Ropes & Crawford 1986), Glycymeris glycymeris (Ramsay et al. 2000) (Fig. 2C), Lithophaga lithophaga (Galinou-Mitsoudi & Sinis 1995), Arctica islandica (Witbaard & Duineveld 1990), the hiatellid clam Panopea zelandica (Breen et al. 1991) and the geoducks (=geoducs) Panope generosa (Shaul & Goodwin 1982, Breen & Shields 1983, Harbo et al. 1983) and P. abrupta (Sloan & Robinson 1984). While growth line formation in many shallow-water temperate bivalve species reflects periods of little or no growth and has been attributed to seasonal variations in seawater temperature, this is not the case for all species. Notable in this respect are the Atlantic surf clam Spisula solidissima Dillwyn and ocean quahog Arctica islandica from Virginia, America which deposit a growth line annually in the summer and fall (July and September) and in the fall to early winter (September to November), respectively, corresponding to the spawning phase in the reproductive cycle (Jones et al. 1978, Jones 1980). It is believed that the stress of spawning may be sufficient to cause a cessation of shell deposition for a short period as energy is channelled towards the production of eggs and sperm, and this results in the formation of an internal growth line. A correlation between the spawning cycle and growth 110

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line formation in Spisula sachalinensis (Kato & Hamai 1975) and Phacosoma japonicum (Tanabe 1987) has been suggested. Growth line formation in Arctica islandica (Turekian et al. 1982) and Astarte elliptica (Brown) (Trutschler & Samtleben 1988) is apparently coincidental with the seasonal minima in food supply and may simply reflect slow growth due to nutritional deficiency. Lines in shells of the wood-associated deep-sea bivalve Idas argentus from depths of 3600 m in the western Atlantic, south of New England, USA (Dean 1993) and in Yoldia thraciaeformis from a submarine canyon (895–1500 m) off the southeastern Grand Banks of Newfoundland (Gilkinson et al. 1986) may not be seasonally produced. In the deep sea, both temperature and salinity vary little and in these species probably play only a marginal role in controlling shell growth. It is more likely that the growth lines form in response to seasonal fluctuations in food supply or as a marker for spawning (Gilkinson et al. 1986).

Disturbances to shell growth In addition to the annual winter checks in shell growth, irregular growth breaks occur, in which shell deposition is interrupted for a period of one to several days, and reflects periods of environmental and/or physiological stress. In Mercenaria mercenaria, growth breaks may be caused by winter freeze shocks (Pannella & MacClintock 1968, Cunliffe & Kennish 1974), summer heat shocks (Kennish 1980), thermal shocks (Cuniliffe & Kennish 1974, Kennish 1980), shell margin abrasions and storms (Cunliffe & Kennish 1974, Kennish 1980) and spawning breaks (Pannella & MacClintock 1968, Kennish 1980). Apparently spawning breaks in M. mercenaria can be distinguished from other types of growth breaks by the characteristic microstructure pattern in the outer shell layer which appears annually after the onset of sexual maturity (Pannella & MacClintock 1968, Kennish 1980). M. mercenaria from the east coast of North America occasionally produce more than two spawning breaks per year, with male clams typically displaying more spawning breaks than females. Similar spawning breaks have been observed in the shells of Phacosoma japonicum from Japan. When P. japonicum reaches sexual maturity in the third year, growth increment formation ceases suddenly just before spawning, and after spawning the growth increments gradually increase in width as growth recovers (Sato 1995). This temporary cessation in shell growth produces an annual spawning break. The occurrence of these breaks in the shells of Mercenaria mercenaria and Phacosoma japonicum could be useful for sex determination and reconstructing sexual maturity patterns of living and fossil bivalves (Sato 1995). However, such an interpretation would require that spawning breaks could be identified with some certainty from those caused by other environmental perturbations.

Storms, fishing, temperature and other effects Apparently shell breaks caused by storms have different characteristics depending on the severity of the storm and the depth of water inhabited by the bivalves. Cunliffe & Kennish (1974) interpreted shell breaks, as storm breaks, in Mercenaria mercenaria and Mya arenaria, in which silt was trapped within deep indentations extending through the outer shell layer into the middle layer. During storms, silt can become trapped between the shell secreting mantle epithelium and the shell margin giving rise to a shell break. However, in the absence 111

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of records of storm frequency, only circumstantial evidence is available to support the observation that growth breaks in these two species are the direct result of damage and storm disturbance, particularly since growth breaks of essentially similar description have been reported in razor clams, Ensis siliqua, from Portuguese coastal waters, which are subject to impact from benthic fishing gears (Gaspar et al. 1994), and in E. arcuatus disturbed by suction dredging in waters off the Orkney Islands, Scotland (Robinson & Richardson 1998). Growth breaks were rarely observed in shells from unfished areas. Razor clams damaged on capture, but not retained by fishing gears, escape and repair their shell valves. During the process of shell repair, sand particles become trapped at the posterior shell valve margins between the old and newly accreting shell (Fig. 4A). The frequency of damage (scarring) to the posterior ventral shell margins of Arctica islandica, collected from the southeastern North Sea, is believed to be related to the intensity of the bottom trawl fishery operating in the area (Witbaard & Klein 1994). Intensity of fishing activity and scar frequency are correlated in Glycymeris glycymeris from the coastal waters off the Isle of Man, UK (Ramsay et al. 2000). Anthropogenic activity may also affect the shell deposition process in other ways. Mercenaria mercenaria collected within a mile of Oyster Creek, Barnegat Bay, USA, displayed more shell breaks and slower summer growth than clams collected from nearby coastal waters (Cunliffe & Kennish 1974). These breaks were caused by changes in seawater

Figure 4 Photomicrographs of acetate peel replicas of shell sections of A: Ensis siliqua shell breaks caused by fishing disturbance, note the sand grains embedded in the break (arrows); B: Mytilus edulis growth band (arrow) caused by exposure to chlorination; C: Anadara granosa disturbance growth lines (arrows) formed as a result of exposure to low salinity sea water and D: tidal bands (arrows) in Cellana toreuma. The outer shell layer has been affected by boring organisms. Scale bars=100 µm except A, where scale bar=0.5 mm.

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temperature associated with the discharge of heated effluent from the local Oyster Creek nuclear power plant. Many of the breaks occurred concurrently with rapidly decreasing or increasing temperatures associated, respectively, with abrupt power plant shutdowns or the abrupt renewal of power plant operations (Kennish 1976, 1978, 1980). Chemicals in thermal effluents similarly affect shell growth in Mytilus edulis. Annual interruptions to growth occur in mussels occupying the water intake culverts of the Wylfa nuclear power station, North Wales (Thompson et al. 1997, 2000). During the summer (May to November) the sea water entering the power plant is chlorinated to discourage mussel settlement. However, some mussels successfully settle, survive and grow in these conditions, and leave evidence of their exposure to the chlorination in the form of prominent growth lines within the shell (Fig. 4B). The formation of growth lines in the shell of the blood cockle Anadara granosa (Fig. 4C) has been related to the seasonal deluge of monsoon rain into the coastal waters off Penang, Malaysia (Richardson 1987b). Other naturally ocurring events during a bivalves’ life affect shell growth. For example in the laboratory, the growth of Glycymeris glycymeris, a robust and heavy shelled bivalve, when excavated from the sediment and interfered with by the predatory crab Cancer pagurus, is temporarily interrupted with the formation of a weak growth line and small depression in the shell surface (Ramsay & Richardson unpubl. obs.). A bivalves’ natural burrowing movements in and around the sediment surface have been shown to damage and chip the shell edge, e.g. Ensis siliqua, Lutraria lutraria and Mya arenaria (Checa 1993). It may, therefore, be difficult in some species to distinguish between growth lines formed in the shell as a result of predator interference and those arising from the natural movements of the organism. In thin shelled bivalves, shell breaks arising from damage from fishing gears are likely to be more pronounced than those caused by predatory crabs, which in turn may be more obvious than growth breaks caused by other perturbations in the organisms’ environment. In species which deposit tidal growth bands (see below), it may be possible to determine different types of disturbance from the spacings of the bands and from the degree of interruption to the banding. At present, seasonal changes in growth can be distinguished from disturbance events by changes in the width of the growth increments. Seasonal changes in growth are reflected in a gradual narrowing of the increments, a period of almost no shell deposition, followed by a widening of the growth increments. Disturbance events interrupt the normal pattern of growth increment deposition and are followed by a period of recovery in which narrow increments are deposited. Cockles interfered with by crabs leave evidence of the attack in the form of a disturbance to the normal pattern of growth increment formation (Richardson et al. 1980b). Similarly, cockles exposed to chlorination show disruption to the normal pattern of tidal increments deposited in the shell (Thompson & Richardson 1993). At present it is not possible to ascertain from the banding patterns which environmental factor is responsible for the formation of the different types of growth breaks, although in the future, using carefully controlled field and laboratory experiments, it may be possible to identify with some certainty between growth breaks arising from predator attacks, fishing disturbance and the bivalves’ own natural activities.

Applications of the patterns Using estimates of a bivalves age obtained from counting the growth lines, growth curves for a range of species have been constructed including Modiolus modiolus (Anwar et al. 113

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Figure 5 Age distribution of a sample of Mercenaria mercenaria from Southampton water, UK. Above average recruitment occurred in 1969, 1976, 1977 and 1984 when exceptionally warm summer sea surface temperatures coincided with below average freshwater flow into Southampton Water.

1990), Mercenaria mercenaria (Jones et al. 1989, Richardson & Walker 1991), Mytilus edulis (Richardson et al. 1990), Spisula solidissima (Jones et al. 1978, Jones 1980) and Arctica islandica (Witbaard & Duineveld 1990). From a knowledge of the bivalves’ age and date of death, a histogram of the frequency of individuals spawned each year can be constructed. Jones (1981) found that recruitment of Spisula solidissima was episodic and occurred in years when shell growth was good and the sea surface temperature (SST) was below average. Richardson & Walker (1991), using a similar approach, demonstrated above average recruitment of Mercenaria mercenaria, an introduced species into Southampton Water, UK, when exceptionally warm summer SST coincided with below average freshwater flow into Southampton Water (Fig. 5). Using a standardisation analysis similar to that applied to tree ring widths, Jones (1981) investigated the variation in width of the annual increments in a sample of ~300 Spisula solidissima and showed an inverse correlation between growth and mean annual SST with better growth during cooler years. By contrast a 26-yr growth chronology, based on 100 Mercenaria mercenaria, demonstrated a significant correlation between the yearly standard growth index and SST (Jones et al. 1989). Long-term growth record in Arctica islandica from the Fladen Ground (northern North Sea), indicate that the growth of some individuals, aged ~100 yr or more, have been influenced by periodic incursions of Atlantic water into the area (Witbaard 1996, Witbaard et al. 1997). Differences in the annual growth rates are somehow influenced by changes in sedimentation rates and accumulation of organic matter transported by a system of eddies. Unlike Jones’ (1981) study of Spisula solidissima, no significant correlation between shell growth and local bottom water temperature was found in Arctica islandica. The observed systematic variation in the size of the annual increments illustrates the considerable potential for reconstructing the marine climate record from bivalve shells. Caution, however, is needed when making generalisations regarding the relationship between temperature and growth in bivalves from coastal waters, because growth of Spisula solidissima was inversely correlated with temperature whereas growth in Mercenaria mercenaria was positively correlated and no correlation was observed in Arctica islandica. 114

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Both studies are exciting developments in growth-line research, as the potential now exists for investigating long-term trends in the environment from the growth record. With suitable material from museum collections and archaeological deposits and with the application of appropriate statistical analyses, it is conceivable that a longer record of environmental change could be extracted from some of the longer-lived bivalves. If annual shell growth rates are related to SST in bivalves, as Jones (1981) has demonstrated in Spisula solidissima, then it would be feasible to construct long-term chronologies (500–1000 yr) of variations in growth from the increment record. Combined with stable isotopic records as proxies for seawater temperature and elemental analyses (see below), the shells of Arctica islandica could be used as the “tree of the sea”, a phrase suggested by Witbaard (1997), and like terrestrial tree records the incremental records in bivalves could be used to reveal long-term changes in the marine climate. Another aspect of shell growth in Mercenaria mercenaria, seen in peels of shell sections, is evidence of three stages of growth—youth, maturity and old age (Cunliffe & Kennish 1974). As juveniles (~1–2 yr), clams grow small concentric ridges on their outer surface, which apparently aid in anchoring them in the substratum and protect them from being washed out by currents and storms. In this stage the growth increments have shapes that tend to terminate perpendicular to the shells outer surface. When maturity has been reached, lasting 5–8 yr, the surface becomes characteristically smooth without concentric ridges and the internal growth increments are no longer recurved. In old age the inner crossed lamellar layer replaces the outer prismatic structure, the increments become thin, breaks in shell growth become more frequent and the shapes of the increments become perpendicular to the outer surface. However, under appropriate conditions, clams in old age can be induced, by transplantation into more favourable conditions, to grow their shell in a similar way to that which they did during maturity (Cunliffe & Kennish 1974, Kennish 1980).

Microgrowth patterns Daily and tidal growth bands Barker (1964) described a hierarchy of five cyclic groupings of growth bands and growth increments in the shells of several bivalves. He suggested, without experimental evidence, that the bands and increments reflected the annual changes in temperature and salinity (first order), equinoctial storms and tides (second order), the fortnightly tidal cycle (third order), day and night cycles (fourth order) and daily tidal rhythms (fifth order). Pannella & MacClintock (1968) and Rhoads & Pannella (1970) ascribed the patterns of growth bands and increments in the shells of experimentally marked M. mercenaria transplanted into the natural environment for periods of 1 yr and 2 yr, to a daily deposition. A similar conclusion was reached independently by House & Farrow (1968) and Farrow (1971, 1972) who described daily bands in the shell of the intertidal bivalve Cardium (=Cerastoderma) edule. Deposition of the growth increment occurred during the day while the growth band was laid down at night. Whyte (1975) claimed the reverse. Supposed daily banding has been observed in the rock boring clam Penitella penita with morphologically distinct increments deposited during periods of quiescence and growth alternating with increments produced during periods of active boring (Evans & LeMessurier 1972). A daily periodicity of increment and band deposition in intertidal species, whose behaviour and physiology are controlled by the ebb and flow of the tide seemed an unlikely interpretation. Richardson et al. (1979, 1980b, 1981) resolved the question of the periodicity of the patterns in Cerastoderma edule using experimentally marked cockles transplanted 115

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into the natural environment at different tidal elevations, or held under different conditions of illumination or continuous darkness in simulated tidal conditions in the laboratory. Cockles were date-marked using cold-shock treatment, a method designed to interrupt temporarily shell formation and provide an internal mark to which all subsequent shell growth could be related. Marked cockles were transplanted into the natural environment for periods up to 2 months or into laboratory tanks where they received a microalgal food supply and were subjected to a simulated semi-diurnal cycle of immersion and emersion. In cockles (Richardson et al. 1979, 1980b), intertidal clams, e.g. Tapes phillipinarum (Richardson 1988b) and mussels Mytilus edulis (Richardson 1989) the bands and increments are deposited with a tidal periodicity and independently of the imposed light or dark regime. The bands are laid down during emersion, whereas the increments are deposited during immersion when the animals are actively feeding (Richardson et al. 1981). A tidal periodicity of band formation in intertidal bivalves is now widely accepted (Richardson 1990), although the case for daily or tidal band formation in species growing subtidally has still not been fully resolved. Tidal currents operate in shallow coastal subtidal habitats and many bivalves are buried below the sediment surface in turbid waters where they would not normally experience diurnal patterns of illumination. Daily increments arising from diurnal changes may be deposited in Mercenaria mercenaria (Pannella & MacClintock 1968, Rhoads & Pannella 1970), although in several species held continuously immersed, the bands reflect an endogenous (innate) rhythm of shell deposition. Richardson et al. (1979) held cockles in a raft box in the Menai Strait, North Wales, under continuous immersion and exposed them to submarine daylight or continuous darkness and showed that the banding was weaker in definition compared with intertidal individuals. Similar weakly defined bands were formed in the shells of intertidal species, e.g. mussels (Richardson 1989) and clams (Richardson 1987a, 1988b) (Fig. 2F, p. 108 held continuously immersed in the natural environment or under controlled laboratory conditions of water flow, food supply and illumination or darkness. Deposition of weak bands was related to the total linear increase in shell length and not to the number of days the animals were held in their environments; slow growing shells deposited fewer bands than faster growing shells during the same time period (Fig. 6).

Figure 6 Relationship between the number of weak endogenous growth bands and shell growth in continuously immersed Mytilus edulis (䉱) and Tapes philippinarum (䊉). (Redrawn from Richardson 1988b, 1989.)

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Seasonal patterns Seasonal shell growth has been studied from the patterns of growth increments and bands in Mytilus edulis (Richardson et al. 1990), M. trossulus (Richardson unpubl.), Cerastoderma edule (Farrow 1971, 1972, Richardson et al. 1980c), Mercenaria mercenaria (Barker 1964, Pannella & MacClintock 1968, Rhoads & Pannella 1970, Kennish & Olsson 1975, Kennish 1980, Fritz & Haven 1983, Peterson et al. 1983, 1985, Grizzle & Lutz 1988), Ensis ensis and E. siliqua (Henderson & Richardson 1994), Chamelea gallina (Rámon & Richardson 1992), Donax vittatus (Rámon et al. 1995), Anadara granosa (Richardson 1987b) and Phacosoma japonicum (Sato 1995). A winter period of growth cessation is usually preceded by a gradual narrowing of the growth increments, whereas during the winter narrow growth increments may coalesce to form a distinct internal growth line and an associated surface growth ring. In the spring the growth

Figure 7 Photomicrographs of acetate peel replicas of shell sections of A, Cerastoderma edule and B, Mytilus edulis to show the deposition of narrow increments during the winter (open arrows) and wide increments in late summer (filled arrows). Scale bars=100 µm. (From Richardson et al. 1990: fig. B).

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increments gradually increase in width (Fig. 7). From a comparison of the width of the growth increments in Cerastoderma edule from North Wales with the SST, Richardson et al. (1980c) observed that shell growth was not directly correlated with temperature; shell deposition continued after water temperatures began to decline (September to November) and did not begin during the spring (March-April) until after temperatures had begun to increase. Similarly shell growth (daily banding) in C. edule from South Wales did not correlate directly with seawater temperature and it was speculated that breaks in growth were associated with frosts (Farrow 1971). The winter break in C. edule and the sharpness of its incision into the shell profile was observed to be more acute in cockles collected from higher shore levels. A greater prominence of crossed-lamellar structure in the outer shell layer was associated with the winter reduction in shell growth rate; lamellae in this shell structure become markedly deflected during the winter growth stoppage (Farrow 1972). Intertidal C. edule from Norway only grow for 5–6 months of the year during the summer when SST are suitable for shell growth. During the remainder of the year little or no shell growth occurs at temperatures close to freezing point, at a time when food availability is low, and a marked break in shell growth results (Richardson et al. 1980c). Differences in the definition of the winter growth cessation and the change in direction of the lamellae in the crossed lamellar layer of the shell, could be applied to cockles obtained from the fossil record to determine the conditions of growth in past littoral environments. Air temperatures The width and definition of the deposited tidal bands in cockles has been attributed to the temperature at the time of emersion (Richardson et al. 1981). In North Wales, maximum low waters of spring tides occur approximately twice a day, (semi-diurnal tidal regime), during the late afternoon and early morning, whereas neap tide low waters occur around midnight and midday. Using cold-shock marked cockles, Richardson et al. (1981) demonstrated that deposition of the wider and more strongly defined bands occurred during the late afternoon low tide and coincided with maximum air temperatures. The weakly defined bands formed during emersion in the cool of the early morning. Thus during spring tides a pronounced pattern of wider strong dark and weak tidal bands, alternates with a more uniform weaker defined pattern of banding during neap low tides (Fig. 2E, p. 108 and Fig. 8A). The relationship between air temperature and growth band definition has been confirmed in laboratory experiments. Cockles exposed to experimentally heated air (21–24.5°C) and ambient air temperatures (16°C) during alternate simulated low tides, laid down wider and more strongly defined bands during the heated periods of simulated low water (Richardson et al. 1981). Using experimentally marked Mytilus edulis chilensis transplanted onto the shore at Camilla Creek, in the Falklands, Gray (1997) and Seed et al. (2000) compared the tidal growth band record with in situ hourly records of seawater and air temperatures. These investigators demonstrated that during spring low tide emersion an unusually distinct growth band was laid down in the shell coincidental with an anomalously high air temperature. If the width and definition of the growth bands could be calibrated with air temperatures (band thermometry), then the possibility exists for reconstructing air temperature records in intertidal species where air temperatures are unknown. Tidal regime The amplitude and form of the tidal regime has been shown to influence the definition and width of the bands deposited in cockle shells. Cockles Clinocardium nuttalli, growing at low water along the coast of Oregon, USA, are exposed to a mixed diurnal/ 118

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Figure 8 Photomicrographs of acetate peel replicas of shell sections of Cerastoderma edule. A: from low water of spring tides to show the alternation of banding during spring tides (S) and deposition of weaker bands during neap tides (N). Scale bar=500 µm. B: from high water of neap tides to show widely spaced increments are formed during spring tides (S) and narrow increments are deposited during neap tides (N). Scale bar=100 µm. (From Richardson et al. 1979: fig. A, Richardson 1993: fig. B.)

semi-diurnal tidal regime. During neap tides they experience bi-daily emersion, which results in a semi-diurnal banding pattern, and daily emersion during spring tides, with the formation of a diurnal band pattern (Evans 1972, 1975). During spring tides a weakly defined band is also laid down between each emersion band even though the cockles remain continuously immersed. Band deposition in bivalves from North Wales is influenced by the prevailing semi-diurnal tidal regime such that during low waters of spring tides cockles from low water are emersed twice daily but remain continuously immersed during neap tides. This results in a pronounced spring neap lunar pattern in band strength, with alternate groups of clearly defined bands laid down at spring low tides and weakly defined bands deposited during neap tides in Cerastoderma edule (Richardson et al. 1980b) (Fig. 8A), Mytilus edulis (Richardson 1989), Tapes phillipinarum (Richardson 1987a) and Spisula subtruncata (Richardson 1988a). The reverse occurs in cockles inhabiting the higher shore levels where narrow increments and stongly defined bands are deposited during neap tides and widely spaced increments are formed at spring tides (Fig. 8B). Ohno (1985) observed a pattern of banding in the shells of Fragum unedo from low water around Ishigaki Island, Japan, where the prevailing mixed semi-diurnal tidal regime, consists of a daily tidal pattern of two high tides and two low tides of unequal amplitude. Bivalves were emersed daily during low tide of spring tides with the formation of daily bands, while weak bands were deposited during neap tides when they remained continuously 119

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immersed. The influence of the mixed semi-diurnal tidal regime was not, however, apparent in shells of the blood cockle Anadara granosa (Richardson 1987b). Differences in the strength of the bands in relation to tidal elevation and to the characteristics of the tidal regime could be used to interpret the tidal conditions prevailing in ancient coastal waters. Pannella (1976) has demonstrated that suitably preserved fossil bivalve shells may be used to reconstruct the tidal regime of past oceans (see also Ohno 1989). Evidence from experimentally marked and transplanted cockles (Richardson et al. 1980b) and mussels (Richardson 1989, Gray 1997) indicates that it is feasible to determine both the organisms elevation on the shore and the prevailing tidal regime from the shell banding patterns. Spring neap lunar cycles The measurement of incremental growth in intertidal and subtidal bivalve shells provides the opportunity for investigating small-scale, tidal or daily changes in shell growth in response to environmental factors. The width of the increments in the shells of subtidal and intertidal bivalves has been shown to vary during the spring neap lunar tidal cycle (Pannella & MacClintock 1968, Rhoads & Pannella 1970, Farrow 1971, Rosenberg & Runcorn 1975, Rhoads & Lutz 1980). Richardson et al. (1980b) analysed the variation in increment width in intertidal Cerastoderma edule from North Wales over consecutive spring neap lunar tidal cycles. Cockles from high water of neap tides grew significantly more during spring high tides when they were immersed, and thus able to feed for longer periods, than during neap tides when they were infrequently immersed during high tide. The reverse occurred in cockles from low water of spring tides where they grew significantly faster during neap tides when they were continuously immersed. During spring tides, cockles are emersed twice daily and thus the period available for feeding during immersion is shorter than when continuously immersed during neap tides. Cockles from mean tidal level on the shore, where there is no difference between the proportion of time emersed and immersed between neap tides and spring tides, however, showed a significant (5%) increase in shell growth during spring tides over neap tides. This small, yet significant enhancement in shell growth during spring tides was attributed to an increase in water flow across the shore and increased suspension of particles between neaps and spring tides (Richardson et al. 1980b). Ohno (1983) and Lønne & Gray (1988) similarly noted the influence of tidal level in determining the width of the growth increments in C. edule. On the wave-swept rocky intertidal low shore terraces of LaDesombocadura, Concepcion, Chile, growth of the shell of the mussel Semimytilus algosus from the mid- and lower shore, is not influenced by the spring neap lunar cycle. Only mussels from the high shore display a spring neap lunar variation in the patterns. In this locality the tidal range is small (~1 m) and mussels continually experience wave splash throughout the spring neap lunar tidal cycle during low and high tide, so that they are rarely completely uncovered except in the upper shore, and therefore are able to feed optimally (Abades et al. 2000). While differences in increment width have been noted during spring and neap tides in the shells of bivalves growing subtidally (Pannella & MacClintock 1968, Rhoads & Pannella 1970), no satisfactory explanation has been put forward for the differences. The relationship between variations in suspended sediments during the flood and ebb tide of spring and neap tides and their influence on the availability of inorganic and organic material for shell growth are at present unknown. Is more organic material suspended and available for shell growth during spring tides than during neap tides, and is this chanelled into enhanced shell growth during spring tides compared with neap tides? 120

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Gastropods

Growth rings, lines and ridges The shell of a typical gastropod is a conical spire composed of tubular whorls and contains the visceral mass of the animal. The apex contains the smallest (oldest) whorls with successively larger whorls coiled about a central axis culminating in the largest whorl and the aperture. For most species the outer shell surface offers little in the way of marks or rings that could be reliably used to age the shell and measure growth rates. Also, in older individuals the margin of the shell lip around the aperture thickens masking any potential annual marks. The top shell Monodonta lineata, however, has annual growth checks which are a distinctive feature of the external surface of the shell (Williamson & Kendall 1981), and in the keyhole limpet, Fissurella crasa (Bretos 1980) and the Antarctic patellid limpet Nacella (Patinigera) cancinna (Picken 1980) two growth rings, one light and one dark ring, are formed annually. The dark ring is caused by a seasonal decrease in SST and the light ring is thought to result from changes in growth during spawning. Sections of the calcified opercula of Turbo setosus reveal three types of growth band (A, B and C) (Sire & Bonnet 1984). Apparently, band type A deposition is related to disturbance, type B to a daily growth rhythm and type C to a sub-daily growth pattern. Sire & Bonnet (1984) successfully counted the daily bands in the opercula to estimate the age of individual T. setosus. Santarelli & Gros (1985) identified annual striae (fine rings), on the operculum of the whelk Buccinum undatum, which they validated using stable isotope records from the shell (p. 131) and correlated them with rings on the operculum. The configuration of the shell, except the limpet shape, is generally unsuitable for producing a continuous growth sequence without repeated serial sectioning and some complicated interpretations of the sections. For this reason mesogastropod and neogastropod shells have not been extensively studied. Ekaratne & Crisp (1982, 1984), however, were able to demonstrate the occurrence of growth bands in the newly formed lip at the margin of the aperture of the shells of Littorina littorea and Nucella lapillus. By contrast, prosobranch gastropods have received more attention owing to the ease with which the shell can be sectioned. Growth patterns have been studied in ablaone, e.g. Haliotis rubra (Prince et al. 1988), H. midae (Erasmus et al. 1994), H. corrugata (Shepherd & Avalos-Borja 1997) and H. fulgens (Shepherd et al. 1995a); slipper snails, e.g. Crepidula fornicata (Ekaratne & Crisp 1984) and limpets, e.g. Patella vulgata (Ekaratne & Crisp 1982, 1984), Siphonaria gigas (Crisp et al. 1990) and Cellana toreuma (Richardson & Liu 1994). Abalone shell sections are prepared by rasping the spire with a grinder until a minute hole appears in the shell and then polishing and etching the surrounding shell surface to reveal a series of lines (Muñoz-Lopez 1976, Prince et al. 1988, Shepherd et al. 1995a). Prominent growth lines appear as concentric prismatic layers alternating with aragonite nacre, although minor lines are present. In a number of species the thickness of the lines is dependent on temperature. In Haliotis corrugata (Shepherd & Avalos-Borja 1997), H. laevigata (Shepherd & Hearn 1983) and H. fulgens (Shepherd et al. 1995a) the growth lines are deposited during maximum summer SST and/or as a result of spawning, whereas in the Omani abalone H. mariae (Shepherd et al. 1995b) the lines are deposited during minimum SST. The rate of deposition of these lines is apparently not related to diet, temperature or photoperiod (Erasmus et al. 1994). Several studies have indicated that during the first year of growth up to three growth lines are deposited in the shell of some species (Prince et al. 1988, Erasmus et al. 1994) whereas in H. rubra (McShane & Smith 1992) and in H. iris 121

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(Schiel & Breen 1991) deposition is not an annual process. Large variations can occur in the number of lines deposited between populations of H. rubra and in a large number of individuals the lines are difficult to ascertain (McShane & Smith 1992). Tidally produced growth bands similar to those described in the shells of intertidal bivalves have been observed in intertidal Crepidula fornicata, Patella vulgata, Nucella lapillus and Littorina litorrea shells (Ekaratne & Crisp 1982, 1984), Siphonaria gigas (Crisp et al. 1990) and Cellana toreuma (Richardson & Liu 1994) (Fig. 4D, p. 112). Seasonal changes in the width of the increments in Nucella lapillus, Littorina littorea and Patella vulgata were found to be primarily influenced by temperature, although in P. vulgata depression of increment widths during the summer was probably influenced by gametogenesis (Ekaratne & Crisp 1984). Limpets forage during emersion and/or immersion, and often migrate from one tidal elevation to another, so the shells potentially contain a record of an individual gastropods’ migratory and feeding activities. Diurnal growth ridges and sub-diurnal growth striations have been observed on the shell of Acmaea antillarum from Venezuela (Kenny 1977). Under laboratory conditions of either constant darkness or continuous illumination, Kenny (1977) appeared to demonstrate that growth ridge production in this limpet was inhibited and stimulated, respectively. However, because continuous illumination is likely to promote the growth of surface algae on the rocks on which the limpets feed, whereas darkness supresses algal growth, ridge production is more likely to be related to the more luxuriant growth of the food source and increased shell growth rather than to the period of illumination or darkness.

Statoliths A new and exciting development in the study of gastropod growth is the identification of growth increments in the calcareous Statoliths of prosobranch and opistobranch larvae (Bell 1982, 1983, 1984, Granna-Raffucci & Appeldoorn 1995) and growth rings in the Statoliths of juvenile and adult neogastropods, Buccinum undatum, Nucella lapillus, and the mesogastropod Littorina littorea (Fig. 9A-D). Larval Statoliths are viewed directly in the larvae. Under laboratory conditions Bell (1982, 1983) demonstrated a close relationship between the number of increments and days after hatching in several unspecified gastropod larvae and showed that deposition of the increments was independent of feeding; larvae fed every other day displayed a similar number of increments to those fed each day (Bell 1984). However, when L. scabra larvae were reared in constant light or constant darkness the increments were indistinguishable or non-existent, indicating a possible light dark influence in increment formation. The rate of increment formation in Statoliths of veligers of the queen conch Strombus costatus and S. gigas apparently remains constant after hatching and is independent of feeding; starved veligers continue to deposit increments (Granna-Raffucci & Appeldoorn 1995). The utilisation of daily increments in larval Statoliths opens up possibilities for the study of larval nutrition, duration in the plankton and dispersal patterns as well as competency to metamorphose. The Statoliths of juvenile and adult gastropods lie in fluid filled cavities, the statocysts, organs of equilibration, in the proximity of the pedal ganglia of the foot (Fretter & Graham 1994). The pair of statocysts are accessed by careful dissection of the foot to remove the Statoliths, which when mounted in resin with their surfaces ground and polished, reveal a series of growth rings. The periodicity of the rings in Buccinum undatum, Nucella lapillus, and Littorina littorea has not yet been established and work is presently underway to 122

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Figure 9 Low power (A, C, E) and higher power (B, D, F) photomicrographs of ground and polished statoliths. A, B: from the gastropod Littorina littorea to show the annual growth rings (arrows); N, natal ring; scale bars=25 µm. C, D: from the gastropod Buccinum undatum, annual growth rings (arrows); N, natal ring; scale bars=50 µm. E, F: from the cephalopod Illex gahi to show daily growth increments (arrow). Scale bar in E=0.5 mm and F=250 µm.

investigate their formation. However, it is likely that they represent annual variations in shell growth. Statoliths in these species offer the opportunity for investigating ontogenetic changes in growth similar to those routinely afforded by cephalopod statoliths (see below) and to those already documented for bivalves.

Cephalopods Cephalopods, the most complex of the molluscs, possess skeletal structures which contain growth laminations, lines or rings that have been used both to estimate age and to analyse 123

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past growth and environmental history. The beaks (Clarke 1965, Raya & Hernández-González 1998), statoliths (Clarke 1966, 1978, Kristensen 1980, Lipinski 1980, Jackson 1993), radulae and gladii (Spratt 1978, Jackson 1994, Perez et al. 1996, Perez & O’Dor 2000), and cuttlebones (Choe, 1963, Ré & Narciso 1994) possess periodic structures of varying clarity.

Beaks A pair of chitin beak like jaws are used to bite and tear off large pieces of tissue from their prey and are situated in the buccal cavity. Both the upper and lower beaks have a similar microstructure (Nixon 1973, Mangold & Bidder 1989) and contain a pattern of growth rings (Clarke 1965) when viewed in section under oblique reflected illumination (Raya & HernándezGonzález 1998). Whereas Clarke (1965) observed cycles of micro-ring width between the rostral tip and the free edge in the lower beak of the squid Microteuthis ingens, Raya & Hernández-González (1998) used the upper beak of Octopus vulgaris to count the rings because of the more complete increment sequence. Both concluded, without experimental evidence, that the bands were probably laid down daily. No clear growth “checks” were found during a morphometric study of the beaks of O. dofleini (Robinson & Hartwick 1986).

Statoliths The statoliths of cephalopods are paired calcareous structures composed of aragonite that lie in two adjacent cavities, the statocysts, within the cartilage of the skull and are situated ventro-posteriorly to the brain (Clarke 1978, Lipinski 1980). The statoliths are ~2 mm in length (Fig. 9E, F) and each lies against a ciliated area, the macula principes at or near the anterior end of the statocyst, and is orientated with its long axis approximately in the dorsoventral plane of the cephalopod. Statoliths are involved in a squid’s reception of gravity and detection of acceleration (Radtke 1981, 1983). Statoliths of Loligo forbesi, Sepia officinalis and Eledone cirrosa are usually dissected out by first removing the funnel, flexing the head backwards (dorsally), slicing the skin and the cartilage horizontally near the midline of the skull between the posterior ends of the eyes and removing the statoliths with fine forceps (Clarke 1978, Radtke 1983). The statoliths of juvenile gonatids consist of four main parts: lateral dome, dorsal dome, rostrum and wing (Clarke 1978, Rodhouse & Hatfield 1990). Hurley & Beck (1979) dissolved whole Illex illecebrosus in sodium hypochlorite and pepsin to extract the statoliths. However, prolonged exposure to chemicals may result in the loss of statoliths from formalin-preserved specimens (Clarke 1978). The statoliths of the adults of some squid species often have quite different shapes, particularly with regard to wing development, while the shape of the statoliths of the same species may change with growth (Lipinski 1980). The statoliths of the sepioid Idiosepius pygmaeus are paired calcareous structures situated within bilobed statocysts (Jackson 1990), whereas those of Alloteuthis subulata have poorly developed lateral and dorsal domes and relatively short wedge-shaped rostra compared with the well developed lateral and dorsal dome and long finger shaped rostrum of the statoliths of Loligo (Arkhipkin & Nekludova 1993). The paired statoliths of Nautilus sp. are completely different from those of other cephalopods. Each pair of statocysts has numerous small (1.7–17.2 µm) ovoid statoliths that half fill the statocyst cavity (Jackson 1994). The statoliths of Octopus dofleini, unlike 124

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squids, are of a soft, chalk-like consistency and display no concentric rings (Robinson & Hartwick 1986). Differences in the biochemical composition of the statocyst endolymph in Sepia officinalis and Loligo vulgaris give rise to distinct statolith crystallisation processes that result in a different statolith microstructure. This may explain the better definition of the growth increments in L. vulgaris than in Sepia officinalis (Bettencourt & Guerra 2000). Conventionally statoliths are sectioned, although Jackson (1989) found that dehydrating the statolith, clearing in xylene and mounting in DPX gave a good degree of increment resolution (see Lipinski 1980 for a detailed account of the techniques for statolith preparation). Canada balsam has been used to mount/embed paralarval statoliths (Arkhipkin & Bizikov 1997). Usually the statolith is temporarily or permanently attached to a microscope slide and the statolith lateral dome ground to the desired position. In Loligo vulgaris reynandii the area superficial to the medial inclusion of the wing of the statolith was selected as the patterns were consistently visible throughout the statolith (Lipinski et al. 1998). The resulting preparation when viewed in the light microscope reveals the presence of a series of lines or rings (Fig. 9E, F). The readability of some statoliths has been considerably improved by the use of ninhydrin staining or by etching the statoliths with a mixture of 0.0IN HCl and 10% CCl3COOH (Lipinski 1986).

Growth patterns Growth lines were first noted in squid statoliths by Clarke (1966) who suggested they might be used in age determinations. Patterns of growth rings, increments, bands and lines have been found within the statoliths of many species of squid and in the statoliths of several species of sepioids (Jackson 1994). The clarity of the statolith rings varies among the different species. Those of Illex sp. are most easily read, followed by Loligo sp., whereas Histioteuthis macrohista and Moroteuthis ingens statoliths are hardly readable (Lipinski 1980). A ~10% difference is normally expected between replicate counts of increments in the same statolith. Counts from the statoliths of adult squid Photololigo sp. are significantly more variable than from juveniles (Jackson & Moltschaniwskyj 1999). The periodicity of the patterns has been investigated in several studies (e.g. Hurley et al. 1985, Jackson 1990, Arkhipkin & Nekludova 1993). “Ring” has traditionally been used as a common descriptor of the patterns, although there is a problem with this description as any single “ring” is a three-dimensional structure (Jackson 1994). Lipinski et al. (1991) and Lipinski (1993) advocate the use of “growth ring” and suggest that, because an observed “ring” in the microscope is composed of a dark and light ring, each part of this structure should be referred to as an increment. Throughout the statolith literature there is inconsistency in the use of the term “increment” (Secor et al. 1993). The main difficulty appears to lie in an objective, accurate and precise recognition of an “increment”. To enable a comparison to be made with the bivalve microgrowth patterns in the previous section the term “daily increment” has been adopted here in discussions of the statolith. Evidence for a daily periodicity of increment formation in statoliths is compelling. Hurley et al. (1985) were the first to investigate the periodicity of increments in statoliths. They fed strontium labelled shrimp for 24 h to field caught short-finned squid Illex illecebrosus, and then held them in the laboratory for between 13 and 20 days; two days later some squid were again fed the labelled shrimp. Using an electron probe, a strontium x-ray map of each statolith was generated and compared with the appearance of the increments in the ground 125

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and polished statolith. A strontium peak coincided with the introduction of the strontium labelled diet; those squid fed two days apart with the strontium labelled meal showed a double strontium peak in the statolith. General agreement between the number of increments and days elapsed was found, although differences of up to three increments were noted between the observed and expected number. This discrepancy might have resulted from a failure to observe the increments (Hurley et al. 1985) or that increments were not deposited each day. Daily deposition of increments in statoliths has been independently established for other squid species, e.g. Alloteuthis subulata (Lipinski 1986), Idiosepius pygmaeus (Jackson 1988), Sepioteuthis lessoniana (Jackson 1990) and Loliolus noctiluca (Dimmlich & Hoedt 1998). These authors injected or immersed their squid in tetracycline hydrochloride or Calcein to stain and internally mark an increment in the statoliths to which subsequent increment formation could be related. However, these kinds of marking procedures involve a certain amount of physiological stress to the squid (e.g. confinement in low oxygen conditions during and after capture, temperature shock and exposure to chemicals), despite apparently normal behaviour after injection or exposure. The result is the formation of a prominent check in the statolith associated with the initiation of the fluorescent band (Jackson 1990, Dimmlich & Hoedt 1998, Lipinski et al. 1998). The induction through trawling, of a well-defined stress mark or check in the statolith of the paralarvae of several gonatid species, was sufficient to act as a mark within the statolith to which all subsequent growth and increment formation could be related (Arkhipkin & Bizikov 1997). The statoliths of the paralarvae of Octopus vulgaris have been marked successfully with alizarin complexone (Fuentes et al. 2000). Using these marking procedures several studies have established close agreement between the number of increments counted after the tetracycline mark and the number of days each animal survived post-staining, thus confirming the increments have a daily periodicity of formation in Illex illecebrosus (Dawe et al. 1985), Alloteuthis subulata (Lipinski 1986), Sepioteuthis lessoniana (Jackson 1990) and Loliolus noctiluca (Dimmlich & Hoedt 1998). Sepia hierreda, from the north west African coast apparently, has a non-daily pattern of increment deposition (Raya et al. 1994). Statolith increments, similar to those observed in squid statoliths, have not been observed for any Octopus species (Jackson 1994). Non-daily deposition of increments in the statoliths of embryo Alloteuthis subulata has been demonstrated during incubation in the open sea where it is thought that formation is more likely to be controlled by water temperature and light cycles (Morris 1991). Increments are not apparently deposited in the embryonic statolith of the ommastrephid squid Illex illecebrosus (Balch et al. 1988). By contrast, live gonatid paralarvae maintained for between 1 and 4 days at 2–4°C until they died, formed daily increments in their statoliths (Arkhipkin & Bizikov 1997). Lipinski (1993) has proposed that increments (his growth layers) in embryos represent sub-daily units, while those visible in the adult squid statolith are deposited daily.

Growth zones Since increments in the squid statolith are deposited daily they potentially contain information about the age (number of increments), growth (width of the increments), ontogenetic events (checks) and shifts (zones or bands) providing information from the time the animal hatches until its death (Arkhipkin & Bizikov 1997). Growth zones within the statolith microstructure are characteristic in squids (Arkhipkin 1996) and are usually distinguishable by increment 126

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width and especially by colour in cold water oceanic and neritic species, e.g. Gonatus fabricii (Kristensen 1980), Illex illecebrosus (Morris & Aldrich 1984) and I. argentinus (Arkhipkin 1990). Kristensen (1980), Arkhipkin (1993) and Arkhipkin & Nekludova (1993) identified four zones (1–4) in the statolith of Gonatus fabricii, Loligo gahi and Alloteuthis subulata, respectively. In Loligo gahi the statolith consists of an egg-shaped nucleus with a central dark brown primordium (zone 1, diameter 13–21 µm) (Arkhipkin 1993) whereas in Gonatus fabricii the nucleus has an inconsistent diameter (~160 µm) (Kristensen 1980). The postnuclear zone (zone 2) contains narrow increments (l-4 µm) and is separated from the outer zones of the statolith (zones 3 and 4) by a prominent natal ring (Arkhipkin 1993) (Fig. 9E, F; p. 123) and characterised by prominent periodic increments (Kristensen 1980).

Spring neap lunar cycles Kristensen (1980) counted daily increments in zone 3 of the statolith of G. fabricii and termed these “first-order” bands. He observed that the bands formed groupings of ~14 clearly defined increments constituting a “second-order” band which alternated with 14 weakly defined increments to form another “second-order” band. Together these two “secondorder” bands comprised a “third-order” band. In zone 4 the clearly defined increments in the “second-order” band were thick striped whereas the weakly defined bands of the other “second-order” band had a uniform definition. Kristensen (1980) interpreted this pattern of “second-order” bands (mean 13.20 ±0.21 S.D. bands) in G. fabricii as reflecting a fortnightly pattern and two “second-order” bands (=a “third-order” band) a monthly periodicity. Similarly, Rosenberg et al. (1981) counted the putative daily increments in the statolith of the North Atlantic squid Todarodes sagittatus and observed a fortnightly (mean 14.02±0.84 S.D.) increment pattern. Kristensen (1980) has postulated that since the water temperature in which Gonatus fabricii occurs is relatively constant throughout the year, this environmental factor is unlikely to be responsible for controlling the formation of the “second-order” bands. More likely, he has reasoned, circadian rhythms in behaviour, metabolism and feeding affect CaCO3 and organic material deposition in the statolith. Such behavioural changes may be controlled by fortnightly variations in the spring neap lunar cycle in a similar manner to that reported in bivalve shells (Rhoads & Pannella 1970, Rhoads & Lutz 1980, Richardson 1993) and fish otoliths (Pannella 1971, 1980, Campana & Neilson 1985).

Population studies Confirmation that the natal ring was formed at the time of hatching was demonstrated in newly hatched Sepioteuthis lessoniana (Jackson 1990) and other species (Lipinski 1986, Natsukari et al. 1988). Using the identification of the natal ring and by back-counting daily increments in the statoliths of Todarodes sagittatus, Rosenberg et al. (1981) calculated the approximate date each individual squid had hatched and estimated the distribution of hatching times of the squids by month. Similarly, age estimates of individual squids from statolith growth increment counting have been used to identify cohorts of new recruits and for determining seasonality in reproduction by back-calculating hatching dates (Jackson 1994). Based on statolith age analysis the lifespan of Idiosepius pygmaeus is short, 67 days and 79 days for male and female sepioids, respectively (Jackson 1990), and the estimated size and 127

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age at which they first become sexually mature is 6.8 mm and 42 days for males whereas females mature at around 13 mm and as young as 60 days. Male and female Loligo opalescens mature as early as 6 months in Califonian waters, USA (Butler et al. 1999).

Ontogenetic changes The statoliths of Moroteuthis ingens have an inner opaque zone (zone 3) and an outer translucent zone extending to the statolith margin (zone 4) and contain different numbers of increments; the outer zone containing more increments than the inner zone (Jackson 1993). In M. ingens the transition from opaque to translucent zones within the statolith takes place between 112 days and 209 days after hatching and is thought to represent a habitat shift from an epipelagic existence to a demersal one (Jackson 1993). A marked change from the opaque zone to the translucent zone may represent individuals that settled quickly into their demersal habitat. Similar zones have been identified in the statolith of the demersal Antarctic squid Psychroteuthis glacialis (Jackson & Lu 1994). In this species the inner zone of the statolith consisted of less well defined increments that changed abruptly into an outer zone with very distinct increments which were thought to represent pelagic and demersal phases of growth. An abrupt change in increment width and the growth axis of the statolith of the paralarval Abralia trigonura has been related to migration from an epipelagic to a mesopelagic habitat coupled with the onset of diel vertical migration (Jackson 1993). Arkhipkin (1996), although able to distinguish two zones in the statolith of the planktonic squids Cranchia scabra and Liocranchia reinhardti, noted that there was an absence of any stress check or sharp change in increment width and no clear boundary between the two zones. This he suggested was due to a rapid transformation of the food capture apparatus between the paralarval phase (zone 1) and the juvenile phase (zone 2) and therefore no period of short-term starvation and the formation of a stress mark, which is commonly observed in the statoliths of ammastrophid squids. Differences in statolith microstructure have been noted among squids as a result of changes in locality (Arkhipkin 1993). Juvenile Loligo gahi, for example, which hatched during winter in the cold waters of the Argentine basin, had well defined narrow (2–3 µm) increments. By contrast, juveniles hatching in the winter but which fed in the warm waters of the Patagonian Shelf displayed a faster growth rate reflected in wider (4–5 µm) less well defined statolith increments (Arkhipkin & Scherbich 1991). Statolith size or weight may provide clues about the past environmental conditions of a squid’s growth, particularly when combined with age estimates. Jackson (1991), for example, found that slow growing L. chinesis during the winter had larger statoliths than faster growing summer conspecifics.

Gladii The gladius of Moroteuthis robusta (Bizikov & Arkhipkin 1997) and Illex illecebrosus (Perez & O’Dor 2000) contain growth increments. The gladius is a chitinous transparent plate lying deeply in the muscles along the dorsal mid-line of the mantle and consists of a broad lanceolate dorsal plate, the proostracum, gradually tapering posteriorly into a small brood cup or conus, which is set deeply into a long, transparent, cartilaginous rostrum (see Bizikov & Arkhipkin 1997 for details of morphology). Growth marks (900–1200 µm) and increments (15–50 µm) are visible inside the transparent outer layer and cross-section of the rostrum 128

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and middle and inner layers of the proostracum of Moroteuthis robusta. In the inner layer the increments form groups of 10–18 increments. Two types of “stress mark” were observed in rostrum sections—“growth stress marks” and “traumatic marks”. The “growth stress marks” consisted of several (4–10) narrow layers, with usually one to three marks in each rostrum and it is believed these marks are caused by events in the squids’ life that sharply reduced growth (Bizikov & Arkhipkin 1997). “Traumatic stress” marks were only occasionally found in a few rostra and consisted of non-shell fine grained white substance, which Bizikov & Arkhipkin (1997) interpreted as consisting of coagulated blood or lymph which had poured into the shell sac during injury and had later become enclosed with successive rostrum increments. Owing to the rarity of M. robusta, a boreal Pacific nektonic squid, Bizikov & Arkhipkin (1997) were unable to verify the periodicity of the increments and growth checks and confirm their interpretations. Perez & O’Dor (2000) identified a series of growth phases from the gladius of Illex illecebrosus. They found that paralarval growth ended at approximately 10mm gladius length (GL) with a change in growth at 30– 40 mm GL associated with a shift from a macroplanktonic to a micronektonic habit and transition from the Gulf Stream to slope water, a growth transition at 68 mm GL at the Scotian shelf/slope water front and finally a change to linear growth at 90 mm GL in shelf waters after a nektonic lifestyle was attained.

Cuttlebones When viewed in the light microscope a cuttlefish cuttlebone reveals stripe lines (Choe 1963), growth increments and lamellae which consist of two zones, a wide translucent zone and a narrow opaque zone (Ré & Narciso 1994). Choe (1963) claimed the stripe lines in the cuttlebone of the cuttlefish Sepia esculenta, S. subaculeata and Sepiella maindroni were formed daily. He found one stripe line was formed per day under “good” conditions of nourishment, but found that this relationship did not hold in cases where the nutritive and environmental conditions became disturbed. With insufficient feeding the stripe lines did not appear or were indistinct with a reduced distance between adjacent lines, these daily lines were considered to be non-daily. Ré & Narciso (1994) later demonstrated in Sepia officinalis a non-significant relationship between the number of growth increments and the number of days after hatching. The periodicity of the growth increments was primarily related to the growth rate of the juvenile cuttlefish rather than to its chronological age. Therefore periodic patterns in cuttlebones can not be used for estimating an individual’s age or readily assessing the effect of environmental conditions on growth.

The Nautilus shell The formation of new chambers in the Nautilus shell occurs episodically and involves the forward movement of the animal from the last formed septum, a wall dividing adjacent chambers, the simultaneous filling of this vacated space with cameral liquid, and sealing off the cameral liquid by the calcification of a new septum (Ward et al. 1981, Ward & Chamberlain 1983, Mann 1992). Introduction of Nautilus pompilus into an aquarium induced the formation of a black line on the outside of the shell and a reduction in septal spacing within the shell (Landman et al. 1989). 129

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Isotopic records in molluscs

General principles Molluscs construct their shells from calcium carbonate in the form of aragonite, calcite or both. Urey (1947) first suggested that variations in the temperature of the sea water from which CaCO3 precipitated should lead to measurable variations in the 18O/16O ratio of the carbonate. Thus, molluscs could be expected to record in their shells the water temperature they experienced during growth. Epstein et al. (1951) and Epstein & Lowenstam (1953) empirically determined the nature of this temperature relationship to be nearly linear between ~5°C to 30°C, with lower ratio values at higher temperatures. Craig (1965) modified the original calcite equation slightly to the form: T(°C)=16.9-4.2(␦18OcalciteS-␦18OW)+0.13(␦18OcalciteS-␦18OW)2 where ␦18OcalciteS represents the deviation of the calcite shell sample 18O/16O ratio from the Pee Dee belemnite (PDB) reference standard while ␦18OW represents the 18O/16O ratio of the water in which the molluscs grew, also relative to the PDB standard. As with all palaeotemperature equations, a reasonable estimate of the oxygen isotope composition of the sea water (␦18OW) is required, and is usually determined from water samples collected in the study area from which the shell was precipitated (Jones et al. 1983). Where the shell is entirely aragonite then the equation of Grossman & Ku (1986) has been used: T(°C)=20.19-4.56(␦18OaragoniteS-␦18OW)+0.19(␦18OaragoniteS-␦18OW)2

Sample preparation Individual powdered samples of calcium carbonate are usually drilled from shell cross-sections or from the surface of the shell (Fig. 1B, p. 106) using drills with small diameter drill heads (~0.5 mm). Recently an automated micro-sampling technique has been developed (Weidman & Jones 1994). The carbon dioxide gas produced by reacting individual sample powders in purified phosphoric acid at 60°C and cryogenically removing water is analysed in a micromass stable isotope ratio mass spectrometer. Values for ␦13C are produced automatically during the ␦18O analyses. While for oxygen isotopes the main cause of variation appears to be temperature (Wefer & Killingley 1980), the factors controlling the ␦13C composition of marine carbonate are more complex and less well understood than for ␦18O (Romanek et al. 1987).

Shell records The integration of geochemical and schlerochronological analysis of modern and fossil molluscs has provided information on life histories and the environment that could not have been obtained by conventional approaches. For example, when serially sampled in a detailed fashion (Fig. 1B, p. 106) systematic oxygen isotope changes provide information on age, growth rate and season of calcification of molluscs. The carbon isotope composition of 130

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shells, in conjunction with oxygen isotopic and growth increment records, can potentially be used to estimate changes in productivity and nutrient concentrations in both modern and ancient environments (Jones et al. 1986).

Growth line studies High resolution records of ␦18O in molluscs have been used to reconstruct SST records in a variety of molluscs, including giant clams Tridacna maxima (Romanek et al. 1987, Romanek & Grossman 1989, Aharon 1991), the mussels Mytilus edulis and M. californianus (Killingley & Berger 1979), horse mussels Modiolus modiolus (Margosian et al. 1987), fan mussels Pinna nobilis (Richardson et al. 1999, Kennedy et al. pers. comm.), queen scallops Aequipecten opercularis (Hickson et al. 1999), the bivalves Arctica islandica (Weidman & Jones 1994), Area and Macrocallista (Erlenkeuser & Wefer 1981), Spisula sachalinensis and Mactra chinensis (Khim et al. 2000), the gastropods, Turitella (Allmon et al. 1992) and Strombus sp. (Wefer & Killingley 1980, Geary et al. 1992) and the pteropods Limacina and Cliopyramidata (Kalberer et al. 1993) and Cresis and Styliola (Jasper & Deuser 1993). We have seen previously that the molluscan shell contains an incremental record of shell growth. A number of studies have been conducted on bivalves using stable oxygen isotopes to validate the periodicity of the growth lines in the shell. Jones et al. (1983) and Krantz et al. (1987) demonstrated a close correspondence between the number of major lines and yearly ␦18O cycles thus confirming in Spisula solidissima, that the growth shell lines are formed annually and these have been used to determine accurately age and growth rate in this species. The oxygen isotope records of serially sampled carbonate powders from two Placopecten magellanicus shells taken off the Virginia coast, USA, demonstrated annual cycles which closely approximated the isotopic composition predicted as a function of the observed salinity and temperature (Krantz et al. 1984). Tan et al. (1988) demonstrated that the external surface growth rings in P. magellanicus coincided with the most elevated ␦18O values during the annual cycle indicating that their formation occurred during the coldest months of the year. Similarly, annual cycles in the ␦18O profile allowed the age of a specimen of Tridacna maxima to be determined, while the cycle length was found to be a measure of the yearly shell growth rate (Romanek et al. 1987). Annual cycles in the ␦18O profile taken along the calcite shell of Pinna nobilis from the Mediterranean were related to rings on the aragonite adductor muscle scar. These rings were then used to determine the age and growth rate of populations of this pinnid (Richardson et al. 1999). Killingley et al. (1980) found cyclicity in the 18O/16O ratio in the shell of a vesicomyid clam, Calyptogena sp. from the Galapagos rift spreading zone, which they suggested was reminiscent of seasonal variations in growth or might have arisen as a result of cyclicity in vent activity. Fewer studies using stable oxygen isotopes have been conducted to determine the age and growth of gastropods and cephalopods. Wefer & Killingley (1980) found cyclicity in the 18O/16O ratio in the shell of the conch Strombus. Seasonality of rings (striae) on the operculum of the common whelk Buccinum undatum, was investigated using isotopes to validate the seasonal fluctuations in seawater temperature in the shells and to correlate them with the rings on the operculum (Santarelli & Gros 1985). Cespugilo et al. (1999) demonstrated using oxygen isotopes that the shell of Nassa mutabilis from the Adriatic, Italy, is laid down throughout the year with highest accretion rates during the summer (warmer) months. 131

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Radioisotopes Among the various methods used to estimate the growth and age of molluscs, those involving radioisotopes have found application in some species. Turekian et al. (1975) estimated the age of a deep sea clam Tindaria callistiformis from a depth of 3806 m in the North Atlantic using 228Ra; Radium-228 is produced from the decay of long-lived 232Th. An 8.4 mm clam was estimated to have an age of 100 yr and shell sections of similar sized clams showed ~100 regularly spaced growth lines which were thought to have an annual periodicity. These investigators speculated that down-slope movement of organic rich sediments from shallow water, activated on a seasonal basis, might have given rise to the deposition of annual bands due to the response of the clam to annual fluctuations in food supply. The same technique was applied to determine the growth rate of an unidentified mytilid mussel and a vesicomyid clam from Clambake I on the Galapagos Rift zone (Turekian et al. 1979). The radioactive decay of the short-lived natural radionuclides of the uranium and thorium decay series, (in particular 210Pb: 22-yr half life, 210Po: 138-d half life, 228Ra: 5.7-yr half life and 228Th 1.9-yr half life) has been used to determine the growth rate of the ocean quahog Arctica islandica. Turekian et al. (1982) measured the distribution of 228Th and 228Ra in a serially sampled A. islandica for “decay chronometry” and concluded that the radiometrically determined growth rates for this species were comparable with those estimated from growth line counting and that the bands had an annual periodicity (e.g. Weidman & Jones 1994). Supporting evidence for the deposition of annual growth lines in A. islandica is presented by Bennett et al. (1982). Using marked, released and recaptured A. islandica they showed, using 210Pb and 228Ra, that the two most recently deposited growth lines had been laid down over the last two years. Similar measurements of 210Pb/226Ra activity ratio in the shells of Panope generosa indicated annual growth lines in the shells of 2–4 yr old and 115 yr old specimens. Possible contamination of the shell layers may occur in older shells, particularly where the outer organic periostracum has been eroded. The external layers of the shell near the umbo often contain much higher concentrations of natural radionuclides than the layers near the growing margin, suggesting that secondary additions of natural radionuclides to the older parts of the shell may occur (Bennett et al. 1982). Using “decay chronometry” Cochran et al. (1981) determined the growth rate of the nautiloid cephalopod Nautilus pompilus using the radioactive disequilibrium of 210Pb and 210 Po in the septa of the shells of two specimens. Measurements of 210Pb and its grandaughter 210 Po provide a chronometer to reveal the growth rate of the Nautilus shell. Although both radionuclides are present in sea water, only 210Pb is incorporated into the aragonite of the shell. There it decays to produce 210Po and the 210Po/210Pb ratio (APo/APb) is a measure of the length of time elapsed since shell formation (Cochran & Landman 1984; Landman et al. 1989). The periodicity of septa production in N. pompilus in the natural environment and in the laboratory has been estimated by Cochran & Landman (1984) and Landman et al. (1989). In the sea a septum was produced after ~180 days whereas in an aquarium, septa formation occurred every 50–80 days, and was dependant on the maturity of the Nautilus (Cochran & Landman 1984). Rates of septal formation translate into growth rates of approximately 0.12 mm to 0.08 mm of ventral circumference per day for immature and mature animals, respectively (Cochran & Landman 1984). The formation of a new septa ceases at maturation in N. scrobiculatus and N. pompilus. The septa in the spiral shell of Nautilus sp., like the cuttlefish bone of Sepia therefore cannot be used for estimating the age of this cephalopod. 132

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Isotope records and their use as records of environmental change

Temperature reconstruction

Living molluscs Bivalves The determination of seawater temperature using the 18O/16O ratio in sequential samples of the calcite and or aragonite molluscan shell offers the opportunity for reconstructing the seawater temperature of the environment in which the organism has been growing, a technique that has a particularly useful application in circumstances where local records of seawater temperature are unavailable or difficult to obtain, such as on the continental shelf or in the deep oceans. Such an example is provided by Margosian et al. (1987) who reconstructed the bottom seawater temperature in a cove in Nova Scotia using oxygen isotope records from the shell of Modiolus modiolus. It was speculated that between 1980 and 1983 the sea water in the cove had been unusually warm and this had caused an outbreak of a temperature-related sea urchin disease that had devastated populations of Strongylocentrotus droebachiensis along the Atlantic coast of Nova Scotia. In the absence of bottom seawater temperature records in the region there was no means of verifying whether the sea had been unusually warm during the period. Using two shells, they demonstrated from the reconstructed seawater temperatures, that the waters in the cove had not been unusually warm during the period of the disease. The utility of shells for the reconstruction of SSTs has been demonstrated using the fan mussel Pinna nobilis (Kennedy et al. pers. comm.). This pinnid resides among seagrass, Posidonia oceanica, meadows in the coastal waters of the Mediterranean where they attain a size of >65 cm and an age of >10 yr (Richardson et al. 1999). Although these pinnids are large, only sequential samples from the first 4–5 yr of growth can be used to estimate accurately the SST. Since with increasing size (age) and slower growth, time-averaging of the ␦18O signal occurs and maximum and minimum temperatures are underestimated (Fig. 10A). This difficulty was overcome by using four shells of overlapping size and age to construct a decadal chronology of SST in the southeastern Mediterranean. Gastropods The ␦18O records in shells of the gastropod Littorina littorea, living subtidally in shallow (0.5 m depth) waters in a bay on the west coast of Sweden, were found to be in agreement with the observed seasonality in seawater temperatures in the area and demonstrated that shell deposition continued during the winter when temperatures were minimal (Andreasson et al. 1999). Variations in d18O were also noted in response to peaks of freshwater influx into the bay during the spring and such variations in ␦18O may be useful for detecting seasonal freshwater influx in shells from other localities (Andreasson et al. 1999). Isotope-derived sea surface water temperatures, obtained from shells of the pteropod Cavolina longirostris from the Persian Gulf correlated with the actual temperature and salinity conditions in the Gulf (Hoefs & Sarnthein 1971). Similarly, Bernal (1980) noted that the ␦18O in the shell of the pteropod Limacina helicina collected from plankton hauls in the California Current and in the eastern Chukchi Sea reflected the difference in seawater temperature between the two localities. 133

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Figure 10 Stable isotope records from the shell of Pinna nobilis collected in 1995 from the Southeast Mediterranean. A: temperature record based on d18O. A date has been assigned to each seasonal cycle. B: d13C record from the same shell. (From Kennedy et al. pers. comm.)

Cephalopods Analysis of oxygen and carbon stable isotopes in the cephalopod statolith could be used to reveal a squids’ past history of growth. Unfortunately only whole statoliths have so far been analysed and this has only provided a record of the average sea water temperature in which the squid lived (Radtke 1983). Isotopic temperatures determined from the cuttlebone of Sepia officinalis fell within the range of seawater temperatures measured in the Ria de Arosa from where the cuttlefish were collected (Bettencourt & Guerra 1999).

Fossil molluscs Given reasonable assumptions about local nutrient availability and ambient-water mass salinity and isotopic composition, it would be possible to extract palaeotemperature and palaeosalinity records from the isotopic composition of individual molluscs shells (Bice et al. 1996). Reconstructed seawater temperature records in living and fossil molluscs have been usefully compared. The palaeotemperature of the last interglacial period (LIP) (between 115000 and 135000 yr BP), determined from the shell of the gastropod Strombus bubonius collected in Pleistocene beaches from the Island of Majorca, western Mediterranean, has been compared with the temperature of modern living representatives from the shallow waters of the Gulf of Guinea (Cornu et al. 1993). The ␦18O chronology in the shells of these thermophilous gastropods indicates that the reconstructed sea surface temperature from the modern shells, (seasonal temperature difference 2–6°C), is in rough agreement with sea surface temperatures obtained from climatological maps. However, the seasonal temperature difference in the fossil material, (7–9°C), was several degrees higher during the last interglacial period than at present (Cornu et al. 1993). The ␦18O records in fossil shells from 134

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interglacial Pleistocene deposits of Bermuda indicate temperature conditions within 1–2°C of the present temperature conditions (Epstein & Lowenstam 1953). Several studies have been undertaken to determine the palaeotemperature of geological epochs. Whereas Muhs & Kyser (1987) found in Epilucinia californica that the waters off southern California were cooler during the last interglacial stage than at present, Taira (1976) showed in fossil shells from littoral Pleistocene deposits from central Japan that during the last interglacial (130000 yr BP) SST were a few degrees higher than present. Analysis of the isotopic variation in the shells of Chlamys gemmulata indicated either a substantial decrease in seawater temperature or an increase in the ice-caps at about 0.75 Ma, probably in the latter part of the Günz Glaciation and thereafter minor oscillations (during the Cromer interglacial) with a slight trend towards warming or decreasing ice melt at ~0.5 Ma (Stevens & Vella 1981). Oxygen isotope data from the shells of apparently well preserved midPliocene Aequipecten opercularis from the southern North Sea Basin indicate seasonal temperatures similar to the present (Johnson et al. 2000). Donner & Nord (1986) compared the ␦18O chronologies in a modern Modiolus modiolus shell with those in the shells of Mytilus edulis and Modiolus modiolus from Holocene raised beaches. The SST estimated from the ␦18O records in the modern M. modiolus corresponded to the observed annual amplitude of the surface waters in the area. Using limited shell material, covering the period 520 BP to 4300 BP, no fluctuations were found in the maximum summer seawater temperatures during the past 4500 yr. Using suitably preserved ammonites and nautiloids, gryphaeid oysters Pycnodonte and the bivalves Trigonia and Pinna from the Tithonian to the Eocene of the James Ross Island and Alexander Island areas in Anatarctica, Ditchfield et al. (1994) constructed a record of high latitude seawater temperature variations. They found a marked cooling of palaeotem-peratures from the late Jurrasic to the Albian, a warming during the midCretaceous and a gradual cooling from the mid-Cretaceous to the Eocene. Seawater temperatures of the late Paleocene shallow Arctic Ocean have been determined from high resolution records in the shells of Camptochlamys alaskensis from the Prince Creek formation, exposed near Ocean Point, North Slope, Alaska (Bice et al. 1996). C. alaskensis records an annual temperature range of 6°C (11–22°C) suggesting very moderate highlatitude marine temperature seasonality during the late Paleocene. Oxygen derived temperature records in well-preserved aragonitic shell material from the glauconitic limestones and marls at Copenhagen suggest an average seawater temperature record of 12–14°C, possibly indicating a cooler climate in the Danish Paleocene compared with the late Cretaceous and Eocene (Buchardt 1977). A comparison of the isotope derived temperature record from C. alaskensis with modern Chlamys species suggests that Camptochlamys alaskensis probably inhabited water depths of 30–50 m (Bice et al. 1996). A lighter ␦18O value in samples taken at the shell margin in C. alaskensis is thought to reflect a gradual freshening of the ambient water probably indicating that the scallops died as a result of reservoir salinity falling below the lower limits of salinity tolerance, thus providing a record of palaeosalinity (Bice et al. 1996). The degree to which the ␦18O derived temperature reflects precisely the actual SST is unclear, although where records of measured SST are available to compare directly with the ␦18O record, molluscan shells record to within 1°C or 2°C of the actual temperature (Epstein & Lowenstam 1953). A direct comparison of in situ SST in a shallow water seagrass meadow, where fan mussels Pinna nobilis were being studied, with the shell-derived isotope temperature, showed the accuracy of the shell temperature record to be ~1°C (Kennedy et 135

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al. pers. comm.). A similar accuracy of ±1.2°C was obtained from the isotope derived record in the shell of Arctica islandica (Weidman & Jones 1994).

Thermocline development, water depth estimations and upwelling Stable isotope records extracted from annual growth increment records in surf clams, Spisula solidissima, from 10m and 45m depths in the mid-Atlantic Bight were found to reflect changes in the available nutrient concentrations on the Shelf over the year (Arthur et al. 1983). The ␦18O and ␦13C records from the clams from the two depths recorded well-mixed conditions during the winter months and the development of a thermocline during the summer. Clams from the shallower depth also recorded a depletion in the ␦18O record which was related to a temporary decrease in surface-water salinity. The magnitude and timing of the ␦18O decrease was consistent with the spring flood conditions in the regional rivers. An offset of +1% was observed in the entire ␦18O isotopic record in the shell of a fossil (60000 yr BP), Spisula compared with the profile from a modern specimen (Jones et al. 1984). The high sea level stand at 60000 yr BP was ~30 m lower than the present sea level resulting in an ice volume effect upon the ␦18O in the oceans of +1%. Jones et al. (1984) concluded that this glacial influence was reflected in the isotopic composition of the shell of Spisula. Similar offsets between Pleistocene and modern Spisula shells have since been related to known temperature and ice volume effects during the late Pleistocene (Krantz et al. 1987). The possibility of using isotopes in mollusc shells as palaeosalinity indicators has been explored by Hendry & Kalin (1997). Stable oxygen and carbon isotope analyses of oysters Praexogyra hebridica found in Bathonian inner-ramp limestone from central England demonstrated an offshore to nearshore palaeoenvironmental change. The ␦18O record suggested brackish waters in shells from the landward regions while the ␦13C (see below), although not reflective of a palaeosalinity gradient, suggested that there had been preferential removal of organic carbon from the hydrodynamically restricted and poorly oxygenated lagoon waters of the nearshore environments (Hendry & Kalin 1997). A decrease in amplitude of the ␦18O cycles observed in Spisula solidissima as the depth of water increased could be used as a relative depth indicator (Krantz et al. 1987). Stable oxygen and carbon isotope profiles in the shells of scallops Placopecten magellanicus from the outer continental shelf of the south Atlantic Bight and the Virginia Bight trace the hydrographic processes of the two regions (Krantz et al. 1988). Seasonal phytoplankton blooms were recorded in the carbon isotope record, and the shells from the Virginia Bight showed the influence of spring run off and summer water column stratification. Upwelling currents are generally enriched in light carbon isotopes because the total dissolved inorganic carbon (DIC) contains more 12C than 13C. Photosynthetic activity in surface waters selectively removes 12C from the ambient dissolved DIC, whereas in deeper waters, the oxidation of organic debris releases large amounts of 12C. Therefore during upwelling, water whose carbon is isotopically light is brought to the surface (Killingley & Berger 1979, Krantz et al. 1988, Geary et al. 1992). Incursion of warm surface waters results in heavier values of ␦13C being deposited in the carbonate shells of molluscs during the incursion (Killingley & Berger 1979, Rollins et al. 1987). Using the 13C/12C ratio in sequential samples from a single shell of the California mussel, Mytilus californianus, Killingley & Berger (1979) concluded that fluctuations in the ␦13C records paralleled the Bakun upwelling index. However, in the three annual cycles of ␦13C presented there appears 136

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to be correspondence only between the upwelling event and the ␦13C peak in 1977. The events shown in 1975 and 1976 are offset, with the peaks in ␦13C occurring before the peak in the upwelling index. Records of the El Niño temperature anomaly event along coastal Peru have been observed in the incremental and stable isotope records in the shells of the intertidal venerid bivalve, Chione subrugosa, and the subtidal carditid, Trachycardium procerum (Rollins et al. 1987). Incursion of warm surface waters of the Equatorial Countercurrent into the colder waters of the Peruvian Province were expected to result in deposition of heavier values of ␦13C in the carbonate of the shell during the incursion event. At the same time, the warmer waters were expected to result in lighter ␦18O values in the molluscan shell carbonate (Rollins et al. 1987). While shells of both species showed a discernible and pronounced break in growth at the shell valve margin following the 1982–83 El Niño event, Chione subrugosa displayed an inconsistent stable isotope pattern, whereas Trachycardium procerum preserved the expected trend in salinity and temperature change associated with the event. The El Niñoinduced growth breaks present in all the Chione subrugosa shells examined showed a rapid onset with slow and erratic post-check recovery; often the bivalves growth did not fully recover and the ventral shell margins were strongly blunted. Heavier ␦13C values from the shells were observed to correlate with elevated SST changes along the coast of Peru, and the lighter ␦18O values in the post-El Niño deposited shell were indicative of the incursion of the warmer countercurrent (Rollins et al. 1987). ␦13C isotope profiles from the shells of the gastropod Strombus spp from three different shallow water localities, S. graciloir from the Pacific coast of Panama and the Caribbean coast of Panama and S. pugilis from the eastern coast of Florida showed contrasts among localities in seasonal temperature, salinity and upwelling (Geary et al. 1992). Oxygen and carbon isotopic profiles of well-preserved Turritella apicalis and T. gladeensis from Pliocene beds near Sarosota, Florida, USA, revealed detailed records of the palaeoenvironmental and palaeoclimatic conditions prevailing at the time. The isotope records indicated that shell growth occurred throughout the year in a seasonal subtropical to warmtemperate palaeoenvironment (Jones & Allmon 1995). Growth was punctuated by episodes of deposition of heavy ␦18O and light ␦13C in the shells which was indicative of a pattern of seasonal upwelling. This study, together with the investigations of Killingley & Berger (1979) and Rollins et al. (1987) highlight the geoarchaeological possibilities for investigating ␦13C variations in fossil and sub-fossil mollusc shells to determine the frequency of paleoupwelling events. For example, it may be possible to recognise the frequency and magnitude of ancient El Niño events along the coast of South America using shell material collected from widespread shell middens (Rollins et al. 1987). Preliminary research by Rio et al. (1992) into the ontogenetic change in ␦13C in the shells of the hydrothermal vent bivalves Calyptogena magnifica and Bathymodiolus thermophilus, appears to suggest that the presence of sulphide-oxidising symbiotic bacteria and methane-oxidising bacteria, respectively, in the host tissues, may be responsible for enrichment and depletion of ␦13C, respectively, in the shells when compared with species that do not possess these associations. Analysis of the carbon isotope composition might thus prove to be a useful tool in the characterisation of fossil shells from cold seeps (Rio et al. 1992). “Bomb-signal” chronometry has been used to validate the annual periodicity of growth lines in Arctica islandica from the Atlantic and the North Sea. A pulse of 14C around 1960, resulting from atmospheric nuclear-bomb testing, is recorded in shells of this clam (Weidman & Jones 1993) and has been used to determine radiometrically the growth rate of A. islandica 137

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(Turekian et al. 1982), and as a mark with which to compare the growth line record (Witbaard et al. 1994).

Ontogenetic changes

Bivalves A number of studies have demonstrated in bivalves that the magnitude of the seasonal ␦18O values decline with increasing size and age of the mollusc (Jones et al. 1986, Krantz et al. 1987, Margosian et al. 1987, Dare & Deith 1991, Weidman & Jones 1994, Kennedy et al. pers. comm.) (Fig. 10A, p. 134) and is the result of time integration of samples arising from the slowing down in shell growth with age. Profiles of ␦13C from Spisula solidissima and Placopecten magellanicus show light values in the spring and/or fall associated with seasonal phytoplankton productivity. Trends towards lighter ␦13C values through ontogeny (e.g. Fig. 10B) suggest, in some species, the effects of metabolic changes from a fast-growing juvenile into a sexually mature adult (Krantz et al. 1987). The aragonite shell of the photosymbiont-bearing bivalve Tridacna maxima contains a record of the physiological and environmental changes the organism has experienced during its lifetime. The ␦18O and ␦13C record in the shell significantly changes at ~110 mm (~10 yr) dividing the shell isotope record into two distinct parts (Jones et al. 1986). T. maxima reaches sexual maturity at this size and the change over from the first to the second growth phases is accompanied by a decrease in the rate of calcification and a re-ordering of energy priorities between biomineralisation and reproduction (Jones et al. 1986). Prior to sexual maturity shell growth is fairly rapid in T. maxima occurring all year round, however, at the onset of sexual maturity shell growth rate is limited to the cooler season. At the change over, the ␦13C values become erratic and increasingly depleted and this, it has been suggested, may be due to factors such as erratic feeding by T. maxima and a possible decrease in the role of the symbionts in this bivalve (Jones et al. 1986). The depletion of the carbon values with respect to equilibrium suggest that T. maxima is combining different amounts of light carbon derived from metabolic processes with environmental carbon to form its shell. The production of metabolic CO2 is thought to be derived from the zooxanthellaeenhanced metabolic rate in the host bivalves tissues. The zooxanthellae enhance production of metabolic CO2 by the host which cannot be removed and the carbon pool becomes diluted leading to a depletion of the ␦13C record in the skeletal carbonate (Jones et al. 1986, Romanek et al. 1987). The ␦13C record suggests that the removal of CO2 becomes particularly acute after Tridacna reaches sexual maturity and energy allocation between calcification and reproduction changes. A comparison of the oxygen and carbon isotope record in the symbiontbarren gastropod Terebra areolata collected from the same locality with the record in Tridacna maxima reflected only environmentally-driven changes in the oxygen reservoir used in calcification (Jones et al. 1983, Krantz et al. 1984). It has been suggested that depletion in the ␦13C record may prove useful in identifying the presence of photosymbionts in extinct species of fossil molluscs, such as certain rudists, inoceramids and cardiids which are thought to host algal symbionts (Jones et al. 1986, Romanek et al. 1987). Species possessing photosymbionts need to be in the photic zone and could also prove to be valuable paleodepth indicators. However, some bivalve species, e.g. the heart cockle Clinocardium nuttalli, although possessing photosymbionts do not induce 138

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any effects upon the oxygen or carbon isotopic composition of the shell (Jones & Jacobs 1992). Such photosymbiont associations in photosymbiont bearing bivalves may, therefore, go undetected in analysis of material from the fossil record. Kinetic isotope effects, which are inherent in fast-growing scallop shells Pecten maximus, and horse mussels Modiolus modiolus, tend to favour the incorporation of lighter carbon and oxygen isotopes; the highest values of ␦18O and ␦13C are most likely to reflect equilibrium with the environment (Mitchell et al. 1994). These findings may, therefore, have implications for environmental analyses using isotope data from fast-growing mollusc shells.

Gastropods Many shelled pteropods are planktonic, migrate through the water column and are widely distributed throughout the world’s oceans (Grossman et al. 1986, Jasper & Deuser 1993). Seasonal changes in the hydrography of the upper water column were found to be accurately recorded in the ␦18O variation in the shells of six pteropod species, three non-migratory species, e.g. Cresis acicula and three diurnally migratory taxa, e.g. Styliola subula (Jasper & Deuser 1993). The ␦18O isotopic records in the shell of Cresis acicula were consistent with shell formation above 50 m, whereas the records in the migratory species reflected average calcification depths of between 50–75 m; average ␦13C variations revealed the annual cycle of primary production (Jasper & Deuser 1993). The pteropods Limacina inflata and Cliopyramidata undergo vertical migrations of several hundred metres and their shells reflect water temperatures of the species’ shallower limits (50–120 m) (Kalberer et al. 1993). Pteropods frequently accumulate in Pacific sediment traps (Grossman et al. 1986, Kalberer et al. 1993) and since many large pteropods have life spans of ~1 yr, their shells retrieved from the traps may record past mean annual SST (Kalberer et al. 1993). Bernal (1980) noted differences in the ␦18O between the apex and last whorl of the shell in large specimens of Limacina helicina and related these to environmental changes during growth. Isotopic variations within single shells may, therefore, provide a record of seasonality and migration. Applied to fossil pteropod shells, this method could be useful in paleoceanographic reconstruction (Jasper & Deuser 1993) and provide a record of pelagic seasonality during, for example, glacial epochs (Grossman et al. 1986). However, some shells may not conform to this pattern of growth and may be unsuitable for this kind of study. For example, although the shell of Cuvierina columnella, is large and cylindrical and can be sectioned along the growth lines, it does not grow incrementally and therefore does not contain a clear seasonal record of growth. The shell apparently grows quickly to its final size and shape and then during the remainder of the organism’s life carbonate is deposited in the form of overlapping layers (Grossman et al. 1986). Generally molluscs produce planktotrophic or lecithotrophic larvae, the former depend on smaller planktonic organisms for nutrition whereas the latter type of larvae are nourished by yolk of the eggs from which they develop. This dichotomy of feeding type is readily recognisable using shell morphology (Jablonski & Lutz 1980). In the deep sea many prosobranch gastropods are thought to have planktotrophic development based on their larval shell morphologies. Patterns of dispersal in the water column for this type of larvae are almost completely unknown (Killingley & Rex 1985). Larvae may migrate vertically to surface waters, disperse at midwater depths, have development in the benthic boundary layer or employ some combination of these alternatives (Lutz et al. 1980, Killingley & Rex 1985). Analyses of the d18O composition of the shells from both adults and larval stages from nine species of prosobranchs enabled 139

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Killingley & Rex (1985) to unravel the pattern of dispersal of the larvae in the water column. Larval and adult shells of lecithotrophic species had similar ␦18O, reflecting larval development in an egg capsule on the sea bed with little or no dispersal. Whereas the planktotrophic species showed differences in ␦18O between larval and adult shells, indicating that the larvae migrate vertically to warmer surface waters. Ontogenetic changes similar to those described for bivalves have been recorded in the shell of Strombus (Wefer & Killingley 1980). In shells in which the spire had not been eroded it was possible to match the ␦18O curves with the ambient seawater temperature curve and estimate their time of settlement. Using ␦18O measurements, Wefer & Killingley (1980) established that the lip of the shell of Strombus was constructed within 0.5 yr, and thickened within 2.5 yr. It was also found that during the first 3 yr of growth the conch shell grew preferentially during the warmer months of the year, whereas in later life carbonate was deposited during both the warm and cool seasons. Since large conchs tend to move offshore into deeper water it might be possible to observe, from the ␦18O shell record, differences in SST and estimate the time the snails migrated inshore and offshore (Wefer & Killingley 1980).

Cephalopods The habitat and ontogeny of Nautilus pompilus have been inferred from the ␦18O and ␦13C record in the septa of the shell (Cochran et al. 1981). A pronounced break in ␦18O from nearly uniform light values in the first seven septa to heavier values after the seventh septum corresponded to the hatching of N. pompilus. Similar findings were obtained for N. macromphalus (Taylor & Ward 1983). However, an attempt by Cochran et al. (1981) to extract a temperature (water depth) interpretation from the ␦18O data for the eighth and remaining deposited septa was complicated by a positive correlation between ␦18O and ␦13C, otherwise information on patterns of vertical migration might have been obtained from the shells. The isotopic composition of the cuttlebone of fossil and living specimens of Sepia and its relatives might be useful, however, in both palaeographic and bioecological research and provide information on the environmental conditions of growth (Bettencourt & Guerra 1999).

Elemental records in mollusc shells The possible use of mollusc skeletal parts as an indicator of elements in ambient sea water has received considerable attention. Living molluscs provide an integrated record over time of elements accumulated from their aquatic environment in concentrations generally proportional to those in sea water (Carriker et al. 1982). Thus, theoretically, estimates of the degree of incorporation of elements could be made by measuring the relative concentration in the calcified hard parts of molluscs. Bivalves can accumulate elements, compounds and other particles adventitiously in their shell margins during shell formation. Active incorporation of minor and trace elements during bivalve shell formation varies with taxonomic species, ontogeny, seasonal and environmental concentrations of elements in ambient sea water, and physiology, shell mineralogy and microgrowth increments within the same shell mineral type (Carriker et al. 1991, 1996). 140

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Bivalves Bivalve shell mineralogy is known to reflect both environmental and biological factors, but that the relative importance of temperature, salinity and genetics varies among taxa (Carter & Seed 1998). A general relationship between low temperature and the evolution of calcite was proposed by Lowenstam (1954a,b) and later by Dodd (1963, 1965a, 1966), who in his evaluation of three northeastern Pacific Mytilus, demonstrated correlations between both salinity and average annual temperature and shell size, thickness, percentage aragonite and/ or calcite. Subsequent studies (e.g. Malone & Dodd 1967) have, however, shown, that the influence of temperature on Mytilus shell mineralogy is difficult to characterise because of the confounding effects of shell size, shell thickness, spawning season and other factors. Nevertheless the presence of calcite in some of the subfamilies of the Mytilidae partially correlates with species preference for cool temperatures (Carter 1980). Most analyses of the chemical composition of bivalve shells have been carried out on the entire shell, one of the valves, shell layers, or randomly selected spots within the shell valve. Because chemical composition can vary from one part to another in the shell of a bivalve, as well as ontogenetically, an analysis of one part of the shell may not necessarily give concentrations typical of the whole shell (Carriker et al. 1996). The shell record of environmental minor and trace elements and anthropogenic enhancements has promise as a potential tool for studying the effects of environmental controls on mineralogy. A variety of techniques have been used to measure the concentrations of minor and trace elements in molluscan hard parts. Techniques such as flame photometry (Dodd 1965b), X-ray fluorescence spectrometry (Hallam & Price 1968, Bourgoin & Risk 1987, Thorn et al. 1995), atomic absorption spectrophotometry (Carriker et al. 1980, Dodd & Crisp 1982), cathodoluminescence (Barbin et al. 1991, Barbin 1992), electron microprobe (Rosenberg 1973, Rosenberg & Jones 1975, Lutz 1981) have helped to expand our understanding of the distribution of elements in mollusc shells. Development of proton microprobe (µ-PIXE) (Carell et al. 1987, Coote & Trompetter 1995, Kuisma-Kursula et al. 1995, Carriker et al. 1996), instrumental neutron activation analysis (INAA) and a-track autoradiography (Carell et al. 1987) and more recently the development of laser ablation inductively coupled plasma spectrometry (LA-ICP-MS) (Gray 1985, Jarvis et al. 1992) have opened up the possibility for studying a range of elements in the chemical record of growth. Analyses are usually undertaken using the shells of organisms that have been sacrificed. In a novel approach, Carriker et al. (1982) scoped the feasibility of monitoring ontogenetic changes in the chemical elements in the shells of live oysters. Organisms were periodically removed from their environment, placed in an atmosphere of a neutral gas at concentrations as low as a few parts per million and the shells analysed with a proton microprobe, and then returned to their habitat. The distribution of several elements in various parts of the bivalve shell has been studied in thin sections of the chondrophore of Mya arenaria (Sr: Ca ratios, Palacios et al. 1994), in the nacreous layer of Mytilus edulis (e.g. Sr, Lutz 1981; Pb, Bourgoin 1990), the prismatic layers of M. edulis (e.g. Sr and Mg, Dodd 1965a) and Crassostrea virginica (e.g. Mg, Carriker et al. 1980) and the foliated calcite of C. virginica (e.g. Sr, Carriker et al. 1980; Mn, Barbin et al. 1991). Differences were also noted in the distribution of certain elements in the shell valves of rapidly growing C. virginica. Elements were concentrated in the prismatic region and the inhalant margins of the right shell valve, while on the left valve they were concentrated around the exhalant margin (Carriker et al. 1991). In areas where the exterior surface of the prismatic layer of the oyster shell had weathered, Carriker et al. 141

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(1991) noted that Mg, Si and Mn levels increased, whereas Na, Al, Cl, Ti, Fe, Br and Sr showed a decrease. Calcium carbonate in molluscan shells incorporates trace and minor elements primarily through atomic substitution (Dodd 1967). Mann (1992) has suggested that since Mg2+ and Sr2- are diadochic with Ca2+ in the crystal lattices of aragonite and calcite, the degree of ionic substitution in these minerals differ. The aragonitic lattice favours substitution for calcium ions with radii greater than Ca2+ such as Sr2-, whereas the calcite lattice favours ions with radii less than that of Ca2+, such as Mg2+. Because of its size, Mn2+ will theoretically fit more readily into the calcite than the aragonite structure (Mann 1992). The effects of temperature and salinity on elemental concentrations in minerals has been experimentally determined for inorganically precipitated aragonite and calcite (Mann 1992); strontium concentrations correlate negatively with temperatures in aragonite and calcite (Holland et al. 1964; Katz 1973; Lorens 1981). Pingitore & Eastman (1986) showed a positive correlation between Sr concentration in calcite and the Sr level of the solution. A positive correlation exists between Mg concentration and temperature in calcite (Burton & Walter 1987). Although the solubility concept in simple salt solutions can be readily understood and quantitatively defined it becomes quite complex within biological systems. Many investigations have documented correlations among elemental concentrations in skeletal carbonate with temperature and salinity (Mann 1992). Some of the literature shows conflicting results including positive, negative and non-correlation among trace elements concentrations and environmental variables. These discordant results clearly indicate environmental factors do not uniformly and directly control Mg and Sr concentrations in skeletal carbonate (Mann 1992).

Strontium thermometry Strontium thermometry is potentially a powerful tool for reconstructing SST and is based on an inverse relationship between water temperature and Sr: Ca ratios in scleractinian corals. There are a number of living bivalve species that could provide potential watertemperature records in the temperate oceans and estuarine environments if a suitable strontium-temperature relationship were derived. Numerous workers have studied the relationship between strontium concentration within the molluscan shell and temperature, often with apparently conflicting results (Lutz 1981). For example Pilkey & Goodell (1963) demonstrated significant correlations between temperature and Sr in the shells of the saddle oyster Anomia simplex (inverse relationship), and the slipper limpets, Crepidula fornicata and C. plana (direct relationship). Dodd (1965b) demonstrated seasonal variations in the Sr content of both the calcite and aragonite in Mytilus edulis shells and reported a small positive correlation between Sr and seawater temperature in the calcite outer prismatic layer of the shell, whereas Sr was inversely related to temperature in the aragonitic nacreous layer. However, while Lutz (1981) could not detect any apparent variation in Sr in the aragonite shell of M. edulis, Hallam & Price (1968) demonstrated in Cerastoderma edule shells collected from a range of environments in Europe with differing temperatures and salinities, a negative correlation between Sr and the average July water temperature; however, the within-site variability was quite large. Translucent growth lines in the chondrophore of fossil and modern Mya arenaria were found to contain higher Sr : Ca ratios than the areas between the translucent lines (Palacios 142

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et al. 1994). These cycles of high and low Sr: Ca ratios in profiles of the chondrophore could constitute a useful ancillary criterion for age validation of these soft-shelled clams (Palacios et al. 1994). Seasonal changes in the concentration of Sr were noted in the shell of a modern Spisula solidissima and both a modern and fossil Pleistocene Mercenaria mercenaria; a decrease in Sr was associated with the winter period in M. mercenaria and with the summer growth decrease in Spisula solidissima (Stecher et al. 1996). A positive, significant correlation between the average Sr: Ca ratio and estimated age in Mya arenaria is suggestive of an ontogenetic trend which could be related to age, growth rate or both (Palacios et al. 1994). By contrast, larger Mytilus edulis shells were found to have a slightly lower Sr concentration at a given temperature (Dodd 1965b). Fresh water and sea water usually differ considerably in their Sr: Ca and Mg: Ca ratios. These ratios increase rapidly with salinity to about 10 but subsequently remain nearly constant (Dodd & Crisp 1982). The source of most of the Ca, Mg and Sr in mixtures of fresh water and sea water is the latter, thus except at low salinities the trace element to Ca ratio of mixtures will differ little from that in sea water. Thus Dodd (1965b) found that salinity variation did not appear to affect the Sr concentration of the outer prismatic layer of M. edulis, although the Mg concentration in this layer increased markedly with decreasing salinity and showed a weak correlation with temperature. A good correlation between the boron content of the shell of M. edulis and salinity was found by Furst et al. (1976). In the absence of experimental evidence to relate shell growth to gametogenesis, Coote & Trompetter (1993, 1995) have speculated that distributions of Sr and F detected in the shells of various bivalves (e.g. Paphies subtriangulata, Crassostrea gigas and Tiostrea spp.) using a proton microprobe, may have been deposited during the annual spawning periods. It is thought that living molluscs are able to discriminate more efficiently than ancient molluscs against Sr relative to Ca in sea water, so that modern mollusc shells generally contain lower Sr: Ca ratios than ancient shells (Ragland et al. 1969). The average Sr: Ca ratios of fossil gastropod and bivalve shells were found to be consistently different from those of recent shells (Ragland et al. 1969). Although it has been speculated that the trace element to Ca ratios of mollusc shells could be used to determine the palaeosalinity of past environments, Dodd & Crisp (1982) suggest that these ratios only offer potential for palaeosalinity determinations in waters of salinity of about 10.

Cephalopods Daily increments were most clearly defined in areas of high Sr content in the statoliths of juvenile and adult chokka squid, Loligo vulgaris reynaudii. Strontium was concentrated in the wing and adjacent areas, whereas Ca concentrations were highest on the edge of the lateral dome. By contrast Sr and Ca were uniformly distributed in the statoliths of paralarval squid (Durholtz et al. 1997). Cyclic changes in Sr were apparent in the septa and venter of two Nautilus species and Price & Hallam (1967) suggested that the observed Sr peaks might be correlated with winter seasons. They further speculated that the observed secular decline in Sr might either be related to migrations during the first few years of life from cooler to warmer waters or that the changes might be unrelated to the environment and simply be the result of an ontogentic trend. Although Mg and Sr concentrations displayed greater variability in juvenile portions of the shell of Nautilus than in the mature portions, the decreased growth rate displayed by the 143

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shell as it approached maturity did not apparently affect the Mg or Sr concentrations (Mann 1992). Mann (1992) suggested that either the physiochemical system matures during ontogeny and achieves increasing control over skeletal chemistry or the organism adjusts to the new conditions and behavioural maturation stabilises elemental concentrations by reducing stress. Concentrations of Mn, inferred from cathodoluminescence of aragonite, increased in the shells of N. pompilus and N. macromphalus with ontogeny and luminescence correlated with the growth lines (Barbin 1992).

Combined isotope and elemental analyses Recently a combined approach in which the element ratios and the isotopic composition of molluscan shells have been studied has aided in understanding the relationships between temperature and salinity and element incorporation (Klein et al. 1996a,b, Leng & Pearce 1999). As has been shown previously palaeotemperature has been widely deduced from skeletal 18O : 16O ratios, but these ratios are dependent on salinity. Without an independent measure of salinity, 18O: 16O ratios cannot provide accurate data on past temperature and climate (Klein et al. 1996a). Using a comparison of the Mg: Ca ratios and 18O: 16O ratios in sequential samples drilled from the shells of experimentally marked Mytilus trossulus with direct measurements of seawater temperature and chemical analyses of the sea water, Klein et al. (1996a) demonstrated that Mg: Ca ratios could provide an accurate weekly estimate (~±1.5°C) of seawater temperature. In a study of the effect of metabolic activity (vital effects) on skeletal Sr: Ca ratios in the shell of M. trossulus, Klein et al. (1996b) concluded that Sr: Ca ratios are primarily related to variations in metabolic activity, but may be modified by salinity variation. Skeletal Sr: Ca ratios were found to be significantly higher in the shell of a fast-growing mussel (i.e. those with low mantle metabolic activity) compared with those in an older slow-growing specimen, suggesting fast-growing mussels may be useful in recording variations in seawater salinity (Klein et al. 1996b). Variations in trace elements and isotopic composition in the shells of Mactra isabelleana from marine and estuarine environments along the coast of Argentina were recorded by Leng & Pearce (1999). They found cyclic variations in Sr, Mg and Ba in the estuarine shells which matched closely the variation in ␦18O and ␦13C. The highest concentrations of these elements were coincident with ␦18O peaks although there was a lack of statistically significant correlations between the trace elements and isotope data, suggesting that the patterns of trace element variations cannot only be related to environmental factors, although predominantly controlled by them (Leng & Pearce 1999). The absence of any correlation between isotopes and trace elements in the marine shell tends to suggest physiological effects, rather than environmental control, over the incorporation of trace elements into the shell.

Upwelling Biogeochemical profiles in mollusc shells are potentially important tools for studying the dynamics of both modern and ancient continental upwelling systems (Krantz et al. 1988). Studies of the geochemistry of Cd in the oceans have provided insights into oceanographic processes related to primary productivity and ocean circulation (e.g. Bruland 1980). Limited evidence suggests that molluscs similarly incorporate Cd into their shells in proportion to 144

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ambient seawater concentrations (Sturesson 1978, Carriker et al. 1980). Despite the prediction that Ca: Cd ratios in mollusc shells should contain a record of the hydrographic conditions during the life of the organism, Krantz et al. (1988) were unable to demonstrate unequivocally that these ratios in the shells of Argopecten gibbus and Placopecten magellanicus accurately reflected Cd concentrations under normal environmental conditions. They did, however, observe that nutrient inputs and subsequent phytoplankton blooms were recorded in the carbon isotope and Cd: Ca profiles in scallops collected from the outer continental shelf of the south Atlantic Bight and the Virginia Bight. Shell profiles from the Virginia Bight showed the influence of spring runoff and summer water-column stratification. Stecher et al. (1996) suggested that marked increases in Ba concentration in the shell of Mercenaria mercenaria were linked to periods of phytoplankton productivity. The 1982–83 El Niño event along the Peruvian coastline resulted in anomalous or insignificant chemical differences in the shells of Chione subrugosa and Trachycardium procerum between the pre- and post-El Niño events (Rollins et al. 1987). In T. procerum the Sr: Na ratios decreased in the shell increment deposited after the El Niño while in Chione subrugosa the Sr: Na ratios were not significantly related to El Niño.

Metal pollution analysis The use of mollusc shells as sentinels for metal pollution monitoring in marine waters has several advantages over that of the soft tissues. The shells are easy to store and handle and appear to be sensitive to environmental heavy metals over the long term. Since shell growth occurs incrementally they can provide a signal over a discrete time period, unlike the tissues which are strong accumulators of metals and integrate the chemical contamination signal over the life of the organism. Refinement of techniques for determining elements using bivalves is important if global monitoring is to become a reality (Goldberg 1975, Goldberg et al. 1978, Phillips 1980). The accumulation of metals has been mainly studied from the content of the soft tissues. However, metals can accumulate in the shell, which can act as a receptor for these metals (Lin & Liao 1999). Koide et al. (1982) found Cd, Zn, Pb and Ag levels were higher in the tissues of Mytilus edulis and M. californianus than in the shells, although Cu was greater in the shell than in the tissues. Bourgoin (1990) demonstrated that Pb levels in the nacre of M. edulis collected from near a lead smelter off the coast of Quebec and Dalhousie, Canada, were only a tenth of the levels in the tissues. By contrast, lead levels in whole shells of the New Zealand cockle Chione (Austrovenus) stutchburyi were similar to those in the soft tissues with a good correlation between shell size and the highest Pb concentrations (Purchase & Fergusson 1986). Lead levels were highest in the umbo region (oldest part) and lowest in the posterior younger regions of the shell. Cadmium, Cu, Mn and Zn were found to be most concentrated in the prismatic calcite layer of the shell of the oyster Crassostrea virginica (Carriker et al. 1980). Whereas much of the Mn detected in the shell of Scrobicularia plana was incorporated in the matrix, an appreciable amount of Cu, Fe and Zn was thought to be incorporated directly from solution by adsorption (Bryan & Uysal 1978). Lead and Cd enrichment of Mytilus edulis shells has been demonstrated experimentally by Sturesson (1976 and 1978, respectively). Mollusc shells could prove useful in providing an historical record of contamination. Bertine & Goldberg (1972) analysed the shells of M. edulis and the razor clams Ensis siliqua 145

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and E. directus, which had been collected from the Belgian coast during the past 100 yr and curated in museum collections, but could find no evidence of a recent increase in metal contamination as a consequence of man’s activities. Chow et al. (1976) found that where there were high concentrations of human populations and large amounts of anthropogenic inputs from adjacent land into the coastal environment, Mytilus edulis and M. californianus shells displayed unusually high levels of Pb. The relationship between human habitation and industrialisation, and concentrations of metals in mollusc shells has been explored on numerous occasions. Markedly higher concentrations of metals (Cd, Cu, Zn, Pb, etc.) were found in the shells of M. edulis and M. californianus collected from industrialised and populated areas, compared with those in areas devoid of societies (Koide et al. 1982). Bourgoin & Risk (1987) in a comparison of lead levels in the shells of recent and fossil Mya truncata (8200 BP) from the Northwest Territories in the eastern Canadian Arctic, found lead levels were five times lower in fossil shells than modern individuals. Interestingly, concentrations were not significantly different between the modern shells from a control site and a municipal dump site. The freshwater bivalve Margaritifera margaritifera is worthy of mention here since an analysis of the ~100-yr incremental record in the shell has revealed decreases in Ag, Au, Fe and Co, whereas Mn and S have increased strongly in response to acidification of some of the rivers in central Sweden after 1940 (Carell et al. 1987). Geographical variations in the Cu, Zn and Pb content of the shells of the limpet Patella sp., collected from the rocky intertidal coastline of Wales, were accounted for by differences in their exposure to drainage water from Pb, Zn and Cu mines discharging into Cardigan Bay, Wales (Perkins 1992). A combination of growth increment analysis with elemental investigations is a powerful tool for interpreting the high resolution, detailed record preserved in marine mollusc shells. The development of laser ablation ICP-MS (LA-ICP-MS) has opened up the possibility of ablating and analysing discrete portions of the incremental record (see Fig. 11). Using LAICP-MS analysis, Price & Pearce (1997) demonstrated in spot samples taken across shell

Figure 11 Photomicrographs of 50-µm shell sections of Modiolus modiolus shells to show A, the positions of the annual growth lines (arrows). IN: inner nacreous layer, PL: prismatic layer. B, C, positions of the laser ablation rasters (AR). (From Richardson et al. 2001.)

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profiles of Cerastoderma edule from a number of sites in the British Isles that growth periods in the shells between 1993 and 1995 were characterised by short-term fluctuations in Zn and Cu. However, they were unable to demonstrate any correlation in the events among the shells, any obvious trends with time or any obvious seasonal changes related to temperature or salinity. These investigators speculated that the observed elevated metal levels in some of the shells might have been caused by contaminated river water runoff from mining and mineral processing and local contamination from electroplating effluent. Richardson et al. (2001) investigated concentrations of the contaminant metals Cu, Pb and Zn along shell profiles (Fig. 11) of six Modiolus modiolus collected in 1984 from two sites in the southern North Sea, an “impacted dump” site and a “control” site. The impacted site to the east of the Humber estuary had historically received a mixture of sewage sludge and industrial waste while the other control site, off the Norfolk coast, was distant from known point source inputs. Since individual M. modiolus can attain ages of ~30 yr and each shell contains a clear annual incremental growth record (Anwar et al. 1990) each increment could be assigned a date, thus enabling changes in metal concentrations in the shell during the past 20 yr (1964–84) to be investigated. Differences in metal levels were found between the two sites, specifically between 1968 and 1976, with significantly elevated levels of Pb and Zn in the shells from the dump site which were not observed in the control site shells (Fig. 12). The implementation of the Dumping at Sea Act (1974) and subsequent decline in dumping in the North Sea may be the cause of this observed decrease in metals in the impacted site shells (Richardson et al. 2001).

Future research goals The validation of annual growth lines within the shells of long-lived species such as Arctica islandica has opened up the possibility for investigating long-term trends in the environment from the growth record. Using suitable material it may be possible to construct long-term chronologies (500–1000 yr) of variations in growth from the incremental record. Together with stable isotopes as proxies for seawater temperature and elemental analyses, bivalve shells could be used to investigate both climatic change and changes in environmental quality in the marine realm. In the future, statolith ageing studies could be used to analyse the life histories of species, including oceanic squids, to obtain life-history information for poorly known species (Jackson 1993). Ecological uses of statolith increment analyses such as temporal or geographical variations in growth responses to ambient biological or physical features, and how increment width patterns within the statolith microstructure reflect ambient changes in food availability and temperature could be ascertained (Jackson 1994). With the development of techniques for fine resolution sampling of increments it may be possible to obtain stable oxygen isotope records across the cephalopod statolith and provide a chronology of water temperature records that could be used to track the movement of squids through waters of different temperatures. Age specific information on the timing of maturation and duration of spawning may be revealed from the statolith increment patterns. Obvious zones or prominent checks within the statolith could be used to determine the length of time an individual squid spends in the pelagic zone before settling into its demersal habitat, thus providing information on past habitats and environmental perturbations. 147

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Figure 12 Annual variation in copper (Cu), zinc (Zn) and lead (Pb) concentrations in the shells of Modiolus modiolus from a dump site (A, C, E) and a control site (B, D, F) in the southern North Sea. (From Richardson et al. 2001.)

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The effects of physiological variables and ecological factors on the distribution and concentration of chemical elements in the shell should be explored, together with the extent to which elemental chemistry of the shell varies randomly or progresses systematically during growth, and the extent to which the environment can modify these patterns needs to be studied. Some of these questions are at present being addressed and with the progressive refinement of analytical techniques, opportunities will arise for studying the various environmental factors controlling the incorporation of chemical elements into the shell.

Acknowledgements The late Alan Ansell was instrumental in persuading me to begin researching and writing this review. His untimely death in 1999 encouraged me to forge ahead and complete the task. I am grateful to Jess Taylor for her sterling efforts and continued perseverance in locating the literature to enable me to write this review and to David Roberts for his help in producing the figures.

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Oceanography and Marine Biology: an Annual Review 2001, 39, 165–205 © R.N.Gibson, Margaret Barnes and R.J.A.Atkinson, Editors Taylor & Francis

THE EVOLUTION OF EYES IN THE BIVALVIA BRIAN MORTON The Swire Institute of Marine Science and Department of Ecology and Biodiversity, The University of Hong Kong, Hong Kong, China e-mail: [email protected]

Abstract A pair of cephalic eyes located on the axes of the anteriormost filaments of the inner, left and right, demibranchs of the ctenidia and comprising simple, sensory pigment cups, occurs in many representatives of the Arcoida and Pterioida. Such eyes, linked to the cerebral ganglia, also occur in some larvae and may represent an adaptation that is retained into adult life in only a few older bivalve lineages. Ectopic pallial eyes also occur in many representatives of the Arcoida and Pterioida on specialised sub-folds of the outer mantle folds and are typically most numerous posteriorly. These, too, are generally of simple construction and in the Arcoida comprise either a sensory cap or cup of pigmented and sensory cells. The cells of the sensory cap are formed into an “ommatidium-like” eyespot. Sensory reception is, moreover, ciliary-based in the former and microvillous in the latter so that the ommatidial structure is analogous to, not homologous with, eyes of superficially similar design in other phyla, notably the Arthropoda. More complex invaginated eyes occur in Enigmonia (Anomiidae) and Ctenoides (Limidae) on the outer mantle surface and the middle folds, respectively. The most complex, inverse pallial eyes occur on the middle mantle folds in representatives of the Pectinoidea. They have a lens, double ciliary distal and microvillous proximal retina, argentea and pigment cup. Somewhat simpler pallial eyes occur in the Cardioidea, including the Tridacnidae, on the inner mantle folds, but there is still a lens, sensory retinal cells, argentea and either a pigmented tentacle epithelium (Cardiidae) or zooxanthellae serving as a reflecting surface (Tridacnidae). Eyes virtually as complex as those of the Pectinoidea occur in the Laternulidae (Anomalodesmata: Pandoroidea) but on the inner mantle folds. A ciliated, accessory sense organ accompanies more complex bivalve pallial eyes and is especially well-developed in Laternula. Pallial eyes are thus of seemingly stochastic occurrence in the Bivalvia and their progressive sophistication has not, hitherto, been thought to follow a general plan. This is not so, however, and increasing sophistication follows a loose phylogenetic timetable; that is, older lineages have simpler eyes whereas the eyes of younger lineages are more complex. Moreover, each eye is structurally unique to each family and its representatives. The function of such complex eyes remains problematical. Virtually all bivalves, even those with no eyes, have a shadow “off” reflex which provokes adduction, siphonal retraction or digging, or a combination of all three reactions. Those with the most complex eyes do little more when stimulated by a shadow. Laternula truncata (Laternulidae), for example, simply flicks sand grains over the siphonal apertures to camouflage them. Members of the Pectinoidea with an “off” and an “on” response to light can detect adjacent movement and could, theoretically, respond to this by swimming. They rarely do, however, and adduction is the usual response and usually only after either mechanical or chemical stimulation. The pectinid eye can also form a simple image but this is probably not resolvable in the optic lobes of the visceral ganglia which receive such stimuli and initiate a response to them. Ectopic eyes, in particular, may have developed from the expression of the eyeless (ey)

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homeobox gene, as in other metazoans. But, more importantly, why have such complex eyes evolved when simpler ones in other bivalve phylogenies seem able to achieve the same defensive response, and an even wider array of equally successful lineages, notably the numerically dominant Heterodonta, have no eyes? The concave mirror, or argentea/tapetum, of the pectinid eyes with a retina positioned at the focal point allows movement but not objects to be detected on the distal retina. This structure makes such an eye more efficient at low light intensities, thereby improving the chances of predator avoidance over, effectively, a longer length of the day and/or at greater depths. Such variations in light intensity are detected on the proximal retina. In the Bivalvia, therefore, miniscule improvements in visual acuity, that is, spatial resolution but not spatial vision, have conferred a selective advantage over evolutionary time. Natural selection operates upon each eye structure to improve it at independent paces in the lineages that possess them so that there has not been, until now, a distinguishable picture of phylogenetic improvement with time as there is with the cephalic eyes of the Gastropoda. Rather, there is individual sophistication as and when the ey gene is expressed stochastically. Increasing sophistication of a few eyes (as in the Pectinoidea and Laternulidae) may also be energetically less expensive than thousands of them (as in the Arcoida), conferring yet another selective advantage.

Introduction There are numerous publications on bivalve eyes and this paper will identify and discuss most of them. Broadly, such studies fall into three categories: anatomy, behaviour and physiology, and only a few discuss the evolution of the eye, usually in the context of the Mollusca as a whole (Milne & Milne 1956, Salvini-Plawen & Mayr 1977, Salvini-Plawen 1982). In a recent essay, Dawkins (1997) pointed out that even Charles Darwin was assailed by doubts that such a complex structure as “the eye…, could have been formed by natural selection, seems, I freely confess, absurd in the highest possible degree.” (Darwin 1859:217). Dawkins also quotes from an unpublished essay by Darwin written 15 years before On the Origin of Species, as follows: “[the human eye] may possibly [my italics] have been acquired by gradual selection of slight but in each case useful deviation.” The quotation from On the Origin of Species, is, however, completed as follows: Yet reason tells me, that if numerous gradations from a perfect and complex eye to one very imperfect and simple, each grade being useful to its possessor, can be shown to exist; if farther, the eye does vary ever so slightly, and the variations be inherited, which is certainly the case; and if any variation or modification in the organ be ever useful [my italics] to an animal under changing conditions of life, then the difficulty of believing that a perfect and complex eye could be formed by natural selection, though insuperable by our imagination, cannot be considered real. Even into the early part of the twentieth century, however, a leader in the study of bivalve eye structure, Dakin (1928a) believed that the development of pallial eyes in swimming pectinid bivalves was not determined by natural selection but was an example of orthogenesis, that is, they develop for no reason. Morgan (1903) also thought that some organisms, or their features, seem to be either too well or overly adapted for their surroundings and that, as a consequence, it was not proper to evaluate features and adaptations from a purely utilitarian perspective. Such views, when applied to the seemingly inexplicably complex

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bivalve, notably pectinid, pallial eye are possibly why Charles (1966) could find no underlying plan to its development, why no phylogenetic trend of increasing sophistication has been recognised and why nobody has attempted to explain their evolution in terms of natural selection except Nilsson (1994). Eyes have evolved independently many times throughout the animal kingdom, SalviniPlawen & Mayr (1977) suggesting no fewer than 40 and possibly as many as 65 times. Salvini-Plawen (1982: fig.4) provides a phylogenetic tree of eye evolution that illustrates how structure basically reflects relationships. Nilsson & Pelger (1994) computed the number of changes in the structure of a flat layer of photocells, with a black backing and transparent cover, assuming a 1% change per generation, necessary for it to transform into a vertebrate, fish, eye. The model took but 1829 steps to achieve this transformation. It is, therefore, actually, remarkably easy for a complex eye to evolve very rapidly. Nilsson & Pelger’s final pessimistic estimate required only 364000 generations to evolve a good fish eye with a lens. The most complex bivalve eyes occur in representatives of the Pectinoidea and have been studied by many authors (Morton 2000a). They are sophisticated enough to be able to form an image, an observation first reported by Patten (1886) and Wenrich (1916) and explained by Land (1978, 1981:536; fig.36c). It is considered that such eyes allow the possessor to avoid predation, although, as Morton (2000a) argues, this is not so welldocumented as generally believed. It could be that function varies from eye to eye. Yonge (1936a), for example, believed that the hyaline organs (eyes) of the Tridacnidae focus light on the zooxanthellae in the mantle tissues beneath them. There are, however, two categories of eyes in the Bivalvia. The first are “true” branchial, or cephalic, eyes that occur in only some bivalves and are positioned at the bases of the anteriormost filaments of the left and right inner demibranchs of the ctenidia. They have nervous connections with the cerebral ganglia. The second are “ectopic” (Dawkins 1997) pallial eyes that occur only in some bivalves, typically on the posterior mantle margin, often in association with the siphons and have nervous connections with the visceral ganglia. Again, however, virtually all bivalves must have some kind of pallial photoreceptors because they all, with the exception of cave-dwelling, e.g. Congeria kusceri (pers. obs.) and abyssal species, have a “shadow reflex”. This reflex is an “off” response to a shadow passing over the siphons causing, for example, the shell valves to shut, the siphons to retract or digging to be initiated. Such simple photoreceptors, which are possessed by most bivalves, are pallial and difficult to identify even in the best prepared histological sections. Sharp (1883, 1884) first “identified” simple photoreceptors, or retina cells, in the mantle margins of Ostrea virginica, Mytilus edulis, Venus mercenaria, Mya arenaria, Dreissena polymorpha, Solen ensis and S. vagina. Such cells may be photocells or, possibly, the pigmented figments of Sharp’s imagination. Notwithstanding, some such light-sensitive cells must exist and Darwin (1859:217) pointed out that “any sensitive nerve may be rendered sensitive to light”. This does appear to be the case and Kennedy (1960) showed that the pallial nerves of the eyeless bivalve Spisula solidissima each contain a single afferent fibre which responds directly to illumination and apparently mediates the shadow reflex of siphonal retraction. This paper, however, focuses on true cephalic and discernible ectopic pallial eyes, their distributions within the Bivalvia, their structure and function(s) and, finally, their evolution and the underlying mechanism of natural selection that has effected their development. It is function that is most intriguing because, for a number of reasons, which will be discussed, even the most complex eyes elicit in their possessors no more than the simplest

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defensive response when stimulated, even the swimming taxa of the Pectinidae. The following are arguments against visual acuity in the Bivalvia. 1.

2.

3.

4.

5.

6.

Bivalves are the classic example of sedentary organisms, even the most actively swimming scallops, e.g. Amusium pleuronectes (Morton 1980) and A. balloti (Joll 1989), do so very infrequently and only when mechanically stimulated vigorously. If complex pallial eyes are for protection, as seems most plausible, the question must be: from what? That is, if the only escape response is to shut the shell valves, retract the siphons, dig deeper or, even, in the most extreme case of the Pectinidae, swim away, then the simplest pallial photoreceptors are all that is necessary to give such a signal warning of impending danger. As pointed out by Nilsson (1994:206) “ark clams…are equipped with an absurd [my italics] number of eyes”. Land (1978:129) also points out: “Why there are so many proximal photoreceptors in the scallop remains a mystery. With 60 eyes and 5000 proximal receptors per eye, the mollusk has some 300000 cells doing a job that could be done adequately by perhaps a dozen.” If eyes are for protection, as in the case of scallops, for example (Yonge 1936b), why is it, in reviews of bivalve protective mechanisms, structural (particularly of the shell), behavioural and physiological defences are always highlighted but eyes are usually not mentioned (e.g. Harper & Skelton 1993)? In terms of anti-predation devices, more has been written about the abilities of some bivalves to autotomise various parts of their bodies, particularly the siphons, e.g. Solen (Stasek 1967, Morton 1984a) and pallial tentacles, e.g. Lima (Gilmour 1967) and Galeomma (Morton 1973a), in these cases also releasing noxious secretions, and the production of concentrated sulphuric acid from a remarkable pallial organ in species of Atrina (Pinnidae) (Liang & Morton 1988), than the defensive function of eyes. Only Nilsson (1994) addresses this issue comprehensively, likening arcoid eyespots to light-sensitive burglar alarms rather than sophisticated, image-forming eyes. If scallop eyes can form a simple image at the focal point and detect movement, what is the point of developing such a sophisticated light receptor when it is unlikely that the central nervous system could form any picture of an advancing predator? “It is, for instance, doubtful if they [Pecten maximus] can perceive images at all clearly” (Rees 1957:23). Bivalves are essentially acephalic. The range of pallial eye structure in bivalves is wide, despite the very restricted distribution of such photoreceptors in the class. A further question must therefore be, why has such a diverse array of optical structures evolved when they have not in the more active and diverse Gastropoda? Notably, why have the complex pectinid and laternulid eyes evolved when a suite of simple photoreceptive cells is collectively sufficient for the detection of changes in light intensity or adjacent movement? If complex eyes are more useful, for example, in detecting predators, why do not all bivalves possess them, rather than simple light-sensitive cells? Why are they restricted also to only some species in a few genera in a narrow range of families? Moreover, as has been discussed (Nilsson & Pelger 1994), if a complex eye can be evolved easily and quickly, why have not simpler eyes in older lineages progressively evolved into more complex ones? A corollary to this question is: why do only a few bivalves have such eyes, when the vast majority do not and are apparently no less “successful”? Finally, Darwin argued (see earlier) “if any variation or modification in the organ should be ever useful [my italics] to an animal…a perfect and complex eye could be formed by natural selection”. As described above, however, even the most complex pallial eyes of some bivalves seem to confer little additional usefulness 168

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other than the detection of movement. If this is so, what is the driving force selecting for their evolution? Morton (2000a), for example, has questioned the popular belief that starfishes are major scallop predators and there are no records of pectinids responding to fish by swimming and only two of scallops (and both are anecdotal) swimming in response to changes in light intensity in the natural environment (Ansell et al. 1998a, Dibden & Joll 1998). There is a large literature, however, which has demonstrated through studies of nerve discharges in the laboratory, that scallops do respond to light being turned on and off (Land 1966a,b). Light responsiveness is not disputed and will not be discussed further. Of more interest is the question of the selective advantage of the response. This paper reviews the occurrence and structure of bivalve cephalic eyes and examines the range in form of ectopic pallial eyes and ascribes to them a loosely progressive pattern of increasing phylogenetic sophistication with time. It seeks explanations for both sets of observations and discusses the underlying variation in pallial eye structure from a simple plan and describes what such structures might “see”. It finally seeks an explanation as to how the evolution of complex pallial eyes, presumably from simple photoreceptors, has occurred within the framework of natural selection.

Eye structure in the Bivalvia According to Charles (1966), bivalve eyes cannot be related to any development from a basic plan, unlike those of gastropods in which a clear phylogenetic sequence of increasing sophistication can be seen (Salvini-Plawen & Mayr 1977: fig. 11), so that “the most interesting organs are the eyes of the Bivalvia” (Salvini-Plawen & Mayr 1977:247). Pelseneer (1911), however, proposed a system of classification for the bivalve eye, recognising them as (I), branchial, or cephalic, and (II), pallial. The latter were further categorised as follows: II A.

B.

Marginal eyes (a) Eyes without a closed cavity (Arcidae) (b) Eyes with a closed cavity (Pectinidae) Siphonal eyes (a) Cardium (=Cerastoderma) (Cardiidae) (b) Anatina (=Laternula) (Laternulidae)

Representative species of the families possessing the above categories of eyes have been described previously and the relevant literature will be identified below. The eyes of a few other species are also described for the first time. For the purposes of this review, however, although the broad outline classification of Pelseneer will be followed, it will not be rigorously adhered to and the eyes will be examined initially at the species and genus levels to see if a better picture of their evolution can be constructed.

Branchial, or cephalic, eyes Pelseneer (1899, 1908, 1911) described the occurrence of cephalic eyes in most species of Avicula (=Pteria), various species of Area and Pectunculus (=Glycymeris and Limopsis), 169

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species of Anomia, Mytilus and Lithodomus (=Lithophaga), and many species of Modiola (=Amygdalum), Modiolaria (=Musculus), Meleagrina (=Pinctada), Malleus and Isognomon. Such eyes, therefore, seem to be limited to the older, “filibranch”, orders of the Bivalvia, that is, the Arcoida and Pterioida. In most species, the eyes are located symmetrically on the left and right sides of the body at the base of the anteriormost filaments of the inner demibranchs of the ctenidia. In Anomia and some species of Pteria, however, there is only one such eye, usually on the left side. The veliger larvae of representatives of the Anomioidea (Anomia), Pterioidea (Pinctada), Mytiloidea (Mytilus), Arcoidea (Area), Limopsoidea (Philobrya) and Ostreoidea (Ostrea), however, possess a pair of cephalic eyes (Cragg 1996), the right being lost in the subsequent ontogenies of the Anomiidae. Cephalic eyes are retained into the adult of most of these bivalves but only occur in the larvae of oysters (Ostreidae), Baker & Mann (1994) observing that such eyespots gradually begin to degenerate after metamorphosis. By the time the dissoconch post-larval state is reached, the eyespots are represented only by a thin line of pigment. It is possibly significant (as will be discussed) that cephalic eyes occur only in members of the Arcoidea and Limopsoidea (Arcoida), the Mytiloidea, Pterioidea and Anomioidea (Pterioida) and it seems possible that, as with the byssus (Yonge 1962), such structures are a larval feature that has been lost in the adults of some, e.g. the oysters, but neotenously retained in the ontogeny of other lineages such as the Arcoida and Pterioida. The cephalic eye of Pteria brevialata (Pterioidea) has been described by Morton (1995). The paired eyes occur at the bases of the anteriormost filaments of both inner demibranchs, as illustrated for Isognomon costellatus by Stasek (1963:93, fig.2). Each eye (Fig. 1) forms as a shallow cup in an otherwise pigmented, ciliated, ctenidial epithelium (CE) and comprises long (up to 20 µm), distally pigmented cells (PC) with apical cilia (CI). Proximally, such

Figure 1 Pteria brevialata (Pterioidea). A section through the cephalic eye (after Morton 1995). CE, ciliated epithelium; CI, cilia; N, nerve; NF, nerve fibre; PC, pigment cell; TON, true optic nerve.

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Figure 2 Philobrya munita (Limopsoidea). A section through the cephalic eye (after Morton 1978). CE, ciliated epithelium; CI, cilia; L, lens; PC, pigment cell.

cells are in nervous connection via fine fibres (NF) with a true optic nerve (TON) that connects with the cerebral ganglia. The paired cephalic eyes of Philobrya munita (Limopsoidea) have been described by Morton (1978) and also arise from the bases of the anteriormost filaments of the inner demibranchs at the junction of the ctenidia and labial palps (Fig. 2). As in Pteria brevialata, there is a cup of distally pigmented cells (PC) up to 8 µm tall, arising from the surrounding, ciliated epithelium (CE). These cells encompass a simple, homogenous lens (L) in their bowl. The above two structures constitute the narrow range of known bivalve cephalic eye form. They connect with the cerebral ganglia and are, thus, true (as opposed to ectopic pallial) eyes, possibly representative of the ancestral bivalve condition. Interestingly, however, no such cephalic eyes have been described from representatives of the protobranch lineages, including the Nuculoidea, Nuculanoidea and Solemyoidea, most often thought to be representative of the ancestral bivalve. Morton (1996a), however, believes that the Protobranchia was an early offshoot from the primitive bivalve stock and, thus, fundamentally different from the mainstream of autobranch, that is lamellibranch, evolution in which cephalic eyes first evolved. Either this, or they have been lost in the protobranchs.

Pallial eyes Sharp (1883, 1884) described a range of extremely simple pigmented, light-sensitive, spots on the siphons of a variety of bivalves, such as Dreissena polymorpha and Solen vagina, which are not usually described as having them. Clearly, Dreissena polymorpha with a shadow reflex and a diurnal cycle of activity (Morton 1969) must perceive light (and dark) 171

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but no light-sensory cells have been described for it. Moreover, the posterior mantle margin and siphons are so densely pigmented that to isolate any light receptive pigment spots among this mass of epithelial cells would be difficult, even though they must occur. For example, Light (1930) showed that the positions of pigmented spots on the inner and outer surfaces of the siphons of Mya arenaria bore no relation to the position of pear-shaped cells which were assumed to be light sensitive. Kennedy (1958a,b) showed that stimulating the siphons of Mya and Venus with light caused multifibre discharges in the finest siphonal nerves. The shadow reflex in Spisula was initiated by stimulation of the pallial nerve itself, close to the visceral ganglia (Kennedy 1960). The siphons of species of Solen, similarly thought to possess light sensitive spots (Sharp 1883), can autotomise (Morton 1984a) but there are no recognisable eyes and any light receptive cells must, therefore, be extremely simple structures in an otherwise densely pigmented siphonal epithelial crown because the rest of the mantle margin is hidden in the sediment. Cole (1938) identified simple pallial sense organs in the larva of Ostrea edulis (Ostreidae) but thought that they functioned as mechanoreceptors not light receptors.

Pterioidea The simplest pallial structure that can be considered a multicellular photoreceptor is seen in Pteria brevialata (Pteriidae) (Fig. 3). At regular intervals along the posterior mantle margins

Figure 3 Pteria brevialata (Pterioidea). A section through the inner component of the outer mantle fold and a pallial eyespot (after Morton 1995). GC, gland cells; MMF, middle mantle fold; NF, nerve fibre; OMF(1), inner component of the outer mantle fold; OMF(2), outer component of the outer mantle fold; P, periostracum; PC, pigment cell; PHC, photosensitive cell.

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Figure 4 Isognomon legumen (Pterioidea). A section through the inner component of the outer mantle fold and the pallial eyespot (after Harper & Morton 1994). NF, nerve fibre; OMF(1), inner component of the outer mantle fold; PC, pigment cell.

on the inner component of the outer fold (OMF(1)) of this species occur simple sensory structures that may be light sensitive. The inner surface of this sub-fold, that is, next to the periostracum, has a cluster of taller (8 µm) epithelial cells (PC) that are pigmented distally. The outer surface of this sub-fold generally comprises a squamous (2 µm) epithelium which possesses, usually close to the apex of the sub-fold, a few large eosinophilic cells (PHC) from the bases of which arise extremely fine nerve fibres (NF) that extend towards the pigmented cells on the opposite, inner, surface of the sub-fold (Morton 1995). More obvious eyespots are seen on the posterior mantle margins of Isognomon legumen (Isognomonidae) (Harper & Morton 1994). As in Pteria brevialata, these simple eyespots occur on an inner sub-fold of the outer mantle fold (Fig. 4, OMF(1)) and comprise a cluster of ~4–5 cells (PC) each some 10 µm tall and which are proximally and distally full of pigment granules. A fine fibre (NF) extends from the base of each pallial eyespot and joins up with the pallial nerve.

Arcoidea and Limopsoidea Members of the Arcoida, such as species of Area (Arcoidea) and Glycymeris (Limopsoidea) (Hesse 1900, Küpfer 1915, Jacob 1926, Nowikoff 1926, Braun 1954b, Waller 1980), Litharca, Cucullaea (Waller 1980) and Barbatia (Arcoidea) and Philobrya (Limopsoidea) (Morton 1978, 1987), possess numerous pallial eyespots which are reported to be “ommatidiumlike” in that each one is supposedly based around eyespot units within the faceted arrangement of a compound eye as occurs in the Arthropoda. This eye type is, however, considered to be analogous to, not homologous with, the arthropod eye (Charles 1966). Levi & Levi (1971), for example, showed that the pallial eyespots of Area noe are covered by dense microvilli and that support cells flare out apically to create the appearance of a faceted compound eye by covering the apical ends of the ciliated photoreceptive cells. Nilsson (1994), however, described two pallial eye types in each of the three species of Arcoida he examined, that is Area zebra, Barbatia cancellaria and Anadara notabilis. The first, compound ommatidial 173

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eyes, have ciliary receptor cells surrounded by pigment cells and no lenses whereas pigment cup eyes have receptor cells with microvilli as the sensory structures but no lenses. Nilsson (1994) describes Barbatia cancellaria, for example, as possessing 300 compound eyes, each with some 130 ommatidia, and about 2000 pigment-cup eyes. No other authors have made this distinction with regard to arcoid eyespot structure. A microvillous-based photosensory cell is, it is argued (Salvini-Plawen 1982), of fundamentally different origin from the ciliary-based photoreceptors that characterise, as we shall see, more “advanced” bivalve pallial eyes. This idea was originally put forward by Eakin (1963) who proposed that deuterostomes have ciliary-based receptors, whereas protostomes have microvillous rhabdomes. There are so many exceptions to this theory, however, that it has had to be modified, for example, by Eakin (1982) himself. It is thus possible that bivalves may have either ciliary- or microvillous-based photoreceptors (or both) but the distinction between primitive microvilli and advanced cilia is also not so obvious as believed initially and may have unnecessarily complicated our view of bivalve pallial eye evolution. Photosensitive clusters of cells occur on the mantle margin of Barbatia virescens (Arcoidea), as in all arcoids, on a specialised inner sub-fold of the outer mantle fold (Fig. 5 A) (Morton 1987). Each eyespot consists of a cup-shaped epithelial depression, some 30– 40 µm in diameter. The cells of the cup comprise two types, first a columnar sensory cell (Fig. 5B, SEC) some 12 µm tall with a round, basal, nucleus (4 µm). Interspersed with these are pigment cells (PC), or support cells, which are packed distally with yellow-brown granules. From the cup cells arise what were considered to be long (12–16 µm) cilia (but see Nilsson 1994 who believes these are microvilli in B. cancellaria), which are directed towards the cup aperture and seem to be bound together to form an amorphous lens-like structure. The faceted nature of the surface of the arcoid ommatidial eye, that is, as in Glycymeris and Barbatia, therefore (Waller 1980), is not formed by rhabdomes but is merely a reflection of the rhabdomal arrangement of pigmented and ciliated sensory cells (illustrated in Nilsson 1994: fig.5). A cluster of nerve fibres (NF) oriented towards the pallial nerve arises from the

Figure 5 Barbatia virescens (Arcoidea). A, A section through the inner component of the outer mantle fold and pallial eyespot. B, a detail of the eyespot cells (after Morton 1987). AO, accessory organ; CI, cilia; L, lens; NF, nerve fibre; PC, pigment cell; SEC, sensory cell.

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Figure 6 Philobrya munita (Limopsoidea). A section through the inner component of the outer mantle fold and pallial eyespot (after Morton 1978). AO, accessory organ; NF, nerve fibre; OMF(1), inner component of the outer mantle fold; P, periostracum; PC(1), pigment cell type 1; PC(2), pigment cell type 2; PEG, periostracal groove; PEN, pallial nerve; SC, secretory cell.

base of the pigment cup of B. virescens. A second group of nerve fibres, as in the eyespots of Philobrya munita but not Glycymeris glycymeris, is directed towards another group of adjacent pigmented epithelial cells, the accessory organ (AO). A series of non-ommatidial eyespots occurs along the posterior, dorsal and ventral mantle margins (18 per lobe) of Philobrya munita (Limopsoidea) (Morton 1978). The eyespots (Fig. 6) on a specialised inner component, or sub-fold (OMF(1)), of the outer mantle fold, comprise a cap of pigmented cells, some 10 µm tall, containing granules of two types. The first group of epithelial cells (PC(1)) is distally packed with unstaining yellow-brown granules. Internal to these is a second group of epithelial cells (PC(2)), densely packed with granules which stain black in Heidenhain’s haematoxylin. Below each cap of pigment cells is a cluster of nerve fibres (NF) with sickle-shaped nuclei which effect a nervous connection with the pallial nerve (PN). From the pallial nerve arises another cluster of nerve processes which extend towards the bases of a second group of less densely-pigmented epithelial cells on the inner surface of the outer mantle fold, and which has been termed the accessory organ (AO). A pallial eyespot of Glycymeris glycymeris (Limopsoidea) is illustrated in Figure 7. Such structures occur as tiny black dots (illustrated in Morton 1996a: fig.29.3) along the entire lengths of both mantle lobes and on the outer folds, that is, under the periostracum and shell. Each eye on its own papilla (OP) consists of a sensory pigment cup (PC/SEC) only ~10 µm in diameter. Sensory and pigment cells cannot be differentiated at the light microscope level but 175

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Figure 7 Glycymeris glycymeris (Limopsoidea). A section through the inner component of the outer mantle fold and a pallial eyespot. CI, cilia; ON, optic nerve; OP, optic papilla; Pc/SEC, pigment cell/sensory cell; SEV, secretory vacuole.

the cup itself has vacuoles (SEV) and cilia (CI). From the base of each eyespot arises an optic nerve (ON) that connects with the pallial nerve. An accessory organ, as in Philobrya, has not, however, been identified.

Anomioidea The pallial eyes of Enigmonia aenigmatica (Anomioidea) were described by Bourne (1907), who wrongly identified the nervous connections in them, and illustrated from above by Morton (1976). When seen from the upper or left side, the bivalve being byssally attached and lying on its right valve, some 22 “eyes” are clearly visible under the golden brown left valve (Fig. 8). The eyes are located on the outer surface of the mantle and are illustrated in section in Figure 9. Since the general epithelium cells (POE) under the mantle are pigmented brown, the thin unpigmented cornea (C) overlying the lens of each eye appears white. The lens appears to comprise two cell types, that is, a central core of lighter staining cells (LC), surrounded by more darker staining ones (RC) with slightly larger nuclei, that is, 2 µm versus 1.5 µm (Fig. 9). The retina (RA) comprises pigment cells ~25–30 µm tall which are formed into a shallow cup directly under the lens. The retina is, however, formed by an invagination of the inner mantle surface (PIE) and the pigment cells, thus form a channel; importantly, however, this invagination results in the nuclei of the retina, although proximal, appearing to be distal, that is, closer to the lens. Fibres (possibly either cilia or microvilli) arise from the distal surfaces of the retina, unite and depart from one side of the retina between pigmented cells and a pair of cells which appear to be somewhat swollen and vacuolated (VC). These fibres eventually form the optic 176

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Figure 8 Enigmonia aenigmatica (Anomioidea). An individual seen from the right side showing 22 pallial eyespots underneath the right shell valve (after Morton 1976).

Figure 9 Enigmonia aenigmatica (Anomioidea). A section through the pallial eye. AO, accessory organ; C, cornea; CSN, ciliated sense organ nerve; LC, lighter staining lens cell; MF, muscle fibres; ON, optic nerve; PIE, pigmented inner epithelium; POE, pigmented outer epithelium; RA, retina; RC, darker staining lens cell; VC, vacuolated cell.

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nerve (ON). A branch of this nerve (CSN), however, extends towards the edge of the cornea and makes contact with another small cluster of cells that can be termed an accessory organ (AO) and which appear to be lightly ciliated.

Limoidea Only some species of Limoidea possess pallial eyes (Dakin 1928a). Species of Limaria and Platilimaria do not possess eyes (Morton 1979) whereas in Lima scabra (Bell & Mpitsos 1968), the mantle eyes are reported to be simple lensless pits, or cups, ~600 µm long, 200 µm wide and 150 µm deep, composed of alternating sensory (visual) cells with bundles of cilia and neural processes, and pigmented ones. The latter are also believed to secrete a lens, or vitreous layer (Dakin 1928a, Charles 1966). The location of such eyes is described simply as “the edge of the mantle” (Bell & Mpitsos 1968:414) so that it is unknown on which fold they are located, although Waller (1975) suggested that they are present on each lobe near the bases of the pallial tentacles, that is, the middle fold. As described above, such eyes seem to have a structure similar to the pigment-cup eyes of representatives of the Arcoida (Waller 1980) and Limopsoidea in comprising a cup of sensory and pigment cells surrounding an amorphous lens. An eye of Lima squamosa was described by Hesse (1900: plate XXV, figs.7–13) who noted that it was formed as an invagination of the mantle near the periostracal groove. The pallial eye of the same species was also illustrated in simple terms by Salvini-Plawen & Mayr (1977: fig.8B) and Salvini-Plawen (1982: fig.3I) and described as being of a “pinhole” type. The pallial eye of Lima (=Ctenoides) excavata was described by Schreiner (1896) and that of Ctenoides floridanus by Morton (2000b) who showed it to be similar to that of Lima squamosa (Hesse 1900). In Ctenoides floridanus, each mantle lobe possesses ~18 superficially simple orange eyespots at the base of the pallial tentacles. In section (Fig. 10), each eye comprises a lens (L) overlain by a thick layer of collagen (10 µm) (CO) and a wide haemocoel (50 µm) which together constitute the cornea (C) contained within the thin epithelium of the inner surface of the middle mantle fold. Transverse fibres (TT) connect the epithelium to the eye capsule. The walls of the capsule comprise pigmented cells (PC) up to ~15 µm tall while the base, possibly being the light receptive retina, is made up of pigmented cells and vacuolated cells both ~25 µm tall (VC). From the bases of these cells arise fibres that make up an optic nerve (ON) which links up eventually with the pallial nerve. Pigmented cells appear to have an apical covering of microvilli (MI). The pallial eye of C. floridanus is formed by an invagination of the outer surface of the middle mantle fold but sees light through the cornea on the inner surface of this fold (Morton 2000b). The centre of the eye capsule of C. floridanus is filled with an amorphous mass (AM) of tissue that is thought to be derived from the vacuolated cells. Such a filling is necessary in this solitary example of an invaginated open eye because the capsule lumen is, thus, also open to the sea and to any suspended particles contained therein. The other important feature of the limid invaginated eye is that it illustrates the way in which, in phylogenetic terms, the bivalve photoreceptor has moved from a specialised sub-fold of the outer mantle fold (and thus beneath the shell and periostracum) to the middle one (and thus beyond the shell).

Pectinoidea The most well-understood and complex bivalve pallial eye is typical of species of the Pectinidae and Spondylidae. The first comprehensive studies of a pectinid eye were of 178

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Figure 10 Ctenoides floridanus (Limoidea). A section through the pallial eye (after Morton 2000b). AM, amorphous mass; C, cornea; CO, collagen; L, lens; MI, microvilli; ON, optic nerve; PC, pigment cell; TF, transverse fibres; VC, vacuolated cell.

Pecten jacobaeus by Hesse (1900) and P. maximus by Dakin (1910) who showed that the retina comprised proximal and distal cell layers, with a crystalline argentea and cup of pigmented cells below and a Cartesian oval-shaped lens above it. Hesse (1900) and Dakin (1928a) also described the eyes of Spondylus gaederopus and the latter author also examined a species of Amusium while Barber et al. (1967) described the fine structure of the eye of Pecten maximus. The eye is of a similar construction in all pectinids and Morton (1980, 1993, 1996b) has described the general organisation of the eyes of Amusium pleuronectes, Leptopecten latiauratus and Minnivola pyxidatus, and their relationships with the mantle folds. The pallial eye of Patinopecten yessoensis, a subtidal (2–80 m), boreal, free-swimming, scallop from the Bohai Sea (China), Korea and Sea of Japan (Bernard et al. 1993) has been described by Morton (2000a). As in all scallops, the eyes of P. yessoensis are developed on the middle mantle folds, the inner ones forming the vela that facilitate swimming. In an adult specimen, there were 27 eyes on the lower, right, and 45 on the upper, left, mantle margins. Sections of the eyes revealed the 179

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Figure 11 Patinopecten yessoensis (Pectinoidea). A section through a pallial eye (after Morton 2000a). A, argentea; C, cornea; DR, distal retina; DRN, distal retinal nerve; L, lens; ON, optic nerve; OT, optic tentacle; PC, pigment cell; POE, pigmented outer epithelium; PR, proximal retina; PRN, proximal retinal nerve.

following structure (Fig. 11). Each eye is situated on its own tentacle, the epithelial surface of which is darkly pigmented (POE) and which may be >40 µm tall. In most pectinids, the cornea (C) is flatter, e.g. Pecten maximus (Dakin 1910), but in Patinopecten yessoensis, as in Pecten (=Chlamys) pusio (Patten 1886), the cornea is enlarged and comprises cells which can be up to 40 µm tall, each with, as in the general epithelium, a distal nucleus. Immediately under the cornea is a lens (L) housed in its own chamber. In Patinopecten yessoensis and Pecten pusio, the enlarged cornea and the lens form a Cartesian oval, whereas in P. maximus, the lens alone has this form. The lens of Patinopecten yessoensis is ~ 160 µm in diameter and has a core of darkly-staining cells, surrounded by lighter ones. Beneath the lens is the distal retina (DR) from the distal surface of which arise appendages. Those of the distal retina of Pecten irradians are composed of concentric lamellae each continuous with ciliary stalks connecting them to the sensory cell. Transverse sections of the stalks show them to have a 9+0 filament pattern characteristic of non-motile cilia with a sensory function (Miller 1958a,b). A 9+0 structure to the distal retinal cilia is also seen in P. maximus (Barber et al. 1967). These cilia join the cell body adjacent to a nerve fibre to eventually form the distal retinal nerve (DRN) which emerges from the eye at one point laterally. The cells of the distal retina have a proximal nucleus. Beneath this is the proximal retina (PR), also with proximal nuclei, and from the distal surface of which arise appendages that eventually unite with nerve cells to form the proximal retinal nerve (PRN). The appendages of the proximal retina of P. irradians are long microvillous extensions that resemble kinetodesmal fibrils, structures characteristically associated with ciliary basal bodies (Miller 1960). Barber et al. (1967) in their TEM study of 180

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the pallial eyes of P. maximus demonstrated that both retinas are ciliary-based although the receptive surface of the proximal one was composed of microvilli. The microvillous, membranous appearance and ciliary character of the proximal retinal appendages thus suggest that they too, like those of the distal, are light receptive. The proximal retinal nerve emerges from the opposite side of the eye to the distal and unites eventually at its base with the distal retinal nerve. In life, forming a union with the proximal retina is the argentea (A), or tapetum, the fine structure of which has been described for P. maximus by Barber et al. (1967) who showed it to comprise cells containing up to 30 layers of membrane-bound guanine crystals (Land 1966a). Such a structure is one of the few examples of an invertebrate tapetum outside the Arthropoda and gives the pectinid eye its metallic, mirrored appearance. Beneath the argentea is a row of cells that in Patinopecten yessoensis are only lightly pigmented but which in Pecten maximus are more so (Dakin 1910, 1928a) and is called the pigment cup (PC). The distal (DRN) and proximal retinal nerves (PRN) unite external to the eye to become the optic nerve (ON). The pectinid eye does not have an accessory organ, although it is possible that one or more of the complex array of tactile tentacles of the middle mantle fold which surround each eye can be considered such a structure.

Cardioidea The eyes of species of Cardioidea have been described by numerous authors (Kishinouye 1894, Zugmayer 1904, Weber 1909, Roche 1925, Braun 1954a,b), the most comprehensive accounts being by Barber & Land (1967) and Barber & Wright (1968) of Cerastoderma edule (Fig. 12). Each of some 60 eyes occurs atop a siphonal tentacle and is angled towards the

Figure 12 Cerastoderma edule (Cardioidea). A section through a pallial eye. AO, accessory organ; C, cornea; ON, optic nerve; PIE, pigmented inner epithelium; REC, receptor cell; REF, reflecting cup.

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outside. The cornea (C) is thin and covers a lens/retina (REC) of cells surrounded by a cup of refractive, electron-dense, crystal-containing cells described by Barber & Wright (1968) and termed a reflecting cup. The angled orientation of this eye is better explained when it is seen that the inner epithelial surface of the tip of each tentacle is also pigmented (PIE) and presumably serves as an additional reflecting surface. Nerve fibres emerge from the light receiving cells inside the reflective cup of the eye and pass down the tentacle as the optic nerve (ON). The eye is thus invaginated. Adjacent to the eye, however, is a ciliated, epithelial accessory organ (AO) (Weber 1909 describes two such structures) from the base of the somewhat elongated (10 µm) cells of which arise fibres that connect with the optic nerve. The greatly expanded siphonal tissues of giant clams (Tridacnidae) contain thousands of eyespots (Fankboner 1981), although they do not apparently occur in Hippopus hippopus and Tridacna tevoroa (Schneider 1998). The tridacnid eye has been described by Kawaguti (1966), Stasek (1966) and Fankboner (1981). An eye of Tridacna maxima is illustrated in Figure 13. The cornea (C) is a thin sheet of tissue overlying a pear-shaped group of lens cells (L), the lens itself being some 1–2 mm in diameter. The lens cells are contained within a cup of retinal cells (RA) from the bases of which arise cell blebs that possess a ciliary axoneme composed of 9×2+0 microtubule doublets which splay outwards from the cilium’s basal plate (Fankboner 1981) and are believed to be the photoreceptive portion of the retinal cell. These connect with nerve fibres that unite to form an optic nerve (ON). Adjacent to each eye is an accessory organ (AO) that comprises a cluster of more elongate epithelial cells possessing cilia. From the bases of these cells arise other nerve fibres (AON) that connect with the optic nerve. The eye is surrounded by zooxanthellae (Z) and it is possible that they are here acting as a reflective pigment cup, albeit also benefiting from the focused light (Fankboner, 1981). There is no other pigment cup or argentea.

Figure 13 Tridacna maxima (Tridacnidae). A section through a pallial eye. AO, accessory organ; AON, accessory organ nerve; C, cornea; L, lens; ON, optic nerve; RA, retina; Z, zooxanthellae.

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Laternulidae One of the most complex bivalve eyes occurs in some species of the Laternulidae, alone among the extraordinarily diverse subclass Anomalodesmata (Morton 1981). They were first identified by Pelseneer (1911) in Anatina (=Laternula) and described by Morton (1973b) and Adal & Morton (1973) for Laternula truncata. In this species there are nine eyes born on tentacles around the siphons: five around the exhalant, four around the inhalant. Each eye (Fig. 14) also has a distinctive sensory appendage on its outer edge, the accessory organ (AO). A thin cornea (C) covers the lens which is concave medially. In section, darklystaining supporting cells occur laterally (RC) in the lens and interlink with a central core of more lightly-staining cells (LC). Beneath the lens is a double-layered retina. The distal retina (DR) has ciliary stalks with a 9+0 filament pattern and form concentric lamellae (as in the Pectinidae) which join up with the cell body adjacent to a nerve fibre proximally to exit the eye, as in Pecten maximus, from one point between the lens and pigment cup as the distal retinal nerve (DRN). Below the distal retina is the proximal one (PR) also with ciliary lamellae arising from the distal surface and these, again as in P. maximus (Dakin 1910), leave the eye between the lens and pigment cup eventually to form the proximal retinal nerve (PRN). The surrounding pigment cup (PC) comprises cells ~20 µm tall that contain dark pigment granules distally. The cells of the pigment cup (or tapetum) contain granules that are arranged in three layers each possessing its own characteristic type (Adal & Morton 1973). The nerves from the two retinas unite outside the eye to form the optic nerve (ON).

Figure 14 Laternula truncata (Laternulidae). A section through the pallial eye and sensory appendage (after Adal & Morton 1973). AO, accessory organ; AON, accessory organ nerve; C, cornea; CI, cilia; DR, distal retina; DRN, distal retinal nerve; E, epithelium; LC, lighter staining lens cell; ON, optic nerve; PC, pigment cell; PR, proximal retina; PRN, proximal retinal nerve; RC, darker staining lens cell; S, sclerotic coat.

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From the optic nerve of Laternula truncata, however, arises another nerve (AON) that connects with an adjacent sensory appendage or accessory organ (AO). This organ is similar to the accessory sense organs already described for some arcoids, pterioids, Enigmonia, Cerastoderma and Tridacna but that of Laternula is much more specialised and the cilia (CI) are not simply located apically, as in the taxa identified above, but are long and contained within a channel so that their ends project from an aperture at the tip of the appendage. The eye appendage contains ~28 cilia with a 9×0+2 microtubule structure which make contact with microvilli lining the cells of the surrounding channel. Other intertidal, e.g. Laternula cf. gracilis and L. rostrata, and subtidal laternulids, e.g. L. crecinna (~26 m) and L. anatina, also possess siphonal eyes. L. elliptica from Antarctica, however, does not appear to (pers. obs.).

Discussion Commensurate with the adoption of a sessile life style, enclosed within adductable shell valves, the bivalve head is absent (either never having been present or lost) and in the majority of species there are few obvious anterior sense organs. Exceptions are found among the deep and fast burying representatives of the Solenoidea, e.g. Solen and Sinonovacula (Morton 1984a,b) that have sensory tentacles around the pedal gape. Adult cephalic eyes appear restricted to members of the Pterioida, e.g. Mytilus, Pinctada, Pteria, Malleus, Isognomon, Amygdalum and Musculus, and Arcoida, e.g. Area and Philobrya (Pelseneer 1899). They are little more than pigmented ciliary-lined cups filled with a crystalline material and located on the axial face at the base of the anteriormost gill filament of either both or only one (Anomiidae) inner ctenidial demibranch. They connect with the cerebral ganglia and comprise only simple sensory cells and, because they occur deep within the recesses of the mantle cavity and are covered by the densest, anteriormost layers of the shell, can have little role in photoreception (Rosen et al. 1978). Pelseneer (1911) points out, however, that despite their smallness and deep situation, they are visible through the shell of some modiolarids (=Musculus) and Malleus (although this is deeply buried) (Yonge 1968), and in some unnamed forms with thick shells, the regions above the eyes are covered by a translucent “window”. The cerebral ganglia are generally considered to innervate the labial palps, anterior musculature and the anterior mantle and receive impulses from a pair of statoliths, located near the pedal ganglia. The visceral ganglia play a much more important role in the Bivalvia, innervating the ctenidia, heart, posterior mantle and siphons. Anterior and posterior pallial nerves unite to form the circumpallial nerves and impulses from the finest pallial light receptive nerves to the most complex eyes, which are normally most well-developed posteriorly, are received by the visceral ganglia. Dakin (1910) first showed that in Pecten maximus and P. jacobaeus, the left lateral lobe of the visceral ganglia is bigger than the right, a situation that could be correlated with the greater number of pallial eyes on the left mantle margin. In Hong Kong’s byssally-attached, equivalve, Chlamys nobilis, for example, there are ~33 eyes on both mantle lobes whereas in the inequivalve, swimming Amusium pleuronectes, there are between 8–10 times more eyes on the mantle margin of the upper (left) shell valve than the lower (right) (pers. obs.). Nevertheless, and despite their inequality in swimming species, the optic lobes of the visceral ganglia are modest structures, illustrated for Pecten maximus by Dakin (1928b: fig.6), and dwarf in comparison, for example, with 184

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the huge ones conferring visual acuity upon cephalopods (Wells 1966). It thus appears that although bivalves, especially pectinids, may have good spatial resolution (the ability to detect movements made by objects subtending small angles) (Nilsson 1994) they have poor (if any) spatial vision (the ability to reconstruct their environment visually). The visceral ganglia are structurally incapable of processing the vast amounts of information necessary to construct an image of the world around the bivalve so that their eyes are not “eyes” in our sense of visual perceptiveness but, as Nilsson (1994) puts it, movement-sensitive “burglaralarms”. In the Bivalvia, besides eyes, there are other sense organs that monitor the environment. All possess an equilateral pair of chemosensory osphradia in the ctenidial axes which may receive spawning cues and synchronize gamete emission, especially in pectinids (Beninger et al. 1995). In older autobranch lineages of the Pterioida and Palaeotaxodonta, there is also a paired mechanoreceptor, the abdominal sense organ, located under the posterior adductor muscle. The fact that this organ is asymmetrically developed in some scallops, for example, present to the right but not the left in Chlamys multistriata, might suggest an analogous relationship with the unequal development of the pallial eyes. In fact, however, it is the opposite and the development of the right and reduction (or loss) of the left abdominal sense organ is related to the expanded role of the lower bowl of the right valve and its mantle in the circulation of water currents and particle movement, e.g. rejection, in the pallial cavity. This relationship is borne out by the fact that the cemented oyster Ostrea edulis also has a right, lower, abdominal sense organ, but not a left, upper, one (Haszprunar 1983, 1985). For the great majority of bivalves, therefore, sensory perception of the external world is from the posterior where either simple, largely unfused, mantle margins or more complexly united siphons sample the surrounding water (Yonge 1957, 1982). The mantle margin of all bivalves is tactile both on its general surface and, more particularly, from the array of tentacles and papillae that arise from the edge of the inner and middle folds and are especially abundant around the tips of the siphons, particularly the inhalant where they form a sensory screen for the incoming water. They also develop, albeit less frequently, across the exhalant orifice. Yonge (1957, 1982) suggested that the bivalve mantle margin could be divided into three folds; inner muscular, middle sensory and outer secretory. There are obvious exceptions to this generalisation because folds may be duplicated and in representatives of the Arcoidea (Area, Barbatia), the Limopsoidea (Philobrya, Glycymeris) and widely diverse Pterioida (Pteria, Isognomon, Enigmonia), simple cup-shaped photophores and ommatidium-like eyespots develop on a specialised sub-fold of the outer fold, beneath the periostracum (Waller 1980, Morton 1982a, 1987). In the Pectinoidea, well-developed pallial eyes develop on the middle mantle folds, as do simpler ones in the Limoidea (Morton 2000b). Conversely, species of cockles (Cardiidae) and giant clams (Tridacnidae) have eyes on the inner folds (Stasek 1966, Barber & Wright 1968). Across the broad spectrum of the Bivalvia, therefore, the pallial fold generalisation of Yonge (1957, 1982), in relation to sensory perception, does not apply: eyes can develop on the outer (Arcoidea, Limopsoidea, Pterioidea), middle (Pectinoidea, Limoidea) or inner (Cardiidae, Tridacnidae, Laternulidae) mantle folds. The most basic response to light in the Bivalvia is the shadow “off” reflex leading to either adduction, siphonal withdrawal or digging (or a combination of all three). The pallial eyes of pectinoids are the only ones in which a resolved image could be formed by reflection (Land 1968, 1981). Land (1965) showed that the lens of Pecten maximus had a focal length that was at least twice as great as the depth of the eye, so that any image formed in the eye 185

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must be formed at the spherical argentea. The image is actually created on the distal retina. Hartline (1938) showed that the distal retina responds to the offset of light (the primitive “off” shadow reflex). The distal retinal cells would thus be activated either by the leading edge of a dark object or the trailing edge of a light object crossing the field of view (Land 1966b, 1978). This permits responses to be made to moving objects that do not cast direct shadows by the sequential dimming of adjacent photoreceptor cells (Land 1966b). The proximal retina, which does not receive a focused image, responds to the onset of light (Hartline 1938). This low-resolution retina therefore, may, be responsible for grosser phototaxic behaviours such as responses to slowly changing light levels. The scallop eye thus has two independent types of retinal photoreceptors that give opposite responses to light (Gorman & McReynolds 1969): the image-forming distal depolarising retina responds to movement, the hyperpolarising proximal one only to longer-term changes in light intensity. Rees (1957:23) describes a scallop’s behavioural response to stimulation of the distal retina. They [Pecten maximus] can also perceive movement whether or not it involves a change in brightness; they will react by shutting their valves [my italics] when, say, a small white card only three-fifths inches square is moved against a black background more than a foot away. P. maximus also reponds either to changes in light, e.g. a moving hand, or starfish predators, by adduction, jumping and swimming (Thomas & Gruffyd 1971). Only starfish predators of the scallop induced the swimming response “and then only in a small proportion of trials” and “by contact” or “crude extracts” of the starfish. Von Buddenbrock & Moller-Racke (1953) showed that P. maximus individuals would close their shell valves in response to small movements in the environment. But how valuable is this ability in the natural environment? The scallop Minnivola pyxidatus is a subtidal (5– 100 m) species in Chinese waters (Bernard et al. 1993) and possesses the usual array of advanced pallial eyes (Morton 1996b). One of its predators is the muricid Rapana bezoar and in choice experiments with this species and a range of potential natural prey, Minnivola pyxidatus was always the first to be attacked (Morton 1994). Despite its complex eyes, M. pyxidatus could not detect the large advancing predator and it was not until Rapana bezoar actually touched the long pallial tentacles of the scallop that any escape response could be detected, by which time it was usually too late because the gastropod literally jumped onto and immobilised its victim. Gould (1971:79) states that “Placopecten and Amusium respond to predators by flight (photographs in Rees 1957)”. Rees’ photographs show no such thing and are, moreover, of Chlamys opercularis a species which because of functional design, cannot swim at all well and only responds to the touch of a potential predator, the asteroid Asterias rubens. It does so by gaping widely and then only at the last minute by attempting to swim (Rees 1957:27–31, figs I-VI). Some of Rees’ photographs actually show Chlamys opercularis straddled by the starfish and no swimming escape response being initiated. A few more examples from other bivalve taxa will illustrate the same point. Pallial eyes do not protect Isognomon legumen (Isognomonidae) from being the favoured prey of a suite of drilling predators (Harper & Morton 1997). Spondylus gaederopus and Leptopecten latiauratus are cemented and byssally attached pectinioids, respectively (Dakin 1928a, Morton 1993), and both possess the complex pallial eyes typical of the Pectinidae but neither are capable of an escape response other than to adduct the shell valves. Clearly, the complex 186

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pectinid eye has been retained in these immobile scallops but still only to initiate the most basic bivalve defence response, that is closure of the shell valves. Species of Amusium, e.g. A. pleuronectes (Morton 1980) and Patinopecten yessoensis (Morton 2000a) both have the usual complex pectinid pallial eyes and representatives of both genera are capable of dramatic and extensive bouts of swimming, e.g. Amusium pleuronectes again (Morton 1980) and Placopecten magellanicus (Caddy 1968). In the former species, which is the most accomplished bivalve swimmer (Morton 1980), however, individuals rarely do so and have to be vigorously encouraged to swim. Occurring, as they do, at depths of between 10–80 m on the continental shelf (Bernard et al. 1993), what could they see moving anyway? Morton (1980) points out that the distance Amusium pleuronectes can swim, that is >10 m (restrained by the aquarium wall) at a speed of 73 cm s-1, in combination with an exceptionally thin, smooth, internally ribbed, hydrodynamically efficient shell and a fishlike crypsis, are unlikely to be adaptations evolved to avoid predation. Instead, they point to a highly mobile life style, perhaps associated with reproductively-linked, life-cycle migrations, because the species is only caught in the winter months, for example, on the continental shelf of southern China. Eyes may, thus, be unrelated to any swimming ability, despite the assertion of Yonge (1953b) to the contrary. In Shark Bay, Western Australia, A. balloti was recorded to have swum a distance of 23.1 m in a single event, and a maximum accumulative distance of 30.8 m in four events. Speed was generally between 80–100 cm s1 but a maximum of 160 cm s-1 was recorded (Joll 1989). The study of Joll is significant in that it was undertaken in the natural environment, swims being documented by divers but still only initiated by them “tapping” the shell, not by being “seen” by the scallops. In the sea, light changes with depth in a highly predictable manner (Kirk 1983). At the surface, downwelling light from the sun and moon dominates and is affected by water clarity. Deeper, downwelling light becomes less important with respect to vision and by ~800 m there is no light (Denton 1990). Decapod eyes, however, become better adapted to low ambient levels and point sources of light with increasing habitat depth when downwelling light becomes less important (Johnson et al. 2000). It is possibly significant, therefore, especially with regard to the Pectinidae that the concave mirror of the argentea/tapetum with a retina positioned at its focal point, allows for enhanced photon (and thus light) capture, allowing the scallop to see in lower light intensities caused by depth and turbidity. Such an eye is, therefore, an eyespot with a mirror behind it and may have evolved to improve the efficiency of photon capture at deeper depths or inshore under conditions of high turbidity. Morton (1982a) has shown that deep-water species of the Arcidae, e.g. Bathyarca pectunculoides, do not possess such photophores, nor do deep-water species of the Pectinoidea, e.g. Propeamussium lucidum (Morton & Thurston 1989), for the obvious reason that there is no downwelling light at such inhabited depths. Nor, moreover, does the shallow subtidal Trisidos semitorta (Arcidae) (Morton 1982b) and it is, thus, clear that the occurrence of pallial eyes is not a universal feature of these families. Bivalve pallial eyes can be regarded as “ectopic” (Dawkins 1997) and the simplest such eyes in, for example, genera of the Arcoida, are structurally similar to that of the cephalic eye which has a common form throughout its occurrence in the Bivalvia. In the autobranch bivalves, whether infaunal or epifaunal, the posterior mantle margin is where the inhalant and exhalant streams circulate water through the mantle cavity and this area, therefore, is the best position for ectopic eyes because this is their primary focus for sensory perception of the world around them. 187

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Pallial eyes occur on the distal tips of the siphonal tentacles (inner mantle fold) of other species of Cardiidae, e.g. Laevicardium and Fulvia (Schneider 1995) but not in species of Fragum (Morton 2000c) nor Hemidonax (Hemidonacidae) (Ponder et al. 1981). The Tridacnidae, or giant clams, are also related closely to the Cardiidae and Schneider (1995) considers them to be a subfamily of the latter, a view which Morton (2000c) has found physiological evidence to support, that is, giant clams and representatives of the Fragiinae, e.g. Fragum erugatum, possess zooxanthellae and have a unique duct system to effect the movement of such cells between the digestive diverticula and the kidneys. The eyes of giant clams are similar to those of Cerastoderma edule. They consist of a cup containing a lens and there is an adjacent ciliated sense organ. There is not, however, a reflective pigment cup, although some authors (Fankboner 1981) suggest that zooxanthellae contained in the greatly enlarged siphonal, i.e. the fused inner mantle folds, component of the mantle are focused around the numerous eyes and could function as such. Stasek (1965) and Wilkens (1986) showed that a defensive reaction of giant clams is to direct a jet of water from the inhalant siphon at, for example, grazing fishes. Such precision could only be achieved if there was a directional stimulus provided by a suite of photoreceptors which were stimulated in the opposite direction by a shadow, so that the eyes do, indeed, have a photosensory function, in contrast to the view of Yonge (1936a) who thought of them as hyaline organs. Possibly by virtue of their numbers and because each one is linked into a complex pallial nerve net, tridacnid eyes are, like the more individually sophisticated pectinid eyes, also capable of detecting movement, thereby facilitating the directional defence response of siphonal squirting. Figure 15 represents a phylogeny of the Bivalvia based on Morton (1996a). In it, the incidences of cephalic and pallial eyes are indicated. As can be seen, true cephalic eyes are limited to representatives of the Arcoidea, Limopsoidea, Mytiloidea, Pterioidea, Anomioidea, Ostreoidea and Limordea. Pelseneer (1911) states that small cephalic eyes (ocelli) occur in Lima excavata and L. squamosa and have the same invaginated structure as those of Area, and as illustrated here for Philobrya munita (Fig. 2, p. 171). All such cephalic eyes occur in the same branchial position and all are a simple cup of ciliated pigmented and sensory cells with basal nervous connections to the cerebral ganglia. Genera of the same seven superfamilies, except for the Mytiloidea, also possess pallial eyes and in all, except the Pectinoidea, these eyes occur on the outer mantle fold (typically, a specialised sub-fold), or on the outer surface of the mantle in the case of Enigmonia aenigmatica (Anomioidea). In the Pectinoidea (and Limoidea), they occur on the middle mantle fold. Waller (1998: fig.4) has produced an alternative phylogeny of the Pteriomorphia in which the Limoidea is allied more closely with the Arcoida and the Anomioidea is placed in a clade with the Pectinoidea and the true oysters (Ostreidae). On the basis of an analysis of 185 Ribosomal DNA, however, Campbell et al. (1998) do not agree with this latter grouping (the Anomiidae and Limidae, moreover, were not analysed) so that there is as yet no firm consensus on bivalve phylogeny. It is nevertheless clear that, whichever phylogeny is adopted, ancestral cephalic eyes are clearly restricted to the Arcoida and Pterioida and the occurrence of pallial eyes is also restricted to these same two lineages plus the Cardioidea (Heterodonta and including the Tridacnidae) and Laternulidae (Anomalodesmata: Pandoroidea). As this study shows, the bivalve mantle margin possesses photoreceptors with a range of complexity. Almost all bivalves, even if eyeless, respond to sharp changes in light intensity (the shadow reflex) by retraction of the siphons, pallial contraction and adduction. In the absence of eyespots, light sensitive nerves have been considered to be receptors. These may be sensory axons or a photosensitive region of the pallial nerve itself (Kennedy 1960, Charles 188

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Figure 15 A phylogeny of the Bivalvia (after Morton 1996a) showing those lineages possessing cephalic eyes (*) and the occurrence of pallial eyes (solid bars).

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1966). The surf clam, Donax vittatus, has no obvious eyes but responds to abrupt changes in light intensity by adjusting its position in the sediment (Ansell et al. 1998b). Individuals respond to shading by moving up in the sediment, a return of light stimulating reburial. The same response was seen in Cerastoderma edule (with eyes) (Richardson et al. 1993) suggesting that such behaviour may be more widespread in burrowing bivalves than previously thought (Ansell et al. 1998b) but that well-differentiated eyes are not necessary for its initiation. This study identifies ten categories of bivalve pallial eyes, the characteristics of which are summarised in Table 1 and illustrated in Figure 16. There is no obvious pattern of increasing phylogenetic sophistication as there is in the Gastropoda (Salvini-Plawen & Mayr 1977: fig. 11). Nevertheless, it is generally true that the more modern bivalves possess more complex eyes on the inner mantle folds, which are in more intimate sensory contact with the environment, while simpler eyes occur in more ancient phylogenies under the

Table 1 A comparison of pallial eye structure in various phylogenies of the Bivalvia represented by Types A-K.

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Figure 16 A pattern of pallial eye structure in those lineages of the Bivalvia which possess them, showing an increasing, general, level of sophistication as eye development shifts from the outer to the middle and inner mantle folds. A, Pteria; B, Isognomon; C, Glycymeris; D, Philobrya; E, Barbatia; F, Enigmonia; G, Ctenoides’, H, Patinopecten; I, Cerastoderma; J, Tridacna; K, Laternula.

periostracum and shell and, thus, on the outer mantle fold and isolated from the environment. An intermediate situation occurs in the Pectinidae and Limidae. It is also true, moreover, that each bivalve eye has a unique construction and in some, e.g. the Arcoida, cap-shaped ommatidia and pigment cup eyes may occur in the same individual (Nilsson 1994). This is similar to the situation in the Limidae, but at the generic level, where species of Lima possess 191

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simple cup-shaped eyespots, whereas in Ctenoides floridanus the eye is a more complex, invaginated, structure (Morton 2000b). In the Pterioidea, there are numerous simple photocells with a pigmented epithelium on the opposite side of the mantle fold possessing them (Type A). In the Isognomonidae, the pallial eyes are simple cap-shaped clusters of pigmented cells (Type B). In the Limopsoidea, there are also simple, cap-shaped, pigmented eyespots with a nervous connection to the pallial nerve and to an accessory organ (Type C). An eye of essentially similar, but cupshaped, construction and without an accessory organ occurs in Glycymeris glycymeris (Limopsoidea) (Type D). In Barbatia virescens (Arcoida), eyespots with a structure similar to that of the cephalic eyes (Waller 1980) adorn the posterior mantle (Type E). In Enigmonia (Anomiidae), the eyes are located on the outer surface of the mantle (not the marginal lobes) but there is a distinctive cellular lens and the pigmented sensory cup is formed by invagination of an area of the underlying inner mantle epithelium (Type F). In some representatives of the Limidae, e.g. Lima, the pallial eyes are also simple cups composed of alternating sensory and pigment cells (Dakin 1928a, Charles 1966, Bell & Mpitsos 1968, Salvini-Plawen 1982) and may thus be like Types D or E (Limopsoidea and Arcoidea). Ctenoides floridanus, however, has an invaginated eye with a lens and simple vacuolated ciliated retina, and is located on the middle mantle fold. This is thus a distinctly different type of eye (Type G) (Morton 2000b). The above categories of eyes all seem to have a common underlying structure of simple light sensitive cells that progressively become surrounded by a cup of pigmented cells derived from the underlying epithelium but also developing a nervous connection with another area of sensory cells (the accessory organ) on the adjacent epithelium. C. floridanus is an advance on this arrangement in that each eye is formed from an invagination of the outer surface of the middle mantle fold, and does not possess an accessory organ. The Pectinoidea constitute a highly advanced extension of this process of progressive sophistication and pigment cup enclosure of more sophisticated lens, an inverted retina, an argentea and tapetum. Such eyes also develop on the middle mantle fold and may be related to the assumption of monomyarianism in the Pectinoidea and perhaps in some, the evolution of swimming as a defensive response to predation (Yonge 1953a,b). In the Pectinoidea (Barber et al. 1967), complex pallial eyes occur in virtually all shallow-water genera including Pecten, Chlamys, Amusium and Spondylus (Type H). In the Limidae and Pectinidae (Types G & H) there is no obvious additional nervous connection with a simple sensory accessory organ to each eye but the complex array of tentacles around the mantle margin, also on the middle fold and each with its own nervous control, may represent an elaboration of such a primitive initial development in Types A-F. In three other families of bivalves, pallial eyes develop on the inner mantle folds and are associated intimately with the siphons and can be termed “siphonal” eyes. In the Cardiidae, e.g. Cerastoderma edule (Barber & Wright 1968), the eyes develop on the siphonal tentacles and constitute a simple lens surrounded by a cup of electron dense cells (iridiophores) backed, on the opposite epithelium, by more pigmented cells. There is also an adjacent, ciliary, accessory sense organ. This retina is of the inverse type (Pelseneer 1911) and the nervous supply from the optic nerve to the sensory cells passes between lens and retina (Type I). A superficially similar structure, but which is not invaginated, is seen in the Tridacnidae with thousands of eyes associated with the greatly hypertrophied siphons. Here, however, entrained zooxanthellae are concentrated around the eyes and constitute the reflective cup and because the eye is not of inverse type, as in the Cardiidae, nervous connection with the cup of sensory cells is from 192

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their bases. Again, however, there is an associated, ciliary, accessory organ (Type J). An eye of fundamentally similar structure to that of the Pectinoidea was described for Laternula truncata (Anomalodesmata) by Morton (1973b) and Adal & Morton (1973). As in the pectinid eye, there is a complex lens, a double-layered, ciliary-based retina and an enclosing pigment cup. Unlike the pectinids, however, there is no argentea but there is a ciliated accessory organ that is here formed into a sensitive tentacle (Type K). Sensory ciliated tentacles of essentially similar construction to that of L. truncata are seen in many other anomalodesmatans, e.g. Clavagella australis (Morton 1984c) but are most specialised in the deep-water predatory septibranchs (but without eyes) where they respond to the vibrations of swimming crustacean prey to orient the raptorial inhalant siphon and effect capture, e.g. Cuspidaria and Cardiomya (Reid & Reid 1974, Reid & Crosby 1980). Accessory siphonal ganglia in cuspidariids co-ordinate the complex messages received from the sense organs. Salvini-Plawen (1982) suggested that the ciliated accessory organ of older bivalve phylogenies could have been incorporated into the eye structure of representatives of the Pectinoidea to create the ciliated distal retina; this is not so in Laternula truncata, however, where there is a double, ciliary-based retina and a ciliated accessory organ (Adal & Morton 1973). As an alternative to Salvini-Plawen’s view, is it possible that the complex tentacles of the pectinid (and limid) mantle margin may be derived from the primitive accessory organ? Salvini-Plawen (1982) used the above theory to explain why there is a ciliary-based distal retina atop a microvillous proximal one, light reception in the limoid/ pectinid clade having to be, in his view, by microvilli. But the proximal retina does possess cilia (Barber et al. 1967) so that there is no need to invoke the accessory organ to explain what Salvini-Plawen (1982) perceived to be an evolutionary anomaly. It thus seems that there is a general picture emerging of increasing sophistication with regard to the bivalve pallial eye from a very simple structure, as in Pteria brevialata (Morton 1995). That is, the structure of the complex inverted pallial eyes of the Cardioidea, Limoidea, Pectinoidea and Laternulidae can be explained by reference to that of the simplest in the Pterioidea and Arcoidea and includes a general and progressive elaboration of the lens, retina, reflecting pigment cup and accessory sense organ. There also seems to be a general picture of increasing sophistication with time, the earlier eye categories possibly evolving in the Palaeozoic (Arcoida and Pterioida), and more complex ones in the Mesozoic (Cardiidae, Tridacnidae and Laternulidae). This picture is not absolutely true, however, because the most advanced eye is seen in the Pectinoidea and it is possible that this particular structure evolved “out of sequence”, much earlier. Here, however, the calculation by Nilsson & Pelger (1994) that a sophisticated (fish) eye could take but 364000 generations to evolve is significant. That is, the palaeontological timescale need not be a reflection of the level of sophistication of the bivalve eye, even though it has the general appearance of being so. That is, again except for the Pectinoidea, older bivalve lineages have simpler pallial eyes on the outer mantle folds, whereas more modern phylogenies have more complex ones on the inner folds. The time scale of 364000 generations for a complex eye to evolve from a simple one (Nilsson & Pelger 1994) is short. If this is so, why have not the simpler eyes of the older lineages become more sophisticated? They have had, in their long ancestries, ample time to develop “better” eyes. Perhaps it is because they are developed on the outer fold, beneath the periostracum, and the shell in Enigmonia, and are thus constrained by what is morphologically an external “cataract”, no physical improvement to the eye being capable of significantly improving either spatial resolution or spatial vision. 193

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One can see why the Tridacnidae have developed more complex eyes in that thousands of eyespots on the expanded siphons, although not individually capable of responding to movement, can do so collectively if, as seems likely, they are linked into a complex, sequentially stimulated pallial nerve net, and thus facilitate the “aiming” of a jet of expelled siphonal water at any fish (Stasek 1965). Such eyes may also focus light on groups of symbiotic zooxanthellae entrained in the siphonal tissues, i.e. inner mantle folds, below them (Yonge 1936b, Stasek 1966), which is why Yonge (1936a) referred to them as hyaline organs but still derived from true eyes (Yonge 1953a). The more sophisticated pallial eyes of the shallow burrowing Cardiidae (Cerastoderma edule) and Laternulidae (Laternula truncata) defy an interpretation of enhanced “purpose” because simple eyespots could provoke the same, defensive, reflex of valve adduction and tentacle flicking for camouflage, respectively, when either a shadow or movement is detected. The obvious value of a sophisticated eye, especially in a sessile species, is predation avoidance and this could constitute a powerful force for natural selection, as Morton (1996a) suggested for the Bivalvia. The end of the Palaeozoic ushered in the Mesozoic Marine Revolution (Vermeij 1977) with the evolution of new suites of predators many of which, then and now, feed on bivalves (Skelton et al. 1990). At this time, bivalve families diversified widely (Fig. 15), most functional clades being involved. In this expansion, however, there is no evidence that the stimulus of predation has resulted in a proliferation of eye sophistication in any clade or broadened its occurrence in the class as a whole. Indeed, the vast majority of post-Mesozoic bivalves do not possess discernible eyes, either cephalic or pallial, and respond only to shadows perceived by what must be the simplest photoreceptive cells or nerves. In a review of swimming in the Pectinoidea, Morton (2000a) has shown that shallowwater scallops are preyed upon by a variety of crabs, starfishes and neogastropods. The possession of complex eyes seemingly, therefore, offers little defence against such an array of predators. Interestingly, however, a number of authors state that scallops such as Chlamys opercularis, Patinopecten yessoensis and Pecten ziczac (Stephens & Boyle 1978, Karpenko 1980, Wilkens 1981) react to starfish either when they are touched or stimulated by chemical cues from the predator, but not visually. There is some evidence that seagrass beds confer a degree of immunity from predation, e.g. Equichlamys bifrons in Tasmania (Wolf & White 1997) and Argopecten irradians in Long Island bays, New York (Bricelj et al. 1993). Hamilton & Koch (1996) have shown that A. irradians orients visually towards seagrass beds from a distance of 25 cm but not further away. Stokesbury & Himmelman (1996) have shown in the Gulf of St Lawrence that movement by Placopecten magellanicus reduced predation of it by the crab Cancer irroratus. As noted earlier, if sight and flight is not wholly concerned with predator detection, there is some evidence that swimming, at least in the more specialised scallops, is partly to do with directed movement. For example, Cliche et al. (1994) have shown that in the field, 49% of Placopecten magellanicus had moved >60 m, preferentially downstream, after 44 days of observation. This is not so, however, for Amusium balloti in Shark Bay, Western Australia, which though the most adept swimmer, like its congeneric A. pleuronectes (Morton 1980), is resident and only makes localised movements when stimulated to swim (Joll 1989). Conversely, the Antarctic scallop, Adamussium colbecki, although a much poorer swimmer, is among the earliest immigrants to areas of sea bed uncovered by the retreat of glacier tongues in the Ross Sea (Ansell et al. 1998a) and population densities can decline from tens per square metre to zero within hours (Ralph & Maxwell 1978). In situ observations 194

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of A. colbecki using a remotely operated vehicle suggested that: “the scallops appeared to be stimulated [to swim] either by mechanical stimuli or turbulence generated by the approach of the ROV or possibly by the increase in light intensity [from the lights on the vehicle].” (Ansell et al. 1998a: 372). This anecdotal suggestion that scallops may swim in response to changes in light intensity is supplemented by the observation of Dibden & Joll (1998) that Amusium balloti usually began to swim in response to the lights of an underwater camera being towed along the bottom in their immediate vicinity. The perception of light, therefore, may be more related to directional movement than predator detection (which seems to be more related to mechanical and chemical stimuli) although waving eel grass beds may visually attract those scallops that live in them back to their protection. The vast majority of bivalves survive with the simplest light sensitive cells or nerves. It is tempting, therefore, to speculate that the complex pallial eye of the Bivalvia is a structure that has slipped past the scrutiny of natural selection and is either an example of orthogenesis (Dakin 1928a) or has no utilitarian value (Morgan 1903), but these speculations seem unlikely and counter-intuitive. There is, of course, also the point that the sophisticated pectinid eye may have evolved when the family first arose in the early Mesozoic (Triassic) (Waller 1978), perhaps when most representatives either lived intertidally or in very shallow waters and had, then, a much more significant anti-predation role. Primitive members of the Pectinidae were, however, byssally attached, resting on their right valves (Harper et al. 1996). It is, moreover, unknown if such ancestors had eyes. If they did, they may have been simpler structures, adduction being the only defence against visually-detected predators. As scallops have possibly moved into deeper waters and, coincidently, assumed a free-living life style, eye structure may have improved to increase photon capture but the sense organ has never, it appears, been effective (or relied upon) in terms of anti-predation. It has, nevertheless, been retained. An example of this is Plicatula (Plicatulidae) and Spondylus (Spondylidae). The former arose early on in the evolution of the Pectinoidea and became cemented before the evolution of eyes in the superfamily, whereas the latter arose in the Jurassic, after the evolution of eyes, is also cemented, but has retained them (Yonge 1951). In fact, Spondylus possesses pallial eyes as complex as any pectinid and yet its only defence to predation (other than shell spines) is to shut its valves. Complex eyes are not needed for this function and it is thus possible that such a sense organ, at least in the Pectinidae, arose and has been elaborated progressively over time but has less functional value now in the postMesozoic world. Hinnites (=Crassodoma (Bernard 1986)) multirugosus is initially free but cements at a late stage in ontogeny (Yonge 1951) so that its complex pallial eyes may be more important for the juvenile. Conversely, in the Antarctic scallop Adamussium colbecki, juveniles up to 45 mm in shell length are found exclusively attached by byssus threads to mobile adults (Ansell et al. 1998a), so that eyes are more important for the latter. This is especially so since the shell valves of A. colbecki are exceptionally thin and thus highly vulnerable to attack. In an analysis of post-Palaeozoic divergence and taxonomic radiation in the Bivalvia, Skelton et al. (1990) point out that not only has the actual and relative frequencies of pterioid families declined but so too has the frequency of the swimming (again mostly pterioid) clade. For a group that has the highest incidence of pallial eyes with the greatest level of structural sophistication, therefore, this is poor testament to the value of vision! For species of the Pectinoidea with the most advanced eyes and which constitute the most significant swimming clade, however, it is possible that the detection of nearby movement by the distal 195

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retina does allow adduction to occur fractionally earlier than in other bivalves with only a shadow reflex (when a predator would literally be already on top of them) and thus to constitute a selective advantage. Swimming heightens that advantage but is so energetically expensive it is not undertaken lightly and unless the predatory stimulus is strong. Light detection on the proximal retina may be more responsible for life-style movements related to relocation (Hamilton & Koch 1996). The above examples of the bivalve eye clearly demonstrate that the earliest, cephalic, eye has been retained in some of the oldest lineages of the Subclass Autobranchia. It appears that it either never evolved in the second major bivalve lineage (the Subclass Protobranchia) or it has been lost. It has also either been lost or never developed in all the more modern lineages of the Autobranchia. Similarly, except for the Pectinoidea, the pallial eyes of the Arcoida and Pterioida show a limited evolutionary tendency for an increase in complexity. Indeed, the opposite seems true, because the modern descendants of these two Palaeozoic orders retain the simplest pallial eyes and yet have flourished and radiated widely. Such eyes are, therefore, an adaptive consequence of attempts to improve sensory perception of the environment. They also represent a slow general progress towards improvement in terms of the potential for enhanced visual resolution. It cannot, therefore, be said that the evolution of the pallial eye has given the bivalves a greater visual perception of the environment around them, unlike most other animal groups in which eyes have evolved. Rather it has kept them, at best, in a world of vague shadowy movement and that is, perhaps, the key. Nilsson (1994:206) has shown that Barbatia cancellaria possesses ~39000 ommatidia (an “absurd” [my italics] number). An average of 755 of these monitor any one direction in space. The more complex eyes of the Pectinidae need fewer eyes (one) to monitor the same space. Such eyes are, therefore, like man-made, movement-sensitive, burglar alarms. Fewer, more complex eyes improve the efficiency of spatial resolution but spatial vision (the ability to see an object) is not improved because of the inherent inadequacy of the bivalve nervous system. The visceral ganglia, therefore, are responsible only for collecting together all the retinal responses to movement and relaying onwards to the adductor muscle a message to respond to a threshold level of stimulation. In the case of the Pectinidae this message is either first to adduct or second to swim. First identified for Drosophila, the homeobox gene eyeless (ey) is capable of inducing ectopic eyes on the wings, legs or antennae of the fly (Halder et al. 1995). The homolog, Pax-6, or small eye, of this gene in vertebrates is also essential for eye development and has been identified in the squid Loligo opalescens (Tomarev et al. 1997). It may, moreover, function as a master control gene throughout the Metazoa (Halder et al. 1995). If this gene acts in the same way in the Bivalvia, then the development of branchial, or cephalic, eyes in those lineages herein shown to possess them can be explained by the expression of this gene. More importantly, it may also explain how pallial, ectopic, eyes are developed in some of these lineages but also in other, cephalically eyeless, families, notably the Cardiidae, Tridacnidae, Laternulidae and Pectinidae. The expression of the gene may also operate at the species level, for example, siphonal eyes in Laternula truncata but not L. elliptica; at the genus level, for example, eyes in Cerastoderma but not Fragum and, as shown here, more generally at the family and order levels. This review, however, exposes a fundamental lack of understanding about bivalve eyes. That is, although we may now better understand how such eyes develop and even their function as “burglar alarms” (Nilsson 1994), we are still a long way from understanding the factors and forces that have stimulated their selection and remarkable elaboration. Clearly, 196

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however, once the ey gene is expressed, elaboration can be rapid (Nilsson & Pelger 1994) and even though each step in this process may be trivial, it must be effected through natural selection acting on each lineage possessing ectopic pallial eyes, possibly at different rates, at different times and under the influence of different driving forces, one of which is, however, most likely to be predation.

Conclusions 1. Cephalic, true eyes associated with the cerebral ganglia and located on the axes of the anteriormost filaments of the inner, left and right, demibranchs of the ctenidia and comprising simple, sensory, pigmented cups, occur in some representatives of the Arcoida and Pterioida. Such eyes may represent a larval (paedomorphic) feature that is retained into adult life in only some older bivalve lineages. 2. Ectopic pallial eyes also occur in many representatives of the shallow-water Arcoida and Pterioida and consist of either a pigmented sensory cap or a simple cup that is formed on the outer mantle fold (often a specialised sub-fold) and, thus, under the periostracum. In Pteria, with the simplest eyespots, such light receptors are photosensitive cells lying on top of a pigmented epithelium. 3. Pallial eyes also occur in the Anomiidae, e.g. Enigmonia aenigmatica, but on the left mantle lobe only and beneath the shell. The lens is formed by the outer epithelium of the mantle and the inner epithelium invaginates to form the pigmented, sensory cup beneath it. This process is a most unusual attempt at eye formation by invagination and results from the horizontal position adopted by the bivalve. 4. An invaginated eye also occurs in some representatives of the Limidae, e.g. Ctenoides floridanus. In this case, the outer surface of the middle fold invaginates, abutting the periostracal groove and the epithelium forms a lens and a pigmented, sensory cup. Because the eye capsule remains theoretically open to sea water, it is filled with cellular secretions. Light is perceived through the inner surface of the middle fold. 5. The most complex eyes occur in representatives of the Pectinidae (and Spondylidae), again on the middle mantle folds. Each eye is of the invaginated type but comprises a double-layered retina, surrounded by an argentea and a pigment cup and a lens with a retina above that is in the shape of a Cartesian oval. 6. An invaginated eye occurs in representatives of the Cardiidae, each one situated on top of a siphonal tentacle. The retina encloses a lens but the reflecting cup is the pigmented epithelium of the optical tentacle itself, as in Pteria with the simplest eyespots. 7. In some tridacnids, many thousands of pallial eyes, or hyaline organs, occur on the greatly expanded siphonal tissues made up of the inner mantle folds. These comprise a simple retina surrounding a lens which is, in turn, surrounded by masses of symbiotic zooxanthellae. 8. An eye virtually as complex as that of the Pectinidae occurs in the Laternulidae (Anomalodesmata) and each one is again situated on top of a siphonal tentacle, that is, the inner mantle fold. There is a double-layered retina internal to a pigment cup and a lens, with nerves departing the eye between them. 197

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9. A ciliated accessory sense organ of largely unknown function accompanies many eyes, although in Laternula truncata it is a sophisticated mechanoreceptor. Representatives of the Limidae and Pectinidae do not have such an accessory sense organ for each eye although the complex array of sensory tentacles that characterise the mantle margins of representatives of these two families may be such, albeit highly modified, structures that have replaced them functionally. 10. There is a clear, well-understood, picture of increasing complexity associated with a phylogenetic tree exhibited by the true, cephalic, eyes of the Gastropoda. The ectopic pallial eyes of the Bivalvia do not show such a trend (except in a very general sense) and each eye structure is unique to a species, genus or family. 11. Ectopic pallial eyes are of sporadic distribution within the Bivalvia. Most taxa do not possess such structures (nor cephalic ones), and light perception is probably by pallial light-sensitive nerves. 12. There is, however, a general picture of increasing sophistication. Phylogenetically older lineages of bivalves (Pterioida and Arcoida) have eyes of simple construction on the outer mantle fold. The most complex eyes are seen in the Heterodonta and Anomalodesmata on the inner folds intimately associated with the siphons. Complex invaginated eyes, especially in the Pectinoidea also occur on the middle fold and Ctenoides (Limidae) illustrates how such a structure came to occupy this position. 13. All bivalves possess a shadow, “off”, reflex that results in adduction (except in cave-dwelling and abyssal species), siphonal retraction, digging or combinations of all three. The more complex eyes of the Pectinidae, with a Cartesian oval lens, however, are also able to detect a simple image and movement on the distal retina and, it was believed, respond to these by swimming away. The thousands of eyes in the expanded siphonal tissues of the Tridacnidae achieve the same result and on detecting a moving shadow direct a jet of water at it from the exhalant siphon. 14. The pectinid literature suggests, although the evidence is only anecdotal, that scallops rarely swim in response to a moving predator perceived visually by the distal retina. Rather, they have to be stimulated either mechanically or chemically, to undertake the energetically expensive escape response of swimming. In representatives of the Pectinidae, the proximal retina detects more long-term, subtle changes in light intensity to which they may respond by relocational swimming. 15. Ectopic pallial eyes in the Bivalvia may represent the switching on of the eyeless (ey) homeobox gene. Once present, they subsequently come under the influence of natural selection to gradually improve structure and function. What drives the process of natural selection is not at all clear, however, except that an improved eye has no disadvantages and may even be energetically less expensive than thousands of eyespots. Furthermore, it may enhance survival through fractionally faster response times to, say, a moving shadow that may be a predator, and thereby effect its slowly increasing sophistication. 16. Finally, bivalve pallial eyes are concerned with spatial resolution, not spatial vision, permitting responses to movement not objects. In their simplest form they thus perceive changes in light intensity. In their more complex structure, they also perceive short-term (movement) and long-term (diel) changes in light intensity. No bivalve eye, despite its sophistication, can visualise an object because of the inadequacies of the nervous system. Their evolution within the class has followed a general and, seemingly stochastic, gradual pattern of improvement, nudged along by natural selection, probably acting through the medium of predation. 198

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Acknowledgements I am grateful to Dr J.D.Taylor, The Natural History Museum, London, for the supply of specimens of Cerastoderma edule, Glycymeris glycymeris and Tridacna maxima and for reading the first draft of the manuscript of this paper, as did Dr E.Harper, University of Cambridge. Two anonymous referees are also thanked for their constructive criticisms and advice. Mr H.C.Leung, The University of Hong Kong, is thanked for histological assistance.

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PRACTICAL MEASURES OF MARINE BIODIVERSITY BASED ON RELATEDNESS OF SPECIES R.M.WARWICK & K.R.CLARKE Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth, PL1 3DH, UK e-mail: [email protected]

Abstract In contrast to terrestrial biodiversity, marine biodiversity has a number of distinctive features that suggest that a broader strategy for its conservation might be more appropriate than a local reserve-based one. Traditional diversity measures based on species richness and evenness often have disadvantages in the assessment of biodiversity change on wide spatial scales and long timescales. Alternative measures based on the degree of relatedness of species overcome these problems to varying degrees. They fall into two categories. Taxonomic distinctiveness measures are used as a means of preferentially selecting species from an inventory for conservation purposes: species that diverge close to the base of a phylogenetic or taxonomic tree and have few close relatives will preserve more evolutionary history than those that diverge further up and have more congeners. Complementary subsets of species can also be selected to provide representativeness of the widest range of evolutionary characters. Taxonomic distinctness measures, on the other hand, are a means of comparing patterns of relatedness in community samples in the field, and monitoring changes in these patterns over space or time. They measure either the average distance apart of all pairs of individuals or species in a sample, traced through a taxonomic tree, or the variability in structure across the tree. These measures are beginning to find application in broad scale geographical comparisons of biodiversity, in environmental impact assessment and in evaluation of surrogates for biodiversity estimation.

Introduction The Convention on Biological Diversity (CBD) was signed at the UNCED “Earth Summit” in Rio de Janeiro in June 1992, came into force in 1993, and has been ratified by more than 150 countries (Glowka et al. 1994). It imposes obligations on the signatories in respect of the conservation and sustainable use of biodiversity. Current marine conservation measures derive from the terrestrial practice of protecting rare or endangered species or habitats, the priorities for which are derived on a rather ad hoc basis. In Europe, for example, this is being implemented under the auspices of the European Community “Habitats Directive” (92/43/EEC) in which priority habitats and species are included in Special Areas of Conservation (SACs) forming a network of protected areas (Natura 2000). Whether such a strategy is appropriate for the marine realm has not been seriously questioned, despite the fact that the biodiversity of marine organisms has a number of distinctive features (Heip et al. 1998) that might imply its ineffectiveness. In general, marine species are less in danger of extinction. Marine systems 207

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are more open than terrestrial or freshwater ones, and barriers to dispersal are weak, so that local extinctions are easily replenished by new recruits, which are often produced in large quantities by highly fecund adults. Remediation of degraded habitats on land is dependent on the relatively slow colonisation of the large static primary producers, whereas in the sea these are very small, often mobile, with a rapid turnover. Environmental change in the sea has a much lower amplitude and longer frequency than on land, on both temporal and spatial scales (Grassle et al. 1991), so that natural stresses are less. Anthropogenic pressures on marine organisms are relatively diffuse rather than localised. Man exploits over 400 species as food resources from the marine environment (Heip et al. 1998), that are obtained in a relatively unmanaged “hunter-gatherer” mode. Furthermore, although much pollution from the air, land and fresh water ultimately enters the sea, it is widely dispersed both physically and via the food chain. All these differences argue for a broader strategy for the conservation of marine biodiversity than a reserve-based one. The conservation of marine biodiversity is imperative, however, primarily because the diversity at higher taxonomic levels is much higher in the sea, where there are 14 endemic animal phyla, so that the total of genetic resources is very high. It can also be argued that the maintenance of marine biodiversity is essential to sustain a wide range of ecosystem functions, goods and services that are crucial to Man (Costanza et al. 1997), quite apart from the moral issues of global stewardship. A prerequisite for the management of biodiversity per se on this broader spatial scale is the need to define it in ecologically meaningful ways that are practical to measure, so that the effects of environmental degradation, remediation or conservation measures can be monitored. “Biodiversity” includes diversity within species (genetic diversity), between species (organismal diversity) and between communities (ecological diversity), in the terminology of Harper & Hawksworth (1994). This review concerns the level of organismal diversity, a term that we prefer, like Harper & Hawksworth, to the more usual “species diversity” because it embraces taxonomic categories above species rank, which is important in the context of what follows.

Species diversity as a measure of biodiversity At the organismal level, the most widely used biodiversity measures are those based on the number of species present, perhaps adjusted for the number of individuals sampled, e.g. Margalef’s species richness index d, or indices that describe the evenness of the distribution of the numbers of individuals among species, e.g. Pielou’s J’, or that combine both richness and evenness properties, e.g. Shannon’s H’ (see Magurran 1991 for a review). These indices may be of value as comparative biodiversity measures in situations where sampling methods, sample sizes and habitat types are carefully controlled, as might be the case in a local environmental impact study, but are of doubtful utility for more diffusely collected data on wider spatial and longer temporal scales (Clarke & Warwick 1998b, Warwick & Clarke 1998). In most cases these indices are very sample-size dependent (Fig. 1), which will often invalidate analysis of data with uncontrolled or unknown sampling effort. A notable exception is Simpson’s index (e.g. Lande 1996). The dependence of richness measures, such as the simple observed number of species (S), on the sampling effort is one of the most fundamental difficulties in any field assessment of diversity, particularly in marine environments where one is rarely at the asymptote of the species208

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Figure 1 Six diversity measures based on species abundance distributions, determined from subsamples of increasing numbers of individuals drawn randomly (without replacement) from the full set of 140344 individuals in a pooled (pre-impact) sample of macrobenthos from the Bay of Morlaix (Dauvin 1984). a: number of species S; b: Margalef’s species richness d=(S-1)/logeN; c: Shannon diversity H’=Sipilogepi(where pi=Xi/N); d: Pielou’s evenness J’=H’/logeS; e: Brillouin’s index H=(1/N) loge(N!/Pi/ Xi!); f: Simpson diversity, in the form D°=1-Si{Xi(Xi-1)/N(N-1)}.

area relationship. The avoidance of estimates that are sensitive to the degree of sampling effort is thus a major criterion of this paper. In addition, there is usually no statistical framework for testing whether the species diversity measured at any one time or place departs significantly from what might be expected in the absence of anthropogenic perturbation. Interpretation of changes in species 209

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diversity is also complicated by the response to environmental degradation being nonmonotonic, with intermediate levels of disturbance sometimes elevating richness (Wilkinson 1999 and references therein). Thus, depending on the point at which the assemblage starts on the disturbance scale, species diversity may either increase, decrease, or even stay the same, with increased environmental deterioration. Species diversity can also be very dependent on differences in natural environmental variables; macrobenthos and meiobenthos, for example, both tend to have a higher species richness in sandy sediments than in silty ones. This makes broad comparisons difficult unless habitat type is carefully controlled. Furthermore, changes in evenness or richness-based species diversity are not explicitly linked to changes in functional diversity, and so their ecological significance can be difficult to assess. For example, assemblages of macrobenthos constituting a single trophic group (e.g. deposit feeders) may be equivalent (or higher) in species diversity to assemblages constituting a range of trophic groups (deposit feeders, suspension feeders, carnivores, grazers). Perhaps most importantly, changes in community composition in response to anthropogenic disturbances of various kinds, but which are unaccompanied by changes in species diversity, have repeatedly been revealed by multivariate analyses of community data (Gray et al. 1990, Warwick & Clarke 1991, Dawson Shepherd et al. 1992). These changes can even sometimes be reflected at the highest taxonomic levels (e.g. proportions of phyla) in multivariate analyses (Warwick 1988, Warwick & Clarke 1993). Species diversity, based on evenness and richness properties, thus seems in some way to be homeostatic, except at high levels of disturbance, and may not be a reliable measure of important changes in biodiversity. For example, in the North Sea there are indications that certain major taxa are decreasing at the expense of others in response to both natural variability and anthropogenic pressures (North Sea Task Force 1993), which indicates a major change in biodiversity but may not be detectable as a net change in species diversity. If we continue to use these traditional indices for monitoring purposes, changes in biodiversity may go undetected until a very advanced stage of environmental degradation is reached.

Measures of biodiversity based on taxonomic distance between species “A measure of the biodiversity of a site ought ideally to say something about how different the inhabitants are from each other” (Harper & Hawksworth 1994). Simply to say whether or not they belong to the same species is clearly insufficient and in the last decade a variety of different measures have been devised to measure the degree to which species are taxonomically related to each other. These measures fall into two categories and have been developed for rather different purposes. 1) Taxonomic distinctiveness. These are measures focused on individual species, and provide a means of weighting species in respect of priorities for conservation. A species not closely related to any others would have higher priority for conservation than a species with many close relatives because it diverges closer to the root of a phylogenetic tree and its conservation will preserve more of the evolutionary history (Nee & May 1997) of the group. If one species in a taxonomic group is already 210

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protected then, in order to conserve as wide a possible range of (evolutionary) characters representative of that group, the next species to be preserved should be as different as possible, a concept known as complementarity. 2) Taxonomic distinctness. These are properties of an assemblage and measure features of its overall taxonomic spread. Comparisons are made of one assemblage with another, with the primary motivation of environmental assessment and monitoring of biodiversity change, usually over wide space and time scales. In both these types of measure, the ideal phylogenetic tree representing the relatedness of individual species will be a fully resolved cladogram in which the branch lengths have been determined by molecular methods. Although this may be possible for certain groups of terrestrial organisms, for the vast majority of marine taxa such information is simply not available. The development of taxonomic distinctness measures has therefore proceeded largely on the basis that equal branch lengths can be inferred between the hierarchical levels of conventional Linnean classifications. Williams & Humphries (1994) point to the arbitrariness of such hierarchies but many such classifications are based on cladistic principles, e.g. marine nematodes (Lorenzen 1981, 1994), and most marine biologists would agree that they are quite realistic in phylogenetic terms. Even Humphries et al. (1995) concede that they are “arguably better than nothing”. Certainly we would regard species belonging to the same genus as more closely related than species belonging to different genera but the same family, and so on up the taxonomic hierarchy. For the purposes of this paper we will therefore use hierarchical Linnean classifications as a proxy for cladograms. This means, of course, that taxonomic trees will often have three or more branches emanating from the same node, whereas in “proper” cladograms there can be only a dichotomy, a difference that should be borne in mind in the examples that follow.

Taxonomic distinctiveness

Root weight Vane-Wright et al. (1991) and Williams et al. (1991) provided a quantitative weighting of the taxonomic distinctiveness of a species based simply on the number of nodes or branch points from that species to the base of the tree. Thus, in Figure 2a, species 1 passes through only one branch point, whereas species 2–7 each pass through two branch points. The taxonomic distinctiveness of the species is simply inversely proportional to this “nodecount”. Thus, species 1 will have a higher conservation status, and species 2–7 will have lower status but equal to each other. Clearly this method has a disadvantage in that species 2 and 3 are accorded the same distinctiveness as species 4–7, whereas the former have only one other conspecific in their genus and the latter three, which should accord species 2 and 3 a higher distinctiveness. A modification by May (1990) solves this problem by counting the sum of the branches at all branch points, rather than the number of nodes, for each species. For species 1 this value is 3, for species 2 and 3 it is 5, and for species 4–7 it is 7. Again, distinctiveness is inversely proportional to the branch count. Note that both these measures are only dependent on the topology of the tree and are unaffected by the differences in path lengths contrasted in Figure 2b and c. 211

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Figure 2 Six different taxonomic trees illustrating the possible classification of seven species into three higher taxa (say genus, family and order), illustrating various points discussed in the text. In each case the three step lengths between taxonomic levels are set equal to 33.33, and the values of AvPD (F+) and AvTD (D+) are calculated on this basis. They show, inter alia; a: the highest taxonomic distinctiveness of species 1, followed by 2 and 3, with 4–7 having the lowest distinctiveness (using May’s modification of the root weight methodology); b and c: different values of AvTD and AvPD in trees with identical topology but different path lengths; d and e: the inability of AvPD to distinguish between trees that have a different evenness of the species distribution across higher taxa, as opposed to AvTD which does make this distinction; c and f: trees with the same value of AvTD but with contrasting VarTD of (c) 0 and (f) 634.9.

Phylogenetic diversity A similar node-counting method described by Nixon & Wheeler (1992) also gave the highest weights to taxa diverging nearest to the base of the tree but also took no account of branch lengths. Vane-Wright et al. (1991) and Williams et al. (1991) focused on this approach because of the lack of information on branch lengths in most cladograms. For the taxonomic trees based on Linnean hierarchical classifications that are used in this paper, at least an ordering of branch lengths is possible, even if the relative numerical values assigned to them are somewhat arbitrary. Where path lengths are quantified, Faith (1992, 1994) defined 212

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phylogenetic diversity (PD) as the total path length constituting the full phylogenetic (in our case taxonomic) tree. Sections of the branch that are shared by more than one species are divided equally between them and the taxonomic distinctiveness of an individual species is then simply its path length to the base of the tree. Thus, in Figure 2a, adopting the standardisation we shall frequently use in this paper—that the branch length from the base of the tree to the terminal taxa is set to 100 and the step lengths between hierarchical levels are equal—the contribution to total PD from species 1 is (33.3+33.3+33.3/7), of species 2 is (33.3+33.3/2+33.3/7) of species 4 is (33.3+33.3/4+33.3/7) etc. Summing these contributions across species gives, naturally, a total PD of (33.3×7+33.3×3+33.3)=366.3. Subsets of species that span a greater proportion of the tree will give a high contribution to phylogenetic diversity and should be the targets for conservation from the point of view of complementarity and representativeness of the range of characters exhibited by that group of organisms. In the marine literature we are not aware of cases in which these principles of taxonomic distinctiveness, representativeness or complementarity have been formally followed in practice for the selection of species for conservation, or of the habitats in which these species are found, and there remains a gulf between this branch of theory and the practice of marine conservation. This suggests either that biodiversity per se is still not regarded as a marine conservation criterion, or that the practical pay-offs of a phylogenetic distinctiveness approach to selecting target species for priority conservation status have not been sufficiently articulated. In contrast, the development of taxonomic distinctness measures for environmental assessment and monitoring of biodiversity change over wide spatial and temporal scales has begun to find practical application in the marine literature, and the remainder of this review concentrates on this topic.

Taxonomic distinctness

Average taxonomic distinctness (AvTD) In has been known for many years that in grossly perturbed situations communities are maintained in an early stage of succession and often comprise guilds of closely related sibling species or single species with a high genetic diversity. Knowlton (1993) has tabulated the marine taxa known to have sympatric sibling species and there is a remarkable concordance between the soft-bottom macrobenthic taxa she lists and those identified by Pearson & Rosenberg (1978) as characterising organically polluted habitats. Macrobenthic examples include the species complex comprising types of the well known “pollution indicator” polychaete Capitella capitata (Grassle & Grassle 1976), and meiobenthic examples include the copepod genus Tisbe (Bergmans 1979, Gee et al. 1985), the polychaete genus Ophryotrocha (Åkesson 1984) and the nematode genus Pontonema (Bett & Moore 1988, Warwick & Robinson 2000). Unperturbed benthic communities in a late stage of succession comprise a wider range of more distinct species belonging to many phyla, i.e. they have a high taxonomic distinctness. Measures of phylogenetic diversity described in the previous section have not been carried over into the area of environmental monitoring and assessment, where the emphasis is not on choosing species to conserve but monitoring for environmental degradation, the benefits of remediation or the effectiveness of conservation measures. The considerations here are 213

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rather different; the raw material is often a set of community samples, sometimes with recorded abundances for each observed species and sometimes simple presence/ absence data (species lists). The outcome required is not a preferential selection of species from the inventory for conservation status but an assessment of whether sampled assemblages display some pattern in biodiversity through time or in space. An average taxonomic distinctness measure should reflect both richness in higher taxa and the evenness component of diversity. Figure 2b and c show that it cannot therefore rely solely on topology because the topology is identical but the latter clearly exhibits greater biodiversity. Figure 2d and e illustrate a disparity in taxon evenness, with the latter representing a less taxonomically diverse assemblage than the former, both in the sense of possessing greater vulnerability to species loss and in potential functional inefficiency. Such a measure might be constructed by averaging out the distinctiveness of each species, as defined in the previous section. This gives an index which we can call the Average Phylogenetic Diversity (AvPD, denoted by F+) for the tree; it is simply the total PD divided by the number of species S. Note that total PD itself is not, under one of our main criteria, a practically useful statistic because the total path length in the taxonomic tree will be highly positively correlated with the number of species S, and therefore be strongly dependent on sampling effort. AvPD might appear to have overcome this problem but it has several drawbacks: it has a focus exclusively on “character richness” (in the terminology of Humphries et al. 1995) and does not distinguish Figure 2d from 2e, in spite of the latter’s intuitively lower diversity, and is now negatively correlated with S and thus sampling effort (Fig. 3). Instead, Warwick & Clarke (1995) define taxonomic indices in terms of average “distance apart” of all pairs of individuals (or species) in a sample, tracing these distances through the taxonomic tree. These measures are chosen to satisfy the above requirements of incorporating higher taxon richness and evenness concepts (see the D+ values in Fig. 2) and also possessing an insensitivity to sampling effort (Fig. 3). “Average taxonomic diversity” (D) is simply the average path length between every pair of individuals in a sample (Warwick & Clarke 1995), and is defined as =[SSi<jwijxixj]/[n(n-1)/2]

D

(Equ. 1)

where xi(i= 1,..., s) denotes the abundance of the ith species, n(=Sixi) is the total number of individuals in the sample, wij is the “distinctness weight” given to the path length linking species i and j in the hierarchical classification, and the double summations are over all pairs of species i and j (Note that the path length between two individuals of the same species is set to zero). In more formal statistical terms, D is the expected path length between any two randomly chosen individuals from the sample (without replacement), and bears a simple relationship to standard diversity indices: when wij=1 (for all i<j), i.e. when the taxonomic hierarchy is ignored, D reduces to a form of Simpson diversity (e.g. Pielou 1975), namely:

(Equ. 2)

Indeed, the Simpson index was first constructed from the probability that any two individuals, selected at random from the full set, are from the same species (Simpson 1949). Average taxonomic diversity D can therefore be seen as a generalisation of Simpson diversity, 214

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Figure 3 As Figure 1, but for six biodiversity measures based on taxonomic relationships between species, a and b are based on subsamples of differing numbers of individuals, as in Figure 1, whereas c-f are based on subsamples of differing numbers of species drawn randomly (without replacement) from the species presence list (=137 spp.). a: (average) taxonomic diversity based on abundances; b: (average) taxonomic distinctness based on abundances; c: (average) taxonomic distinctness from presence/absence data; d: total “phylogenetic diversity” from presence/absence data; e: average phylogenetic diversity from presence/absence data (=PD/S); f: variation in taxonomic distinctness from presence/absence data.

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incorporating an element of taxonomic relatedness. (In fact, K.Shimatani pers. comm., has shown that there is a close relationship between D and the sum of Simpson diversity calculated at each level of the taxonomic hierarchy). A second index, “average taxonomic distinctness”, D* (Warwick & Clarke 1995), is modified to remove some of the dependence of D on the species abundance distribution represented by the {xi}. It divides the taxonomic diversity of equation (1) by the Simpsontype index of equation (2), i.e. D is divided by its value when the hierarchical classification collapses to the special case of all species belonging to a single genus. The resulting ratio, D*, is then more nearly a function of pure taxonomic relatedness of individuals. The algebraic definition of average taxonomic distinctness is *=[SSi<jwijxixj]/[SSi<jxixj]

D

(Equ. 3)

and an alternative way of viewing this is as the expected (weighted) path length between any two randomly chosen individuals from the sample, conditional on them being from different species. A special case is the use only of presence/absence information for each species. The {xi} are then all thought of as equating to unity (for species which are present), and D and D* reduce to the same statistic, namely +

D

=[SSi<jwij]/[s(s-1)/2]

(Equ. 4)

where s is the number of species present and, for the double summation, i and j range over these s species. The mean values of all three of these indices have been shown to be independent of sample size, i.e. the number of individuals in the case of D and D* and the number of species in the case of D+ (Clarke & Warwick 1998b). In Figure 3 these indices are calculated from computer simulated subsamples of different numbers of individuals drawn, without replacement, from a large sample comprising the summation of five sets of ten grab samples of macrobenthos taken in the Bay of Morlaix, France, between May 1977 and February 1978, a period of minimal community change (Dauvin 1984). (For the statistics based only on presence or absence of species, such as D+, the simulations draw random subsamples of different numbers of species). The lack of dependence, in mean value, on sampling effort implies that D+ in particular can be compared across studies with differing and uncontrolled degrees of sampling effort (subject to assumptions concerning comparable taxonomic accuracy). This may be of particular significance for historic (diffusely collected) species lists from different localities or regions, which at first sight may seem unamenable to valid diversity comparison of any sort. Furthermore, Clarke & Warwick (1998b) have devised a randomisation test to detect a difference in the average taxonomic distinctness, for any observed set of species, from the “expected” D+ value derived from a master species list for the relevant group of organisms. The null “expectation” is that the species present at any one place or time behave like a random selection from the regional species pool. Figure 4 is a histogram of D+ values for 1000 random subsamples of a fixed number m of species, from a full list of free-living marine nematodes of the UK (s=395 species): (a) m=122, (b) m=111, corresponding to the sublist sizes for combined samples at intertidal sandy sites in the relatively clean Exe and polluted Clyde estuaries respectively. The true D+ values for both localities are also indicated: for the Clyde, the null hypothesis that the average distinctness equates with that for the UK 216

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Figure 4 Histograms of D+ values for 1000 random subsamples of a fixed number of m species, from a full list of free-living marine nematodes of the UK (s=395 species), corresponding to the sublist sizes for combined samples at intertidal sandy sites in the Exe and Clyde estuaries, respectively. The measured D+ values for both localities are also indicated: for the Clyde the null hypothesis that the average distinctness equates with that for the UK as a whole is clearly rejected (P<0.1%).

as a whole is clearly rejected (P<0.1%). Calculation of D+ from simulated subsamples of different numbers of species from the master list can be used to produce a “probability funnel”, against which distinctness values for any specific area, pollution condition, habitat type etc. can be checked, and formally addresses the question of whether a putatively impacted locality has a “lower than expected” taxonomic spread (Clarke & Warwick 1998b). Most papers to date have used the simplest possible weighting of step lengths between levels in the taxonomic hierarchy to calculate these distinctness measures, i.e. equal 217

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increments of length between each successive level: e.g. w=1 (species in the same genus), 2 (same family but different genera), 3 (same order but different families), 4 (same class but different orders), 5 (same phylum but different classes), 6 (different phyla). The number of taxonomic levels used in standard classifications varies considerably from taxon to taxon however (e.g. Rogers et al. 1999 define 13 levels for fish), and for comparative purposes standardisation of these weightings is appropriate (Clarke & Warwick, 1999). As suggested earlier, the simplest such standardisation sets the path length w to 100 for two species connected at the highest (taxonomically coarsest) possible level, so that the above weights of 1 to 6 become w = 16.7, 33.3, 50, 66.7, 83.3 and 100, respectively. Although this may appear somewhat arbirtary, using data on free-living marine nematodes from 16 localities/ habitat types in the UK, Clarke & Warwick (1999) showed that the relative values of taxonomic distinctness for the 16 sets are robust to variation in the definition of step length. For example, there is a near perfect linear relationship between values calculated using a constant increment at each level and a natural alternative in which the step lengths are proportional to the number of species per genus, genera per family, etc. Warwick & Clarke (1998) also found indications that taxonomic distinctness measures may not suffer from some of the other disadvantages of species richness measures. For freeliving marine nematode assemblages from Britain and Chile they showed that, although some habitat types may have naturally lower values of taxonomic distinctness than others, unless the habitats are degraded in some way the D+ values are not outside expectation. That is, they do not generally fall below the lower 95% limit of the simulated distribution under a null hypothesis that the assemblages behave as if they are a random selection from the regional species pool. This ameliorates the problem with species richness measures of biodiversity, which are much more strongly affected by habitat type and complexity as noted above, thus making comparisons difficult between datasets from different habitats or where habitat type is uncontrolled. Warwick & Clarke (1998) further showed that taxonomic distinctness in marine nematodes is explicitly related to trophic diversity: a reduction in trophic diversity is associated with a reduction in taxonomic distinctness, although not necessarily with a reduction in species richness.

Variation in taxonomic distinctness (VarTD) Another aspect of the taxonomic structure recently explored by Clarke & Warwick (2001) is the “evenness” of the distribution of taxa across the hierarchical taxonomic tree. In other words, are some taxa over-represented and others under-represented by comparison with what we know of the species pool for the geographical region? This is particularly relevant when comparing biodiversity at larger spatial scales where, in addition to environmental degradation from anthropogenic causes, habitat heterogeneity is likely to influence diversity patterns. For all groups of organisms, specific taxa attain their highest diversity in particular habitats and if certain habitat types are absent from an area, then we might expect some groups of species to be under-represented and others over-represented compared with the regional picture. This will result in a more uneven (more variable) distribution across the tree. Clarke & Warwick (2001) hypothesised that, under anthropogenic disturbance, the species that disappear first tend to be those representative of higher taxa which are relatively species-poor (i.e. those recognised as having a high taxonomic distinctiveness as defined above and therefore of high conservation priority). The remaining species are then from a smaller number of groups, each of which tends to be relatively more species-rich. This effect should manifest itself both as a 218

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decrease in average taxonomic distinctness and a decrease in the variability of pairwise relatedness of species in the taxonomic tree. However, one can also envisage other (biogeographic) patterns in which average taxonomic distinctness might be expected to decrease or remain stable at some locations but the unevenness in phylogenetic structure increases. Any statistic that measures this variability should ideally have similar sampling behaviour to that of D+, i.e. lack of dependence on sample size or sampling effort. While average taxonomic distinctness will be effective in contrasting situations in which there are a restricted number of higher taxa, for a given number of species, with cases where the same number of species are more taxonomically disparate, it will not distinguish the trees in Figure 2c and f, which have the same number of species and an identical AvTD but for which the tree in Figure 2f has a more uneven structure across the taxonomic units than Figure 2c. The presence of some genera with many species would tend to reduce AvTD but this could be counterbalanced by the presence of families represented by only one (or a very few) species. Such a difference in structure will be well reflected in variability of the full set of pairwise distinctness weights making up the average. Variation in taxonomic distinctness (VarTD, denoted by L+) is therefore defined as

(Equ. 5)

where

(Equ. 6)

Clarke & Warwick (2001) have shown that VarTD has the same desirable sampling properties as AvTD, primarily a lack of dependence of its mean value on the sample size (except for rather small samples where it has a slight negative bias). As with AvTD, the VarTD statistic for any local study can be tested for “departure from expectation”, based on a master taxonomy for that region, by constructing a simulation distribution from random subsets of the master list. Clarke & Warwick (2001) went on to summarise the joint distribution of AvTD and VarTD, values from real datasets being compared with a fitted simulation “envelope” in a 2dimensional (D+, L+) plot. When applied to species lists of free-living marine nematodes, and related to the master list for UK waters, the combination of AvTD and VarTD separated out, in different ways, some degraded locations (low D+, low to normal L+) and the pristine island fauna of the Scillies (normal D+, high L+). The two indices were in this case demonstrated to be measuring effectively independent features of the taxonomic tree (but see below for contrasting data on other faunal groups). The combination of D+ and L+ was regarded as a statistically robust summary of taxonomic relatedness patterns within an assemblage, with the potential to be applied to a wide range of historical data in the form of simple species lists.

Taxonomic dissimilarity between samples or areas AvTD and VarTD are attributes that are specific to a particular sample or area, and as such are akin to the more conventional measures of alpha and gamma diversity. However, it is also possible to construct a measure of the degree to which two samples are taxonomically 219

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related to each other, which is more equivalent to beta or difference diversity. Clarke & Warwick (1998a) defined such a measure, termed an “optimum taxonomic mapping statistic”, M. For each species in one sample, its closest taxonomic relative in the second is defined, scoring 1–5 for a species of the same genus, family, order, class and phylum respectively, and 6 if it has no phyletic counterpart (the weightings would, of course, be different with different numbers of hierarchical taxonomic levels). These scores are averaged over all the species from the first sample. This score depends on the order of the samples (it is not a reversible “one-to-one map”) because, for example, some species in the second sample may not be mapped onto by a species in the first sample. So the complementary average is also taken of the optimal mapping of the second sample onto the first and these two values are then averaged. Standardising path lengths as earlier (setting the branch length from the base of the tree to the terminal taxa to 100, with equal step lengths between hierarchical levels) then gives a symmetric index of taxonomic dissimilarity between samples, the complement of which is a mean of taxonomic similarity (Izsak & Price, in press).

Applications of taxonomic distinctness measures Although taxonomic distinctness measures have only been applied to data on field samples very recently, and the number of studies is still quite limited, some potential advantages of these methods over traditional species richness estimators of biodiversity are now becoming evident.

Geographical comparisons of biodiversity The sampling effort and habitat type independence of taxonomic distinctness has enabled comparisons of biodiversity on regional scales for starfish assemblages in the Atlantic Ocean (Price et al. 1999). Using D* as a biodiversity measure, they found that there were no clear trends associated with either latitude or water depth and questioned the emerging paradigms concerning these patterns. Piepenberg et al. (1997) compared the biodiversity of starfishes and brittle-stars in the Antarctic (Weddell Sea) and Arctic (NE Greenland) and although 86 species were identified in the Weddell Sea and only 26 off NE Greenland, many species in the Weddell Sea were closely related so that the assemblages were not significantly different from each other in terms of taxonomic diversity and distinctness. Izsak & Price (in press) have compared beta diversity of echinoderms in terms of taxonomic dissimilarity over three spatial scales, local (<10km), intermediate (10–100s km) and oceanic (100s-1000s km). They showed that taxonomic dissimilarity was significantly higher at small spatial scales and suggested that small areas may be characterised by the greater likelihood of species migrations and extinctions. In a time series of data on demersal fish assemblages from the North Sea, Hall & Greenstreet (1998) found that both D and D* closely tracked changes in species diversity indices. This is encouraging, since D* measures biodiversity attributes that should be completely orthogonal to richness- and evenness-based species diversity, as well as being more robust to sampling effort, so the implication in this case was that the conclusions drawn from species diversity were not particularly prone to sampling artefacts. The use of D* as a biodiversity measure in situations where traditional species diversity indices are inappropriate (as with diffusely collected historical data) is therefore supported by these observations. In their comparative study of 14 nematode assemblages from the British Isles, Clarke & 220

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Warwick (1999) examined the effects of manipulating the weightings of path lengths artificially (setting some step lengths to zero) in an attempt to see whether there were any characteristic differences in the phylogenetic structure of biodiversity between island (Isles of Scilly) versus mainland (Britain) faunas. They found that the average taxonomic distinctness of nematodes from the islands was no different from that of mainland sites but that there was a greater spread of diversity at the very highest taxonomic level (of subclasses), balanced out by a lower representation of taxa at intermediate levels, so that overall D+ was no higher than on the mainland. Subsequently, Clarke & Warwick (2001) extended this analysis to examine VarTD for the same data and found that L+ separated out the Isles of Scilly datasets as distinctive in a way that was not apparent from the D+ values. All three subsets of the Scillies data (species lists from sand, intertidal algae and the total inventory for all habitats) fell above the upper limit of the L+ probability funnel, indicating a higher than expected variation in distinctness of species pairs. These distinctively high values of VarTD may result from the reduced habitat diversity. One major nematode habitat, fine silty sediments, is absent. There are no rivers or estuaries, which are sources of fine sediment in mainland coastal waters. The sea is exceptionally clear here; kelp (Laminaria ochroleuca), for example, occurs at depths of 30 m, the deepest in Britain. This means that there is no fine sediment associated with secondary habitats such as seaweeds and their holdfasts. The proportions of the three main nematode groups, enoplids: chromadorids: monhysterids, is 43.1:36.3:20.6, compared with average values for the complete British fauna of 26.5:46.2:27.3. Enoplids favour clean habitats and are not at all characteristic of sedimentary habitats (Warwick et al. 1998), whereas monhysterids are more characteristic of fine sediments. The relative over-representation of the former, and under-representation of the latter, is thus commensurate with the absence of fine sedimentary habitats. Theories of island biogeography have largely been developed from data on species that are easily censused and for which complete inventories can be produced in relation to island size, such as birds, reptiles and certain groups of insects (MacArthur & Wilson 1967). For groups such as free-living nematodes, or other small cryptic taxa, a complete census is rarely possible, except for very small areas, and the list for the Scillies archipelago is certainly not complete—increased sampling effort would undoubtedly reveal more. AvTD and VarTD, with their appealing sampling properties, therefore offer a useful alternative and might also help to address long-standing questions concerning island biogeography that cannot be resolved by species counts alone: whether, for example, increasing numbers of species are a function of increasing island size per se, or are related to the larger number of habitats.

Environmental impact assessment Although much further work needs to be done, from the above it does seem that the VarTD measure of biodiversity may have some potential for monitoring the effects on biodiversity of habitat loss and associated remediation efforts. Loss of a particular habitat type may not affect the overall species diversity of a region but the elimination of taxa typical of that habitat type could be detectable as an increase in VarTD. Less speculatively, average taxonomic distinctness measures have been put to more immediate use for the assessment of environmental impacts on biodiversity. In the UK nematode study, Clarke & Warwick (2001) found that environmentally degraded locations such as the Clyde estuary (industrial and domestic pollution), Fal estuary (heavy metal pollution) and 221

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Liverpool Bay (industrial and domestic pollution) were characterised by decreased D+ and L+, a response that (unlike species richness) seems to be monotonic in respect to increasing environmental stress. In a study of the impacts of oil drilling activities on the macrobenthos in the vicinity of the Ekofisk oil field in the North Sea, Warwick & Clarke (1995) found that D and D* continuously decreased along the gradient of increasing environmental contamination, whereas species diversity remained constant. The increase in sensitivity of these measures, relative to species diversity, was not however confirmed by similar studies of other North Sea oil fields (Somerfield et al. 1997). The initial promise of these measures as a more sensitive univariate index of community stress than species diversity has not been borne out by subsequent studies: their strength is rather in their robustness to sampling artefacts. Rogers et al. (1999) studied the impacts of commercial bottom trawling on the demersal fish assemblages of the North Sea, English Channel and Irish Sea, in research beam-trawl surveys undertaken between 1990 and 1996. These data are recorded over 277 ICES quarter rectangles, subsequently grouped (for display purposes) into nine coastal sectors: 1 Bristol Channel, 2 W Irish Sea, 3 E Irish Sea, 4 W Channel, 5 NE Channel, 6 SE Channel, 7 SW North Sea, 8 SE North Sea, 9 EC North Sea (see Rogers et al. 1999 for a map defining these sea areas). The number and duration of tows within each of the 277 ICES quarter rectangles is variable, making the species richness of each sample more a reflection of sampling effort than any measure of diversity and suggesting the use of the methodology of this paper. Rogers et al. (1999) analysed both the quantitative and presence/absence data, using A although not A, but there are sufficient points of interest with the presence/absence data alone to make further analysis here a useful illustration of the methodology. (Note that three of the 277 samples have been ignored because they contained very little information—as few as two species in one case from Area 2—which would have generated significant outliers in the distinctness plots.) First, there is a wealth of taxonomic information that can be exploited in this case. The analysis uses a taxonomy based on phylogenetic principles, compiled by J.D.Reynolds (University of East Anglia) primarily from Nelson (1994) and McEachran & Miyake (1990), which has 13 levels between class and species (Fig. 5). The figure labels the two classes, the orders, some of the main families and all the genera and species used in these studies (taxonomic scope is defined by reliable capture by the beam-trawls). The distinctness structure of this master list then becomes the standard against which the species lists from the various quarter-rectangles are assessed. Note that several of the subgroups are relatively less wellused and Rogers et al. (1999) examine the effects on taxonomic distinctness of adjusting the step lengths in the hierarchy in line with the change in taxon richness between each level. As was seen also in the UK nematode study (Clarke & Warwick 1999), this made negligible difference to the rank order of the distinctness values for each sample, so we shall here again use a constant step length (of 7.69) between each level, standardised to make the maximum path length (species in different classes) equal to 100. Figure 6 shows the AvTD values, D+, for all 274 samples, separated into the nine areas, and plotted against the number of species in each sample. On this are superimposed the results of simulating 5000 random selections from the master list of 93 species (Fig. 5) for each of a range of sublist sizes: 5(1)10(2)30(5)35. The funnel represents the 95% probability limits and, for all subset sizes, the simulated mean (dashed line) is close to the master list value of D+=80.1, reflecting the sample size independence. The latter is also seen in the real data, in that there is rather little suggestion for any of the nine areas that D+ is correlated with the observed number of species. Most importantly, the average taxonomic distinctness is seen to differ between the areas, being markedly lower in areas 8 and 9, and in few (if any) 222

Figure 5 Taxonomic tree for the 93 demersal species that could be reliably sampled and identified in the Rogers et al. (1999) study of NE Atlantic coastal groundfish assemblages. Note the potential richness of phylogenetic information captured by the 14 hierarchical levels.

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Figure 6 Average taxonomic distinctness values, D+, plotted against the observed number of species, for the groundfish assemblages in 274 ICES quarter-rectangles. These are divided into nine NE Atlantic coastal Areas: 1 Bristol Channel, 2 W Irish Sea, 3 E Irish Sea, 4 W Channel, 5 NE Channel, 6 SE Channel, 7 SW North Sea, 8 SE North Sea, 9 EC North Sea. Dashed lines indicate the simulated mean D+ from 5000 random selections from the master list of 93 species, for each sublist size: 5, 6, 7,..., 35; this confirms the unbiasedness and therefore comparability of D+ for widely differing degrees of sampling effort (as here). Intervals within which 95% of the simulated D+ lie (the “expected” range of D+ for a given number of species) are constructed for each sublist size and represented as a probability funnel (continuous lines).

cases do the samples from each area appear to be a selection from the “null” distribution represented by the funnels. Rogers et al. (1999) discuss possible explanations for these differences, noting in particular the contribution to the results made by the spatial patterns of elasmobranchs, arguably a taxonomic group particularly susceptible to disturbance by commercial trawling because of their life history traits. Figure 7 displays the same type of analysis for the VarTD statistic L+. Again, as expected on theoretical grounds, any relationships between L+ and the number of species in each sample are weak or non-existent, with the simulated mean value of L+ (dashed line) being close to its value of 282 for the master list, with only a modest negative bias for very small 224

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Figure 7 Simulated means (dashed line), 95% probability funnels (continuous line) and actual index values for the groundfish data, as in the legend to Figure 6 but for variation in taxonomic distinctness, L+. Here, a slight negative bias is apparent in the mean, but this is only present for the smallest sublist sizes and is negligible in relation to the variability of the index.

sample sizes. The L+ values are generally higher than “expected” from the simulation funnel, but with the lower values corresponding to the areas which also have lower values of D+, in line with the previous suggestion, made in the context of the UK nematode study, that lowered values of average distinctness, through the loss of taxonomically distinctive species, would correspond with lower values of the variation statistic. (For a contrasting situation, in which low or “expected” values of D+ correspond with high values of L+, see the later example on p. 227 of molluscan death assemblage patterns in relation to habitat.) The probability funnels of Figures 6 and 7 are primarily designed to display the distinctness for a single sublist from a particular geographical area or pollution condition (or a small number of contrasting sublists, as in the UK nematode study of Clarke & Warwick 2001), in relation to what might be expected from subsamples from an appropriate master list. Here, there are a large number of “replicate” samples from each of the nine coastal sectors and an appropriate summary is to compute the means and 95% confidence intervals for each (using a pooled estimate of variance, as in standard one-way ANOVA) and assess the extent to 225

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Figure 8 Means and 95% confidence intervals for the groundfish data of: a: average taxonomic distinctness (D+); b: variation in taxonomic distinctness (L+); c: average phylogenetic diversity (F+); d: number of species (S). These are based on unequal numbers of replicates, being the species lists for each quarter-rectangle grouped into the nine coastal Areas specified in Figure 6. A common variance estimate is assumed across the groups, as in one-way ANOVA (the latter gives a highly significant F statistic for differences between groups for all indices). Dashed lines in a and b indicate the values of D+ and L+ from the master list of 93 demersal fish species. The master list F+ is 44, well below the value for any observed sublist because of the large positive bias, and thus non-comparability of F+ for differing sample sizes: the strong negative correlation of F+ and S is clear from comparing c with d.

which each under- or over-estimates D+ or L+ for the master list. This is shown in Figures 8a and b, where the dashed lines give the master list values. The significant degree to which D+ and D+ correlate, for the real data, is also clear but it is important to check this against any innate correlation that would be expected from the construction of the taxonomic tree, seen in correlations between simulated AvTD and VarTD values in the 5000 random selections for each sublist size. Such internal correlations vary with the specifics of each tree; only for trees with very few levels do Clarke & Warwick (2001) show a general result (a strong 226

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negative correlation between D+ and L+). In fact, examples can be found that span a range of possibilities from a moderately high negative correlation (see the mollusc death assemblage study, later), through effectively zero correlation (the UK nematode study) to modest positive correlation (the current groundfish data). These structural correlations vary a little for the different simulated sublist sizes, from about 0.35 for 10 species up to 0.48 for 30 species (the range of sublist sizes covering most samples) but it is seen that the observed positive correlation of D+ and L+ over the 274 samples in this case (0.69, with 95% confidence interval 0.62 to 0.75) significantly exceeds the internal, structural correlation. This finding can be interpreted as indicating that observed lower taxonomic distinctness overall is associated with a relatively lower range of taxonomic distinctiveness of the species present. Coastal sectors with reduced D+ and L+ are clearly associated with sectors that have the highest demersal fishing intensity (Jennings et al. 1999). Finally, Figure 8c shows the means and confidence intervals over the nine areas for the alternative average distinctness measure, Average Phylogenetic Diversity F+, which is seen to behave in a quite different manner to D+. The explanation is not difficult to seek. In the illustrations of Figure 2, laying aside the more subtle distinctions, AvPD was largely seen to track AvTD, both of them placing these simple examples in a reasonably natural distinctness order. The major simplification in Figure 2, however, is that the number of species was held fixed (at 7) for all comparisons. For the groundfish data, there are substantial differences between numbers of species obtained in each quarter-rectangle, reflecting (at least in part) unequal degrees of sampling effort, and the nine areas have differing mean sublist sizes (Fig. 8d). AvPD is seen to be strongly influenced by the sublist size, the means for areas 1 to 4 having exactly the opposite sequence in Figure 8c and d, and the direct correlation between + F and S, over all 274 samples, is -0.64. As a comparative measure of average distinctness, + F cannot be recommended for practical use.

Surrogates for biodiversity estimation Because of the impracticality of routinely attempting comprehensive surveys, “surrogacy” methods will clearly become the norm in biodiversity estimation (Harper & Hawksworth 1994) and the search for appropriate indicators of marine and coastal biodiversity has become an important research goal (Feral 1999). Surrogates might take the form of a subset of easily censused species from the total biota but the crucial issue then concerns how valid a measure this surrogate provides of the true total biodiversity. The species richness of the surrogate could never be expected to be representative and, here again, AvTD and VarTD could play a useful role. On a regional rather than a single habitat basis, a census of all living species from the whole spectrum of habitat types would be very time consuming and costly. The concept of sampling a single “spatially averaged” subset of species such as a death assemblage (e.g. of molluscs), as a surrogate for regional biodiversity, is therefore appealing. Warwick & Light (2001) produced species lists of mollusc (gastropod and bivalve) shells from St Martin’s Flats on the Isles of Scilly and used AvTD and VarTD as appropriate measures to test the extent to which they were representative of the regional living fauna. They showed that for gastropods, AvTD of the death assemblage was fully representative of the regional fauna but for bivalves it was significantly lower. VarTD of the death assemblages was not representative of the living fauna for either class of molluscs. The analysis is again best summarised by 2-dimensional (D+, L+) plots, placing the real AvTD and VarTD pairs in the context of 95% probability envelopes from simulated samples, of comparable sizes, 227

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Figure 9 (AvTD, VarTD) plots for, a: bivalve, b: gastropod death assemblages at St Martin’s Flats, Isles of Scilly, UK. Dots indicate observed (D+, L+) values for species lists recorded from A: surface searches by R.M.Warwick (RMW) and B: by members of the Conchological Society (CS) of Great Britain and Ireland; C: surface searches and microscopic examination of sand samples by CS; D: all RMW and CS lists combined. In parentheses are the numbers of species in each list. In a, crosses denote (D+, L+) values from 2000 sublists of 50 species, randomly selected from a “master list” of the 87 bivalve species known to have had live populations on the Isles of Scilly in recent times (Turk & Seaward 1997). A modelled 95% probability contour for their distribution is indicated and is seen to be an excellent fit, with almost exactly 100 of the 2000 simulated values falling outside the envelope (see Clarke & Warwick 2001, for the construction algorithm for the back-transformed, bivariate normal ellipses). Similar 95% probability contours are shown for sublists of size 30 and 40 (based on further sets of 2000 simulations). In b, sublists of size 15, 25 and 40 are simulated, spanning the observed range of list sizes for gastropods. Individual simulations are not shown but are equally well-fitted by the displayed contours; the plus sign denotes the (D+, L+) values for the master list of 81 gastropod species with recent live records from Scilly.

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drawn from a master list of live records from the coastal waters of Scilly (Turk & Seaward 1997) (Fig. 9a,b). It is seen that all the real data points are outside the envelope for bivalves but not for gastropods. In the latter case, microscopic examination of sediment samples lead to a value within expectation but the surface searches for macro-species have (borderline) higher values than expected for L+, though entirely central and expected D+. This is probably because the process of arrival of gastropods into the sand-flat death assemblage from more remote habitats is more random than for bivalves, most species of the latter being characteristic of the sand-flat habitat itself. Also worth noting is that this is a case where the simulated D+ and L+ are strongly negatively correlated, in stark contrast to the UK nematode study described earlier in which they were uncorrelated, and the groundfish surveys, where they were mildly positively correlated. The simulation methodology, which automatically generates the “expected” null relationships of these indices, is clearly of value in interpreting that observed behaviour in practice.

Acknowledgements We thank Stuart Rogers (CEFAS, Lowestoft) and John Reynolds (UEA) for access to the groundfish data and the phylogenetic classification of Figure 5, respectively, and Jan Light (Royal Holloway College, London) together with members of the Conchological Society of Great Britain and Ireland for assistance with collection of the mollusc death assemblage data. This work forms part of the Biodiversity Core Strategic Research Programme of the Plymouth Marine Laboratory, NERC, UK, and was also part-funded under the RAMBLERS project by the UK Department of the Environment, Transport and the Regions (DETR contract no. CW0295) the UK Ministry of Agriculture, Fisheries and Food (MAFF contract no. AE1137).

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FUNCTIONAL GROUP ECOLOGY IN SOFT-SEDIMENT MARINE BENTHOS: THE ROLE OF BIOTURBATION T.H.PEARSON SEAS Ltd, Dunstaffnage Marine Laboratory, Oban, Argyll PA34 4AD Scotland e-mail: [email protected] and at Akvaplan-niva AS, Polar Environment Centre, 9296, Tromsø, Norway e-mail: [email protected]

Abstract Functional analysis of the structure of marine benthic communities has a chequered history. On the one hand, proponents of such analyses point to the increased understanding of the ecology of communities gained when their component species are grouped into units with comparable functions. On the other hand, critics of the concept suggest that such analyses are both superficial and misleading without a much better knowledge of the life histories and behaviour of benthic organisms than is available at present. Both these points of view are considered in the light of experience gained from some recent functional group analyses of soft-sediment benthos. It is concluded that these analyses have provided a clearer understanding of the influence on benthic faunal distributions of changing environmental conditions along vertical and latitudinal gradients. They have also produced some new insights into the relative importance of differing environmental variables in structuring benthic communities. The role of bioturbation in soft-sediment benthic communities is examined in some detail. The various ways in which bioturbatory roles have been partitioned into functional groups are discussed and a tentative scheme for characterising such roles on the basis of behaviour is suggested as an adjunct to process-based partitioning. It is suggested that the delimitation of groups based on a number of functions that are adapted to a particular environmental pressure is the best means of gaining ecological insights from this type of analysis.

Introduction The division of communities into groups of taxa that share similar functional attributes (functional groups) or exploit a common resource base (guilds) is a useful means of simplifying the analysis of community structure and function (Pianka 1978, Krebs 1985, Giller & Gee 1987). This approach has a long history in benthic community studies, e.g. Blegvad (1914) and has been extensively used by ecologists in Russia (e.g. Turpaeva 1957) to compare the structure of modern benthic associations and by paleontologists to trace the evolution of ancient sedimentary associations (Thayer 1983). Changes in the relative importance of differing trophic groups along gradients of depth and organic enrichment were shown by Pearson & Rosenberg (1978, 1987) to be consistent, comparable and useful in assessing the impact of such environmental variables. Moreover, in a formative review Fauchald & Jumars (1979) demonstrated the utility of using functional attributes to explain problems in polychaete phylogeny and synecology. More recently, in the context of functional form and group models in marine algae, Padilla & Allen (2000) have suggested that grouping 233

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taxa by particular function can be both useful and necessary for solving many ecosystem level questions and for modelling purposes. They suggest that the approach is particularly helpful where qualitative results are more important than quantitative predictions and when there are too many species in a system to consider them all individually. However, despite such demonstrable advantages, functional analyses of benthic community biology are relatively infrequent and have been criticised on the basis of inaccuracies stemming from the plasticity of many functional attributes (Posey 1990). It has been suggested that the limited knowledge of the behaviour and life histories of most benthic species precludes an accurate assessment of such attributes. In addition, grouping taxa together obscures individual responses to environmental change and thus makes the task of interpretation more difficult. Snelgrove & Butman (1994), in reviewing cause and effect in animal-sediment relationships, conclude that the designation of simple functional groups based on still-water observations of feeding or mobility is no longer meaningful; if the concept of functional groups is to be useful it must be modified to include considerations of organism behaviour within the context of the flow and sediment-transport regimes in which they reside. However, notwithstanding such doubts, the approach has continued to attract interest from both applied marine biologists as a basis of indices for the assessment of pollution impacts (Word 1979, Jones et al. 1993) and for relating benthic community structure to environmental forcing functions (cf. Miller et al. 1992). Moreover, the functional group concept has been applied recently to the analysis of the response of zoobenthos to the strong environmental contrasts along latitudinal and depth gradients in the Baltic Sea (Bonsdorff & Pearson 1999). The present review is, therefore, an overview of how the functional group approach has been applied to the study of soft-sediment benthic communities. It also suggests some field and experimental studies which, if undertaken, might provide much needed information to fill the gaps in knowledge pointed out by Snelgrove & Butman (1994).

The benthic habitat In order to assess benthic functionality it is necessary to consider the habitat structure within which the organisms operate. The first and most fundamental structure is the vertical zonation of that habitat. The sea floor is not a simple two-phase system comprising sediments and overlying water column. It perhaps can be described best as a density gradient constrained in its upper layers by physical forces (fluid dynamics) and in its lower layers by biotic forces (bioturbation). Thus as distance from the sediment surface diminishes the free flow of water over the bed is progressively converted to turbulent flow by shear stress. At the sediment/water interface increasing viscosity becomes important, as do microbial binding and bioturbatory activities. Within the sediments, particle settlement and consolidation is continually disrupted by bioturbation, which diminishes with depth at rates dependent on faunal and grain size distributions. The overall zonation of the benthic habitat may be summarised as illustrated in Figure 1. This vertical structure is strongly modified by bed flow gradients that add an infinitely variable horizontal component to benthic space. The speed of water movement over the surface controls both 234

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Figure 1 Vertical zonation of the benthic habitat.

the topography (land form or roughness) and the texture (grain size) of the surface. The behaviour of most benthic organisms inhabiting the interface areas is intimately adapted to bed flow rates. Thus trophic modes, predator-prey interactions and spawning actions are all controlled by and adapted to flow rates (e.g. Miller et al. 1992, Bock & Miller 1996). Conversely benthic faunal activities in the interface zone constrain and modify flow rates by, for example, the formation of bacterial films and aggregations, the deposition of faecal pellets and the construction of pits, burrows and protruding tubes. Bed flows may be unidirectional, intermittent or oscillatory as directed by the hydrographic conditions in any particular area. The form of such flows controls the settlement and eventual distribution of particles and bed form sediment types. Along any gradient of increasing flow rates there is a critical shear velocity above which bulk surface-sediment transport occurs (Fig. 2). Between quiescence and this point in the flow gradient the majority of benthic infaunal and epifaunal organisms can function effectively and exploit surface and boundary layer detrital inputs in a variety of ways. Beyond this point only a small number of infaunal and epifaunal sedimentary taxa, adapted to survive in unstable coarse grain sediments, occur. In areas where flow rates greater than the critical shear velocity predominate, soft-sediments (gravel to coarse sands) are replaced by hard substrata (pebbles to rock). Such areas are dominated by immotile or semi-motile epifauna and the vertical penetration of fauna into the substratum is severely

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Figure 2 Differing current regimes and the most important physical and biological constraints creating shear stress in the benthic boundary layer.

restricted. Hall (1994) provides a detailed assessment of the roles of physical disturbance in the structuring of sedimentary communities.

Benthic habitat processes Beneath the euphotic zone the benthos is entirely dependent on the input of detrital carbon from the overlying water column. Thus both total benthic biomass and production levels are critically related to the degree of benthic-pelagic coupling. Within the benthic boundary layers planktonic detrital sedimentation is modified by bedflows that may augment vertical inputs with material advected horizontally from adjacent areas. In areas of super-critical flow rates the horizontal movement of detrital particles assumes greatest importance whereas at sub-critical rates detrital deposition predominates. Fluctuating flow rates on many varying timescales cause continuous resuspension and redeposition of particles. Such particle cycling by physical forces in the boundary layer is strongly modified by faunal activities such as pit digging, ploughing, tube-building, etc. in soft substrata and by surface roughness characteristics strongly modified by organic growths on hard substrata. The most important of these processes are summarised in Figure 3. Particle cycling is an important factor within the sedimentary substratum. There the physical forces of percolation and diffusion that influence the movement of detritus are much less important than are the bioturbatory forces of burrowing, tubebuilding, irrigation and particle capture, subduction, ingestion and defecation, all of which result in continuous in-sediment particle recycling and remineralisation. On hard substrata, benthic faunal activity is confined to the aquatic and benthic boundary zones 236

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Figure 3 Benthic sedimentary habitat processes.

(Fig. 1) where flow rates in the former and the relative roughness of the latter are the dominant factors influencing the biota.

Biological constraints in layered space The adaptive responses of benthic organisms to the complexity of the three-dimensional but layered nature of their general habitat are equally complex. The basic faunal functions of establishing a living space, obtaining food and breeding are limited in different ways in each of the three major divisions of their environment in accordance with the various forces and factors outlined above. Thus active motility is essential in the aquatic layers in order to capture particles or prey and to escape predators. The most important adaptive influences on successful survival in this dimension are current speed, particle vectors and particle size. Within the benthic boundary layers, where organisms must establish a position within a limited area, bed flow, bed topography and sedimentation rates are the most important formative influences on inhabitants. Within the sedimentary layers, where sedentary burrowers or tube builders predominate, grain size, pore size and particle quality assume the greatest influence.

Functional traits in benthic organisms The various physical and biotic factors that influence life in the benthic environment have resulted in a wide variety of functional adaptations in benthic organisms. Although each 237

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species is uniquely adapted to its own niche, groups of benthic organisms have common functional attributes that relate primarily to resource partitioning and utilisation, predator escape and defence or to breeding requirements. The most fundamental of such attributes concern relative motility and feeding habits and, because these characteristics have been most frequently the focus of attention in studies of comparative functionality in the benthos, they will be given detailed attention here.

Functional analysis of feeding behaviour

Trophic group analysis One of the earliest studies of the feeding ecology of a benthic ecosystem was made by Blegvad (1914) in the Limfjord in Denmark. He divided the soft-sediment benthos into three trophic groups according to food source, namely, detritivores, carnivores and herbivores. Organisms were then further categorised by the type of feeding apparatus used. Thus six types of animals that capture detritus without the use of hard prehensile or masticatory organs were defined. These include pseudopodial feeders (Foraminifera), filter feeding with cilia (Porifera, Lamellibranchia, Ascidia, Cephalochorda), tentaculate feeders (some Polychaeta, Holothurida), proboscoidal feeders (some Polychaeta, Sipunculida, Echiurida), feeding with ambulacral feet (some Echinodermata) and food capture with nematocyst armed tentacles (Actiniidae, Hydroidae). A further four types of animal which use hard prehensile or masticatory organs were described. These were those using a radula (Mollusca), those with a muscular gullet equipped with hard mandibles or teeth (Priapulida and some Polychaeta), those with chitinous, seta covered limbs and a masticatory stomach (Crustacea) and those using calcareous toothed jaws (Echinoidea). Blegvad’s (1914) paper still remains one of the more detailed general studies of benthic invertebrate feeding behaviour. Early objections to this type of classification were expressed by Hunt (1925) and Yonge (1928) who doubted the utility of making an initial division on the basis of the presence or absence of hard mouthparts. Hunt pointed out that Blegvad’s classification was predicated on the shallow water communities of the Limfjord and was not easily applicable to the deeper benthic communities of the offshore areas he studied. He divided the sedimentary benthos into only three groups, carnivores, suspensivores and detritivores, although the last were further subdivided into selective and non-selective particle feeders. Yonge (1928), in a review of invertebrate feeding methods, initially split organisms into those utilising small particles (i.e. microphages), those taking large particles or food masses (macrophages) and those taking fluid or soft tissues. He defined six microphagous and six macrophagous mechanisms. Subsequent investigations in this area have tended to take an approach similar to that of Hunt (1925) and to define wider, less specific trophic groups. Thus, traditionally, five broad trophic groups based on the food resource exploited have been recognised in benthic organisms, namely, herbivores, suspensivores, detritivores, carnivores and omnivores (cf. Barnes 1980), although many authors have split detritivores by strata into surface deposit feeders and subsurface deposit feeders (burrowers) (e.g. Hunt 1925, Pearson 1971). Similarly, suspension feeders may be split in accordance with their feeding position in relation to the boundary layer, i.e. whether they filter particles from the aquatic or benthic boundary zones, or more minutely, from what height in each of these zones are particles taken (cf. Savilov 1957, Turpaeva 1957). Indeed such broad groups can 238

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be subdivided in many different ways dependent on the level of detailed information available on the feeding behaviour and morphology of the species under consideration. Unfortunately, such detailed information is lacking for the majority of species in many, if not most benthic habitats. This ignorance of even the most basic natural history of many benthic species is the greatest barrier to a more widespread use of the functional group concept in benthic ecology. Nevertheless, the habits of many species can be inferred from a knowledge of their general anatomy and by analogy with similar species whose behaviour has been studied (cf. Jumars & Fauchald 1977, Fauchald & Jumars 1979). In a comprehensive summary of polychaete feeding strategies and guilds these authors synthesised the earlier approaches and extended their functional analysis to include relative motility (see p. 243) and food capture mechanisms. They discussed two major feeding modes based on the size of food particles taken and the means by which particles are ingested. Thus macrophages take large particles that are manipulated individually during capture whereas microphages take small particles that are handled in bulk. Macrophages are divided into two submodes, according to the trophic origin of their food, i.e. herbivores and carnivores. Microphages have three submodes based on the strata where they feed, viz. filter feeders exploit suspended particles in the water column, surface deposit feeders take particles from the interface and burrowers feed on material within the sediments. Within these categories twelve subgroups were recognised based on morphological differences in feeding structures. Subsequently, the Fauchald & Jumars (1979) classification has been extended to include all marine benthic invertebrate groups in functional group analyses of changes in community structure along environmental gradients (Pearson & Rosenberg 1987, Bonsdorff & Pearson 1999). A further distinction in forms of suspension feeding has arisen from the perception of the importance of horizontal flow in the boundary layers. In many habitats the horizontal advection of particles from other areas can be as, if not more, important than the sedimentation of detritus from the overlying water column. Many organisms can deploy active mechanisms to trap, intercept or snatch particles flowing past them. Such methods have been defined as active suspension feeding in contrast to the passive suspensivorous modes used to catch falling detritus. Such distinctions ignore the considerable behavioural overlap between these modes that can frequently be deployed sequentially by the same organism in response to changing current speeds. However, these categories have been useful in analysing and contrasting the trophic structure of communities in areas rich in advected detritus with adjacent habitats receiving only falling particles (Josefson & Conley 1997, Josefson 1998) (see Table 1). An experimental approach to categorising types of particle feeding on and above the sediment surface was taken by Miller et al. (1992). These authors related the response of benthic microphages with various types of particle capture mechanisms to changing flow rates and demonstrated a considerable variability in feeding method, both within and between

Table 1 The interaction between current velocity, particle vector and benthic suspensivore feeding behaviour.

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Figure 4 Diagrammatic representation of the response of a group of benthic microphages to an increasing bed stress gradient ranging from quiescence (zero stress) to maximal flow (u*). Black indicates deposit feeding, grey suspension or flux feeding, and white motility. The width or shading of the bar represents the relative magnitude of the observed response. The greatest variability in feeding mode within a species and among all species was seen at flow rates below the critical shear velocity needed to resuspend surface particles. From Miller et al. 1992.

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species at flow rates below the critical velocity. Above that velocity only a few types of suspension feeders and the motile scavengers could feed successfully (Fig. 4). The feeding activities of carnivores and subsurface deposit feeders were shown to be independent of flow rate. Wildish (1977, 1985) classified macrofaunal trophic types of continental shelves into infaunal surface and subsurface deposit feeders and four types of suspension feeders. These four types included three epifaunal groups, comprising bed-load transport feeders, turbulent flow filter feeders and impingement feeders, and laminar flow feeders that included both infaunal and epifaunal taxa. This classification takes no account of carnivorous or omnivorous groups. In a detailed study of foraging and distribution patterns of infaunal deposit feeding annelids from intertidal sand- and mudflats Whitlach (1980) recognised two feeding groups, surface and subsurface foragers. Both were found to partition available food resources on the basis of particle size but the latter also exploited differing vertical levels in the sediments. Two more recent studies of sedimentary macrofaunal populations, one in the North Sea (Dauwe et al. 1998), the other in an upwelling area off the Chilean coast (Gutiérrez et al. 2000), divided the populations into five groups: interface feeders, capable of switching from suspension feeding to surface deposit feeding, surface deposit feeders, subsurface deposit feeders, suspension feeders and omnivores and/or predators. These authors also grouped taxa separately into bioturbation categories (see p. 256).

Lability of food taken Some studies have stressed the importance of the comparative energetic value of the food taken by benthic organisms and grouped taxa into exploiters of labile particles and exploiters of recalcitrant particles. Forbes et al. (1994) have demonstrated that the opportunist depositfeeding polychaete Capitella sp. 1 is physiologically adapted to exploit nitrogen-rich substrata and suggest that it is out-competed by more metabolically efficient taxa as relative lability declines. Similarly, Tsutsumi (1990) observed that gravid females only developed at very high sedimentary protein levels in a Capitella population in an organically enriched embayment in Japan. It thus seems probable that evolutionary selection pressures will differentiate groups of organisms on the basis of food quality requirements. That this may be a basis for the differentiation of subgroups within deposit feeders and suspension feeders has been explored directly or indirectly in a number of recent studies. Graf (1992, 1999) has reviewed the intricacies of the benthic contribution to benthic-pelagic coupling and demonstrated the rapid response of benthic organisms to the seasonal pulses of high quality planktonic material. The initial exploitation of incoming detritus is not confined to the suspension feeders of the benthic boundary layer. Many burrowing infaunal taxa have the ability to transfer sedimenting particles, captured in the interface, rapidly to deeper levels in the sediment. Graf (1992) notes that a burrowing sipunculan species, which reaches high population densities on the Vöhring Plateau (Norwegian Sea), could translocate high levels of chlorophyll a to a depth of 9 cm in the sediment within 8 days following a spring pulse of detrital material. Several groups of burrowing polychaetes (paraonids, maldanids, nereids) in slope sediments of the North Carolina Shelf were found by Levin et al. (1997, 1999) to subduct labile phytodetrital material in competition with more traditional surface depositfeeding taxa (ampharetids, cirratulids, flabelligerids). These authors suggest that deep241

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dwelling organisms can rapidly obtain freshly deposited material, either directly by their own activities or, in the case of the smaller deep-burrowing forms, by accessing material buried by the larger taxa. Fresh, labile surface material can also be drawn into the deeper sediments by other mechanisms such as pumping, siphoning or hoeing (Graf 1992). Josefson & Conley (1997) describe another example of bioactive boundary layer-subsurface coupling from the area of the Skagerrak-Kattegat pelagic plume front. Near the front, high levels of phytoplankton reach the bottom waters directly and support dense populations of the burrowing ophiuroid Amphiura filiformis, together with a commensal bivalve Mysella bidentata. Amphiura filiformis is a passive suspension feeder that extends its long flexible arms into the water column to collect particles, which are then passed down to the mouth deep in the burrow. Mysella inhabits the burrow adjacent to the ophiuroid disk and shares the food obtained (Ockelmann & Muus 1978). Two burrowing echinoids occur in the same area, but at lower population densities and are also accompanied by commensal bivalves. In each case the echinoid passes particles from the surface to its mouth at the bottom of the burrow where some are intercepted by the commensal. Such observations suggest that a simple distinction between surface deposit-feeding and subsurface deposit-feeding groups might not adequately represent benthic-feeding ecology, even at a most general level. A consideration of the quality of the food being exploited and of the means by which it is obtained may be necessary qualifiers to the description of any defined trophic group. Mention should be made of two other types of energy acquisition, direct absorption of solutes and association with symbiotic bacteria, which are important to some classes of benthic organisms under certain circumstances. Direct absorption of soluble organics from pore water has been shown to occur in some tube-dwelling polychaetes (Stephens 1975), particularly those living in carbon-enriched sediments, and holothurians (Feral 1985). It is probable that this energy source is a supplement to one or other form of deposit feeding in such organisms (Lopez & Levinton 1987). A number of different types of thiophylic benthic species, which live in or near the anaerobic zone in sediments, are now known to contain symbiotic sulphide-reducing bacteria that supply much if not all of their energy. Thus, many lucinacean bivalve molluscs that inhabit burrows deep in the sediments in the vicinity of the redox discontinuity zone utilise this energy source (Dando & Southward 1986, Spiro et al. 1986) as do Pogonophora (Southward et al. 1986) and certain gutless oligochaetes living in anoxic sediments (Giere & Langheld 1987, Giere 1996). Thus, in any trophic group classification of the communities of enriched sediments, it may be necessary to include “absorbers” as an additional category.

Functional analysis of motility and habitat utilisation In general, sessile organisms dominate the benthic communities of stable or semi-stable substrata in coastal and shelf areas, where detrital inputs are high, and infaunal organisms as a whole have limited motility compared with sedimentary epifauna. However, relative degrees of motility in benthic organisms are critical in governing where and how food is obtained. One of the starting points of the formative studies of polychaete feeding strategies (Jumars & Fauchald 1977, Fauchald & Jumars 1979), was the observation that most polychaetes in the food-poor benthos of the abyssal north Pacific were creeping or burrowing deposit feeders. These authors therefore assumed that there must be a strong link between relative food availability and motility in the development of polychaete feeding strategies and included motility as one of 242

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the key functions. Trophic group characterisations were complemented by assigning each species to one of three motility groups, i.e. motile, semi-motile or sessile, in classifying those strategies. Their initial insight and the resulting classification have proved to be one of the most useful and successful means of exploring the ecological relationships between differing polychaete taxa. This type of classification has since been extended to include all benthic taxa in studies of factors influencing benthic community structure (Pearson & Rosenberg 1987, Bonsdorff & Pearson 1999). Invertebrate palaeontologists have also successfully defined groups based on a combination of functional characteristics, including relative motility, to assess changes in community structure and development across geological time. Thayer (1983), in an analysis of the comparative abundance of different functional groups in benthic populations from the Cambrian to recent times, showed that, following the early dominance of surface ploughing detritivores (trilobites), there had been a persistent increase in the relative proportion of motile infauna and epifauna. It should be noted that data of this type are biased very strongly to taxa with hard body parts suitable for fossilisation. Thus the under-representation of, for example, the soft bodied vermiform infauna, does not permit the structure of these fossil communities to be readily compared with that of extant benthic communities. Nevertheless, the gradual increase in motile infauna and epifauna over evolutionary time is of interest and may suggest that selection for motility has been a strong influence in the structuring of modern marine benthos. In both evolutionary and ecological contexts motility of sedimentary benthos has to be considered in relation to the sediment/water interface. Traditionally epifaunal organisms inhabit the interface, where suspensivores are generally sessile, whereas carnivores and grazers move horizontally over the surface. Surface detritivores may have varying degrees of motility, for example, some “bulldoze” through the upper surface layers (e.g. sadurid isopods); others rarely change their location voluntarily and use various types of tentacular or sweeping appendages to collect surface particles (e.g. spionid and ampharetid polychaetes). Bromley (1996) criticised the applicability of Thayer’s (1983) categories of bulldozing activities and provided an alternative analysis of the burrowing activities of sedimentary organisms, also based largely on observations of trace fossil structures. In this work four penetration styles, intrusion, compression, excavation and backfilling are recognised on the basis of how the sediment is moved or displaced during burrowing. Thus intrusive behaviour temporarily displaces sediment which falls back as the animal moves on. Such a process has been called turbulent or eddy diffusion and is limited to loosely packed or fluidised media. Compression occurs in somewhat more compacted media and results in sedimentary compaction as the organism forces a passage leaving behind an open burrow. Such burrows will eventually be passively filled by particle advection from above or by active filling by the organism. Excavation also occurs in compacted sediment and consists of loosening material ahead and transfering it out of the developing burrow. Finally, in backfilling the organism loosens the forward particles and transfers them either internally or externally to the rear during progression through the sediment. Although this type of categorisation is a useful analysis from a geological standpoint its mechanistic basis does not distinguish between the many behavioural variations found in benthic infauna, which frequently combine two or more of these processes. Infaunal organisms living below the interface generally construct permanent or semi-permanent tubes or burrows which may penetrate many centimetres both vertically and horizontally. Their degree of motility within such structures is dictated by their feeding strategy and need for ventilatory activity. Tube dwellers are generally the least motile, having movement confined to tube extension with growth and general house-keeping activities. However, many tube dwellers (e.g. some terebellomorph polychaetes), under pressure from predators or adverse conditions, may leave 243

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their tubes and relocate. The activity of burrowing organisms varies from the maintenance of permanent burrows, which may include complex arrays of galleries and chambers extending over a metre both horizontally and vertically in the case of callianassid decapods (Atkinson & Nash 1990, Zeibis et al. 1996), to the simple single shafts of many small polychaetes and molluscs. In contrast, many active vermiform carnivores may move freely through the sediments in search of prey (e.g. priapulids and nemerteans). Sedimentary mixing as a result of withinsediment activity (bioturbation) is one of the most important functions of the benthos (see pp. 244–248). Another aspect of motility in benthic organisms is seen in the need for predator avoidance. For organisms feeding in the benthic boundary layer the sediment is a refuge from epifaunal and demersal predators. Withdrawal into burrows and tubes at the approach of a predator is a reaction common to many surface deposit feeders and suspensivores, including many polychaetes. Moreover, small epifaunal crustaceans (e.g. amphipods, copepods, cumaceans), which feed in the boundary layer, burrow rapidly into the sediment to escape danger. Such surface activity has a strong bioturbatory effect on the upper sedimentary layer (Myers 1977a) and organsisms performing such activities have been termed sedimentary stirrers (Bromley 1996).

Sedimentary bioturbation One consequence of faunal motility is sedimentary bioturbation. Because of their importance to sedimentary biogeochemistry the bioturbatory actions of different benthic organisms have been the subject of increasing investigation. Differing types of activity disturb the sedimentary fabric at various depths. Thus the upper layers of the sediment are stirred, dug, ploughed or bulldozed by many organisms of various sizes in search of prey or detrital food particles. A useful summary of the physical disturbance to sedimentary fabric brought about by the actions of benthic organisms is given by Hall (1994). At one extreme, grey whales can turn over enormous quantities of sediment in Arctic seas in obtaining amphipod prey (Nerini & Oliver 1983, Feder et al. 1994). On the other hand, at the interface many small motile crustaceans, molluscs and echinoderms (e.g. isopods, amphipods, gastropods, ophiuroids) disturb and displace sediment by foraging or avoidance activities (cf. Myers 1977a: 620). Various types of pit diggers, including small fishes and crabs, and mound builders such as callianassid shrimps, echiurians and terebellid polychaetes translocate and deposit large quantities of subsurface material at the interface, (cf. Hughes et al. 1996, Zeibis et al. 1996). Such organisms have a strong influence on the small-scale topography of the sediment surface and thus on the boundary layer current regime. Most infaunal organisms inhabit the unconsolidated aerobic layer immediately below the interface. These include many tube and permanent burrow building organisms varying from static maldanid polychaetes to large decapods. Structures maintained by such animals tend to stabilise sediments. On the other hand active burrowers (e.g. scalibregmid and orbineid polychaetes, echinoids, etc.) that continually displace sediment in the course of their activities have a destabilising effect (Myers 1977a). It has been postulated that the activities of motile subsurface deposit feeders may inhibit or prevent the establishment of immotile suspension feeders, a process termed Trophic Group Amensalism (Rhoads & Young 1970). Some evidence of this effect on small suspension-feeding bivalves has been noted (Myers 1977b) but such biogenic disturbance appears to be only one of a range of sedimentary disturbance mechanisms that influence infaunal distributions. Thus Wildish (1977) suggested that 244

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Table 2 A classification of infaunal bioturbatory activity on a scale from 0 (no bioturbatory effect) to 4 (large bioturbatory effect) (from Swift 1993).

differential food supply controlled by turbulent mixing was the most important factor influencing the composition of benthic communities. Because detrital food resources are first available at the sediment/water interface, the lower consolidated anaerobic sedimentary layers are exploited by fewer species. Inhabitants of these layers must necessarily maintain contact with the overlying water at least for respiratory purposes and many may also be adapted to survival in sulphidic conditions. They maintain, therefore, extensive tube or burrow systems that traverse the unconsolidated upper sedimentary layers. Most such species irrigate these systems on a regular basis (cf. Myers 1977a, Kudenov 1978, Marinelli 1992, Fuller 1994), thus stimulating sedimentary oxidation and pore water flux (Kristensen & Blackburn 1987, Boudreau & Marinelli 1994, Rysgard et al. 1995). The various activities of organisms in the sediments have been summarised by Swift (1993) into a classification of bioturbatory activity (Table 2). This classification defines different activities associated with motility, feeding and burrowing in the sediments. Each activity is given a score ranging from 0–4 based on an estimate of its bioturbatory potential. This scheme allows comparison of the total bioturbatory potential of differing associations of organisms by summing the individual scores for each type of activity. Four differing types of motility are identified ranging from sedentary to freely motile within a permanent burrow system. Feeding types range from carnivores or filter feeders with no bioturbatory effects, to animals that feed at depth and egest material at the sediment surface. The latter include some maldanid polychaetes that were termed “conveyer belt” feeders by Rhoads & Young (1970) because of their continuous transference of sediment from feeding voids in the deeper layers to the surface. The next most bioturbatory action was deemed to be undertaken by organisms using the reverse process of feeding at the surface and egesting at 245

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depth typified by some other maldanid and spionid polychaetes. The two other defined types of feeding activity were ingestion and egestion of participate material at the sediment surface and ingestion and egestion beneath the surface. The former are typified by, for example, small surface deposit-feeding opisthobranchs and amphipods and the latter by orbiniid polychaetes. Five types of burrowing activity are listed from non-burrowing epifaunal activity to the construction of extensive deep burrow systems that result in net sediment transport to the surface by, for example, callianassid shrimps. Intermediate categories include pit digging and displacement burrowing with and without net particle transport. Dauwe et al. (1998) took a different approach to the analysis of bioturbatory activity. In a comparative assessment of community structure at four North Sea sites, with differing hydrodynamic regimes and sedimentary carbon inputs, four categories of bioturbatory activity were defined among the macrofauna present. These were: 1) Diffusive mixing. Vertical bioturbation as a diffusive transport process resulting from the activities of, e.g. free-living polychaetes, subsurface deposit feeders and carnivores and burrow excavating crustaceans. 2) Surface deposition. The defecation (egestion) of particles at the sediment surface undertaken by, e.g. filter and surface deposit-feeding tubiculous polychaetes and sedentary bivalves 3) Conveyor belt transport. The translocation of sediment from depth within the sediment to the surface during subsurface deposit-feeding or burrow evacuation. The gravitationally-forced downward movement of particles follows such a process. 4) Reverse conveyor belt transport. The subduction of particles from the surface to some depth by feeding or defecation. A diagenetic model was used to predict the potential effect of bioturbation on the distribution of food in the sediments at each study site. The model suggested that for a given bioturbation coefficient the total mineralisation at depth was optimal when the detrital input was of intermediate quality but when input quality was high it was not possible for bioturbation to redistribute detritus deeply. It was found that the proportions of the various bioturbation categories at each of the sites were related to the quantity and quality of the organic carbon available at each site in agreement with the model predictions. Thus, in areas where the sediments contained intermediate to low quality organic matter subsurface deposit feeders, penetrating deep into the sediment and causing most of the diffusive mixing, predominated. In areas with abundant high-quality organic matter available the fauna was dominated by near-surface feeders producing copious biodeposits. A summary of the results of this study is given in Figure 5. The prevalence and importance of the rapid subduction of high-quality detrital carbon from the surface to depth in the sediments has been highlighted by Levin et al. (1997, 1999). A number of polychaete groups, including maldanids, paraonids and lumbrinerids that feed at depth in the sediments were shown to have ingested freshly deposited phytodetrital material. Tube-dwelling maldanids that normally feed head-down in the sediments were found to subduct fresh surface detritus into feeding voids at the base of their tubes. It is suggested that such material translocated by large-bodied polychaetes provides a resource at depth for an association of smaller infaunal species including cossurids, oligochaetes and paraonids. The rapid transference of surface detrital material to deeper levels has also been described for sipunculids (Graf 1992) and arenicolids (Hylleberg 1975). This phenomenon has been associated with the seasonally pulsed nature of phytoplanktonic detrital inputs to the benthos in shelf and slope areas. Thus, the ability to cache at depth surface material, obtained during high detrital input episodes linked to 246

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Figure 5 A comparison of the relationship between diffusive bioturbatory activity and the quality of detrital input to the sediments at four stations in the North Sea with differing hydrodynamic and sedimentary regimes. The highest levels of bioturbation were seen at the stations with intermediate levels of detrital quality. See text for further explanation. Based on Dauwe et al. 1998.

seasonal blooms in the overlying waters, is suggested as a successful strategy for benthic survival (Jumars et al. 1990, Levin et al. 1997). It is possible that this type of feeding behaviour might be frequent in organisms that adopt a head-down feeding posture and are normally thought of as conveyer belt bioturbators (i.e. moving particles from depth to the surface). Those that are involved additionally in periodic active subduction of particulate material must be considered as even more significant contributors to overall bioturbatory patterns in the sediments. However, there is evidence that some head-down feeders rely on the dissolved and particulate carbon derived from anaerobic diagenesis in the deeper sediment layers rather than on subducted material. Clough & Lopez (1993) studied the 247

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carbon sources utilised by the capitellid polychaete Heteromastus filiformis, which feeds head-down in the anoxic layers as much as 15cm below the sediment surface. They suggest that it was dependent on the breakdown products of refactory carbon in those layers that were unavailable to most other aerobic organisms that lacked the ability to feed in the sulphidic environment while maintaining contact with oxygenated overlying waters. A number of other capitellid species are head-down feeders characteristic of carbon enriched and sulphidic sediments (e.g. Capitella spp. and Mediomastus spp.) (Pearson & Rosenberg 1978, Pearson et al. 1983).

Adaptive behaviour in the benthic boundary layer The complexity of conditions in the interface between sediment and water column has been briefly described above, where it was pointed out that within the benthic boundary layers bed flow, bed topography and sedimentation rates are the most important formative influences on inhabitants. Within this area fauna may take particles from either the water column or the sediment surface or may be active or passive predators. However, one of the most common attributes of organisms in this habitat is facultative adaptation to the often rapid and frequent changes in bed flow and sedimentation rates which commonly occur in the boundary layers. A number of studies have shown that switching from suspension feeding to deposit feeding in response to changing flow or depositional rates is a strategy common to many interface organisms (Snelgrove & Butman 1994 and references therein). Miller et al. (1992) and Bock & Miller (1996) studied variations in the feeding behaviour of a range of organisms in response to varying flow regimes and sediment fluxes. Oscillatory flows induced by wave motion are often the characteristic flow regimes in shallow waters and have been shown to be influential in structuring benthic communities along depth gradients in immediately subtidal areas (Oliver et al. 1979). In experiments involving 17 species from several feeding guilds Miller et al. (1992) observed behavioural responses to oscillatory flows of varying strength. The overall results are summarised in Figure 4 (see p. 240). In general, animals reacted very rapidly to changes in the flow regime at low velocities. Increased flows tended to prompt a switch from deposit feeding to suspension feeding in a number of species. The changes in feeding behaviour in response to a change from still water to low flows generally involved a change in the position or rate of movement of the particle collecting apparatus. Thus, organisms with long, thin palps (e.g. spionid and spiochaetopterid polychaetes), use them to pick particles from the sediment surface at times of still water. As current speeds increase they coil them helically to capture particles from the near bed flow and can rotate them to feed effectively in both halves of the wave cycle. On the other hand the long flacid tentacles of terebellid poychaetes are restricted and thus prevented from feeding as bed flows increase to critical velocities resulting in particle resuspension. Similarly, siphonate feeding by bivalve mollucs was found to be restricted at moderate to high flow levels, as was the ability of surface deposit feeders with short palps or muscular tentacles such as ampharetid polychaetes. Obligate suspension feeders with stiff crowns of tentacles, such as serpulid polychaetes, can extend their crowns even in strong flows but at the expense of considerable distortion, which may seriously reduce their feeding efficiency. Antennal suspensivores, including amphipods, decapods and cirripedes, can continue to feed at high flow rates. In general, for obligate and facultative suspension feeders it was found that flows more 248

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energetic than those needed to move sediment did not alter the feeding mode but affected the apparent success rate of particle capture and the time spent feeding. A sedentary omnivorous polychaete ceased taking particles in high flows. Similarly, a motile scavenging gastropod stopped feeding in high flows but a motile scavenging hermit crab was unaffected. No response to changing flow rates was shown by a predatory sea star. Bock & Miller (1996) studied the response of two pairs of polychaete species with differing trophic behaviour patterns to the interactive effects of fluid flow, bed characteristics and suspended load. Two species of obligate deposit feeders were found to show little systematic response to flow and bed differences, although one did vary the time spent deposit feeding when fine material was deposited at low flow levels. As flow and suspended particle concentrations were increased, two palp-coiling facultative suspension feeders increased the time spent feeding. The time spent suspension feeding was also increased in decreasing flows when fine and/or high quality material was available. Miller and his co-workers make a distinction between suspensivores feeding in the wave boundary layer (equivalent to the benthic boundary layer in Fig. 1, see p. 235), where turbidity through resuspension occurs, and those feeding above that boundary layer in the outer flow. They note, however, that coiled palp suspensivory is effective at both levels. A number of workers have distinguished between groups of filter feeders on the basis of the height above the sediment surface at which particles are collected. Turpaeva (1957) in a general assessment of trophic relationships in marine benthic biocoenoses contrasted “filterers-A”, which took particles from the lowest bottom layer of water with “filterers-B”, which exploited the higher bottom layers. This distinction is similar to that made by Wildish (1985) between bed-load transport feeders and other suspension feeders (see p. 241). Another way,of classifying suspension feeders is to differentiate between passive and active modes of particle capture. The former are also termed impingement feeders (Wildish 1985). Josefson & Conley (1997) suggested that large populations of a passive suspensionfeeding brittle star found beneath frontal areas in the Kattegat were supported by the vertical sedimentation of rich supplies of algal detritus in that area. In general, passive suspension feeders predominate in quiescent areas whereas active feeders are more numerous in areas with strong current flows. Many of the latter are also capable of feeding successfully in still waters, so that this ecological distinction is not clear cut. However, Josefson (1998) emphasised the importance of considering the particle vector in any comparison of suspension-feeding behaviour. He suggested that at low current velocities detrital particles moved downwards, which favoured passive suspension feeding. At intermediate velocities particles moved laterally favouring active suspension feeding, whereas at high current speeds particles were resuspended and suspension feeders became inactive. The studies of Miller et al. (1992) favour this hypothesis at least for tentaculate and some siphonal suspension feeders but some impingement feeders, such as sponges, and active feeders, such as cirripedes, can feed at high current speeds.

Biodeposition and resuspension The net affect of biodeposition and resuspension is another functional aspect of benthic activity that interfaces with both bioturbation and sedimentation and is focused on the benthic boundary layer. Graf & Rosenberg (1997) have reviewed this topic in some detail and 249

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emphasise the distinction between direct and indirect effects. Graf (1999) characterised organisms that modified the topography of the surface-sediments as benthic engineers. In order to establish and maintain their presence at the sediment/water interface many organisms build and maintain structures in the interface zone that modify the topography and thus the hydrodynamics of the boundary layers. Indirect effects stemming from various forms of such topographic modification include tube and mound building, burrow digging and pit excavation. A simple pit dug in the sediment will collect particles. Yager et al. (1993) showed experimentally that particle flux into pits from the main lateral flow across the mouth increased with both increasing aspect ratio and roughness, thus increasing food supply to pit inhabitants. Such pits are dug by many surface dwelling organisms. Burrows may be regarded as pits with a particularly high aspect ratio and many burrows have cone shaped entrances that serve the same purpose, e.g. those of arenicolid and some maldanid polychaetes (Cadée 1976, Kudenov 1978). Mound building has also been shown to have indirect effects on the deposition and burial of particulates by altering the flow regime in the turbidity layer (Huettel et al. 1996). Similarly, the projection of tubes above the sediment surface interrupts flow and may enhance particle settlement, particularly when tube mats or lawns are formed (Graf 1999). The direct effects of biodeposition and biologically driven resuspension are important both in physically structuring the benthic boundary layer and in controlling the flux of particulates and solutes across it. The production of faeces and pseudofaeces by benthic organisms re-packages particles ingested from either the water column or sediments into pellets that are frequently redeposited at the sediment surface. Such depositions alter both the physical and chemical characteristics of the sediment/water interface and thus the functional responses of both the depositers and other associated organisms. Faecal mounds, produced by, for example, arenicolid polychaetes, can both bury adjacent species and provide a feeding substratum for others (Hall 1994). Deep-burrowing thalassinidean shrimps can eject up to 12 g dry matter ind.-1 d-1 (Hughes & Atkinson 1997). Conversely, biodeposition of faeces and pseudofaeces from mussel beds can reach 70 g C m-2 d-1 (Muschenheim & Newell 1992). Graf (1999) has suggested that particle deposition and resuspension driven by physical processes can be enhanced by a factor of from 2 to 10 by biological activity.

Other benthic faunal functions possibly suitable for characterising functional groups Reproductive strategy differs widely in marine benthic invertebrates. Three basic larval modes of development are found, planktotrophic, lecithotrophic and direct with brood protection. Planktonic larvae once released spend a variable amount of time feeding in the plankton before finally settling to the bottom and thus attain broadcast dispersal. Lecithotrophic larvae are free living, but carry yolk sacs that limit their dispersal abilities. Larvae under brood protection are released as juveniles in the vicinity of their parents. Each mode has differing ecological implications for the ultimate distribution and success of the eventual adult populations. Thus, the variation in larval strategy could be a basis for a comparative functional classification of community structure. However, Strathmann (1985) has suggested that the possession of a feeding larval strategy may be a chance evolutionary consequence rather than confer any real ecological advantage. Brooding is associated in many taxa with small adult size possibly to facilitate adequate ventilation of all young, 250

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implying that the development of a large adult size might necessitate a free-feeding larval stage. Although such arguments tend to be circular, it does suggest that variation in larval strategy might not be of fundamental importance to the structure of adult benthic communities. Moreover, in a recent review on the relative importance of recruitment limitation to the development of soft-sediment populations and communities, Olafsson et al. (1994) conclude that post-larval settlement processes have a much more critical influence on benthic community structure than any variability in larval recruitment levels. It is probable, therefore, that larval mode does not play a major role in structuring adult sedimentary communities.

Multifunctional groups A number of studies of the functional response of benthic populations and communities to environmental change have made use of multifunctional rather than monofunctional groups. By combining a number of differing functional attributes to create a group of organisms that respond in a similar way to environmental challenges, the basis for reliably comparing common responses is broadened. The first to utilise such an approach consistently were Fauchald & Jumars (1979) in their study of polychaete feeding guilds, discussed above. These authors combined the functions of feeding source and method of acquisition with motility mode to define a range of feeding guilds. Comparison of the distribution of these guilds among polychaete families provided some novel insights into the evolutionary development of polychaetes and their ecological role. The Fauchald-Jumars feeding guild approach was adapted to other phyla than polychaetes by Pearson & Rosenberg (1987) to compare and contrast the benthic community structure down a depth gradient in the Irish Sea in relation to changing food availability. This study demonstrated that along a gradient of increasing depth, as both depth and current speed decline and hard substrata grade into increasingly fine sediments, the predominant trophic modes change (Fig. 6). On coarse shallow subtidal surfaces passive suspension feeders partition feeding space vertically, using hard substratum as an anchor for various complex filtering mechanisms. Sedimentary substrata begin to predominate as current speeds decline with increasing depth. In shallower areas these substrata are dominated by active suspension feeders, using various types of pumping or straining mechanisms to capture particles. These organisms may combine suspension feeding with surface deposit feeding and may be motile or semi-motile to take advantage of the frequently variable flow rates in shallow coastal areas. With increasing depth these are replaced by obligate surface and subsurface deposit feeders which are generally semi-motile or sessile and partition food and space resources through a variety of tube-building and burrowing habits. The predominance of subsurface deposit feeders increases and degree of motility decreases with increasing depth and decreasing particle size. This reflects the development of larger and more complex food gathering mechanisms, often requiring a larger adult body size, as food availability declines. At some point, often corresponding to the shelf-slope break, this trend is reversed when increasing scarcity of food re-emphasises the advantages of motility in allowing access to scarce resources. Herbivorous grazers are mostly confined to the euphotic zone but some may occur in areas where macroalgal detritus accumulates. Infaunal carnivores constitute 10–20% of the populations throughout the gradient whereas motile epifaunal predators are most abundant in 251

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Figure 6 The distribution of functional groups in boreal coastal communities along a gradient of decreasing food availability and water movement with increasing depth and sedimentation. Key to the functional groups: Trophic group: H, herbivore; F, suspension feeder; S, surface deposit feeder; B, burrowing deposit feeder; C, carnivore. Motility group: M, motile; D, semi-motile; S, sessile. Feeding mechanism: J, jawed; C, ciliary mechanism; T, tentaculate; X, other types. The line width representing each functional group along the gradient is proportional to its percentage abundance in the community at any one point. A schematic representation of the feeding positon of taxa typical of the various groups relative to the sediment/water interface along the gradient is included. Key to taxa: (a) macroalgae, e.g. Laminaria; (b) echinoids, Echinus (HMJ); (c) limpets, Patella (HDJ); (d) barnacles, Balanus (FSX); (e) (f) epifaunal polychaetes, Pomatoceros (FST), Sabella (FSX); (g) epifaunal bivalves, e.g. Mytilus (FSC); (h) infaunal brittle stars, Ophiothrix (FMC); (i) (j) (k) (l) infaunal bivalves, Chamelea (FSX), Mya (FSC), Cerastoderma (FDC), Angulus (FDT); (m) epifaunal gastropods, Turritella (SMX); (n) tube worms, Lanice (SST); (o) infaunal bivalves, e.g. Abra (SDC); (p) infaunal polychaetes, Spio (SST); (r) infaunal brittle stars, Amphiura (FDT); (s) infaunal echinoids, Echinocardium (BMX), (t) (u) (v) infaunal polychaetes, Ampharete (SST), Maldane (BMX), Glycera (CDJ); (w) infaunal bivalves, Thyasira (BDX); (x) infaunal brittle stars, Amphiura (SDT).

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the shallow areas. Semi-motile or territorial epifaunal predators predominate in the deeper areas. It is suggested that this type of analysis, although based on broad functional categories, imparts a recognisable structure to the observed community changes along the environmental depth gradient and that similar functional patterns might be expected along depth gradients elsewhere. Bonsdorff & Pearson (1999) applied the Fauchald-Jumars feeding guild concept to a study of changing benthic community structure along a latitudinal gradient through the Baltic Sea. They note that the Baltic system and its approaches represent one of the strongest and best documented natural gradients in salinity and seasonal temperatures available, and is also strongly influenced by hypertrophication in shallower areas and by hypoxia at deeper levels. Twenty-three functional groups were recognised (Table 3), forming a cline from complex functional communities in the fully marine areas of the Baltic approaches in the south and west, to functionally poor assemblages in the inner areas of the north and east. Along this gradient, species numbers were significantly related to the salinity values and Table 3 Baltic Sea macrozoobenthic functional groups (from Bonsdorff & Pearson 1999). Trophic group: F, suspension feeder; S, surface detritivore; B, burrowing detritivore; C, carnivore; P, parasite; H, herbivore. Motility group: M, motile; D, semi-motile; S, sessile. Food acquisition: J, jawed; T, tentaculate; X, other mechanism.

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Table 4 The changing distribution of functional groups in the benthos along a South-North transect through the Baltic Sea. Functional group designations as in Table 3. (Bonsdorff & Pearson 1999)

biomass levels to the primary production levels. The overall density of animals in the sediments was highest in the aerobic sediments present at either end of the gradient and consistently low in the deep central areas subject to hypoxia. The total number of functional groups found at each station integrated the effects of these various environmental pressures, resulting in a continuous diminution of functional complexity along the latitudinal transect. Thus 20 different functional groups recorded from the Kattegat-Skagerrak area were progressively reduced to four in the Gulf of Bothnia (Table 4). The most notable functional changes along the gradient were the rapid elimination of burrowing detritivores and sessile organisms of all kinds. This effect resulted in an increase in the importance of motile surfacefeeding suspensivores and detritivores. Another important aspect was the disappearance of organisms with tentacular feeding methods towards the inner parts of the system. No definitive reasons were found to explain these critical changes in functional attributes. Although the strong salinity gradient puts an obvious limitation on the penetration of stenohaline species, this limitation should not inhibit colonisation by euryhaline burrowing and/or tentaculate 254

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organisms. It is suggested that oscillations in salinity and hypoxia on the slopes of the deep basins and in shallower inner areas, would strongly favour motile organisms that could migrate actively away from adverse conditions and return rapidly to exploit newly deposited resources when conditions improve. However, not all tentaculate and burrowing organisms are slow moving or sessile. The overall pattern in the gradual decline in functional groups, from the fully marine western coastal areas to the brackish inner Baltic, is a gradual decrease in specialists and a relative increase in opportunistic generalists. Only a few common species are found across the entire gradient (Rumohr et al. 1996), making it difficult to compare communities in the various areas directly. Thus, in this case the use of functional properties of the biota for comparative purposes led to new insights into the ecology of the system and provided an overview of the key parameters of interest. Olenin (1997) took a somewhat different and broader approach in using multifunctional groups for a comparative analysis of the vertical distribution of benthic macrofauna in the Eastern Gotland Basin of the Baltic. The fauna in different depth zones was characterised on the basis of feeding, motility and habitat type, together with an evaluation of sediment modifying ability. Thus seven trophic groups, three motility groups, three habitat types and eight sediment modifying functions were defined (Table 5). Each sediment modifying action was scored as having either high, low or no importance and the total scores for

Table 5 Attributes used to characterise the benthic fauna of the East Gotland Basin in the Baltic (Olenin 1997).

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species allotted to each trophic-motility-habitat group were used to characterise the bioturbation potential in vertical zones, defined on the basis of hydrodynamic and sedimentary characteristics. This characterisation showed that the sublittoral zone, extending down to 25 m with coarse sediments of boulders, gravel and sand, had the greatest range of bioturbatory activity. All eight sediment modifying functions were of major significance in that area. In the eulittoral zone, extending from 25 m to 80 m, no biodepositing or particle-trapping animals were found but the other six sediment modifying activities were represented. Below this area a transitional zone between 80m and 120m was defined above the stagnant and hypoxic lower levels, where no macrofauna were present. In the transitional zone only burrowing, fluid transport and deposit-feeding activities were represented in the fauna. The boundaries of the lower two zones fluctuate in response to irregular basinal water renewal, thus the transitional zone is subject to intermittent extinction and recolonisation. It was concluded that an understanding of both benthic faunal distributions and their biogeochemical consequences are essential to an understanding of this dynamic brackish water system. The work of Dauwe et al. (1998) has been discussed above (p. 246) but is also apposite as an application of multifunctional analysis. These authors categorised the fauna by a combination of trophic status and bioturbation activity. Five feeding groups were defined, including suspension feeders, interface feeders (capable of alternating suspension and deposit feeding), surface deposit feeders, subsurface deposit feeders and carnivores and/ or omnivores. Four bioturbation categories were recognised as described above (p. 246). The approach was successful in relating community structure in four areas receiving different levels and qualities of detrital input to biodiffusive mixing levels predicted by a simple diagenetic model. This work underlines the need, expressed by Olenin (1997), for combining biogeochemical and faunal studies to improve our understanding of sedimentary ecosystems. A recent study (Gutiérrez et al. 2000) has used the functional categories defined by Dauwe et al. (1998) to assess the changing bioturbatory potential of the benthic fauna in response to varying degrees of hypoxia in an upwelling area of the central Chilean coast. This study showed that higher bottom water oxygen levels and a lower quality of detrital input provided better conditions for strongly bioturbating subsurface deposit feeders, whereas low oxygen levels and high quality organic inputs favoured the dominance of tube-dwelling, surface biodepositing species with a weak bioturbation potential, i.e. a result similar to that from the North Sea comparison.

The utility of functional groups This selective overview of the use of functional groups in marine soft-sediment benthic ecology has demonstrated that the approach has some real advantages in exploring and elucidating animal-sediment interactions and in particular in comparing and quantifying faunal response along differing environmental gradients. Indeed, the comment made by Begon et al. (1996), is worth repeating. They suggested that a study of the collective response of such groups to environmental change could be indicative of particular trends in the response of biota that might be included in the reaction of the community as a whole and yet be of more general importance than the responses of populations of individual taxa. 256

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However, some cogent criticisms made in the past (Posey 1990, Snelgrove & Butman 1994) need to be addressed. The most powerful of these criticisms revolve around problems with the relative inclusiveness of the groups being described and the inevitability of functional overlap between some of the modes being defined. Switching between trophic modes for instance is well known. As noted above many interface organisms take particles from the water column or sediment surface according to the flow conditions. Another apposite example is the omnivorous burrowing polychaete Hediste (=Nereis) diversicolor, which is an active predator, a deposit feeder and a secondary suspensivore through mucus net trapping (Esnault et al. 1990). Such trophic plasticity may well be much more common than thought hitherto and emphasises that confidence about functional group attributions must be dependent on an accurate knowledge of species behaviour. The basis for the inclusion of a species into a functional group must be a clearly defined similarity in the shared attribute. This presupposes an unambiguous definition of that particular function. Considerable progress has been made in the study of the behaviour and life histories of benthic organisms in the past few years. It is now possible to make more appropriate functional attributions for many individual species and groups of species, on the basis of observational studies, than was previously possible. However, there is a strong case for breaking down some of the broader categories of, for example, trophic group or bioturbational activity into smaller units more closely related to environmental forcing factors. This approach has been taken by Miller et al. (1992) in their analysis of the response of a range of organisms to changing shear velocities in oscillatory flows, discussed above. Their careful experimental work demonstrated and defined a range of differing suspensivorous and detritivorous responses to changing flow rates, thus allowing a more rigorous redefinition of feeding habits in the interface zone. A more detailed characterisation of detritivores based on accurate knowledge of feeding and motility within the sediments has yet to be made. However, the recent increase in knowledge of bioturbatory activity, in particular the observations on subduction discussed above, have resulted in a better understanding of some marked functional distinctions between detritivores. It has been noted that Dauwe et al. (1998) and Gutiérrez et al. (2000) used four bioturbation categories: (a) conveyer belt feeders that transfer particles from depth to the surface, (b) diffusive bioturbators that transfer particles locally and non-directionally, (c) reverse conveyor belt feeders that move particles from the surface to depth in the sediments and (d) surface defaecators that ingest and egest particles at the surface. These categories are defined in terms of particle transport processes and make a useful distinction between near-surface feeders causing mainly biodeposition through surface deposition and diffusive mixing and subsurface deposit feeders that penetrate deep into the sediment and cause much of the vertical mixing through conveyor belt and reverse conveyor belt transport. These distinctions, however, remain very general. Each category includes a variety of different types of physical activity by the fauna. Also, by concentrating on particle transfer they ignore some other important aspects of bioturbation such as temporary particle displacement, irrigation and fluidisation. Entire groups of benthic organisms influence bioturbation by these types of action that do not involve any net movement of particles. An alternative way of classifying bioturbatory activity in the sediments is to list the various habits of the fauna that relate to modification of the sediments. Thus, the following activities can be said to result in either particle transfer, particle displacement, irrigation or fluidisation within the sediments or at the sediment/water interface: ploughing, pit digging, mound building, burrowing, tube-building, subducting, benthic gardening, creating feeding 257

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voids, surface defaecating and subsurface defaecating. Some organisms do more than one of these, but each activity has a different modifying influence on the sediments. Ploughing is a sediment displacement activity that, by the definition of Dauwe et al. (1998), would fall into the diffusive mixing category of bioturbation. Typical benthic groups with this type of activity include pectinarian polychaetes, small surface detritivore molluscs, such as hydrobid gastropods and philinid opsithbranchs, echinoids, such as Echinocardium, and many isopod and amphipod crustaceans. Pit digging is also a sediment displacement activity in the diffusive mixing category. As mentioned above there is a wide size range in both digging organisms and in the pits dug. Pit digging is frequently associated with the active or passive subduction of particles trapped by the hydrodynamic properties of such sedimentary depressions. The larger foraging predators such as crabs and fishes create large feeding depressions that may then be occupied by a variety of smaller organisms for either refuge or feeding. Mounds are built by a number of differing activities. Large burrowing decapod crustaceans (e.g. callianassid shrimps, and burrowing fishes, such as Cepola rubescens (Atkinson & Pullin 1996)) create mounds from the ejecta mined in the course of their extensive burrowing activities, whereas some burrow dwelling organisms collect surface particles extensively from around the burrow opening by means of long tentacles (e.g. terebellid polychaetes), or by a proposcis in the case of the large echiurian Maxmuelleria lankesteri (Hughes et al. 1996). Non-edible material accumulates around the burrow opening of such organisms, frequently resulting in the build-up of extensive mounds. Many sessile tube-dwelling and burrowing organisms eject their excreta at the sediment surface and may create extensive faecal mounds around the burrow and/or tube openings. The most well known example of this latter activity is the lugworm, Arenicola marina, cf. Cadée (1976). There are many different types of burrowing activity ranging from active passage through sediments by particle displacement to the formation of permanent burrows. Almost all vermiform benthos secrete mucus to ease their passage through the sedimentary fabric. If a permanent or semi-permanent burrow is formed this movement is slow and a large amount of mucus is secreted, which consolidates the burrow walls, maintaining its structure for a time. In this latter case the occupant will remain within the burrow for extensive lengths of time and irrigate it periodically to maintain aerobic conditions. Examples of this type of burrowing habit include predatory glycerid polychaetes and nemerteans. Active vermiform burrowers such as scalibregmid and orbiniid polychaetes and some holothurians make relatively ephemeral burrow structures but produce large amounts of faecal pellets that are deposited at the interface. They thus act as conveyor belt bioturbators, a category that also includes many tube-building organisms. The extensive mining activities of decapods and fishes have been mentioned above. These organisms can excavate extensive burrow systems that may penetrate up to a metre into the sediments (Nash et al. 1984, Atkinson & Taylor 1991, Nickell et al. 1995, Rosenberg et al. 2000). Other significant burrowing bioturbators include amphiurid echinoderms and many bivalve molluscs and fishes. Tubiculous infaunas have generally similar lifestyles to the permanent burrow makers. Tubes may be secreted or constructed from sedimentary material. In most cases they are permanently inhabited and ventilated through one or more openings at the surface. The process of irrigating tubes and burrows is critical in sedimentary biogeochemistry. In introducing oxygen to sub-interface sedimentary levels it sustains aerobic carbon mineralisation in addition to allowing the organism to respire in what would otherwise be sulphidic conditions. Some tube dwellers are conveyer belt feeders and many of these create 258

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feeding voids within the sediments (Rhoads & Germano 1982), an important aspect of infaunal bioturbation. Some maldanid and capitellid polychaetes typify these tube dwellers. Others are reverse conveyer belt feeders subducting surface material and defaecating at depth. Some maldanid and spionid polychaetes and thyasirid bivalves are included in this category. The utility of these distinctions between groups of sedimentary detritivores, based on sedimentary modifying behaviour, has been tested by comparing changes in their comparative abundance along a eutrophic gradient of increasing inputs of organic carbon to the sediments. The comparison is based on benthic macrofaunal data from a transect of stations across an accumulating sewage sludge disposal ground in the Firth of Clyde (Pearson et al. 1983, Pearson 1987). One end of the gradient lay in undisturbed sediments and the other in the centre of the disposal ground subject to extreme levels of organic enrichment. Carbon levels in the sediment increased progressively towards the centre along this gradient, while sediment grain size and pore water oxygen levels decreased. Figure 7 summarises the changing distributions of the functional groups based on sediment modifying activity along this gradient. Two additional functional groups, not directly based on sediment modifying activity, have been included in the comparison. These are predators, illustrating a trophic group that is not influenced by the changing sedimentary conditions and thiobiotic grazers that are confined to the sulphidic sediments found only at the highly enriched end of the gradient. The figure illustrates that only one bioturbatory group, the surface defaecators, is equally represented throughout the gradient. Ploughing, burrowing and tube-building organisms appear in similar numbers in all but the most enriched areas, where their abundance is reduced. Abundance of tube builders is also somewhat lower in the central part of the gradient. Mound builders and subductors are the groups whose populations decline first along the gradient, followed in turn by pit diggers, subsurface defaecators and feeding void creators. This preliminary analysis suggests that there is some value in using sediment modifying behaviour as the basis for functional group comparisons of community changes along eutrophic gradients. The studies of Dauwe et al. (1998) and Guttiérrez et al. (2000) have demonstrated the value of combining an assessment of trophic groups with bioturbatory action in comparative assessments of community response to different levels of detrital input and quality.

The relationship between bioturbatory activity and the productivity of benthic infauna Rosenberg (1995) and Rosenberg et al. (2000) have related community structure and faunal abundance in the northern Skagerrak at different depths to changing levels of detrital material. They showed that the benthos on the slopes and bottom of deep trenches had higher abundance and biomass than those in adjacent shallower areas. This difference was attributed to the down slope transport of organic particles. Sediment profile imaging (SPI) was used to assess the depth distribution of fauna in the sediments. This technique showed that the burrowing crustaceans Calocaris macandreae and Maera loveni created extensive galleries and feeding voids to depths in excess of 20 cm. The most numerous macrofaunal animals present were the head-down polychaete conveyer belt feeders Maldane sarsi and Heteromastus filiformis and the burrowing ophiuroid reverse conveyor belt feeder Amphiura filiformis, suggesting that considerable resources of detrital food 259

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Figure 7 The distribution along an organic enrichment gradient of functional groups based on bioturbatory activity. The width of each bar represents the relative abundance of each group at any point on the gradient.

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were available at depth in the sediments on the slope and deeper areas. As residual carbon levels in the sediments were no higher in these areas than at shallower depths it was concluded that there was a balance between the input of organic material and the capacity of the organisms to assimilate it. Similar observations were made in continental slope sediments off Cape Hatteras, North Carolina in a large-scale study of the input, accumulation and cycling of sedimentary materials (Blake & Diaz 1994, Rhoads & Hecker 1994). Enhanced abundances of macrofauna were recorded in the mid-slope area at depths of between 800–1000 m, co-incidental with high rates of organic carbon sedimentation (28–121 g C m-2) fuelled by along slope advective transport of planktonic detritus. The fauna in these areas was dominated by shelf organisms commonly associated with organic enrichment (e.g. oligochaetes and scalibregmid polychaetes), rather than the deep-sea organisms found at similar depths elsewhere. Bioturbation rates in the area were shown to be consistently high and SPI revealed the presence of numerous large feeding voids (Diaz et al. 1994, DeMaster et al. 1994). The study area was found to have a high density of feeding pits and faecal mounds indicating that surface sediments were being biologically subducted and subsurface sediment pumped to the surface. This process was thought to inject live diatoms and chlorophyll a to depths of over 10 cm in the sediments. Both these studies, together with those of Dauwe et al. (1998) and Gutiérrez et al. (2000), emphasise the importance of bioturbation in maintaining detritivore productivity under relatively high carbon input levels. The inclusion of a variety of different bioturbatory activities among the members of a benthic community, particularly the activities of deep bioturbators such as the burrowing crustaceans and echinoderms, increases the depth of oxygen penetration and decreases the turn over time of the sediment column, thus maximising carbon mineralisation rates. The exclusion of some categories of bioturbator, either through increasing hypoxia or through other forms of sedimentary disturbance, leads to a decline in overall productivity. This effect suggests that in any analysis of functional groups, designed to improve our understanding of community response to changing environmental circumstances, both the type and effect of bioturbatory activity should be taken into account. The question of how many bioturbatory categories should be defined and whether these should be based on sediment modifying behaviour or on sediment transport processes, or perhaps on a combination of both, remains to be resolved.

Future development of the concept The various applications of the functional group concept to the analysis of community response to environmental change discussed above have demonstrated its utility in assessing the interaction of habitat modification and functional response. Thus, the structural changes in communities along gradients of changing depth, salinity/temperature and hypoxia/carbon enrichment have variously been examined in terms of changes in functional response. The most illuminating assessments have involved the comparison of the distribution and relative importance of multifunctional groups along these critical gradients in the benthic environment. The choice of functions to be examined is closely related to the environmental factors of greatest influence in any given region, community or habitat area. It has been demonstrated that, in the most general terms, the type and distribution of interface inhabitants is controlled by current flow and that of infaunal 261

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detritivores by the rate and quality of detrital input. However, all such factors are interdependent to some extent and faunal adaptations to any particular habitat are a response to a complex of environmental pressures. Nevertheless, functional responses to particular environmental variables can be generalised across groups to develop meaningful ecological comparisons. It is obvious, however, that such comparisons can only be made with confidence on the basis of detailed and accurate information on the behaviour, activities and interactions of the animals in the communities being studied. Myers (1977a,b) demonstrated that careful observation of the behaviour of infaunal benthos in small laboratory aquaria can reveal many details of their feeding and movement patterns. Until relatively recently such studies were rare. With the advent of technologies such as SPI, and high quality underwater video and photography, however, it is now possible to observe benthos in situ and record natural behaviour under a variety of conditions. The comparative examination and analysis of sediment profile images from field sites can reveal important details of in situ behaviour in burrowing and tube-dwelling fauna, as described by, for example, Diaz et al. (1994), Nilsson & Rosenberg (2000) and Rosenberg et al. (2000). Similarly the development of better experimental laboratory equipment (flumes, mesoand microcosms) has allowed controlled studies of community responses to particular variables or suites of variables to be made. It is essential to make greater use of such equipment and the opportunities it presents to investigate fully both community and species responses to environmental change. In this respect the following areas for future research are suggested. 1.

2.

3.

4.

5.

The development of more detailed flume experiments and observations of feeding and breeding behaviour under differing flow regimes to establish the conditions for mean or maximum feeding activity. The development of better means of observing bioturbational behaviour characteristics; including burrowing, excavating, tube-building and tube-dwelling behaviour, surface and subsurface bulldozing, pit digging, hoeing and pelletisation on and within sediments. An assessment of the role of macro- and microfaunal mats and networks, e.g. thiophilic bacterial mats, Foraminifera, etc. in the modification of macrofaunal feeding behaviour and as an additional food source. A consideration of the consequences of individual functional adaptations to, e.g. flow modifications, including methods of particle capture, transfer and loss, solute transfer, absorption, excretion and pelletisation. This should lead to detailed examination of the conditions leading to successional replacement in disturbed communities. SPI technology should be used more widely in field studies to quantify vertical distributions and assess behavioural patterns in benthic infauna.

Acknowledgements This review was initially stimulated by my attendance at two meetings, the conference on Biogeochemical Cycling and Sediment Ecology held in Hel, Poland in 1998 and the Baltic Marine Biologists Symposium in Klaipeda in 1999. Unfortunately illness prevented me from completing the texts of my presentations to those meetings in time to meet publishing 262

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deadlines. However, I am most grateful to the organising committees of both meetings, and in particular to John Gray and Sergei Olenin, for the invitations to attend. The discussions with participants materially assisted the development of my thoughts on functional group analysis and on the role of bioturbation, the themes underlying my presentations to both meetings. The ideas presented here have also been developed by many stimulating discussions over the years with my close colleagues in biology and oenophily Rutger Rosenberg, Erik Bonsdorff and Heye Rumohr. This paper is a synthesis arising from all these influences, so to all thank you, but mea culpa! I am also most grateful to the Editors for their helpful comments and patient support.

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THE IMPORTANCE OF SEAGRASS BEDS AS A HABITAT FOR FISHERY SPECIES EMMA L.JACKSON,1,2 ASHLEY A.ROWDEN,1 MARTIN J.ATTRILL,1 SIMON J.BOSSEY 2 & MALCOLM B.JONES1 1

Department of Biological Sciences, Plymouth Environmental Research Centre, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK (corresponding author M.J.Attrill) e-mail: [email protected] 2 Department of Agriculture and Fisheries, States of Jersey, Howard Davis Farm, Trinity, Jersey, Channel Islands

Abstract Seagrass beds are thought to have a fundamental role in maintaining populations of commercially exploited fish and invertebrate species by providing one or more of the following: (a) a permanent habitat, allowing completion of the full life cycle, (b) a temporary nursery area for the successful development of the juvenile stages, (c) a feeding area for various life-history stages and (d) a refuge from predation. In addition to these primary roles, seagrass beds are thought to maintain fisheries indirectly by providing organic matter that is incorporated into coastal nutrient cycles and which supports secondary production, including fisheries species. Unfortunately, these roles have been distilled from a disparate literature that often reports results using different sampling methods, seagrass species, geographical locations and temporal or spatial scales. The aims of this review are to summarise the literature assessing the importance of seagrass habitats for fishery species, to highlight possible confounding factors that may help to explain some of the contradictory statements in the literature and to identify areas of seagrass ecology that require further investigation.

Introduction The proposal by Petersen & Boysen-Jensen (1911) that beds of the coastal seagrass Zostera marina were the basis of all life in the sea was seriously undermined when the devastating effects of the 1930s seagrass wasting disease on the plant communities (see review by Rasmussen 1977) failed to produce the envisaged catastrophic collapse of fisheries. Although the fundamental links between fishery species and seagrass beds may not be as simple as that proposed by Petersen & Boysen-Jensen (1911), there are many examples of associations between fishery species and seagrass beds. These associations have supported the idea that such beds are important for fishery species (Table 1). There is some support for Petersen & Boysen-Jensen’s (1911) theory that fisheries may depend on these marine meadows and a number of reports have correlated diminishing seagrass cover to declining fish catches. Examples include the King George whiting (Sillaginodes punctatd) in Westernport Bay Victoria, Australia (Kikuchi 1974, Bell & Pollard 1989) and soft-shell blue crab (Callinectes sapidus) in Chesapeake Bay, USA (Shabmann & Capps 1985). Bell & Pollard (1989) commented that fisheries are

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Table 1 Examples of commercially exploited species that have been linked to seagrass beds.

likely to depend heavily on seagrass only where harvests are made in very enclosed estuaries and bays, where seagrass provides the only shelter and where the exploited species spawns within the bay or estuary. This comment appears to contradict the general statement that now introduces much of the current seagrass faunal literature, that seagrasses are “well known” as important habitats for many economically valuable fishes and decapods, particularly in their juvenile stages. This rather limitless declaration appears to be based on Bell & Pollard’s review (1989) which, although thorough, focused on Australian studies. The same comment of regionality may also be applied to the recent review of Connolly et al. (1999), which examines fisheries sustainability. Such general 270

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statements of seagrass importance, based on scientific studies, can often lead to inaccurate assumptions when extrapolated to, for example, different geographical locations, fishery species or seagrass species. For this review, and to avoid any confusion, some commonly used terms need to be defined. First, what constitutes a fishery species? For the purpose of this review, a fishery species is one that is either directly destined for sale, an important target for recreational fishing or captured for mariculture. Caution is needed, however, because in some cases juveniles of a particular species may utilise seagrass beds in regions where they are not exploited, only to migrate to other locations where they may be fished. Of course, other species may have an indirect importance by being, for example, the dominant prey of a more directly exploited species. Studies involving such organisms will be identified where appropriate. Second, seagrass itself is a general term and represents a group of species with a variety of leaf shapes, lengths, rhizome thickness, densities and areal coverage. Different seagrass species often have contrasting and specific environmental requirements and exhibit particular geographical distributions. While there are over 57 recorded species of seagrass, the majority of work has focused on only nine. Table 2 summarises these species, their common names, morphology and distribution (see Phillips & Meñez 1988, for more detail). This review focuses largely on the temperate/subtropical species Zostera marina but other species are also discussed and, to avoid falling into the trap of generalisation, the seagrass species involved will be identified. Although Kikuchi (1974) divided the mobile fauna of seagrass beds into four categories (permanent residents, seasonal residents, temporary visitors which forage in a wider area than the seagrass bed, and occasional migrants), the present review uses a broader division and considers the fishery species found in seagrass habitats as either permanent or temporary residents. The section dealing with temporary residents is subdivided further but on functional response rather than temporal pattern of use. In addition to examining direct links between seagrass habitats and exploited species, the indirect roles of seagrass to fishery success, such as trophic subsidy, are not neglected. Several studies have examined the relative habitat value of seagrass beds to fishery species by comparisons with other habitats, such as kelp forests (Wheeler 1980), mangroves (Ronnback 1999), salt marshes (Boesch & Turner 1984), coral reefs (Jones 1991) and even bare sand (Gibson et al. 1998); these comparisons will be reviewed. Perception of temporal and spatial scales of variability are also important to the understanding, modelling and management of ecological systems such as seagrass beds, while the sampling gear employed can have confounding effects on the comparability of studies. Both these factors will be assessed in terms of their potential influence on the interpretation of results from seagrassfisheries studies. The overall aim of this review, however, is to present evidence that supports or challenges current theories on the processes and links between seagrass beds and fishery species. By highlighting these theories, and the gaps and limitations of current literature on seagrass fisheries, the review also aims to suggest what further information is required for effective conservation efforts or to predict the impacts of further seagrass loss on fishery species.

Permanent residents of seagrass beds Species that may be expected to exhibit the strongest relationship with seagrass habitats are those that inhabit the beds all year round and throughout their entire life history. However, 271

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Table 2 Seagrass species which are the focus of seagrass-fishery relations with a brief description of their morphology and geographical range (compiled from various sources; Den Hartog 1970, Phillips & Meñez 1988).

apart from burrowing animals, the protection provided by seagrass is often limited to small and cryptic species (Edgar & Shaw 1995a). Generally, permanent residents are small in size and, as a result, are of minimal importance in terms of commercial and recreational exploitation (Kikuchi 1974). There are exceptions, for example Thalassia and Halodule beds in Florida (USA) support a large number of pinfish (Lagodon rhomboides) which are indirectly valuable to fisheries. Pinfish are used for bait in long line and sport fishing (Jordan et al. 1997). They are also the main prey item of a number of commercially valuable species, such as sea trout, known to forage in these seagrass beds (Jordan et al. 1997). Other examples include the blue crab in the Zostera marina beds of Central and South USA and brown tiger 272

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prawns (Penaeus esculentus) in northern Australian seagrass beds (Bell & Pollard 1989, Loneragan et al. 1998). O’Brien (1994) suggested that adult brown tiger prawns preferred seagrass (Zostera capricorni) as food but juveniles progressively changed their diet from diatoms to seagrass as they grew. Some seagrass beds are home to both the adults and juveniles of certain species, for example the six-spined leather jacket (Meuschenia frycineti) and blue rock whiting (Haletta semifasciata) identified by Edgar & Shaw (1995a) in southern Australian seagrass beds (Heterozostera tasmanica and Zostera muelleri). In Mediterranean Posidonia oceanica beds, Guidetti (2000) identified different age classes of both annular bream (Diplodus annularis) and black bream (Spondyliosoma cantharus). Such examples may make the species candidates for classification as permanent residents, but require more study. Identifying which species are permanent residents requires seasonal sampling, analysis of lengthfrequency distributions and age classes, or novel methods such as tagging techniques. Even when permanent residents can be identified they are rarely exclusive to seagrass beds. Instead, the seagrass habitat is merely one of a number of local structures or refugia from which to choose. For example, in Mediterranean Posidonia oceanica beds, conger eels (Conger conger), more commonly associated with rock and boulder habitats, conceal themselves in the thick rhizome mat (Francour 1997). Karnofsky et al. (1989) found that lobster (Homarus americanus) in a Massachusetts bay (USA) dug shelters not only under rocks and boulders, habitats with which they are usually associated, but also under seagrass (Zostera marina). Although the rock shelters probably afforded better protection, they had to be of a suitable size, whereas the Zostera shelters could be modified and therefore made more permanent. The loss of seagrass habitat would probably have an immediate and observable impact on the survival of these “permanent residents”, particularly if the relationship is an obligate one, and therefore their identification by fisheries managers is an important consideration. Despite the few examples given above, the majority of commercially important species only use seagrass beds for either a small part of their life history, as a temporary foraging area or a short term refuge from predation. They fit into Kikuchi’s (1974) category of “temporary residents”.

Temporary residents of seagrass beds

Foraging Seagrass beds are often quoted as important foraging sites for a number of species, including those of fishery value (Schmidt 1989, Edgar & Shaw 1995b, Buckel & Stoner 2000). There are even a few examples of exploitable species that feed directly on seagrass. Francour (1999) found that Mediterranean saup (Sarpa salpa) fed primarily (although not exclusively) on Posidonia oceanica; adults of the commercially fished echinoid Sphaerechinus granularis also feed directly on Zostera marina in northern France (Guillou & Michel 1993). However, it is proposed that the main reason that commercial species forage in seagrass beds is the high density of potential faunal prey items present (Adams 1976b, Webb 1991, Tupper & Boutilier 1995). Simple foraging models suggests that many fish swim (with or without a pattern) until they find food, stop to eat it, then swim 273

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again until more food is found. Under this scenario, fish will spend more time where there is food (Connolly 1997). Prey items, such as harpacticoid copepods, amphipods and polychaetes, which form a major part of the diet of many fish species associated with shallow inshore areas (Klumpp et al. 1989, Webb 1991), are often found in greater abundance within seagrass. However, swim-search patterns may not be the optimal foraging behaviour for predators in seagrass beds. A predator swimming through seagrass would have difficulty in detecting a prey item because the moving vegetation would interrupt visual cues. Hover searches, where the predator remains static and waits for the prey to move, may be more successful (Diana 1995). The adults of some commercially valuable species may incorporate the seagrass beds into a larger foraging area (Heck & Thoman 1984, Blaber et al. 1992), although the possibility of higher densities of prey organisms is likely to make seagrass a more important component than other areas. Seagrass beds may not always support higher densities of prey items than other areas or the density of certain species may depend on the structure of a particular bed (Connolly 1994a). Brook (1977) concluded that the majority of fish captured in Thalassia beds (Florida, USA) were foraging over a wide area because stomach contents analysis revealed a significant proportion of non-seagrass fauna. Connolly (1994b) suggested that the link between King George whiting juveniles and Zostera muelleri habitat is due to food supply and that the importance of seagrass beds may depend on the abundance of associated fauna. Jordan et al. (1997) observed that a variety of recreationally valuable predators, such as red drum (Sciaenops ocellata), crevelle jack (Caranx hippos), spotted seatrout (Cynoscian nebulosus), southern hake (Urophycis floridanus) and gulf toadfish (Opsanus beta) feed on the pinfish that inhabit the seagrass beds of the Gulf of Mexico. Pinfish growth rates have been observed to vary with seagrass (Thalassia testudinum) density (Spitzer et al. 2000) and it may be that this variability in prey size is reflected in the density of predators. To determine which fishes or decapods are temporary foragers may require detailed analysis of stomach contents. This information can then be used to assess the importance of the seagrass bed as a foraging area for a particular species and aid in the construction of both energy budgets (Adams 1976b) and trophic pathways. These help fisheries managers in assessing the relative value of seagrass beds in terms of the production of particular species and the larger implications of seagrass loss or restoration. Many studies have tried to evaluate the food selectivity of fishes quantitatively by using the ratio of food in their stomachs to the available food in the environment (Thayer et al. 1975, Schmidt 1989, Edgar & Shaw 1995b). Thayer et al. (1975) collected 33 species of fishes from a North Carolina (USA) seagrass bed and found that guts contained crustaceans, gastropods and polychaetes of species commonly associated with seagrass and occasional pieces of Zostera marina. Schmidt (1989) correlated the diets of young barracuda with dominant seagrass infauna and again found fragments of seagrass (Halodule and Thalassia species) in the stomach contents analysed. Other studies have utilised stable carbon isotope analysis to assess trophic linkages in seagrass beds (e.g. Klumpp & Nichols 1983, Thresher et al. 1992). With the apparent enhanced food abundance in seagrass beds, increased growth would be expected but is not always observed (Spitzer et al. 2000). Perkins-Visser et al. (1996) proposed that the abundance and quality of the food, as well as the time available for foraging, determine the actual energy yield from a particular habitat. Thus foraging time is very much dependent on the time spent avoiding predation. 274

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Refuge from predation Seagrass beds are often quoted as offering good protection from predation (Orth et al. 1984, Main 1987, Rooker et al. 1998a, Hindell et al. 2000) and, whereas many studies support this role, the level of protection available varies with the structure of the seagrass bed and is often limited to particular fish size classes (smaller species and juveniles) or cryptic species. Gaining an understanding of the degree of protection provided by seagrass for particular exploited species may help in determining which seagrass beds in a region provide the optimum protection or foraging conditions for that species. Lower predation pressure means less time and energy is required for hiding or escaping and more time can be spent foraging, gaining energy and growing faster (Fraser & Gilliam 1987, Bax 1998). There is often a balance between the benefits and costs of the structural complexity of seagrass habitats. Complexity benefits some smaller fishes by providing refugia, yet is detrimental to visual predators by concealing their prey (Edgar & Shaw 1995a). Organisms therefore might be faced with a trade-off between levels of habitat complexity suitable for protection and for foraging (Werner & Hall 1988, Burrows 1994). One way of minimising predation risk while maximising foraging may be to utilise heterogenous habitats. Holt et al. (1983) hypothesised that this type of heterogeneity was important for juvenile red drum. They found red drum to be more abundant in patchy areas than in homogeneous stands of Halodule wrightii and suggested that this greater abundance was related to the juvenile fishes’ requirements for open feeding areas adjacent to seagrass that provided nearby protection from larger predators. Predator-prey relationships have represented a large portion of the literature on seagrass fisheries in the past (see Orth et al. 1984 for a review of the earlier literature). Studies have assessed the variability in predation pressures between bare sand and seagrass, the majority identifying greater refuge provision in seagrass beds (Rozas & Odum 1988, Ryer et al. 1990). For example, Ryer et al. (1990) showed that the moulting activity of the blue crab was greater in a Zostera marina and Ruppia maritima bed than in an adjacent marsh creek. The protection from predation offered by the seagrass during this vulnerable stage has also been demonstrated in the laboratory (Heck & Thoman 1981), in the field (Ryer et al. 1990) and in tethering studies (Shabmann & Capps 1985, Heck & Wilson 1987, Wilson et al. 1987). Perhaps of greater significance than comparisons with bare sand are the patterns in predator-prey relationships that are observed at different scales of seagrass complexity. It is often assumed that the protection afforded increases with the structural complexity of the seagrass bed. If seagrass beds do offer protection from predators, and this protection does increase with complexity of the habitat, it may also be expected that predator growth rates will be high in low complexity seagrass habitats and decline with increasing seagrass complexity irrespective of prey densities. Buckel & Stoner (2000) demonstrated that large predatory fish such as blue fish (Pomatomus saltatrix) are less able to prey upon juvenile striped bass (Morone saxatilis) with increasing seagrass (Zostera marina) density. Similar results were noted by Savino & Stein (1982), who further attributed these effects to increases in visual barriers for predators. Heck & Orth (1980) hypothesised that in open marine systems, predator success would be inversely proportional to plant surface area and that, due to the constant immigration of possible prey items, there would be no over-exploitation at lower densities. This prediction was supported by Spitzer et al. (2000) in a study on the growth rates of the pinfish inhabiting Thalassia beds in Florida. However, the relationship between 275

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seagrass complexity and predation success may not be a simple linear one (Heck & Thoman 1981, Lipcius et al. 1998). Nelson (1979) hypothesised a threshold effect, whereby protection from predators was significantly greater above a particular plant density. Gotceitas et al. (1997) demonstrated that Zostera marina significantly increased the time required by a predator to catch 0+ age cod (Gadus morhua). They tested this refuge role in a laboratory study where 0+ cod were given the choice of safe and unsafe bottom substrata and Artificial Seagrass Units (ASUs). Below shoot densities of 720 m-2 there was no difference between bare sand and seagrass. This result enforced the threshold hypothesis proposed by Nelson (1979) (see also Orth & van Montfrans 1982, Savino & Stein 1982). One way to test the role of predation in structuring seagrass communities is by measuring the response to its removal. Perkins-Visser et al. (1996) showed that juvenile blue crabs grew faster in predator-free enclosures within Zostera marina than those in similar enclosures deployed outside the beds. Connolly (1994a) tested the importance of canopy to small fishes by removing it and found that fish abundance over the habitat where Z. marina had been removed was not significantly lower than in distant seagrass habitats or controls. All these studies highlight the difficulties in determining whether predation (top down) or food availability and competition (bottom up) controls the overall dynamics of marine ecosystems (Rosaz & Odum 1988, Bax 1998).

The nursery role By far the most studied, and frequently quoted, role of seagrass beds is as a nursery ground for many marine species, including those of commercial and recreational value (Bell & Pollard 1989, Heck et al. 1989, Gray et al. 1996, Jenkins et al. 1997a,b, Rooker et al. 1998a,b). This role has been defined from studies that have identified high concentrations of juveniles and larval stages within the beds. For example, Valle et al. (1999) reported that juveniles of the barred sand bass in Alamitos Bay, California, USA, were found almost exclusively in Z. marina. Similarly, in the Gulf of Mexico, several species of Sciaenidae (drums), which are vital to the recreational fishery, exploit Halodule wrightii and Thalassia testudinum meadows during their early life stages (Stoner 1983, Rooker et al. 1998a,b). Thayer & Chester (1989) stated that up to 90% of the harvestable species in the Gulf of Mexico depend on coastal wetlands and submerged seagrass meadows (Zostera marina) for at least part of their life cycles. Perkins-Visser et al. (1996) found that where the seagrass Z. marina occurs, the juvenile benthic stages of blue crab occur almost exclusively within them, while larval stages of a number of commercial species, including blue rock whiting and leather jackets were observed living in a Westernport (Australia) seagrass bed (Jenkins et al. 1997b). In some areas, the preferential settlement of Mytilus edulis (blue mussel) (Connolly 1994a) and Argopecten irradians (bay scallops) veligers (Connolly 1994a, Irlandi 1996) makes seagrass beds the target of spat collection for aquaculture (De Jonge & De Jong 1992). The question posed, and often answered, by such studies is whether seagrass beds merely concentrate juveniles, or whether the residents actually gain a selective advantage over individuals inhabiting other habitats. Seagrass may improve survival by providing shelter and food. They may also promote the settlement of planktonic larvae and, for those species that do not have a pelagic larval phase, they may act directly as spawning areas. The following sections review the studies which have supported, opposed and explored these possible nursery functions of seagrass beds. 276

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Seagrass beds as spawning grounds Commercially valuable species that are known either to brood or produce demersal eggs, potentially spawn directly within seagrass beds. One example is the annular bream (Diplodus annularis) which inhabits seagrass (Posidonia oceanica) beds when spawning (Francour, 1997). Some species may even attach eggs directly to the seagrass blades, for example the cuttlefish (Sepia officinalis) on Zostera marina beds (Blanc & Daguzan 1998). However, inshore spawners are relatively uncommon in temperate regions and the majority of juvenile fish and decapods within seagrass beds are ocean-spawned species that have been transported inshore by ocean currents. Whereas juvenile and adult fishes of seagrass beds have been well studied, little is known about the importance of this habitat for fish eggs and larvae (Olney & Boehlert 1988). Offshore-spawned larvae supplying seagrass beds Most temporary residents of commercial importance that utilise seagrass beds are species that settle from the plankton and, after spending the initial portion of their lives in seagrass beds, often emigrate to another habitat (Middleton et al. 1984). However, finding a suitable habitat for settling may be crucial for the survival of newly recruited juveniles, and both size and quality of the chosen habitat may determine the carrying capacity of an area (Gotceitas & Brown 1993, Carr 1994, Gibson 1994). A pertinent question is whether the association of a species with a particular type of seagrass bed is a result of active choice or whether initial settlement is random and patterns of distribution are a result of post-settlement processes (Worthington et al. 1991, Jenkins et al. 1997a, 1999). To answer this question, factors influencing the larvae before and after settlement to the seagrass beds have to be addressed (Sale et al. 1984, Worthington et al. 1992a). Pre-settlement processes Larval transport Bell et al. (1987) and Levin et al. (1997) suggested that whereas the associations of fishes within seagrass meadows can be explained by either larval supply and selection of habitat, the emphasis is very much on variability in supply of recruits. The pattern of offshore spawning followed by a pelagic larval stage, where the young fish drift inshore and undergo a benthic stage, is common to many fish species regularly associated with seagrass beds. Eckman (1987) suggested that predation is less important than hydrodynamics in determining the abundance and distribution of early juvenile stages in seagrass beds (see also Eckman & Nowell 1984, Olney & Boehlert 1988, Boström & Bonsdorff 1997, Jenkins et al. 1997b, 1999, Hannan & Williams 1998, Loneragan et al. 1998). While investigating spatial variability in larval supply and settlement, Rooker et al. (1998b) upheld Eckman’s (1987) hypothesis and reported a positive correlation between densities of sciaenids and tidal flow rates. In addition, Bell et al. (1988) suggested that temperature and salinity tolerances are the ultimate causes of larval settlement in estuaries, whereas spawning location, nature of eggs, length of pelagic larval phase and larval behaviour are proximate causes. Knowledge of all these factors, and the consideration of life-history strategies, may aid in the judgement of the relative importance of a seagrass bed to juveniles of particular commercial species (Sogard et al. 1987, Tolan et al. 1997). 277

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Settlement on seagrass beds: passive or active? Settlement of exploitable species to seagrass beds may be through either active selection of a seagrass bed (Worthington et al. 1991) or due to passive settlement (Eckman 1987). Bell et al. (1987) speculated that it is the availability of competent larvae that determines the value of a habitat and that larger structures (in their experiment predator exclusion cages) will receive more individuals than smaller habitats, a speculation supported by Hannan & Williams (1998). Seagrass beds slow currents and enhance the deposition of fine sediments (Fonesca & Fisher 1986). In a similar process, seagrasses are thought to enhance the passive settlement of meroplankton and the rate of this settlement may vary, not only with the species of seagrass but also with certain aspects of plant morphology (Fonesca & Fisher 1986). Zooplankton densities in seagrass beds are twice that of offshore environments (Robertson et al. 1988). Grizzle et al. (1996) noted that Zostera marina blades undergo large amplitude synchronous waving at current speeds exceeding 10 cm s-1, a phenomenon that they termed “monami” (Japanese for “aquatic wave”). These authors suggested that the increased movement of seagrass tips through the water column may enhance larval mussel (Mytilus edulis) settlement by increasing the likelihood of contact between leaf blade and larva. Alternative hypotheses for greater larval settlement at the tips of leaves could be that larvae are attracted to, or caught by, the greater epiphyte cover (Newell et al. 1991) or that the pattern was a result of differential post-settlement predation (Pohle et al. 1991). It has even been suggested that post-larval blue crabs detect and respond to chemical cues from Zostera (Forward et al. 1994). Assuming that fish larvae are able to “recognise” seagrass habitat, Worthington et al. (1991) used ASUs to test whether there was a threshold leaf density important for recognition. At low leaf densities, an epiphyte growing on the ASUs lowered the threshold but at high seagrass densities the added complexity of the epiphytic growth impeded fish settlement (Worthington et al. 1991). Settlement processes are species specific but understanding whether the settlement of the larvae of a fishery species is an active or passive process may be valuable if decisions are to be made on the relative value of different seagrass beds. If settlement is a result of active selection, then seagrass beds of a particular morphology or structure may be the priority for protection. Alternatively, if settlement is passive, the location of the beds (for example their position in relation to the mouth of the estuary or depth) may be a more important consideration. Settle and stay? In a model proposed by Bell & Westoby (1986a), it was hypothesised that the pelagic larvae of fishes and decapods are distributed patchily and settle indiscriminately on the first seagrass habitat that they encounter. These authors further proposed that individuals do not leave a seagrass bed soon after settling, but redistribute to suitable microhabitats within that bed (Bell & Westoby 1986a). Therefore, a seagrass bed that may have been identified as a more valuable habitat (for example, due to leaf height and/or density providing greater predator protection) may support fewer individuals of a species, only because a small number of individuals arrived there. If this hypothesis is true and larval settlement is the driving force, then sites in the same location should show similar distributions of juveniles, assuming that settlement patterns are maintained. Principal component analysis supported this prediction (Bell & Westoby 1986a). Other advocates of the “settle indiscriminately and stay” hypothesis include Rooker et al. (1998a) and Valle et al. (1999). Valle et al. (1999) assessed differential habitat use by Californian halibut (Paralichthys californicus), barred sand bass and other juvenile fishes in Alamitos Bay, California. In addition, they emphasised that seagrass bed characteristics (in this case Zostera 278

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marina) only affect fish abundance at a local scale and that over larger scales it is the location of the bed within the bay that has an effect. The majority of the evidence indicates that recruitment to seagrass beds shows strong responses to seagrass bed structure at local scales (Orth et al. 1984, Bell & Westoby 1986b). At larger scales recruitment may be more influenced by the availability of planktonic larvae (Jenkins et al. 1998).

Post-settlement processes While important, knowledge of the settlement patterns of a particular exploited species is often insufficient information for predicting the value (in terms of their survival) of a seagrass bed. A pertinent question is whether these settlement patterns can be maintained. Summerson & Peterson (1984) suggested that owing to the increased survival of fish and decapods that have “settled and stayed” on seagrass beds (over those that may have reentered the plankton or migrated to other habitats), patterns can indeed be maintained (see also Jones 1991, Tupper & Hunte 1994). The post-settlement importance of seagrass beds is thought to revolve around two nursery functions discussed earlier: refuge from predators (Savino & Stein 1982, Lipcius et al. 1998) and increased foraging efficiency (Heck & Thoman 1984, Perkins-Visser et al. 1996). However, when evaluating the importance of seagrass beds to fishery species, it must be questioned whether the seagrass offers improved growth and increases the chance of survival of its juvenile inhabitants, compared with other habitats. Tupper & Boutilier (1995) hypothesised that the complexity of the seagrass (Z. marina) community meant that there was a greater range of prey items available to young-of-the-year cod, which resulted in better growth and better survival after leaving the seagrass bed. Similarly, Valle et al. (1999) suggested that the occurrence of juvenile barred sand bass almost exclusively within Z. marina was due to greater prey availability, enabling faster growth to a size that is less vulnerable to predation. In Limfjord (Denmark), hatchery reared cod were released to seagrass (Z. marina) beds to improve their initial survival (Støttrup et al. 1994). However, if faster growth within seagrass beds is a result of greater prey availability, then growth rates would be expected to be correlated with food supply. Levin et al. (1997) questioned whether food supply limited the number, or growth rates, of fish recruits in different habitats of a Texan lagoon. They focused on the pinfish and found that recruitment to ASUs was 300% greater than to sand habitats, regardless of whether they supplemented sand habitats with food. While food supply was not the limiting factor, they suggested that supplies may be more effectively utilised in seagrass beds, allowing juvenile fish to grow faster and exceed the food size range of various predators (Levin et al. 1997, Bax 1998). The quality of the food as well as the time available for foraging (linked to predator avoidance) probably determines the actual energy yield from a particular habitat (PerkinsVisser et al. 1996). Olney & Boehlert (1988) questioned whether seagrass affords predator protection for early life-history stages of fishes. They remarked that any degree of protection would be afforded only to those individuals able to orientate to the seagrass blades. They also pointed out that seasonally high densities of planktivorous fishes, such as silver side, spot and silver perch, may be a result of seagrass beds serving as a sink for pelagic eggs and early larvae. However, other studies have illustrated the suitability of seagrass as a refuge from predation (see p. 275). When exploited species take advantage of this protection, and of the elevated prey densities, their survival is likely to be high and initial settlement patterns 279

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may be maintained (as proposed by Summerson & Peterson 1984), but not indefinitely. The juveniles of most commercially important species inhabit seagrass beds only temporarily. Kikuchi (1974) reported that when juvenile fishes appear in Z. marina beds in spring, they feed upon minute pelagic and epiphytic crustaceans, whereas in summer, young sub-adults feed mainly on bryozoans and polychaetes. Other authors have found similar ontogenetic changes in feeding habits (Carr & Adams 1973, Adams 1976b, Brook 1977, Gillanders 1995, Pardieck et al. 1999, Valle et al. 1999). Valle et al. (1999) observed that in Alamitos Bay, California, high densities of small juvenile barred sand bass were restricted to Z. marina whereas larger juveniles and adults were more abundant among rocks and over sandy bottoms. In Newfoundland, Gotceitas et al. (1997) reported that 1+ cod shifted from Z. marina to rock and macroalgae. In many situations, this movement of juveniles from the seagrass bed is related to size and predation. In general, as individual size increases the effectiveness of the seagrass habitat as a refuge declines and species will move to a more suitable habitat. Pile et al. (1996) suggested that this shift out of the seagrass will occur when the risk of predation inside the bed is higher than the energetic value gained by remaining in the habitat. This consideration has important implications when assessing the importance of a seagrass bed for specific juveniles in terms of food availability and in explaining possible periods of residency within the bed. It is important to note that lower densities of a certain size class of juveniles may result from either selection of an alternative habitat or greater predation rates. A laboratory test of field-identified habitat preferences of the pinfish by Jordan et al. (1997) found that, in the absence of predators, juvenile pinfish used seagrass and sand equally and they proposed that the observed patterns were due to predator mediated selection of habitat. However, Jordan et al. (1997) admitted that their study may have been confounded by an edge effect and proposed that the use of available sand habitat may decrease with increasing distance from seagrass cover. The relative importance of differential predation (Stoner 1983) and predator mediated habitat selection (Main 1987, Sogard & Olla 1993, Jordan et al. 1997) needs to be explored in greater detail for individual species. Finally, it should be recognised that despite the plethora of statements that seagrass beds are important nursery habitats, some studies have questioned this role. Heck et al. (1989) found little evidence that juveniles of commercially important fishes and shellfishes used Z. marina as nursery grounds in the Nauseate System (Massachusetts, USA), suggesting that the importance of seagrass to fisheries varies with latitude (a view that is explored in greater detail later in the review). Contrary to other evidence, Halliday (1995) found that die back of Z. capricorni and Halophila species in Queensland (Australia) was associated with an increase in juvenile prawn densities, rather than resulting in the expected decline of juvenile commercial prawn (Penaeus plebejus). In general, however, studies contradicting the view that seagrasses are important fisheries nursery grounds are rare.

Seagrass detritus as the basis of the coastal fisheries food chain Thresher et al. (1992) reported that the food chain supporting the larvae of the blue grenadier (Macruronis novaezelandiae) was not based on either phytoplankton or terrestrial organic matter. Instead, stable carbon isotope analysis showed that it was actually based on microbial decomposition of seagrass (Zostera marina) detritus. Others have used stable isotopes (outlined by Fenton & Ritz 1988) as a way of tracking seagrass in food web dynamics 280

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(McConnaughey & McRoy 1979). Dauby et al. (1998) measured 13C/12C ratio (d13C) of over 100 species of plants and animals along the Brittany coast (France) and traced the input of carbon from distinct producer groups, and in particular Z. marina. Using multiple stable isotope analysis in a tropical Australian estuary, Loneragan et al. (1997) showed that d13C values of juvenile prawns (Penaeus esculentus, P. semisculatus and Metapenaeus species) closely matched values of seagrass of various species and seagrass epiphytes. However, these authors also noted that the strength of the similarity was dependent not only on the proximity of other habitats but also the season (wet or dry), highlighting the caution needed in interpreting these kinds of studies. Similarly, Fry (1981) found that whereas d13C values in the brown shrimp (Penaeus aztecus) from Texan (USA) seagrass beds matched that of seagrass, shrimp found in open bays of the estuary had ratios closer to that of phytoplankton. Despite this example of trophic subsidy rather than trophic dependence, Fry (1981) noted that most of the shrimp caught on ebb tides at the estuary entrance had the d13C comparable with seagrass and suggested that these habitats supplied more shrimp to the fisheries overall. Seagrass detritus may form the basis of, or at least contribute to, coastal nutrient cycles and indirectly promote the health of a fishery. Wood et al. (1969) stated that seagrasses provide large quantities of detrital matter to coastal ecosystems. Bach et al. (1986) demonstrated that the export of Zostera marina detritus in a Beaufort (North Carolina, USA) estuary equalled, if not exceeded, that of Spartina alterniflora. Adams (1976b) also suggested that the basis of the fish food chain in Zostera beds is detritus and its associated microbial community, while Brook (1977) bridged the gap between detritus and higher trophic level predators (including valuable commercial and sport fishes) by identifying a number of transient foragers. Much seagrass detritus would appear to settle on nearby sediments. Ferrell & Bell (1991) found that the number of fishes on sand adjacent to Z. capricorni was significantly higher than sand distant from seagrass. It has also been suggested that the presence of seagrass may lead to organic enrichment of unvegetated sediments nearby, thereby enhancing food production for fishes (Shaw & Jenkins 1992). Jenkins et al. (1993) reported that juvenile greenback flounder (Rhombosolea tapirina) may benefit indirectly from seagrass through organic enrichment of sediments and corresponding elevation of food production. Overall, the evidence suggests that the probable role of seagrass detritus in nutrient cycling should not be neglected because such cycles may represent an important input to coastal fisheries.

The relative value of seagrass to fishery species compared with other habitats When considering the importance of seagrass beds to fisheries, one of the first questions asked is: do the fishery species inevitably need this habitat to sustain their populations? Proposals at the International Seagrass Workshop led to a large number of comparative studies (McRoy 1973), many of which assessed the relative importance of seagrass meadows to fishery species. Seagrass communities have been compared with a number of other inshore habitats, particularly unvegetated ones (Ferrell & Bell 1991, Heck et al. 1995, Boström & Bonsdorff 1997, Connolly 1997, Sheridan 1997, Gray et al. 1998, Arrivillaga & Baltz 1999, Guidetti 2000). These studies often assumed (perhaps incorrectly) that natural densities of fishery species would be a quantitative measure of habitat quality, with higher densities 281

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reflecting either a behavioural selection or higher level survival relative to other habitats. Very few studies actually attempted to understand the mechanisms producing the patterns (but see Levin et al. 1997). The studies addressing the complexities of these processes were discussed earlier in this review (p. 277). Usually, and somewhat predictably, higher numbers of fishery species are identified in seagrass beds compared with bare sand habitats (for example Arrivillaga & Baltz 1999) and the species compositions tend to differ markedly between the two (see Gray et al. 1996). In contrast, overall fish densities are not always higher in seagrass beds when compared with adjacent bare sand (Edgar & Shaw 1995a). In general, species with small individuals, juveniles or those with cryptic habits dominate seagrass beds, whereas large mobile fishes or species able to school, burrow, or camouflage themselves against the seabed are more abundant on bare sand. Therefore, while species composition and species number can be variable between habitats, differences in total abundance are often less apparent. Instead of concentrating on differences in composition and abundance of fishes between bare sand and seagrass, Edgar & Shaw (1995a) attempted to quantify the difference in production between the two. Their study, which addressed the consequence of seagrass (Heterozostera tasmanica and Zostera muelleri) loss, found that most of the juveniles of fishery species were equally distributed between seagrass and bare sand. However, production values were comparable with North American studies and seagrass values surpassed those of bare sand habitats (Adams 1976a, Lubbers et al. 1990, Edgar & Shaw 1995a). Perhaps of greater significance than comparisons with non-vegetated habitats are those with different forms of submerged aquatic vegetation. Any form of vegetation increases the complexity of a habitat, thereby providing a higher availability and variability of microhabitats, which in turn support a more diverse fauna (Wheeler 1980). Gotceitas et al. (1997) examined whether juvenile Atlantic cod utilise Z. marina as a habitat in Newfoundland (Canada). They assessed different habitat types commonly found in the area and found juvenile cod to be almost exclusive to the Zostera beds. Sogard & Able (1991) compared Z marina, the marine alga Ulva lactuca and marsh creeks as habitats for epibenthic fishes and decapods. They found that both vegetation habitats were preferred to unvegetated sediment but that Zostera was a superior habitat to Ulva for epibenthic fishes. However, Ulva provided a significant refuge from predation and supported faster growth than the Zostera habitat. They concluded that Ulva is therefore an important habitat in areas lacking seagrass but cannot be considered an equivalent substitute. Continuing the theme in a laboratory-based study, Borg et al. (1997) showed that, given the choice, juvenile cod preferred vegetated habitats of Zostera marina, the brown alga Fucus vesiculosus and algae of the genus Cladophora to bare sand. However, this preference was only apparent during the day. These authors proposed that the shelter provided by the macrophytes is not necessary at night. Differences were evident between vegetation types in terms of the size of juveniles; small juveniles were able to utilise all the vegetation types provided but larger individuals were restricted to Fucus (Borg et al. 1997). Seagrass is not always the more important habitat. Heck & Thoman (1984), in a study of submerged aquatic vegetation in Chesapeake Bay (USA), found that Zostera marina was not regarded as an important nursery area for fishes because it did not support more individuals than bare substrata. The results of Heck & Thoman (1984) may have been due to the close proximity of the studied bare substrata to seagrass beds. Ferrell & Bell (1991) found that areas of bare sand adjacent to Z. capricorni beds constituted a specific habitat for a number of species, and supported higher fish densities than areas some distance from 282

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seagrass. One theory put forward for this difference was that the export of seagrass detritus may lead to organic enrichment of nearby non-vegetated sediments, thereby enhancing food production for fishes (Sogard 1989, Shaw & Jenkins 1992; see also p. 280). Some species may use unvegetated areas as long as refuge is available nearby (Summerson & Peterson 1984). If this assumption is true, then comparisons of seagrass and adjacent bare sand may be inappropriate for predicting changes in fish assemblages after the loss of the seagrass. The incorporation of near and far bare sand habitats is important in any comparison with this purpose. Ferrell & Bell (1991) point out that areas adjacent to seagrass should be managed as carefully as the seagrass itself and the appropriate area of this “buffer” should be assessed. The location of the seagrass bed can also influence species composition and fish densities. Jenkins et al. (1997b) showed that species diversity was greatest in seagrass compared with bare sand. However, when compared with bare sand, a greater total abundance was not evident in the shallow Heterozostera sites, but only in the deeper Posidonia beds. This study led Jenkins et al. (1997b) to propose that the loss of both intertidal and subtidal seagrass would result in a significant decline in species diversity but that the loss of seagrass in deeper subtidal areas would have a greater consequence on fish densities than loss in the intertidal zone. Hanekom & Baird (1984) found no significant difference in the numbers of fish species at Zostera marina and non-Zostera sites. However, they attributed this similarity to the turbidity of the estuary they studied, which they proposed might have aided predator evasion, thus reducing the attraction of Zostera as a refuge (see also Blaber & Blaber 1980). It would appear that habitat choice depends on the requirements of an individual during a particular life stage, season or even time of day (Jansson et al. 1985, Sogard & Able 1991, Borg et al. 1997). Whether habitat selection is an active or passive process, it may be worthwhile to assess the range of habitats available to a species in a given area in addition to seagrass.

The importance of scale The studies discussed in previous sections highlight one of ecology’s most crucial questions, that of scale. Both the attributes of seagrass habitats and the recruitment of fishes are highly variable in space and time. To provide useful information, the temporal and spatial context of any study must therefore be explicit (Mason & Brandt 1999).

Spatial scales of variability Bell & Westoby (1987) were among the first to identify that patterns in fish assemblages associated with small-scale, seagrass bed characteristics (for example, density, biomass or bed heterogeneity) weakened when studies moved from local to larger geographical scales (Fig. 1). For example, the importance of seagrass beds to commercially important fishes and shellfishes may vary with latitude. Heck et al. (1989) found the nursery function and species composition of Z. marina meadows at Cape Cod (northern Atlantic coast of the USA) to be strikingly different from Chesapeake Bay and North Carolina further south. A similar latitudinal difference was identified by Sogard & Able (1991), who compared the faunal communities of New Jersey seagrass beds with other Z. marina ecosystems along the 283

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Figure 1 A summary of the scales of spatial patterns that may affect seagrass-fishery relationships and examples of recent studies that have addressed them.

east coast of the USA. They found that juvenile blue crab did not exhibit the preference for Zostera that was evident in Chesapeake Bay (Heck & Orth 1980, Orth & van Montfrans 1987) and two Texan bays (Zimmerman & Minello 1984, Thomas et al. 1990). Other largescale disparities have been identified and Sogard et al. (1987) questioned the assumption that seagrass (Z. marina) meadows are important nursery grounds for warm temperate to tropical systems. They further proposed that the proportion of permanent residents in a seagrass bed would increase with decreasing latitude as the extent of winter migrations 284

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outside the bed decline. These regional differences in functional relationships and interspecific interactions emphasise both the importance of local studies and the need for caution in comparing seagrass beds from different regions. At large geographical scales, it is possible to identify variation not only in the range of certain species of seagrass (see Table 1, p. 270) (Phillips & Meñez 1988) and zoogeographical species pools but also in the concentrations of studies that address seagrass fisheries relationships. These study “hot spots”, most notably in Australia and North America, are evident in Table 2 (p. 272). The majority of studies directly relating seagrasses to fisheries appear to be Australian, including two thorough reviews (Bell & Pollard 1989, Connolly et al. 1999). Both reviews conclude that specific seagrass meadows represent important habitats for many Australian fishery species, including various species of king and tiger prawn, blue swimmer crab (Portunus pelagicus) and the western rock lobster (Panulirus cygnus). Connolly et al. (1999) highlight many gaps in the present understanding of the links between seagrass and fisheries, including the relationships between finfishes and seagrasses (much of the work in Australia being on decapods) and give comprehensive recommendations for future research. The majority of the ideas, conclusions and suggestions in Connolly et al.’s (1999) review have application in other parts of the world and should not be overlooked because of their apparent focus on Australian seagrass beds. Reducing the scale further, coastal location may be another factor in determining the value of a seagrass bed to fishery species. Many of the studies substantiating the claims of seagrass importance to fisheries are based on beds within estuaries or sheltered coastal regions that, even in the absence of seagrass beds, may be important nursery areas (Boesch & Turner 1984, Baltz et al. 1993). In particular, there seems to be a focus on shallow seagrass beds within estuaries (Sogard & Able 1991, Szedlmayer & Able 1996, Rosaz & Minello 1998) with a few notable exceptions (e.g. Pihl & Rosenberg 1982). Therefore, since estuaries are already established as nursery areas in the literature, is the perceived importance of seagrass beds confounded by their estuarine location? The answer is obviously site specific. Detailed habitat comparisons are required to determine the relative value of the seagrass bed compared with other habitats (see p. 281). This need to assess relative importance applies not only to habitats within the same estuary but also to those within the same shallow coastal regions and bays because these areas are also noted for their nursery importance, even when unvegetated (Gibson et al. 1998). As the previous section of this review indicated, the depth of the seagrass bed is another important consideration. Bell et al. (1992) examined differences in fish assemblages in deep and shallow margins of the seagrass Posidonia australis in New South Wales, Australia. For the majority of locations, they reported significantly more fishes in deep seagrass than shallow seagrass during late spring and early summer. The mean shoot density was lower in the deeper beds and it was initially proposed that the difference in assemblage may be due to greater numbers of bare-sand species able to utilise the deeper beds. Further investigation revealed that deep Posidonia assemblages were more similar to shallow Posidonia assemblages than those of deep bare substrata (Bell et al. 1992). In French P. oceanica beds, however, Francour (1997) identified lower fish densities in deeper meadows when compared with shallow beds. In shallow seagrass beds, the refuge status may be related to both the complexity of the seagrass and the depth of the bed. Not only is the vulnerability of larger piscivores to avian predation thought to be greater in shallow waters, but these larger fishes may also have difficulty moving and foraging and must tolerate higher fluctuations in temperature and oxygen (Ruiz et al. 1993, Pardieck et al. 1999). 285

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Bell & Harmelin-Vivien (1982) found that juveniles of many species were more abundant in shallow sublittoral rocky reefs than Posidonia beds at depths of 15m to 20m. They suggested that this difference was due to pelagic larvae being driven to the shore by currents and settling on the most readily available shelter. Most larval settlement studies (see p. 277) have documented patterns within individual beds and have not considered whether recruitment affects the patterns observed over larger geographic areas. This lack of larger spatial consideration needs to be addressed in order to elucidate the links between seagrass beds as juvenile habitats and the productivity of the fisheries to which the juveniles recruit. The proximity to other habitats may influence the relative importance of one seagrass bed over another. Sedberry & Carter (1993) looked at possible nursery habitats that were available to juvenile stages of economically important reef fishes (including the seagrass Thalassia testudinum) adjacent to a coral reef in a Central American lagoon. They found that the overriding factor in determining the abundance of juveniles was distance to the main reef and its piscivorous predators. Similarly, Raposa & Oviatt (2000) explored the variability in nekton community structure between Zostera marina beds at a small geographical scale (within the same bay), by quantifying the effects of neighbouring shoreline type, distance to the shoreline and the biomass of vegetation. They found that both the distance to the shore and the shore type affected nekton assemblages. Not only has the coastal location of the bed been shown to influence its value as a refuge, foraging site or nursery ground but also its particular position within a bay, lagoon or estuary (Livingston 1984, Sogard et al. 1987, Bell et al. 1988, Sogard 1989, Worthington et al. 1995, Hannan & Williams 1998, Valle et al. 1999). Bell et al. (1988) suggested that the location within an estuary may affect distributions and abundance of recently settled fishes and decapods, and hypothesised that this location effect was because larvae of different species occur in different parts of an estuary when competent to settle. These distributions, they proposed, were the result not only of the site of spawning but also the temperature and salinity tolerances of their eggs and larvae. This hypothesis was later backed up by Hannan & Williams (1998), who found the number of ocean-spawned fishes settling within seagrass (Z. capricorni) habitats decreased with distance from the mouth of a New South Wales lagoon. Monthly length-frequency data gathered over the course of the study season indicated that progressively larger juveniles were found at these distant sites. Valle et al. (1999) observed an analogous pattern in Alamitos Bay, California (USA) and found that, although community composition was similar between sites, the abundance of juveniles of the barred sand bass and California halibut (Paralichthys californicus) decreased with increasing distance from the mouth of the bay. The consideration of which areas of seagrass would be the first to be met by ocean-dispersed fry and larvae is therefore important in any study, particularly when sites are located in lagoons or estuaries with poor circulation. These examples highlight the inadequacies of studies restricted to only one sand or seagrass habitat, one site or to one bay or estuary. Understanding and predicting patterns at large scales is therefore difficult. As Bell & Westoby (1987) identified, it is only at smaller scales (for example individual bed morphology) that patterns in species assemblages are more obvious. Like so many habitats, a “typical” seagrass ecosystem is difficult to define. Many beds exist as vegetational units of various shapes and sizes or have unvegetated zones such as sand bars interspersed among more homogeneous areas (Robbins & Bell 1994, Turner et al. 1999). This heterogeneity does, however, make them a model system to test how spatial patterning of habitats influences ecological processes (McNeill & Fairweather 1993, Robbins & Bell 1994, Irlandi et al. 1995). 286

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First, the size of the seagrass bed, degree of heterogeneity or “patchiness” may influence its value as habitat to certain exploitable species. Irlandi et al. (1995) assessed the survival and growth of the bay scallop (Argopecten irradians) in plots of Zostera marina and Halodule wrightii varying in heterogeneity. Keeping shoot density, biomass and blade length the same, they showed that simple spatial patterning can alter the roles of predation, with more scallops lost to predation in very patchy seagrass beds. Whereas commercial production of the scallops may be reduced in patchy beds, Irlandi et al. (1995) comment that this reduced production also implies greater transfer to higher trophic levels in these beds, potentially supporting larger numbers of other fishery organisms that prey on the juvenile scallops (for example, the blue crab). Such factors should be considered prior to any preferential protection of higher density, homogeneous beds. In a later study, Irlandi (1996) examined the effects of seagrass patch size and energy regime on the growth of the suspension-feeding bivalve Mercenaria mercenaria that is cultured as a commercial substitute for oysters. Small Mercenaria survival did not differ with patch size but larger clams were significantly affected because current flow rates differed between patches. The influence of patch size is not limited to sedentary species (Holt et al. 1983). Jenkins et al. (1997b) showed that the juveniles of King George whiting in a South Australian bay preferred the patches between seagrass, although Connolly (1994c) found that recruits in another south Australian inlet are only caught within the seagrass beds themselves. Once again the variation with locality is evident. Connolly (1994c) attributes this variability to the availability and vulnerability of prey items in each habitat; these interactions have been explored earlier in the review (see p. 273). A question often asked in the literature is whether refuge function of seagrass is correlated with mesoscale variables (for example patch size) or with microscale variables (such as shoot density). Since the 1980s, seagrass research has focused on the role of the small-scale structural complexity in determining species richness and density (Heck & Orth 1980, Stoner 1980, Bell & Westoby 1986a,b, Bell et al. 1987, Sogard et al. 1987, Ansari et al. 1991, Irlandi 1996, Loneragan et al. 1998). Complexity has been variously measured as percentage cover, density, biomass, biovolume and plant species diversity in the case of polyspecific seagrass beds (Stoner & Lewis 1985), although some of these variables may represent seagrass area rather than complexity (Attrill et al. 2000). Variations in morphology and growing conditions (e.g. depths) may result in different species of seagrass in the same location hosting contrasting fish species of economic value, or similar species at significantly different densities. Zostera and Posidonia beds in Botany Bay, Australia were found to serve different functions for juveniles; five species of economic importance were found exclusively in Zostera as recently settled juveniles, whereas none was found only in Posidonia (Scott 1981, Middleton et al. 1984). Zostera apparently provides an area for initial settlement for several of these species (arguably due to depth and position of the beds), whereas Posidonia is utilised later in their life cycles. Rooker et al. (1998b) also investigated two types of seagrass (Halodule wrightii and Thalassia testudinum) and found that particular species of juvenile sciaenids showed a preference for one or the other. Many other studies have found differences in the communities from meadows dominated by different seagrass species (Kulczycki et al. 1981, Martin & Cooper 1981, Huh 1984, Middleton et al. 1984, De Troch et al. 1996, Tolan et al. 1997, Loneragan et al. 1998, Zupo & Nelson 1999). Orth et al. (1984) suggested that the abundance of many species is positively correlated with two distinct aspects of plant morphology; the root rhizome mat and the plant canopy. To test this suggestion, they cleared patches of Zostera muelleri canopy in South Australia. The resulting faunal community was more similar, although not identical to, unvegetated 287

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areas. Although this similarity may be explained by the short-term nature of the study, Connolly (1994a) proposed that the canopy is not the overriding factor that determines the difference between patches with and without Zostera. Rhizomes produce microhabitats and bind the sediment making it more stable but they may also prevent a predator from accessing a prey species or increase prey escape time by impeding the burrowing of the predator (Orth et al. 1984). Increased abundance and diversity of fishes associated with seagrass meadows have frequently been positively linked to the complexity of the seagrass canopy (Heck & Orth 1980, Bell & Westoby 1986b, Ansari et al. 1991). Stoner (1980) found that, irrespective of sediment type or hydrodynamic effects, seagrass biomass was an important factor in the regulation of species abundance, dominance, diversity and trophic organisation. However, Loneragan et al. (1998) reported that although reduced numbers of juvenile tiger prawns were found in the lower biomass seagrass beds, due to their areal extent these beds were still the main nursery area for the valuable northern Australian prawn fishery. The length, biomass and density of leaves are not the only factors influencing physical complexity of seagrass habitats; epibiota can provide an additional level of complexity (Attrill et al. 2000). Bell & Westoby (1987) found that a bloom of the alga Giffordia sp. was correlated with a reduction in decapod and fish abundance, which was attributed to impedance of movement. In contrast, Kulczycki et al. (1981) suggested that large clumps of unattached drift algae are a prominent feature of many seagrass ecosystems and may enhance food and shelter provision by further increasing the complexity of the habitat. When evaluating the relative importance, or perhaps predicting the carrying capacity of, different seagrass and non-seagrass habitats, these sources of variation need to be accounted for, which can cause logistical problems. There are, however, studies that do incorporate many of these factors. Sogard et al. (1987) investigated the relative contribution of physical and vegetation variables in determining densities of fishes on Florida Bay Banks. In addition to measuring a whole suite of seagrass variables (including standing crop, canopy height, shoot density (of each of the seagrass species in the polyspecific bed they studied), blade density, seagrass litter and drift algal biomass), they also determined percentage silt, organic carbon, depth, temperature range and salinity. All sampling was done during both day and night. Multiple regression analysis indicated that although seagrass variables were often interrelated, their differential importance to an individual species indicated that fishes were discriminating between different structural aspects of the seagrass canopy. Resource maps and geographical information systems (GIS) detailing the factors such as the sediment, depth, salinity, temperature and habitat type (including various seagrass variables) of a region, are an important and useful tool and should be considered as a first step in any assessment.

Temporal scales of variability In addition to the spatial components of variability, other studies have identified strong temporal patterns in both the seagrass bed structure and the composition of their fauna. Geographic location and latitudinal position can affect seasonal patterns, day lengths and tidal amplitude. In short, the functioning of any seagrass bed incorporates strong temporal patterns which need to be accommodated in any study wishing to decipher their importance to fisheries (Fig. 2). Long-term fluctuations are now an accepted feature of natural systems 288

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Figure 2 A summary of the scales of temporal variability that may affect seagrass-fishery relationships and examples of recent studies that have incorporated and identified them.

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and interannual variations are evident in the seagrass fishery literature (Nelson 1997). Climatic changes influence primary production and thus annual levels of fishery recruitment and production (Caddy 1986). It can be assumed that the longer the term of the study the more valuable the information (of a predictive nature) will be. Long-term datasets are rare (but see Meng & Powell 1999). In a 3-yr study comparing Zostera capricorni and Posidonia australis, Young (1981) concluded that the differences in the vagile fauna between the two seagrass species were controlled by external events such as seasonal sea temperatures, which led to variable recruitment success. Anderson (1989) analysed a 27-yr dataset of blue crab catches and a 20-yr index of seagrass (Zostera marina) areal coverage from the Virginian section of Chesapeake Bay, reporting a strong correlation between the two when the seagrass data were lagged one year (to match juvenile occupation), although a causal link was not determined. Seasonal patterns of seagrass bed fauna can be influenced by species specific spawning times, larval dispersal patterns and ontogenetic shifts within the year. For example, each of five species of sciaenids inhabiting Halodule and Thalassia beds of a Texan estuary showed distinct settlement periods that rarely overlapped (Rooker et al. 1998b). Also, optimal growth and survival of juvenile red drum (Sciaenops ocellatus) within estuarine seagrass meadows (Texas) was observed for mid-season cohorts but the nursery conditions experienced by cohorts early and late in the season did not favour survival in early life (Rooker et al. 1999). Such seasonal patterns are further complicated by the incorporation of monthly weather events and tidal patterns that may produce favourable current conditions for larval transport (Joyeux 1999). Sampling at different states of the tide, Sogard et al. (1989) found no significant tidal differences between the numbers of epibenthic fishes, but a significant difference in the number of water column species. In a large amplitude tidal system, Hettler (1989) illustrated that estuarine-dependent residents and transients moved regularly between flooded salt marsh and adjacent subtidal habitats and there is no reason to assume that a similar pattern does not occur in intertidal seagrass beds. High tides may make alternative, and perhaps preferred, habitats such as salt marsh available to certain species (Rosaz & Minello 1998). Thus if sampled during high tide, seagrass beds may temporarily appear less important to more mobile species. Conversely, at high tide, shallow subtidal and intertidal seagrass beds may become accessible to foragers, or those seeking refuge, and larger predators may enter these beds without risking avian predation. Monthly patterns can also be observed, including the lunar rhythm of ecdysis in blue crabs, during which the crabs utilise seagrass beds as a refuge during this vulnerable period (Ryer et al. 1990). In addition to tidal variations in assemblages, other diel patterns are evident. Many reports concerning seagrass habitats supporting different and more diverse fish assemblages are based on daytime sampling programmes, even though many estuarine and coastal species of fish display strong diel rhythms of activity (Adams 1976a, Greening & Livingston 1982, Sogard et al. 1989, Stoner 1991). For those studies that have assessed diel variation in seagrass beds, similar strong patterns are evident (Robblee & Zieman 1984, Bauer 1985, Edgar & Shaw 1995a, Rountree & Able 1997, Mattila et al. 1999). Gray et al. (1998) examined whether habitat associations of juveniles of economically important species changed between day and night. More species were collected over seagrass (combined day and night) but a significant diel variation in the structure of sand-associated assemblages was also observed. Summerson & Peterson (1984) suggested that seagrass beds may serve as refugia in a manner similar to coral reefs because species use seagrass as a shelter by day and forage over sand 290

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under the protection of night. Hindell et al. (2000) specifically looked at the spatial, diel and tidal variability in the abundance of piscivorous fishes and their prey within an Australian Heterozostera tasmanica meadow. The Western Australian salmon (Arripis truttacea) was just one of the species to show strong temporal patterns in its foraging behaviour. If samples are not taken both day and night and at different tidal states, important temporary residents may be missed and the role of the bed inaccurately assessed (Ferrell & Bell 1991). Unfortunately, the impracticalities of night sampling may prevent the implementation of an ideal sampling programme. In view of the variability and number of confounding factors that may exist, a number of scientists have moved towards the use of ASUs (Orth & van Montfrans 1987, Sogard 1989, Levin et al. 1997). Jenkins et al. (1998) used replicate ASUs adjacent to natural seagrass beds to examine recruitment of King George whiting on the south coast of Australia. The advantage of the ASUs was that density and size of the “seagrass” could be standardised at all five sites along the 50 km of coastline used in the study.

Limitations of sampling methodologies Current perceptions of seagrass-fishery relationships may be clouded not only by the particular spatial and temporal scales of studies, but may also be limited by the particular sampling methods employed. Despite attempts to standardise sampling gear and methods (Phillips & McRoy 1990), the variability of environments where seagrasses are found often makes this standardisation difficult. The type of sampling gear used, and the temporal and spatial scales at which it is used, all affect the perception of the processes of specific seagrass beds, and hence the roles proposed. Many techniques have been developed and adopted for sampling the mobile fauna associated with seagrass, including diver observations (Tupper & Boutilier 1995, Francour et al. 1999, Guidetti 2000), poisoning (Weinstein & Brook 1983, Bell & Westoby 1987), beach seining (Gotceitas et al. 1997, Jenkins et al. 1997b) and beam trawling (Worthington et al. 1992b, Szedlmayer & Able 1996). As a result, a number of studies have been carried out to assess the relative suitability of these techniques in different situations (Lewis & Stoner 1981, Orth & Moore 1983, Gray & Bell 1986, Rosaz & Minello 1998, Francour 1999). Most of the methods used are qualitative and, although quantitative techniques are available (for example drop nets and throw traps), they do have certain limitations, the most significant being the depth at which the gear can be used (Rosaz & Minello 1997). The majority of seagrass-fishery studies are carried out on shallow-water seagrass beds (i.e. <2 m), and this is reflected in the proposed standardised sampling protocols which promote the use of drop nets, throw traps and suction sampling techniques (Gilmore 1990). Seagrass beds are not, however, limited to depths of 2 m. Francour (1999) critically reviewed fish sampling techniques in Posidonia oceanica seagrass beds in the Mediterranean, which can extend to depths of 40 m, and commented that these beds prohibit the use of throw traps or drop nets (due to depth) and trawls (due to high structural complexity). He concluded that the clarity of the water promotes the use of visual census. In addition to the applicability of sampling method to the seagrass type and location, different methods may be biased to a particular group of organisms (e.g. benthic or pelagic, schooling or solitary). A combination of methods and a range of qualitative and quantitative 291

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approaches may be needed to describe the macrofaunal communities associated with seagrasses. Without a range of sampling gear it may be that inferences on species inhabiting the area are limited to the selectivity of the gear. Rosaz & Minello (1997) give a comprehensive and thorough account of sampling design and gear selection for estimating densities of small fishes in shallow estuarine habitats. They note that many studies assessing the value of seagrass beds involve inter-habitat comparisons. For an unbiased evaluation, the same gear should be used throughout the study. In addition, the use of gear that characteristically exhibits large and unpredictable variation in catch efficiency makes habitat comparisons unreliable and decreases the ability to detect statistical differences. Rosaz & Minello (1997) emphasise that the ease of standardisation (i.e. being able to make a piece of gear function similarly each time it is used) is an important quality of a sampling gear to prevent variation in catch efficiency.

Conclusions and recommendations for conservation Seagrasses are vulnerable to a number of disturbances and require management. With growing fears that stock restoration efforts are being compromised more by habitat loss from coastal development, adverse fishery activities and pollution than by overexploitation, conservation of habitats (such as seagrass beds) is becoming an important part of fisheries management. The priority of such management has been to determine which habitats represent: “geographically or physically distinct areas that one or more species finds indispensable for its survival at some phase in its life history” (Langton et al. 1996). Seagrass beds are becoming increasingly identified as such habitats (Den Hartog 1970, McRoy & Helfferich 1977, Phillips & McRoy 1980, Larkum et al. 1989), mostly with regard to their role as nursery grounds. Examples supporting this claim are numerous (see Table 1, p. 270) but understanding why seagrass habitats have a significant influence on fisheries requires more detailed information. It is clear that fish recruitment to temperate zone seagrasses shows strong responses to habitat structure at local scales but, at larger scales, recruitment is linked more to the availability of planktonic larvae. Such patterns of scale should be borne in mind when selecting sites for comparative studies or conservation. For example, which site may be the first to receive ocean spawned larvae? In addition, sites should be selected with a view to minimising the impacts of other variables such as salinity, sediment type and turbidity. Alternatively, these variables should be measured and accounted for, or the use of experimental manipulations and ASUs considered. The spatial patterns identified in initial surveys that may influence the beds functioning must be incorporated into any further study at a level appropriate to the questions posed. Recent studies have highlighted the temporal variability of the seagrass meadow fauna, and most commercially valuable species appear to be seasonal or temporary seagrass residents. Therefore, survey protocols must take into account seasonal and annual variations in seagrass standing stock, spawning periods, annual recruitment, and the diel and tidal migrations. Once the commercial species using the beds are identified, an understanding of their biology, including detailed ecological assessments of habitat requirements during different stages in their life history, is needed. Ontogenetic or functional phases in a species life history must be integrated with large-scale seagrass distribution (geographical location, larval dispersal, depth, distance from shore, distance to other habitats) and local habitat 292

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characteristics (seagrass biomass, density, substratum and drift algal biomass). With this life-history information and a detailed understanding of local seagrass resources, effective conservation and management of the fisheries-habitat complex is possible. However, to assess whether seagrass beds merely concentrate species, or whether the residents gain a selective advantage over individuals inhabiting non-seagrass beds, or seagrass beds of a different size or morphology, more detailed studies on seagrasses are required. This undertaking requires assessment of growth and survival rates and the many processes defining the community composition of a seagrass bed. In addition to the spatial and temporal patterns, these processes include adult-larval interactions, adult competition, macrofaunal-meiofaunal relationships, migration for reproduction, foraging and response to predators or strong physical gradients (Stoner 1980). Clearly, further studies are required to identify which seagrass characteristics are important and at what scales they are evident. Understanding the processes identified above will allow managers to predict the value of seagrass beds, ensure their protection (i.e. protecting the right beds at the right time) and allow sustainable fishing activities. Detailed maps of the seagrass beds will allow consideration of the fact that whereas a particular “type” of bed morphology may benefit one fishery species more than another, greater areal cover of a less-optimal “type” may make it significant when directing conservation effort. The less obvious ways that seagrasses may benefit fisheries also require more study. First, to what extent do seagrass beds form the basis of coastal detritus cycles? Do root systems continue to release detritus and protect other inshore habitats such as salt marshes long after the canopy has been lost to disturbance? Improvements in multiple stable isotope analysis means that trophic pathways can be mapped more accurately. Offshore migrations may obscure direct links but greater understanding of recruitment patterns and the use of electronic tagging will help to identify possible benefits of seagrass beds to commercial fisheries. It is apparent that seagrass beds potentially have a high importance for some fishery species and, whereas some attempts have been made to investigate the economic and environmental benefits of restoring seagrass beds (e.g. Shabmann & Capps 1985, Anderson 1989), further studies assessing the relative advantages of protecting (via seasonal and areal closures), conserving (by the designation of marine protected areas and no-go zones) or restoring seagrass beds (via transplantation techniques) are needed. Finally, although seagrass research tends to be concentrated in particular geographical “hot spots”, latitudinal variation is an important consideration in determining the roles and value of seagrass beds to fisheries. It is clear that future research is needed to identify and quantify the importance of seagrass as a nursery area, refuge and feeding ground for commercially important species in all parts of the world where seagrasses exist. This information needs to be collected using standard sampling methods to enable the true global role of seagrass beds to fishery species to be recognised.

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SELECTIVE TIDAL-STREAM TRANSPORT OF MARINE ANIMALS RICHARD B.FORWARD JR1 & RICHARD A.TANKERSLEY2 1

Duke University Nicholas School of the Environment, Marine Laboratory, 135 Duke Marine Lab Road, Beaufort, North Carolina 28516, USA e-mail: [email protected] 2 Department of Biological Sciences, Florida Institute of Technology, 150 West University Blvd., Melbourne, FL 32901, USA e-mail: [email protected]

Abstract Selective Tidal-Stream Transport (STST) is used by invertebrates and fishes for horizontal movement. In general, animals ascend from the bottom and are carried by tidal currents during one phase of the tide. During slack water, at the end of this tidal phase, they return to the bottom and remain there during the opposite tidal phase. Through this sequence, horizontal movement takes place in a series of saltatory steps. In coastal and estuarine areas, STST can be characterised as ebb- or flood-tide transport depending upon which phase of the tide is used for transport. Modelling studies indicate STST is a highly effective means of horizontal movement for life-history stages that have weak swimming abilities and for energy conservation by adults with strong swimming ability. Frequently, the direction of STST reverses within a species, especially at different physiological or life-cycle stages. For example, larvae of estuarine crabs undergo ebb-tide transport for migration out of estuaries for development offshore, whereas older post-larvae use flood-tide transport for movement up estuaries to nursery areas. The behaviour underlying STST is ascribed to (a) a tidal rhythm in activity or vertical migration or (b) behavioural responses to environmental cues associated with tides. If behavioural responses are involved, then recent studies suggest that no single cue is used for STST but that animals respond to a sequence of cues during transport. Collectively, STST is well documented in the field, but underlying behaviours need future study.

Introduction This review will consider Selective Tidal-Stream Transport (STST), which occurs among animals living from tidal freshwater areas, through estuaries, to coastal and oceanic habitats. Essentially, horizontal transport is accomplished by vertically migrating into and out of the water column synchronously with changes in the direction of tidal currents. The review is organised to consider (a) tides and tidal currents, (b) mathematical models for STST, (c) field studies demonstrating STST, and (d) underlying behaviour. The last two sections will focus specifically on field studies that demonstrate STST and underlying behaviour for both invertebrates and fishes. Field studies that failed to find evidence for STST (e.g. Lyczkowski-Schultz et al. 1990, Koutsikopoulos et al. 1991) will only be included as they contribute to our understanding of underlying mechanisms. Aspects of STST have been considered within overviews of cross-shelf transport of 305

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invertebrate larvae (Shanks 1995) and transport in estuaries (Weinstein 1988). Similarly, reviews of migration by different animals groups, such as fishes (Harden Jones 1968, 1981, Leggett 1977, Arnold 1981, McCleave et al. 1984, McKeown 1984, Norcross & Shaw 1984, Smith 1985, Boehlert & Mundy 1988), penaeid shrimps (Dall et al. 1990) and non-decapod invertebrate larvae in estuaries (Stancyk & Feller 1986) included discussions of STST. Also, the behaviour underlying STST has been considered in reviews of biological rhythms (Neilson & Perry 1990, Gibson 1992) and fish behaviour (Gibson 1997).

Tides and tidal currents In coastal areas, tidal currents oscillate in a pattern of ebb-tide current, slack water as tidal currents reverse direction, flood-tide current, followed again by a period of slack water. As the tide reverses direction, the outer edges of the current outline an ellipse referred to as the tidal ellipse (Shanks 1995). Since the extent of the ebb and flood ellipses are frequently not equal, residual tidal currents are generated in the direction of the longer ellipse. Thus, in coastal areas, animals could be transported horizontally by entering the water column during one phase of the tide and descending to the bottom during the other; thereby using one tidal stream for unidirectional transport. Alternatively, they could remain in the water column and be transported by residual currents (Fig. 1A). Similar tides occur in an estuary, which is an inlet of the sea reaching into a river valley as far as the upper limit of tidal rise, usually being divisible into three sectors; (a) a marine or lower estuary in free connection with the open sea; (b) a middle estuary subjected to strong salt and freshwater mixing; and (c) an upper or fluvial estuary, characterized by fresh water but subjected to daily tidal action (Fairbridge 1980). Due to river inflow, estuaries have a net flow of water to the ocean, which differentially affects the location and properties of tidal currents along the estuary. Flood tides flow into and up an estuary opposing the flow of the river. They are followed by slack water in which there is relatively little horizontal water movement. As tidal currents reverse direction, both the tidal currents and river flow are in the same direction during ebb tide, after which there is again a period of slack water. In estuaries with semi-diurnal and diurnal tides, the times for a complete tidal cycle are about 12.4 h and 24.8 h, respectively. In addition to oscillating with the tidal cycle, the magnitude of tidal currents varies with depth as a consequence of shear (reviewed by Prandle 1982, Soulsby 1983). Although the exact structure of the current velocity profile varies among systems and the phase of the tide, in most areas current velocities are typically strongest near the surface and decrease to zero at the bottom (Fig. 1B). However, the velocity profile is non-linear since shear, or the rate of change in current velocity with depth, is low at locations high in water column but increases significantly near the bottom as a consequence of bottom friction (Fig. 1B). Thus, vertical migration near the bottom has a much greater influence on the rate of horizontal transport than migration over the same distance near the surface. The traditional view of estuaries is that they have a two-layer circulation system, in 306

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Figure 1 A: Typical vertical profile of net current velocities in a partially mixed estuary after subtracting the effect of oscillating tidal currents. B: Idealised tidal current velocity profile during maximum ebb currents. Note the relatively weak shear (change in velocity with depth) in the water column and the sharp increase near the bottom.

which residual tidal currents have a net outflow in the surface layer, net inflow in the bottom layer, and a middle depth where there is no net horizontal flow (depth of no net motion; Fig. 1A). Thus, objects positioned close to the surface will be transported seaward by residual currents. Similarly, objects positioned below the depth of no net motion will be transported shoreward (i.e. up-estuary). Transport by residual currents is slow with speeds being several orders of magnitude slower than maximum current speeds during ebb and flood tides. Swimming speeds of planktonic larvae of invertebrates and vertebrates are two to three orders of magnitude slower than instantaneous current velocities in estuaries and one to two orders of magnitude slower than residual current velocities (Queiroga et al. 1997). Thus, they cannot swim against tidal currents for horizontal movement and must rely on transport by currents moving in an appropriate direction. Large fishes can swim at speeds faster than tidal currents, and thus, could make headway independent of tidal current direction. However, such behaviour is rarely observed and they also have been shown to use tidal currents to facilitate horizontal transport. In areas with tidal currents, there is a continuum in behaviours that could be used for position maintenance or retention and rapid horizontal transport. Retention involves the maintenance of a population or cohort of planktonic larvae within an area over a time period during which they should have been exported. In estuaries, retention usually applies to

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species that remain in an area bounded by an upper and lower salinity. As outlined by Morgan et al. (1997), retention may be the result of 1) a reproductive rate that exceeds loss due to flushing from the estuary (e.g. Ketchum 1954, Gupta et al. 1994), 2) passive accumulation in areas of low current flow (Castel & Veiga 1990, Morgan et al. 1997), 3) active lateral movement to areas of low current flow (Cronin et al. 1962, Wooldridge & Erasmus 1980), or 4) active vertical migration to reduce net horizontal transport. Considering vertical migration, Bosch & Taylor (1973) proposed that retention of the cladoceran Podon polyphemoides in the Chesapeake Bay resulted from a reverse diel vertical migration, in which animals were near the surface during the day and at depth at night. Thus, seaward transport due to residual currents during the day is counteracted by upestuary transport by residual currents at night. This system is plausible but depends on day length (Norcross & Shaw 1984). During the summer seaward transport would exceed upestuary transport and the reverse would occur during the winter. The opposite pattern would occur if animals underwent a typical nocturnal diel vertical migration pattern, in which they ascend during the night and descend during the day (e.g. Rogers 1940). Vertical migration relative to tides can also underlie retention. The copepod Pseudodiaptomus hessei remains in estuarine areas by ascending in the water column during times of slack water and residing near the bottom during the times of strong ebb- and flood-tidal currents (Wooldridge & Erasmus 1980). Alternatively, the most common tidal vertical migration pattern observed among invertebrates and fishes involves an ascent during flood tide and descent Table 1 Retention in estuaries. Species undergoing tidal vertical migration involving an ascent during flood tide and a descent during ebb tide.

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during ebb tide (Table 1). Thus, horizontal transport is reduced because during ebb and flood tides animals migrate to depths where horizontal currents in the water column are the weakest. Animals can further reduce horizontal movements by vertically migrating around the depth of no net motion (Fig. 1A) (Cronin 1982, Fortier & Leggett 1983, Orsi 1986). In the case of larvae of the crab Rhithropanopeus harrisii, an endogenous tidal rhythm in vertical swimming underlies this migration pattern (Cronin & Forward 1979, 1983, Forward & Cronin 1980). Nevertheless, the same vertical migration pattern could lead to up-estuary movement (see Flood-tide transport, p. 310). Accordingly, the copepod Eurytemora affinis seems to adjust its vertical migration pattern depending on its location in the estuary (Hough & Naylor 1991). In high salinity areas, it ascends on flood tides and descends on ebb tides. Alternatively, in low salinity areas it reverses the pattern and ascends on ebb tides and descends on flood tides, which leads to down-estuary movement (see Ebb-tide transport, p. 310). In considering horizontal transport by tidal currents, there is a gradient in behaviour to affect transport. Minimal behaviour is implied by studies indicating larvae are transported as passive particles (e.g. de Wolf 1973, 1974, Boicourt 1982, Seliger et al. 1982, Stancyk & Feller 1986, Bergman et al. 1989). In these cases, larvae act as suspended objects, which are swirled into the water column by ebb- and flood-tide currents and settle during slack water. Transport results from the net effect of these currents. Animals transported by residual tidal currents display slightly more active behaviour. Although there is evidence for the use of residual tidal current in estuaries (e.g. capelin larvae: Fortier & Leggett 1982, 1983; Atlantic herring larvae: Graham 1971, Fortier & Leggett 1982, Henri et al. 1985; tomcod: Laprise & Dodson 1990) and coastal areas (e.g. fiddler crab larvae: Dittel & Epifanio 1982, Epifanio et al. 1988), the phenomenon is perhaps best demonstrated by Bousfield’s (1955) classic study of barnacle larvae in the Mirimichi estuary. Adult Balanus improvisus live at the head of the estuary and release larvae which remain in the plankton for about 18 days. This presents a problem because water in the estuary is exchanged every 7 days. To prevent export to the ocean, larvae undergo an ontogenetic migration, in which early stages have an average depth above the depth of no net motion and later stages reside below this depth. In this way, early stage larvae are slowly transported towards the mouth of the estuary, whereas late stage larvae and post-larvae return to the area of the adult population. Finally, animals can undergo active vertical migrations relative to tidal currents, which result in horizontal transport (Fig. 2). The study of “Selective tidal-stream transport” perhaps began with Creutzberg’s (1958) demonstration that elvers of the eel Anguilla anguilla use tidal currents for horizontal transport into an estuary. Elvers were abundant in the water column during flood tide and on or near the bottom during ebb tide. The actual term Selective Tidal-Stream Transport (STST) was first coined by Greer Walker et al. (1978), who stated “the essential behavioural mechanism would appear to be a semi-diurnal vertical migration, the fish leaving the bottom at slack water to join one tide rather than another and returning to the bottom at the next slack water.” The period length of the vertical migration would be about 12.4 h. Thus, fish would move up into a current stream when the flow is in a “desired” direction and down to the bottom out of the current stream when the tidal currents reverse direction (Fig. 2) (Holt et al. 1989). In this way, vertical movements effect horizontal displacement (Weinstein et al. 1980), which occurs in a saltatory sequence. Although STST can be used to describe transport in coastal areas where animals are migrating in particular compass directions (e.g. North or South), a considerable number of estuarine dependent species use STST for movement within estuaries. Thus, in estuarine and 309

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Figure 2 Diagrammatic representations of typical vertical migratory behaviours resulting in floodtide, ebb-tide or nocturnal flood-tide transport. Animals oscillate between residence in the water column and on/near the bottom at different phases of the tide. The diel cycle and direction and relative magnitude of the tidal currents are depicted in the upper panel. SW is slack water and arrows in the panels indicate direction of transport.

shallow water coastal areas, it is more appropriate to classify STST behaviour as either flood-tide transport or ebb-tide transport. Flood-tide transport is here defined as movement into the water column during flood tide and residence on or near the bottom during ebb tide (Figs 2, 3). This behaviour would promote rapid transport up an estuary or onshore in coastal areas. Alternatively, ebb-tide transport would entail entering the water column during ebb tide and residing on or near the bottom during flood tide (Fig. 2). This behaviour would be useful for export from an estuary and transport offshore. It is worth noting that the pattern of vertical migration exhibited by many estuarine animals for flood-tide transport and for retention (Table 1) is similar. Animals ascend 310

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Figure 3 Mean abundances of crab post-larvae (megalopae) and juveniles collected in plankton samples as a function of time of day and tidal cycle (depicted in the upper panels). (Redrawn from De Vries et al. 1994.)

during flood tide and descend during ebb tide, which leads either to up-estuary movement during flood-tide transport or to horizontal position maintenance during retention. The distinguishing characteristic is that during retention animals remain in the water column moving seaward on ebb tide and up-estuary during flood tide. During flood-tide transport, 311

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the animals are mainly in the water column during flood tide and avoid horizontal movement during ebb tide by descent to the bottom or moving laterally to near-shore areas. Thus, retention and rapid horizontal transport are at opposite ends of a continuum with the degree and rate of transport depending upon the efficiency of position maintenance during ebb tide. In addition, flood-tide transport in coastal and estuarine areas usually involves migration to settlement, nursery, or reproductive areas. Thus, animals have a destination and transport only occurs over a finite number of tidal cycles that are necessary to reach the destination. In contrast, during retention animals remain in the water column over a long period of time.

Numerical models of Selective Tidal-Stream Transport

Models of vertical migration in tidal currents Because tidal currents are the most predictable component of flow in oceans and estuaries, examinations of STST are particularly well suited for the development of numerical models and simulations that investigate the effectiveness of different migration modes in promoting displacement or retention. Although it is intuitive that synchronised vertical migrations into oscillating shear (tidal) currents can bring about long-term unidirectional transport of larvae (e.g. STST), the outcome is less apparent when the vertical migration period and the tidal period are not equal or synchronised. Thus, most studies have attempted to identify other less obvious conditions under which the interaction between common vertical migratory behaviours (e.g. tidal and diel migration) and tidal oscillations of different periods results in net horizontal displacement. The long-term displacement and transport associated with different migratory patterns and the principal tidal constituents (e.g. M2, S2, K1) has been examined by Hill (1991a,b, 1995). When a simple linear tidal velocity shear field and sinusoidal migration pattern was employed, long-term transport was only possible when the period of the migration cycle matched the tidal velocity cycle. Under non-linear tidal shear (e.g. Fig. 1B), long-term horizontal displacement was also possible for migration periods that were multiples of the tidal period (Hill 1991a,b). This synchrony between the period of vertical migration and the tidal period is the basis for STST. When migration and tidal periods differed significantly, for instance a diel vertical migration pattern in semi-diurnal tidal conditions, maximum horizontal displacement was constrained and a horizontal displacement oscillation took place at the “beat period” between the vertical migration and tidal period (Hill 1995). As the migration period approached the tidal period, the maximum displacement and the time between peak displacement increased. This interaction led Hill (1991a,b) to propose possible mechanisms for long-term horizontal transport that occur when diel migrations, with a period of 24 h, are “phased-locked” with the principal solar semi-diurnal tidal constituent (i.e. S2 with a period of 12 h) or when migration and tidal oscillations are not exactly multiples, for instance diel migrations and diurnal tidal currents of the K1 constituent (23.93 h). Such interactions between diel migration and tidal constituents may explain, at least in part, the onshore migration of Penaeus latisulcatus larvae from offshore spawning areas to nursery grounds in Shark Bay, Western Australia during periods of the year when net tidal flow at night is shoreward (Penn 1975). 312

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As detailed below (p. 315), migration patterns associated with STST frequently possess both tidal and diel components, often with peaks in vertical migration occurring during nocturnal flood or ebb tides (Fig. 2). Using the vertical migratory behaviour of the scallop Placopecten magellanicus veligers as a model, Manuel & O’Dor (1997) used Hill’s (1991a) model of tidal currents to examine the horizontal transport resulting from vertical migration in response to both tidal and diel stimuli. Their results indicated that combined tidal/diel vertical migrations are particularly useful for horizontal transport by small zooplankton, such as scallop veligers, that are unable (a) to traverse the entire water column during a tidal period, (b) to swim fast enough to overcome turbulent conditions, and/or (c) to determine their position in the water column. Smith & Stoner (1993) used similar 2D computer models to examine the effect of diel and tidal vertical migration schemes on the long-term net transport of larvae in two tidal channels dominated by semi-diurnal (Exuma Cays of the Bahama Islands) and diurnal tides (Aransas Pass on the Texas Gulf coast). Diel migrations under both tidal conditions resulted in annual cycles in the net transport, making the timing of spawning or recruitment periods within the annual cycle important. However, annual fluctuations in transport were negligible for larvae exhibiting tidal phase vertical migrations at both sites. Thus, for tidally migrating species, horizontal transport remained relatively steady throughout the year and the seasonal timing of behaviours involving STST was not important. However, a more recent study of the interaction between tidal currents and the day-night cycle by Power (1997) revealed long-term seasonal fluctuations in conditions favouring retention or unidirectional transport using STST. Comparisons among 11 sites in the United States indicated that these patterns also vary significantly among locations, thereby establishing regional opportunities for transport or retention.

Coupled behaviour-circulation models The complex hydrodynamics and rapidly changing physical conditions present in estuaries and near-shore areas makes the development of predictive numerical circulation models for the study of larval transport difficult. Even in areas dominated by tidal flow, dominant circulation patterns can be altered significantly on relatively short timescales by wind waves, freshwater inflow and wind stress (reviewed by Crean et al. 1988). In shallow estuaries and areas where water stratification is minimal, two-dimensional vertically-averaged models are adequate and computationally simple. Yet, three-dimensional models are necessary to describe flow in more complex systems, including stratified and partially mixed estuaries, and the exchange between estuaries and oceans near inlets. Although most circulation models can be used to simulate the transport of passive particles, models that incorporate specific biological processes and behaviours, including active swimming and changes in vertical distribution, provide insights into larval transport mechanisms. Coupled behaviour-circulation models are powerful predictive tools and have been used extensively to model larval migration and advection and to examine the interaction between the vertical distribution of larvae (“particles”) and the vertical structure of flow fields in specific systems (e.g. Seabergh 1988, Wang 1988, Bartsch 1993, Werner et al. 1993, Tremblay et al. 1994, Bartsch & Coombs 1997, Garvine et al. 1997, Hare et al. 1999). Most models, however, have focused on the interaction between long-term (e.g. ontogenetic) changes in water-column position and/or physical processes and vertical gradients that occur 313

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at subtidal frequencies (e.g. wind and buoyancy driven processes). Attempts to model the effects of higher frequency circulation processes (e.g. vertical shear and oscillations in tidal currents) on the transport of particles that exhibit vertical migrations synchronised with the tides (i.e. STST) have been limited. The first computer simulations of STST were conducted by Arnold & Cook (1984), who used two-dimensional models to predict the routes of migrating plaice from feeding grounds to spawning areas in the North Sea and silver European eels crossing the European shelf to the Sargasso Sea. Simulations indicated that migrating plaice exhibiting a semidiurnal migration (STST) would be transported south along a common stream-path to known spawning areas in the eastern and western English Channel. Similarly, if plaice used STST for leaving the spawning area, most were predicted to travel along the western side of the Southern Bight into the central North Sea. When exhibiting diel vertical movements in feeding and spawning areas, long-term horizontal transport was minimal and plaice remained within a relatively confined area despite the presence of strong tidal currents. Similar modelled tracks of migrating eels indicated that it would take between 40–100 days for most eels to reach the edge of the shelf using STST. However, the effectiveness of STST as migratory strategy may vary among starting locations, since the simulated tracks of eels leaving some areas indicated they may fail to reach the edge of the continental shelf in time to complete the oceanic phase of their migration (Arnold & Cook 1984). More recently, Churchill et al. (1999a,b) and Luettich et al. (1999) used drifter tracks and CTD observations coupled with a numerical hydrodynamic model of an estuary inlet to characterise the flow structure within the estuary and adjoining shelf and to determine the possible impact of vertical migratory behaviour (flood-tide transport) on the ingress of fish larvae through the inlet and within the estuary. Both simulated and actual drifter tracks indicated that currents moving through the inlet are dominated by tidal flows that produce a near-shore jet that carries a narrow coastal zone of water into the estuary. Thus, the location of larvae relative to the near-shore jet may influence their chances of being transported through the inlet on flood tides. Water flowing through the inlet split and followed well defined paths once in the estuary. Modelled flood-tide flow patterns were also consistent with the spatial-temporal distribution and abundances of flood-tide migrating fish larvae collected simultaneously at locations across the inlet and within the estuary (Forward et al. 1999b). These results indicate that coupled models of current flow and vertical migratory behaviours hold considerable promise as tools for explaining patterns of larval transport and ingress, identifying dominant transport pathways, and evaluating the effects of estuarine hydrodynamics on the delivery (i.e. “supply”) of larvae to critical nursery habitats or spawning areas.

Models of migration energetics One potential advantage of STST is a significant saving in the energy required for migration (Harden Jones 1980). Using a numerical model of the energetics of fish migration and swimming, Weihs (1978) compared the energy required for migration using steady swimming and swimming only when the tide is in their direction of migration. The results indicated that energy savings from STST can be as large 90% when tidal currents are larger than the optimum swimming speeds. For faster swimming adult fish, significant energy savings were 314

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only possible when STST was combined with active swimming in the direction of transport. However, STST did not always result in energy savings. When both current speeds and swimming speeds were low, energetic savings gained by STST were less than the cost incurred during the “resting phase” of migration. Metcalfe et al. (1990) corroborated the results of Wiehs’ (1978) model using empirical data from acoustic tagging studies of adult plaice (Pleuronectes platessa) in the southern North Sea. Net swimming speeds of fish were used to estimate oxygen consumption during midwater excursions and were compared with estimates of the cost of covering the same distance by swimming continuously without the assistance of tidal currents. The results indicated that STST reduces the cost of migration by 20% compared with constant swimming at optimum speeds. Yet, as predicted by Weihs’ energetic model, when tidal currents were slow relative to swimming speed (<0.2 m s-1), continuous swimming was more efficient, especially for large plaice.

Field studies of Selective Tidal-Stream Transport Field studies of STST consist of relating tidal phase to (a) the abundance of groups of animals over time at one depth in the water column, (b) the abundance of groups of animals at multiple depths in the water column over time, and (c) the horizontal and vertical movements of individuals over time using acoustic tracking devices. The underlying assumption is that animals ascend for transport by tidal currents and descend to be on or near the bottom to reduce horizontal movement. Thus, the time of peak abundance at the shallowest depth is interpreted as the time of greatest horizontal transport. However, STST would also occur if animals were on or near the bottom during one phase of the tide and distributed above the bottom boundary layer during the other phase. During residence in the water column, animals can either move passively with the currents (e.g. Stasko 1975, Parker & McCleave 1997) or they can increase their ground speed by actively swimming with the current (e.g. Moore et al. 1995). Actual residence on or near the bottom to avoid or reduce horizontal movements is rarely verified and has perhaps best been demonstrated by acoustic tracking of adult fishes. For example, cod appear to swim close to the bottom at time of the descent (Arnold et al. 1994) and plaice actually rest on the bottom (Greer Walker et al. 1978). Alternatively, in estuaries, it has been suggested that animals could move laterally to the sides of estuaries where tidal flow is reduced in order to reduce transport by tidal currents. Distribution studies indicate some species undergo lateral movements (Fore & Baxter 1972, Sheldon & McCleave 1985, Raynie & Shaw 1994) but other studies have failed to find evidence for the formation of aggregations near the side of estuaries to prevent transport (Melville Smith et al. 1981, Holt et al. 1989).

Detection and analysis of Selective Tidal-Stream Transport Although the STST behaviours of individuals have been documented using acoustic tracking techniques (e.g. Greer Walker et al. 1978, Arnold et al. 1994) and sonar (e.g. Voglis & Cook 1966), STST is most often inferred from the movements of groups of animals using plankton or trawl samples taken throughout the water column at regular 315

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intervals. As with any periodic signal in a time series, detection of STST requires that sampling occur at appropriate temporal scales. For example, to detect tidally timed migrations associated with STST, a minimum of four samples per tidal cycle (every 3 h for migrations synchronised to the semi-diurnal tidal constituent) for several days are needed to adequately represent the pattern and avoid aliasing and bias (see Fig. 3 for representative results; Platt & Denman 1975, Kelly 1976, Manuel & O’Dor 1997). If vertical migration occurs at tidal periods but ascents during the appropriate phase of the tide (ebb or flood) are brief, then detection may require more intensive sampling. Similarly, shorter sample intervals are needed to differentiate among migration patterns with similar period lengths, such as a diel migratory pattern and one possessing both tidal and diel components (e.g. vertical migration during nocturnal flood tides). Tidal/diel migration patterns can also be misinterpreted to be diel patterns if the tidal signal is obscured by averaging or pooling samples over several days or if different sites are sampled sequentially (Platt & Denman 1975, Manuel & O’Dor 1997). Detection of STST behaviours is also possible with longer time series and less frequent sampling. When two signals with different periods are added together, the resulting time series contains secondary peaks that occur at a frequency that reflects the difference between the two periods (Manuel & O’Dor 1997). For example, as a consequence of the aliasing of the tidal and solar cycles, the phase of the tide shifts about 0.84 h each day. When samples are collected daily, vertical migrations with tidal periods will appear as a periodic daily shift in depth with a period of 14.8 days. An inherent problem with the detection and verification of STST behaviours from field collections is the lack of standard statistical methods for testing hypotheses. Thus, studies of migration and transport mechanisms have often been criticised for lacking statistical rigour (reviewed by Colby 1988). Most conventional statistical tests, such as analysis of variance, are not appropriate since sampling methods and protocols traditionally used to document the distribution and migration of plankton and nekton violate one or more of the underlying assumptions of parametric methods. Consequently, statistics are often applied without adequate verification of the underlying assumptions or conclusions regarding STST behaviours are inferred from patterns without the benefit of statistical confirmation (reviewed by McCleave et al. 1987). Since most sampling protocols result in the temporal or spatial sequences of data, nonlinear and time series methods, including autocorrelation, cross-correlation, spectral analyses and non-linear regression are well suited for verifying and describing patterns in observational data, including detecting rhythmicity (e.g. tidal and diel) in migratory behaviour and determining the phase relationship between abundance patterns and the tidal currents or other tidally influenced variables (temperature, salinity, pressure) (Platt & Denman 1975, Broom 1979, Chatfiled 1989). As outlined by Colby (1988), models of migratory behaviour, including stochastic models, advection-diffusion models and physical models, can be used to described the expected distribution of animals in the water column and to formulate null hypothesis upon which empirical measurements of larval density and currents can be tested. Other non-standard statistical methods may also be useful for providing statistical confirmation of STST. Using the STST behaviour of glass eels of the American eel (Anguilla rostrata) as a model, McCleave et al. (1987) developed a series of methods using chi-square goodness-of-fit analyses of observed and expected catches and non-parametric (Spearmans’ rank) correlation analysis for testing specific hypotheses regarding animal density in relation to depth, currents and tide. Other categorical analyses, 316

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such as logistic regression, can also be used to examine vertical distributions and the influence of light and tidal cues on migratory behaviour (Hosmer & Lemeshow 1989; for examples see De Vries et al. 1994, Garrison 1999).

Field studies of ebb-tide transport of invertebrates Most of the studies of ebb-tide transport of invertebrates have focused on crustaceans, especially brachyuran crabs and other decapods. In the life cycle of most brachyurans, fertilised eggs are attached to pleopods located on the ventral side of the female’s abdomen and are carried for a period of days to months before larvae are released. Actual larval release occurs over a few seconds to minutes and is precisely timed with respect to lunar phase, light:dark (L:D) cycle and/or tide cycle (reviewed by Forward 1987a, Morgan 1995). Population rhythms related to the lunar cycle are usually semilunar (14.5 day cycle) and larvae are most often released around the time of spring tides at the new and full moon. However, studies (Christy 1978, 1986) at locations where spring tides occurred at the quarter phases of the moon led Christy (1982) to propose that semi-lunar rhythms in larval release are cued to the time in the lunar cycle of the largest amplitude nocturnal ebb tides. As such, larval release is timed to maximise the rate of ebb-tide transport. Most brachyurans release larvae near their home site. However, in the case of the blue crab Callinectes sapidus (Table 2) adult females undergo ebb transport and migrate to the spawning site (Tankersley et al. 1998). In preparation for spawning, females aggregate near the entrance to estuaries where they incubate attached eggs. Shortly before larval release, they migrate to the surface during ebb tides at night and are transported passively seaward where they release their larvae in coastal areas. On subsequent nights, females with remnants of eggs attached to their pleopods are observed being transported back into the estuary on flood tides (Tankersley et al. 1998). Thus, the spawning migration involves both ebb- and flood-tide transport of adult females. Although laboratory studies indicate coastal and estuarine brachyuran species release larvae around the time of high tide (Forward 1987a), field studies of larval abundance (Table 2) also provide indirect evidence of the relationship between the time of egg hatching and STST of newly released larvae. In all studies to date, the first larval stage (Stage I zoea) becomes abundant in the water column near the time of slack water after flood tide or at the beginning of ebb tide. The same pattern of larval release has been observed among anomuran and caridean crustaceans (Table 2). The relationship between time of crustacean larval release and the L:D cycle is mixed. In most cases, larvae are released at night but there are studies that also show larvae entering the water column during the day (Table 2). The inconsistent relationship may result from larval release occurring around the time of slack water after flood tide. If this time is close to sunrise, larvae will be abundant during ebb tide during the day. Thus, the most consistent times of larval release are at night around the time of slack water after flood tide. The convergence of times by different species suggests there are shared functional advantages (Forward 1987a). Concentrating larval release into a small time interval would tend to swamp potential predators and release at night would reduce vulnerability to visual predators. Most of the species listed in Table 2 live as adults in estuaries or shallow coastal areas but undergo larval development in coastal waters. The release of 317

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Table 2 Ebb-tide transport of invertebrates. Day/Night indicates whether transport took place during the day and/or night phase. Unknown indicates that transport was only measured during either the day or night.

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larvae around the time of slack water after flood tide would lead to rapid transport seaward away from the adult habitat. Release at night or the beginning of the day would initially expose larvae to lower temperatures. Finally, many species successfully develop in coastal water because larvae are unable to tolerate low salinity water encountered in estuaries (e.g. Costlow & Bookhout 1959). By releasing larvae around the time of slack water after flood tide, larvae would be initially transported seaward in water at the highest salinity available at the adult habitat. A further consideration for estuarine species is whether young larvae undergo tidal vertical migration to assist in ebb-tide transport or just move as passive particles that are rapidly advected seaward because they have limited swimming ability and enter the water column at the beginning of ebb tide. The predicted vertical migration pattern would be residence in the water column during ebb tide and in the bottom boundary layer during flood tide. Lochmann et al. (1995) found no evidence for vertical migration of Callinectes sapidus larvae relative to tides. Alternatively, Queiroga et al. (1997) reported that Stage I zoeae of Carcinus maenas undergo tidal vertical migrations in which they are higher in the water column during ebb tide and lower during flood tides in an estuary. Their calculations indicated that this pattern resulted in movement down the estuary at a velocity that exceeded the vertically integrated water velocity. Similarly, Brookins & Epifanio (1985) found that near the adult habitat in an estuary fiddler crab zoeae were near the surface during ebb tide and deeper during flood tide. Alternatively, Epifanio et al. (1988) found the opposite vertical migration pattern when sampling at the mouth of the estuary. Thus, in some cases larvae have an active tidal vertical migration pattern that would promote seaward transport. The differences between studies may result from the degree of mixing in different estuaries (Lochmann et al. 1995) and study site location. In coastal areas, juveniles of the bivalve mollusc Macoma balthica use ebb-tide transport for horizontal movement (Beukema & de Vlas 1989). Juveniles undergo tidal vertical migration because they are abundant in the water column during ebb tide but are present in lower numbers during flood tide. This migration pattern results in transport from the Wadden Sea to the North Sea.

Field studies of flood-tide transport of invertebrates As with studies of ebb-tide transport, field investigations of flood-tide transport have focused on crustaceans. If adult populations occur in estuaries or shallow water coastal areas and larval development occurs in coastal/offshore areas, then larvae, post-larvae, and/or juveniles must be transported back to adult habitats. Transport across the continental shelf usually involves non-tidal mechanisms, which have been reviewed elsewhere (e.g. Epifanio 1988, Shanks 1995). However, post-larvae of the crab Carcinus maenas (Zeng & Naylor 1996b) and larvae of the polychaete Pectinaria koreni (Thiebaut et al. 1996) undergo flood-tide transport for movement shoreward in coastal areas to non-estuarine habitats (Table 3). During transport, both species were most abundant in the water column during flood tides. Transport of Carcinus maenas post-larvae occurred at night while the polychaete larvae were transported on both nocturnal and diurnal flood tides. For estuarine dependent species of brachyuran and anomuran crustaceans, older larvae, post-larvae, and juveniles move up the estuary to nursery and adults habitats primarily by means of flood-tide transport (Table 3). The consistent pattern is for animals to be abundant 319

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Table 3 Flood-tide transport of invertebrates. Day/Night indicates whether transport took place during the day and/or night phase. Unknown indicates that transport was only measured during either the day or night.

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Table 3 continued

in the water column during flood tide and absent or at reduced levels during ebb tide (Fig. 2). Late stage larvae undergo flood-tide transport during both the day and night, whereas post-larvae and juveniles are consistently transported only at night (see Fig. 3 for sample results). This relationship suggests that post-larvae and juveniles avoid well-lit areas of the water column during the day because their relatively large size increases their vulnerability to visual predators. The life cycle of many peneaid shrimp species is slightly different from other crustaceans (reviewed by Dall et al. 1990). Spawning and larval development take place on the continental shelf (Wickens 1976) and post-larvae migrate to nursery areas in estuaries. Post-larvae undergo flood-tide transport at night (Table 3) for movement up the estuary. Juveniles remain in the estuary several months and then migrate seaward by means of ebb-tide transport at night (Table 2). Among other invertebrates, Wood & Hargis’s (1971) study of the transport of oyster larvae (Crassostrea virginica) provided a direct test of whether larvae are transported as passive particles during STST or whether active behaviour is involved (reviewed by Kennedy 1996). 321

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Wood & Hargis (1971) simultaneously measured the abundance of oyster larvae and coal particles that had the same density as oyster larvae. The oyster larvae clearly displayed floodtide transport because they were abundant in the water column during flood tide and very scarce during ebb tide, which agreed with earlier studies (Carriker 1951, Kunkle 1957, Haskins 1964). Since the abundance of coal particles over time was very different, Wood & Hargis (1971) concluded that flood-tide transport resulted from active behaviour by the larvae. A later detailed study by Anderson (1983) found that oyster larvae were more abundant in the water column from mid-flood to mid-ebb tide with a peak around the time of high slack.

Field studies in offshore areas—adult fishes Collectively, STST is common among adult, juvenile, and larval fishes and is exhibited by members of several unrelated groups. STST among adult fishes in offshore areas (Table 4) is identified by vertical movements relative to tidal currents that result in transport in a particular compass direction that is neither onshore nor into an estuary. Migrations by plaice (Pleuronectes platessa) are perhaps the best studied. During the summer they are abundant on their feeding grounds, such as south of Dogger Bank in the North Sea. In autumn, mature fish migrate south and spawn in the Southern Bight and English Channel mainly during January and February (e.g. Harden Jones 1968, Houghton & Harding 1976, Harding et al. 1978, Arnold 1981, Cushing 1990). After spawning, fish migrate back to the northern feeding areas in late winter and early summer. Trawl data (de Veen 1978, Harden Jones et al. 1979, Arnold & Metcalfe 1995), and studies of individual fish fitted with acoustic tags (Greer Walker et al. 1978, Metcalfe et al. 1990, 1992), indicated fish ascend from the bottom at the beginning of the appropriate tide, move with the current and then descend back to the bottom at slack water. The appropriate phase of the tide for swimming changes as the fish move north and south. Other species (Table 4) that use STST for seasonal migrations in offshore areas include the sole (Solea solea), which migrates offshore in autumn after spawning and onshore in the spring (de Veen 1967, 1978, Greer Walker et al. 1980, Greer Walker & Emerson 1990). Also acoustic tracking of cod (Gadus morhua) by Arnold et al. (1994) indicated individuals undergo vertical movement relative to tidal currents that could facilitate their migration between feeding grounds in the North Sea and winter spawning grounds in the Southern Bight and eastern English Channel (Daan 1978). Finally, the Atlantic mackerel (Scomber scombrus) appears to undergo STST during its pre-spawning migration into the Gulf of St Lawrence (Castonguay & Gilbert 1995).

Field studies in estuaries—adult fishes The life cycle of catadromous fish species, such as the eels Anguilla rostrata and A. anguilla is well known (e.g. Harden Jones 1968). Adults spend most of their time in low salinity areas of estuaries as yellow eels. They undertake a spawning migration as silver eels in which they migrate out of estuaries and spawn in the Sargasso Sea. Leptocephalus larvae develop at sea, after which elvers or glass eels return to coastal areas where they migrate to the head of estuaries and grow and develop into adults. STST is involved in each lifehistory stage within estuaries. 322

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Table 4 Transport of adult fishes. Day/Night indicates whether transport took place during the day and/or night phase. Unknown indicates that transport was only measured during either the day or night. Taxonomy follows Nelson (1984).

Ultrasonic telemetry studies indicate yellow eels use STST during their movements around their home range (Parker & McCleave 1997). When experimentally displaced downstream, they do not swim directly back to the home site but undergo flood-tide transport during both the day and night to return (Parker 1995, Parker & McCleave 1997, Barbin 1998). Alternatively if displaced upstream, they use ebb-tide transport at night for movement back to the home site. During their spawning migration, silver eels utilise ebb-tide transport mainly at night (Parker & McCleave 1997) for movement down the estuary to the ocean. After development in the ocean, glass eels of other Anguilla species migrate up estuaries to the adult home sites by means of flood-tide transport (Table 5). Anadromous species, such as salmon, sea trout and steelhead trout, spend most of their adult lives in sea water, migrate to fresh water to spawn, and return to the ocean as juveniles or smolts. Complete details of the life cycle and orientation during the different phases have been reviewed elsewhere (e.g. Hasler 1966, 1971, Harden Jones 1968). During this life 323

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Table 5 Transport of post-larval and juveniles fishes. Day/Night indicates whether transport took place during the day and/or night phase. Unknown indicates that transport was only measured during either the day or night. Phylogenetic classification precedes the species.

cycle, STST is involved in the up-estuary movements of adults (Table 4) and seaward migration of the smolts (Table 5). Up-estuary spawning migration of adult Atlantic salmon (Salmo solar, Stasko 1975) and sockeye salmon (Onchrohynchus nerka, Levy & Cadenhead 1995) involves flood-tide transport in which adults move with flood currents but hold their position near the bottom during ebb tides. Similarly, spawning migrations of rainbow smelt (Osmerus mordax) in an estuary also involves flood-tide transport (Murawski et al. 1980). Seaward movement of post-smolts of Atlantic salmon (Moore et al. 1995, 1998a, Lacroix & McCurdy 1996) and sea trout smolts (Salmo trutta) (Moore et al. 1998b) involves ebb-tide transport (Table 5).

Field studies in estuaries and bays—fish larvae and post-larvae Many fish species spawn in offshore or coastal areas and have nursery areas in bays and/or estuaries. Although transport of larvae shoreward from the spawning site depends on coastal processes (Boehlert & Mundy 1988, Shanks 1995), the larvae and post-larvae of many species (Tables 5, 6) use flood-tide transport for movement up the estuary. Transport during the day or night varies among species but is consistent among various life-history stages within a species. Vertical movements necessary for horizontal transport by tidal currents depend on the swimming ability of fish larvae (Boehlert & Mundy 1988). For example, yolksac larvae of the weakfish do not undergo flood-tide transport in an estuary but this 324

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Table 6 Flood-tide transport of larval fishes. Day/Night indicates whether transport took place during the day and/or night phase. Unknown indicates that transport was only measured during either the day or night. Phylogenetic classification precedes the species.

behaviour is evident in stronger swimming, older non-yolksac larvae (Rowe & Epifanio 1994a,b). Similarly, a demonstration of flood-tide transport may depend on current flows at the sampling location in the estuary. For example, flood-tide transport of larvae of seven fish species was not apparent at the inlet to an estuary but was clearly present 1 km inside the estuary (Forward et al. 1999b). Currents at the inlet probably prevented larvae from successfully undertaking tidal vertical migrations.

Semi-lunar/lunar cycle in Selective Tidal-Stream Transport Since STST functions for horizontal movement, it is logical that greater transport should occur at times of the strongest tidal currents during spring tides. Thus, there may be a semi-lunar 325

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or lunar cycle in STST. However, evidence for such a cycle is mixed and is usually assessed by relating the relative abundance of animals migrating or number settling after STST to the neap/spring cycle in tidal amplitude. Brachyuran crabs release their larvae to take advantage of ebb tides for transport out of an estuary or offshore (Table 2). Population rhythms related to the lunar cycle are usually semi-lunar (14.5 day cycle) with larvae most often released around the time of spring tides at the new and full moon. However, studies (Christy 1978, 1986) at locations where spring tides occur at the quarter phases of the moon indicate that larval release switches to the quarter phases of the moon. This led Christy (1982) to propose that semilunar rhythms in larval release are cued or synchronised to the time in the lunar cycle of the largest amplitude nocturnal ebb tides. Alternatively, Queiroga et al. (1994) and Paula (1989) found that the crab Carcinus meanas released larvae during neap high tides. They proposed that larval release was related to the time in the day-night cycle of high tide rather than tidal amplitude. Flood-tide transport to settlement sites of post-larval blue crabs (van Montfrans et al. 1990, Mense et al. 1995, Metcalfe et al. 1995) and yellowfin bream (Pollock et al. 1983) in estuaries and Japanese flounder larvae (Tanaka et al. 1989a,b) and lobster post-larvae (Acosta et al. 1997) in coastal areas is greater during spring tides. However, the number of larvae migrating from coastal areas into an estuary by flood-tide transport depends upon the number that arrive at the entrance to the estuary. Since the abundance of animals often depends upon other non-tidal factors, such as weather events, there are cases described for blue crab postlarvae (e.g. Goodrich et al. 1989, Little & Epifanio 1991, Morgan et al. 1996) and stone flounder larvae (Yamashita et al. 1996) where settlement is related to wind events and not the spring/neap tidal cycle. For other species, such as Australian eels, flood-tide transport of glass eels is unrelated to the lunar cycle (Jellyman 1977).

Behaviour underlying Selective Tidal-Stream Transport For species that undergo larval development in offshore and coastal areas but have their nursery area or adult habitat in estuaries, there are two phases to horizontal migration. First, there is onshore transport, which usually involves non-tidal processes and second, STST is used for movement within an estuary (Boehlert & Mundy 1988). Thus, there is a dramatic change in behaviour between offshore and estuarine areas and it is hypothesised that this change is evoked by chemical cues (Forward & Rittschof 1994, Forward et al. 1996a). Larval development of the blue crab, Callinectes sapidus takes place in offshore areas (e.g. Epifanio et al. 1984, McConaugha 1988) and up-estuary movement by post-larvae to settlement sites is accomplished by flood-tide transport (Table 3, p. 320). When tested in an apparatus that mimics the underwater angular light distribution, photoresponses of blue crab post-larvae are different in estuarine and offshore waters at the same salinity. In a vertical column, post-larvae were distributed near the bottom in estuarine water and near the surface in offshore water (Forward & Rittschof 1994). These responses agree with the observed field distribution because post-larvae are near the surface during the day in offshore areas and near the bottom during the day in estuaries (e.g. De Vries et al. 1994). Atlantic menhaden (Brevoortia tyrannus) spawn offshore, develop during shoreward transport and use flood-tide transport during the night for movement up estuaries to nursery 326

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areas (Lewis & Wilkens 1971, Forward et al. 1999b). When tested in an apparatus that simulates the underwater angular light distribution, older larvae that undergo flood-tide transport swam near the surface in offshore water and low in a water column in estuarine water (Forward et al. 1996a). Thus, both blue crab post-larvae and Atlantic menhaden larvae have different behavioural responses in offshore and estuarine waters at the same salinity. The chemical cue(s) for distinguishing between offshore and estuarine water is unknown but may be humic acids (Forward et al. 1997b). Estuarine humic acids are attractive as an estuarine specific chemical cue because they enter estuaries through freshwater inflow but precipitate as the salinity increases. Recent studies indicate that they mimic the effects of estuarine water on metamorphosis in blue crab post-larvae (Forward et al. 1997b). Most studies that consider behaviour involved in STST in estuaries have dealt with the developmental stages of species that undergo flood-tide transport. Field studies indicate that these species are on or near the bottom during ebb tide, ascend during flood tide, and return to the bottom around the time of slack water after flood tide. Although Miller (1988) proposed that this sequence may result from density changes in the water over a tidal cycle, most studies indicate active behaviour is involved. The different phases of flood-tide transport include (a) an ascent during flood tide, (b) depth maintenance in the water column during flood tide, (c) a descent back to the bottom near the time of slack water after flood tide and (d) depth maintenance on or near the bottom during ebb tide. McCleave & Kleckner (1982) discuss the problems involved in each of these phases. The underlying behaviour is usually attributed to an endogenous rhythm in activity or vertical migration or responses to environmental cues that change with tidal phase. Although the two sets of mechanisms are usually considered separate, they are not mutually exclusive.

Endogenous rhythms Boehlert & Mundy (1988) considered recruitment of fishes to estuaries and concluded that an endogenous rhythm in activity and/or vertical migration could underlie STST. For example, during flood-tide transport, animals were observed in the water column during flood tide and on or near the bottom during ebb tide. This pattern could result if the animal was active or swam upward during flood tide. At slack water after flood tide, the animal could swim downward or become inactive and sink to the bottom, remaining there during ebb tide. Endogenous rhythms associated with tides are well known among marine animals (e.g. DeCoursey 1976, Gibson 1978, 1982, 1997, Naylor 1985, Palmer 1995) and are reported in some fishes that under go STST (Gibson 1973, 1976, 1982). The involvement of endogenous rhythms in STST is perhaps best assessed by collecting animals that are undergoing STST and immediately measuring either activity or changes in vertical distribution patterns over time under constant conditions in the laboratory. Among coastal-estuarine invertebrates, Carcinus maenas is the only species studied. The first larval stage (Stage I zoea) undergoes ebb-tide transport, in which it is abundant in the water column during ebb tides at night in an estuary (Queiroga et al. 1994, 1997) and at both day and night in a coastal area (Zeng & Naylor 1996a). First stage zoeae collected from the coastal area have a circatidal rhythm in vertical migration, in which they ascend in synchrony with ebb tides at the collection site and descend during the time of expected flood tides. The period length of this activity pattern is about 12.4 h. (Zeng & Naylor 1996a). 327

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The rhythm is also present in larvae released in the laboratory (Zeng & Naylor 1996c,d). In contrast, the post-larval or megalopa stage undergoes flood-tide transport for onshore movement and is abundant in the water column during flood tides primarily at night (Queiroga et al. 1994, Zeng & Naylor 1996b). Field collected megalopae have a circatidal rhythm in vertical migration similar to that of Stage I zoeae, in which they ascend during the expected time of ebb tide in the field and are near the bottom during the expected time of flood tide. The period length is about 12.4 h, indicating there are two episodes of vertical migration per lunar day. Considering species restricted to estuaries as adults, fiddler crab post-larvae undergo flood-tide transport during up-estuarine movement (Uca sp., Table 3, p. 320). If collected as they enter an estuary, they have a circatidal rhythm in vertical migration, in which they ascend during the time of flood tide with a peak around the time of slack water after flood tide at the collection site (Tankersley & Forward 1994). The period length average is 12.28 h. The presence of the rhythms was predicted because post-larval abundance during floodtide transport was not related to changes in environmental factors (De Vries et al. 1994). This field study found that post-larvae were maximally abundant in the water column during the last half of flood tide before slack water (De Vries et al. 1994), which agrees with the endogenous cycle in vertical migration. The shrimp Penaeus duorarum undergoes flood-tide transport during the post-larval stage for movement up the estuary and ebb-tide transport as juveniles move out of the estuary (Tables 2, 3, pp. 318 and 320). When maintained under constant conditions in the laboratory and exposed to current flow, post-larvae swim upstream during the time of flood tide in the field and downstream during time of ebb tide in the field (Hughes 1972). There is no circadian periodicity even though flood-tide transport only occurs at night (Table 3). An endogenous rhythm related to tides was suggested by Hughes’ (1969b) initial study of swimming by juvenile P. duorarum in currents in the presence of a L:D cycle. When tested under constant conditions, juveniles swam downstream at the time of ebb tide in the field and had a low level of upstream swimming during the time of flood tide. However, the pattern depended on when they were collected in the lunar month (Hughes 1972). There was also a diel component as swimming was reduced during the time of day, which agrees with field observations indicating that ebb-tide transport occurs at night (Table 2). Post-larvae of the blue crab Callinectes sapidus undergo flood-tide transport for upestuary movement (Table 2). If post-larvae are collected during flood-tide transport, they have a circadian rhythm in vertical migration, in which they ascend during the time of day and descend during the time of night (Tankersley & Forward 1994). This rhythm is similar for post-larvae collected in different estuaries and offshore. A tidal rhythm could not be induced by step changes in salinity, salinity cycles or exposure to settlement substratum (Forward et al. 1997a). Thus, in the case of the blue crab, the observed endogenous rhythm in vertical migration does not underlie STST. Among the fishes, spot (Leiostomus xanthurus), pinfish (Lagodon rhomboides), southern flounder (Paralichthys lethostigma) and summer founder (Paralichthys dentatus) larvae undergo flood-tide transport in estuaries, in which they are abundant in the water column during flood tide at night (Burke et al. 1998, Forward et al. 1998). If collected during flood-tide transport, larvae of all of these species had a circatidal rhythm, in which they were active during the time of expected ebb tide in the field and inactive during the time of flood tide (Burke et al. 1998, Forward et al. 1998). Since average period lengths ranged from 12.2 h to 12.4h, there were two peaks per lunar day. Thus, the timing of 328

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activity was opposite from that predicted for flood-tide transport and there was no endogenous diel component. Juveniles (glass eels) of Anguilla rostrata also use flood-tide transport for migration to the head of estuaries (Table 5, p. 324). If collected in tidal fresh water and salinity stratified areas of estuaries, glass eels display a circatidal rhythm in activity, in which they are maximally active during the time of ebb tide in the field (McCleave & Wippelhauser 1987, Wippelhauser & McCleave 1988). There are two activity bouts per lunar day and no apparent diel component. Nevertheless, glass eels collected from non-tidal freshwater areas lack a circatidal rhythm (McCleave & Wippelhauser 1987, Wippelhauser & McCleave 1988). In contrast, Atlantic menhaden (Brevoortia tyrannus) larvae undergo flood-tide transport for up-estuary movement. They are abundant in the water column during flood tides at night (Lewis & Wilkens 1971, Forward et al. 1999b). Under constant conditions in the laboratory, larvae caught during STST have a circadian rhythm, in which they are active at the time of night in the field (Forward et al. 1996b). This rhythm could underlie diel vertical migration in offshore and estuarine areas (Forward et al. 1999a) and regulate the general time in the L:D cycle when larvae are active. However, there is no evidence that larvae develop a tidal rhythm that could contribute to STST in estuarine areas. Collectively, there are similarities between the results of rhythm studies with invertebrates and fishes. Clearly, some animals undergoing STST have tidal rhythms in activity and vertical migration that are synchronised to local tidal times because the timing of the rhythms shifts with local tidal regimes. Entrainment cues are unstudied and could be tidal cycles in pressure, salinity, and/or temperature (Naylor 1985, Palmer 1995). In most cases, STST has a diel component in the field, in which animals are only transported during either the day or night phase of the appropriate tide (e.g. flood tide at night). However, when placed under constant conditions in the laboratory, there are usually two activity or vertical migration bouts per lunar day and little or no relationship to the L:D cycle. Only juvenile Penaeus duorarum have been shown to have a diel component to the rhythm, in which they are active at the time of ebb tide at night in the field (Hughes 1972). Since STST of the other species considered above occurs at night, transport during the appropriate tide during the day is probably inhibited by light. The relationship between the timing of activity and vertical migration under constant conditions in the laboratory and the time of STST in the field is problematic. On the one hand, the time of activity of fiddler crab post-larvae (Tankersley & Forward 1994), pink shrimp juveniles (Hughes 1972), and Stage I zoeae of Carcinus maenus (Zeng & Naylor 1996a) corresponded to the time of STST in the field. However, in all of the other studies (McCleave & Wippelhauser 1987, Wippelhauser & McCleave 1988, Zeng & Naylor 1996b, Burke et al. 1998, Forward et al. 1998), circatidal activity peaks occur during the time of ebb tide in the field. This timing is inconsistent with the flood-tide transport, which predicts animals should be active during the time of flood tide. Three possible explanations have been proposed for the lack of apparent agreement between the timing of STST and the circatidal rhythm. First, collection and laboratory manipulations altered the timing (phase shifted) of the rhythm (Wippelhauser & McCleave 1988, Tankersley & Forward 1994). Second, the rhythm in activity is not related to STST but rather functions to prevent animals from being stranded in the intertidal zone (Gibson 1973, 1976, Zeng & Naylor 1996b). Third, increased activity could represent the behaviour necessary to remain low in the water column or to move laterally away from the main stream towards the edge of estuaries to prevent advection by ebb tides during STST (Burke et al. 1998, Forward et al. 1998). A 329

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reduction in depth and position maintenance activity during flood tide would permit animals to be passively transported by flood-tide currents. If the latter explanation is correct, then the interpretation of the relationship between activity and STST needs to be revised. In this case, position maintenance would require an increase in activity and transport would result when animals become inactive and are passively transported with a tidal currents.

Behavioural responses to environmental cues Behaviour involved in STST in estuaries and shallow coastal areas will be considered because recent studies provide information about which environmental cues are important and the behavioural responses to these cues. The problems associated with cues in the open ocean have recently been considered by Metcalfe et al. (1993) and Arnold et al. (1994). Suggested cues/mechanisms in the open ocean, which will not be considered below, include visual landmarks on the bottom (Arnold et al. 1994), an inertial guidance system (e.g. Harden Jones 1984a,b), magnetic compass (reviewed by Wiltschko & Wiltschko 1995) and infrasound (Sand & Karlson 1986). Let us consider possible cues and the behavioural sequence during flood-tide transport in an estuary. During the summer in a typical estuary, an animal positioned on the bottom near the entrance to an estuary will experience an increase in salinity, a temperature decrease, and an increase in hydrostatic pressure as colder, high salinity coastal water flows over it into the estuary during flood tide. The exceptions are that during the winter, temperature will increase during the flood tide and in estuaries that become hypersaline due to evaporation, the salinity will decrease during flood tide (e.g. Boehlert & Mundy 1988, Lochmann et al. 1995). Nevertheless, in a typical estuary an ascent in the water column during flood tide could be evoked by the increase in salinity or pressure and decrease in temperature. For an animal to sense environmental changes, the factor must change at both a detectable relative rate and by a detectable absolute amount. Both of these changes must occur before a behavioural response is initiated. Thus, neither slower sub-threshold relative rates of change nor changes that do not proceed long enough for the total change to exceed the necessary absolute amount of change will induce behavioural responses. Considering invertebrate zooplankton, if environmental gradients exist, then the changes that occur with increasing depth are a decrease in temperature, and increases in salinity and hydrostatic pressure. Exposure of zooplankton to changes in these factors induces vertical movements in response to light (phototaxis), gravity (geotaxis), and/or an activity change. Exposure to environmental conditions that occur upon ascending (i.e. temperature increase, salinity decrease, pressure decrease) induce downward movement due to negative phototaxis, positive geotaxis and/or an activity decrease. Upon descending, zooplankton encounter the opposite changes in environmental factors, which induce an ascent due to positive phototaxis, negative geotaxis and/ or an activity increase (Fig. 4). Thus, zooplankton have a negative feedback system (Sulkin 1984, Forward 1987b) that is useful for depth regulation relative to environmental factors. This negative feedback system has been attributed to invertebrate zooplankton but the studies described below are also consistent with its application to fish larvae. If an animal is stationary on the bottom of an estuary during flood tide, it will be exposed to those environmental changes that occur when zooplankton descend in the water column (temperature decrease, salinity increase and hydrostatic pressure increase). Thus, the predicted behavioural response is an ascent. Once in the water column, small animals will 330

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Figure 4 Depth regulatory negative feedback system for invertebrate zooplankton. The environmental gradients are the normal changes in temperature, pressure and salinity upon going from the surface to the bottom. Behavioural responses are phototactic, geotactic and activity changes that are evoked by changes in the environmental factors that would be encountered upon ascending and descending. The arrows on the right indicate the general direction of movement for the behavioural responses.

be transported with a parcel of water. Adult fishes can swim faster than the current but sonic tracking studies indicate they drift with flood-tide currents or swim very slowly (e.g. Atlantic salmon: Stasko 1975, American eel: Parker & McCleave 1997). Accordingly, once in the water column, animals experience very slow changes in temperature and salinity that result from mixing, instead of the flow of tidal currents over the animal. This presents a problem because the initial ascent response upon changes in temperature, salinity and pressure only persists for a few minutes once the relative rate of change ceases (e.g. Latz & Forward 1977). Thus, continuation of swimming within the water column during flood tide must be cued by other environmental factors, such as water turbulence (Welch et al. 1999). During slack water at the end of flood tide, animals descend back to the bottom. The cue(s) for this descent is also problematic because if an animal is transported with a parcel of water, the changes in temperature, salinity and pressure that would signal the end of flood tide and beginning of ebb tide do not occur. Thus, there must be another cue that indicates the end of flood tide and evokes a descent to the bottom. During ebb tide, an animal on the bottom would experience a decrease in salinity, an increase in temperature, and a decrease in hydrostatic pressure. Since all of these environmental changes ideally evoke a descent in the water column (Fig. 4), movement off the bottom is inhibited during ebb tide. Presumably the opposite behavioural responses could be used during ebb-tide transport. The following discussion will consider various environmental cues that could be used during STST. 331

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Olfactory cues Creutzberg (1959) hypothesised that during flood-tide transport in estuaries Anguilla anguilla elvers discriminate between ebb- and flood-tide waters by olfaction. He “supposed that during the ebb tide when inland water smell increased elvers stayed near the bottom and during flood tide, when the inland water smell decreased, they rise to higher water levels” (Creutzberg 1959). Migration swimming behaviour could be induced by exposure to a combination of sea water and natural fresh water but not sea water combined with tap water (Creutzberg 1959, 1961, 1963). The activation odour of natural fresh water could be removed by charcoal filtration. Similar results were observed for elvers of A. rostrata and the freshwater cue appeared to be some biodegradable component of either dissolved or particulate matter (Miles 1968). The role of olfaction was further supported by ultrasonic tracking studies of adult A. rostrata. Both silver (Barbin et al. 1998) and yellow eels (Barbin 1998) rendered anosmic had disrupted STST compared with normal animals. Thus, olfaction seems important for STST but McCleave & Kleckner (1982) suggested “that olfaction discrimination does not serve as the sole timing cue for both entry and leaving the water column.”

Salinity During a tidal cycle in a typical estuary, salinity will increase during flood tide and decrease during ebb tide. Thus, the predicted behavioural responses during flood-tide transport are that animals ascend during flood tide in response to a salinity increase and remain near the bottom during ebb tide in response to a salinity decrease. Field studies relating salinity change to flood-tide transport are mixed. Cross-correlation analysis indicated salinity was not related to flood-tide transport of weakfish larvae (Rowe & Epifanio 1994a). Similarly, De Vries et al. (1994) reported that rates of change in salinity were not good predictors of the timing of vertical migratory activity by fiddler crab (Uca spp.) post-larvae. Alternatively, the density of English sole larvae (Boehlert & Mundy 1987) was negatively correlated with salinity at the start of flood tide and the abundance of blue crab post-larvae and Pinnotheres spp. juveniles during flood-tide transport was associated with peaks in the relative rate of increase in salinity (De Vries et al. 1994). Creutzberg (1958) originally proposed salinity as a possible cue for flood-tide transport of eel elvers but was unable to induce behaviour involved in transport with a salinity cycle (Creutzberg 1961). However, both pink shrimp post-larvae (Hughes 1969a,c) and Japanese flounder larvae (Burke et al. 1995) exhibit the appropriate behavioural responses in that they ascend in response to a salinity increase and descend when exposed to a salinity decrease. More detailed studies have related relative rates of change in salinity during flood tide in an estuary to behaviour and salinity sensitivity. Both blue crab and fiddler crab post-larvae undergo flood-tide transport (Table 3) and ascend in response to a salinity increase (Tankersley et al. 1995). The minimum relative rate of increase in salinity that evokes the ascent response is 5.53×10-4 psu s-1 for blue crab post-larvae and 1.33×10-3 psu s-1 for fiddler crab post-larvae. For both crabs the minimum absolute amount of change in salinity necessary for a response was 0.3 psu (Tankersley et al. 1995). A similar study with fishes also found that Atlantic menhaden and spot larvae ascend upon a salinity increase and are unresponsive to a salinity decrease (De Vries et al. 1995a). The minimum relative rate of salinity increase that induced the ascent response in older larvae which would undergo flood-tide transport 332

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in an estuary was 2.24×10-4 psu s-1 for Atlantic menhaden and 1.4×10-3 psu s-1 for spot larvae. There was a large species difference in the absolute amount of salinity change necessary for a response. Atlantic menhaden larvae required a change of 0.3 psu, while spot needed a change of 2.0 psu. The fastest relative rates of salinity increase De Vries et al. (1994) measured during flood tide in an estuary was 2.64×10-4 psu s-1 to 1.32×10-3 psu s-1. Thus, both blue crab postlarvae and Atlantic menhaden larvae have adequate sensitivity to ascend in response to a salinity increase during flood tide. Both of these species lack an endogenous tidal rhythm in activity or vertical migration that could underlie flood-tide transport (Tankersley & Forward 1994, Forward et al. 1997a). Alternatively, fiddler crab post-larvae and spot larvae are too insensitive to detect typical rates of salinity increase that occur during flood tide. Coincidentally, both species have a circatidal rhythm in vertical migration that could underlie flood-tide transport (Tankersley & Forward 1994, Forward et al. 1998). During ebb-tide transport, animals should show the opposite behavioural response to salinity as observed for the above species. The crab Macropipus holsatus undergoes ebbtide transport (Table 2). It swims in response to a salinity decrease and settles to the bottom upon salinity increase (Venema & Creutzberg 1973). Similarly, juvenile pink shrimp (Penaeus duorarum) swim downstream in response to a salinity decrease and upstream upon a salinity increase (Hughes 1969a,c). These responses are appropriate for ebb-tide transport by this developmental stage (Table 2).

Hydrostatic pressure If an animal is on the bottom, one of the most predictable changes in environmental factors with tide is the hydrostatic pressure cycle. Pressure increases during flood tide as water depth increases and decreases during ebb tide. Invertebrate and fish larvae usually respond to an increase in pressure by ascending or increasing activity (e.g. Rice 1964, Blaxter & Hunter 1982, Sulkin 1984), which could be an appropriate response for flood-tide transport. Considering fish studies, Rowe & Epifanio (1994a) found that abundance of weakfish larvae was not related to the rise in sea level (absolute hydrostatic pressure). In contrast, Forbes & Benfield (1986) suggested that movement into the water column during flood-tide transport of post-larval prawns is triggered by pressure change. Also, as post-larvae of the shrimp P. plebejus move shoreward they switch from exhibiting a diel vertical migration to one that is timed with the tidal cycle and used for flood-tide transport. Rothlisberg et al. (1995) suggested that the switch occurs when the pressure change with tide becomes a significant fraction of the total pressure. For animals on the bottom during flood tide, the pressure must increase at a detectable relative rate by a detectable absolute amount before a behavioural response is initiated. Tankersley et al. (1995) considered whether a pressure increase serves as the cue for the ascent during flood-tide transport for fiddler crab and blue crab post-larvae. Both species ascend upon a pressure increase. The minimum relative rate of increase that evoked the ascent response was 2.8×10-2 mbar s-1 for blue crabs and 4.9×10-2 mbar s-1 for fiddler crabs. The absolute amount of change necessary for a response ranged from 2–4 mbar. In the estuary where the test post-larvae were collected, the average tidal range is about 1 m. De Vries et al. (1994) found that the fastest rate of relative pressure increase occurred 3.1 h after low tide and rates ranged from 1.17×10-4 mbar s-1 to 6.4×10-3 mbar s-1. Thus, the relative rate of pressure change is too slow to initiate an ascent response during flood tide. Assuming 333

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an average rate of change of 3.2×10-3 mbar s-1 and linearity, the tidal range would need to be 8.7 m for blue crabs and 15.3 m for fiddler crab before they could detect a pressure increase. Since these tidal ranges are much greater than those in the geographic range of these species, it is unlikely that pressure serves as a cue for the ascent into the water column during flood tide. Alternatively, the responses could function during depth regulation once post-larvae are in the water column (e.g. Sulkin 1984).

Temperature Horizontal temperature gradients exist in estuaries and can attract or repel animals from different areas (Boehlert & Mundy 1988). However, temperature also changes with tide and could be used as a cue for STST. During the summer, it decreases during flood tide while in the winter it increases as warmer coastal water flows into the estuary. There are few studies of the sensitivity of animals that undergo STST to relative rates of change in temperature. Older Atlantic menhaden larvae use environmental cues for flood-tide transport in estuaries (e.g. Forward et al. 1999b) because they lack an endogenous tidal rhythm in activity (Forward et al. 1996b). De Vries et al. (1995b) found that older Atlantic menhaden larvae ascended in response to both temperature increases and decreases, and that upward movement was not impeded by a temperature gradient. The minimum detectable relative rate (threshold) for a temperature decrease was 10.7×10-2 °C min-1 with the necessary absolute change of 0.05°C. For a temperature increase, the threshold rate was 14.79×10-2 °C min-1 and the minimum absolute change was 0.4°C. Thus, the behavioural responses are correct but larvae are not very sensitive (6.4–8.8°C h-1). Measurements of rates of change in temperature during the summer in an estuary also indicated that temperature change tends to be too erratic to serve as a reliable indicator of flood-tide conditions (De Vries et al. 1994).

Currents

Rheotaxis Directional orientation to water currents is common among invertebrates (e.g. Fraenkel & Gunn 1961, Ennis 1986, Shirley & Shirley 1988) and fishes (Arnold 1974, 1981, Champalbert et al. 1994). Animals can either swim into the current (positive rheotaxis) or in the direction of the current (negative rheotaxis). Among fishes, a visual reference is usually needed to detect current direction (Arnold 1981). This may not be the case for invertebrates because crab post-larvae can orient to currents in darkness (e.g. Welch et al. 1999). Chemical cues frequently affect rheotaxis with the most common response being a chemically cued positive rheotaxis. In this case a chemical cue is perceived and evokes upstream swimming towards the source of the chemical. This response is used for a variety of functions, such as food, habitat, and mate location. Conversely, chemically-cued negative rheotaxis could be used for avoidance of predators and adverse chemicals. The problem with current and STST is that currents are similar during ebb and flood tide and a constant rheotaxis would favour retention not net horizontal transport. Thus, during STST the sign of rheotaxis should change with tidal phase. For example, during flood-tide 334

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transport the predicted pattern would be positive rheotaxis during ebb tide for position maintenance and negative rheotaxis during flood tide for transport. Creutzberg (1959, 1961, 1963) found that elvers of the eel Anguilla anguilla showed the appropriate responses for flood-tide transport in an estuary. Sea water diluted with river water, as would occur during ebb tide, induced positive rheotaxis, while sea water, as would occur during flood tide, induced negative rheotaxis. However, at high current speeds in the presence of untreated inland water, elvers clung to the bottom (Creutzberg 1963). Hughes (1969a,c) found the opposite pattern for juveniles of the shrimp Penaeus duorarum, which undergoes ebb-tide transport for movement out of estuaries. Upon exposure to high salinity water that simulated flood tide, juveniles were positively rheotactic. Alternatively, when salinity was reduced, as occurs during ebb tide, they became negatively rheotactic and swam or drifted downstream. The rate of change in salinity was important for a response because a decrease of 2 psu over 20 min was effective but not if the decrease occurred over 40min (Hughes 1969a,c).

Turbulence During STST an animal ascends into the water column during the appropriate phase of the tide and is usually transported with a parcel of water. If STST is regulated by responses to environmental factors, then cues, such as changes in temperature, salinity and pressure, occur very slowly in the parcel of water and are essentially no longer available to stimulate swimming. However, one cue that is present within the moving parcel of water is turbulence. All current flow in nature is turbulent (Vogel 1994), which can be quantified as turbulent kinetic energy (TKE). Since turbulence is related to current velocity (MacKenzie & Leggett 1991), it will increase as tidal currents increase in velocity and decreases to very low levels at slack water. Early studies of turbulence focused on its effect on contact rates between zooplankton predators and their prey (e.g. Rothschild & Osborn 1988, MacKenzie & Leggett 1991). However, more recent studies reported that increased turbulence increased zooplankton swimming activity (Saiz & Alcaraz 1992) and metabolic rates (Alcaraz et al. 1994). Post-larvae of the crab Callinectes sapidus undergo flood-tide transport (Table 3). Welch et al. (1999) hypothesised that turbulence in flow served as a cue to regulate swimming behaviour during STST. When tested in a laboratory flume in darkness, post-larvae ascended in response to a relative rate of increase in TKE and reacted to a relative decrease in TKE by descending. At high levels of TKE, post-larvae were stimulated to swim regardless of the changes in TKE. The levels of TKE that evoked responses were similar to levels in estuaries (Welch et al. 1999). The responses to turbulence increased following an increase in salinity but were inhibited by a decrease in salinity (Welch 1998). Thus, TKE could regulate swimming in the water column throughout one tidal phase in that animals are stimulated to continue swimming by turbulence when current speeds are high but become inactive and descend to the bottom when turbulence levels and current speeds decline near the time of slack water.

Electrical fields When water, an electrical conductor, moves through the earth’s magnetic field, an electrical potential proportional to water velocity and magnetic field intensity is 335

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induced. If there is a return path an electrical current flows which is proportional to the resistance of the generated path and the return path. (Wippelhauser & McCleave 1987) Thus, Deelder (1952), Rommel & McCleave (1972) and McCleave & Kleckner (1982) proposed that glass eels could use the changes in induced electrical field strength as a cue for detecting the presence and direction of currents. Accordingly, behaviour during STST could be cued by changes in electrical field strength. Glass eels respond behaviourally to electrical fields found in estuaries (Rommel & McCleave 1973, Zimmerman & McCleave 1975, McCleave & Power 1978). However, since electrical conductivity decreases as salinity decreases, electrical field strength induced by current flow also decreases with salinity. This leads to the predictions (a) that in freshwater areas the changes in electrical fields with currents are too small for detection, or (b) that the timing of STST should be different between freshwater and estuarine areas because the timing of changes in the magnitude of the electric fields over a tidal cycle will be different. In tidal freshwater areas, glass eels show flood-tide transport (McCleave & Kleckner 1982, Wippelhauser & McCleave 1987), and yellow eels undergo STST (Parker & McCleave 1997). The timing of the descent of glass eels during flood-tide transport was similar in freshwater and salinity stratified conditions (Wippelhauser & McCleave 1987) and yellow eels began moving in fresh water before current speeds increased at the start of ebb tide (Parker & McCleave 1997). These results suggest that changes in electrical field strength are unlikely cues for movements of American eels during STST (Wippelhauser & McCleave 1987, Parker & McCleave 1997). However, the possibility remains for other fish species, such as cod (Gadus morhua, Regnart 1931), Atlantic salmon (Salmo salar, Rommel & McCleave 1973) and European eel (Anguilla anguilla, Berge 1979), which are known to respond behaviourally to electric stimuli.

Models for STST of the blue crab Callinectes sapidus Among the many species that undergo STST, recent studies of the blue crab Callinectes sapidus allow the formation of conceptual models of the behaviour involved in STST for its different life-cycle stages (Forward et al. 1995, Forward et al. 2001). Among females, there are two phases to the spawning migration. First, there is a long-distance down-estuary phase, in which newly inseminated non-ovigerous crabs travel seaward from low salinity areas of estuaries and take up residence near the inlet to estuaries. Second, there is a shorter distance, spawning phase, in which ovigerous crabs migrate from euhaline areas to the entrance of the estuary and coastal waters to release larvae. Although the timing of various components of horizontal migration may differ among estuaries, it is likely that the sequence of events is similar. The initial down-estuary migration of females is initiated after mating as inseminated crabs migrate seaward from brackish water towards the mouth of the estuary. The behaviour underlying this migration is unknown, but may involve ebb-tide transport. If so, then females do not undergo continuous transport because individual female crabs may take weeks to months to complete their down-estuary migration. Upon reaching high salinity regions, female crabs cease horizontal migration as their ovaries and eggs complete development. Crabs that mate in late spring may reach euhaline areas in time to spawn that same year 336

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(Churchill 1921). Crabs reaching the lower estuary in the fall over-winter near the mouth of the estuary and spawn the following spring. The actual migration for spawning is initiated after oviposition of fertilised eggs under the abdomen. Ovigerous crabs with early-stage eggs remain in the lower portion of the estuary and do not engage in ebb-tide transport. However, female crabs with late-stage embryos migrate vertically towards the surface during nocturnal-ebb tides and are transported seaward towards the entrance of the estuary and possibly into coastal waters (Tankersley et al. 1998). Upon reaching the mouth of the estuary, ovigerous females release their larvae. Subsequently, post-spawning crabs reverse STST and undergo flood-tide transport to re-enter the estuary by migrating towards the surface during nocturnal-flood tides. The actual cues and behavioural responses involved in STST of females during their spawning migration are unknown. Regardless of the underlying mechanism, vertical migratory behaviours contributing to seaward transport towards the mouth of the estuary appear to be restricted to gravid female crabs carrying late-stage embryos (Tankersley et al. 1998). Similarly, up-estuary migration on flood tides appears to be restricted to postspawning females. Male blue crabs and females with early-stage embryos do not appear to undergo STST. Newly released larvae undergo ebb-tide transport (Table 2) and are advected seaward where they develop in high salinity water on the continental shelf (McConaugha et al. 1983, Provenzano et al 1983, Sulkin 1984, Sulkin & Van Heukelem 1986). After passing through 7–8 zoeal stages (Costlow & Bookhout 1959), they molt to the post-larval stage, which enters estuaries. Onshore transport of post-larvae from the shelf to an esturary entrance is probably mediated by Ekman currents generated by wind events (reviewed by Epifanio 1995, Roman & Boicourt 1999). Up-estuary movement to nursery areas is accomplished by flood-tide transport (Dittel & Epifanio 1982, Brookins & Epifanio 1985, Mense & Wenner 1989, Little & Epifanio 1991, De Vries et al. 1994, Olmi 1994). The behaviour underlying flood-tide transport of post-larvae could be a tidal rhythm in activity or behavioural responses to environmental cues. Studies of biological rhythms found that post-larvae had a circadian rhythm, in which they were active and ascended in the water column during the time of day in the field (Tankersley & Forward 1994, Forward et al. 1997a). The swimming rhythm lacked apparent ecological significance because it does not contribute to transport up the estuary and increases exposure to visual planktivores during the day. However, it may underlie the weak reverse diel vertical migration observed for post-larvae in offshore areas. Blue crab post-larvae are abundant in the neuston during the day in offshore areas (McConaugha et al. 1983, Epifanio 1988, McConaugha 1988) and at night, a small proportion move down in the water column (McConaugha 1988). This activity pattern is not expressed in estuaries because chemical cues in estuarine water reverse the photobehaviour observed in offshore water, i.e. light inhibits swimming in estuarine water (Forward & Rittschof 1994). Thus, during the day in estuaries, swimming due to the rhythm in activity is suppressed by light. If responses to environmental cues underlie flood-tide transport, then behaviour and cues should be identified for (a) the ascent from the bottom during flood tide, (b) depth maintenance as flood-tide currents carry the post-larvae up the estuary, (c) the descent back to the bottom at the end of flood tide, and (d) position maintenance on the bottom during ebb tide. During flood tide in an estuary in summer or early fall, a post-larva on the bottom will be exposed to a temperature decrease, hydrostatic pressure increase, and salinity increase. Temperature changes during flood tide were too inconsistent to serve as a cue for the ascent 337

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(De Vries et al. 1994). Relative rates of increase in pressure and salinity change in a consistent pattern during flood tide (De Vries et al. 1994) and post-larvae ascend in response to these changes (Tankersley et al. 1995). However, the relative rate of increase in pressure during flood tide is about an order of magnitude below the lowest relative rate that evokes an ascent response (Tankersley et al. 1995). In contrast, rates and absolute amounts of salinity increase during flood tide (De Vries et al. 1994) are adequate to evoke an ascent response (Tankersley et al. 1995). Thus, post-larvae ascend from the bottom during flood tide in response to the rate of increase in salinity. Once post-larvae enter the water column, they are transported with a parcel of water and experience relatively slow changes in salinity as mixing occurs. This presents a problem because Latz & Forward (1977) found that increases in swimming activity of crab larvae due to salinity change lasts only a few minutes, not the several hours during which post-larvae are transported during flood tide. Turbulence (measured as turbulent kinetic energy) varies with tidal state, being highest during both ebb and flood tides than during slack water (McMurray 1980, Welch 1998). Thus, tidally generated turbulence could serve as a cue regulating maintenance in the water column during flood tide, and descent at the end of flood tide. A salinity increase and increasing TKE associated with the accelerating flood tide stimulates swimming by the postlarvae (Welch 1998). Since increased swimming activity of zooplankton causes an ascent (Rudjakov 1970), post-larvae would continue to ascend. During most of flood tide, TKE is above the minimal level of turbulence (threshold) that evokes a constant swimming response (Welch et al. 1999), so post-larvae would be continually stimulated to swim and remain in the water column. At the end of flood tide, the TKE drops below the threshold and the relative rate of decrease in TKE cues post-larvae to decrease swimming and descend in the water column (Welch et al. 1999). This behavioural sequence predicts that post-larvae should settle out of the water column during slack water at the end of flood tide when turbulence declines to a low level. This prediction was verified by a field study, which found that maximum settlement of postlarvae occurred at the time of lowest turbulence (slack water) at the end of flood tide (Forward et al. 2001). For this mechanism to explain flood-tide transport, post-larvae must not swim up into the water column in response to the turbulence generated by the ebb tide. Either of two mechanisms could prevent this ascent from happening. First, if post-larvae require a salinity increase to begin swimming in the water column, they would not get this cue during an ebb tide. A second, and more likely, possibility is that a salinity decrease, as would be experienced by a post-larva on the bottom during ebb tide, suppresses swimming behaviour (Forward 1987b, Welch 1998). The conceptual model for behaviour underlying flood-tide transport of post-larvae is shown in Figure 5 and is divided into four phases. First, post-larvae remain on or near the bottom during the day and nocturnal ebb tides (Phase I). Swimming during the increased turbulence of the ebb tide is suppressed by the decrease in salinity experienced by the postlarvae and light inhibits swimming during the day (Forward & Rittschof 1994). During Phase II, post-larvae ascend from the bottom during flood tide at night in response to the relative rate of salinity increase. Water turbulence stimulates sustained swimming during flood tide (Phase III) and the decline in turbulence at the end of flood tide cues a descent in the water column and attachment to the substratum (Phase IV). It is likely that during Phase III turbulence induces sustained swimming in the water column, but post-larvae are 338

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Figure 5 Model for flood-tide transport and settlement of blue crab post-larvae. (Redrawn from Forward et al. 2001.)

transported as passive particles. Thus, post-larvae do not use one environmental cue for flood-tide transport, but rather they respond to a sequence of cues.

Conclusions Selective tidal-stream transport is common among invertebrates and fishes. In coastalestuarine areas, ebb-tide transport is used for movement out of an estuary or offshore, whereas flood-tide transport is used for movement in the opposite direction. For life-cycle stages such as larvae, which have limited swimming abilities, transport by tidal currents is an efficient method for rapid horizontal movement. However, even large fishes that can swim against tidal currents undergo STST, which can lead to a considerable reduction in the energy necessary for horizontal movement (e.g. Weihs 1978, Metcalfe et al. 1990). Frequently, STST occurs only at night, which is probably an adaptation to avoid visual predators. One notable aspect of STST within a species is the reversal in the direction of migration at different life-cycle stages. This phenomenon is probably very widespread but is only documented among species that have been most extensively studied. To demonstrate these reversals, let us consider three examples among fishes and invertebrates. First, in offshore areas the plaice Pleuronectes platessa migrates with southwardly directed tides to spawning areas and then migrates back to feeding areas with northwardly directed tides (Table 4). Second, glass eels of the catadromous species Anguilla rostrata use flood-tide transport for migration up estuaries, where as adults use ebb-tide transport for movement seaward during their reproductive migration (Tables 4, 5, pp. 323, 324). Third, the opposite pattern occurs for the anadromous Atlantic salmon Salmo salar, as smolts migrate seaward in estuaries using ebb-tide transport while adults return to freshwater reproductive areas using floodtide transport (Tables 4, 5). 339

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Among invertebrates, first stage larvae of the crab Carcinus maenas use ebb-tide transport for migration to developmental areas offshore, and post-larvae return to coastal adult habitats using flood-tide transport (Tables 2, 3, pp. 318, 320). Second, post-larvae of penaeid shrimps use flood-tide transport to migrate to nursery areas in estuaries and juveniles exit estuaries using ebb-tide transport (Tables 2, 3). Finally, the blue crab, Callinectes sapidus, has two reversals in its life cycle. Ovigerous females use ebb-tide transport for movement to the mouth of estuaries for spawning and then re-enter the estuary using flood-tide transport. Newly released larvae use ebb-tide transport for movement seaward towards the developmental area and post-larvae move up-estuaries to nursery areas using flood-tide transport (Tables 2, 3). These reversals are rather remarkable since they require animals to switch transport from one tidal phase to the other. The switch appears to be associated with changes within the life cycle, such as the physiological change between reproductive and non-reproductive states or between larval, post-larval, juvenile, and adult stages. Usually there is a long time interval between the reversals. However, it is not necessary because in the case of the blue crab, ovigerous females undergo ebb-tide transport, release larvae and then switch to flood-tide transport (Tankersley et al. 1998). Since females only migrate at night, the switch appears to occur from one night to the next. Reversals in STST are also remarkable because the behaviour underlying STST also reverses. The behavioural basis for STST is ascribed to either a tidal rhythm in vertical migration/activity or behavioural responses to environmental factors associated with different tidal phases. Tidal rhythms in animals undergoing STST clearly have the time of vertical migration or activity synchronised with one tidal phase. Considering studies of tidal rhythms, the timing of the rhythms adjusts to local tidal times (e.g. Palmer 1995) but there are very few examples of changes in the rhythm between tidal phases. One example is the fiddler crabs of the genus Uca. Post-larvae undergo flood-tide transport and have a circatidal rhythm, in which they actively swim during rising tide (Tankersley & Forward 1994). Alternatively, adults live in the high intertidal and have a circatidal activity rhythm, in which they are active during the time of low tide (reviewed by Palmer 1995). Considering behavioural responses to environmental cues, the most complete evaluation of the cues comes from studies of the blue crab (see p. 336). These studies suggested that no single cue is used for STST but that there is a sequence of cues that function for (a) the ascent from the bottom during the tidal phase for transport, (b) depth maintenance during transport, (c) the descent back to the bottom at the end of the tidal phase and (d) position maintenance on the bottom during the other phase of the tide. If responses to environmental cues underlie STST, then a reversal would entail a change in behavioural responses to specific environmental factors. For example, in the case of blue crab post-larvae the only change that is necessary for a reversal from flood-tide transport to ebb-tide transport would be a switch from an ascent response to a salinity increase to an ascent response to a salinity decrease. Further studies are needed on the behaviour underlying STST and especially the reversals, the study of which may be the most informative way to identify important behaviours. Most of the species that are considered in this review have larval, juvenile and adult habitats in different locations and use STST for movement between these areas. Knowing the underlying behaviour allows predictions of the effectiveness of STST in different areas and the same areas under different conditions. For example, if a tidal rhythm in vertical migration/activity underlies STST, then the success of transport will depend upon the extent 340

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of the tidal currents. Alternatively, if STST results from responses to environmental factors, then transport depends upon the magnitude and timing of these changes.

Acknowledgements The paper was written during the tenure of Grants No. OCE-9819355, OCE-9901146 and OCE-0096205 from the National Science Foundation. We thank Dr John Burke for his technical advice.

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TERRITORIAL DAMSELFISHES AS DETERMINANTS OF THE STRUCTURE OF BENTHIC COMMUNITIES ON CORAL REEFS DANIELA M.CECCARELLI,1 GEOFFREY P.JONES,2 & LAURENCE J.McCOOK3 1

Department of Marine Biology and Aquaculture, James Cook University, Townsville, 4811, Queensland, Australia e-mail: [email protected] 2 Department of Marine Biology and Aquaculture, James Cook University, Townsville, 4811, Queensland, Australia e-mail: [email protected] 3 Australian Institute of Marine Science & CRC: Reef Research, PMB3, Townsville, MC, 4810, Queensland, Australia e-mail: [email protected]

Abstract This review evaluates the generalisation that territorial, herbivorous damselfishes (Pomacentridae) have a major influence on the structure of algal, coral, other invertebrate and fish assemblages on coral reefs. Herbivorous damselfishes are a diverse, widespread and abundant component of reef fish assemblages and their territories take up a significant proportion of the shallow reef substratum. There are several mechanisms by which they potentially affect community structure within territories, including both food consumption and potential “farming” activities, such as “weeding” of undesirable organisms, “killing” coral to grow algae, providing nutrients for algal “crops” and the aggressive “defence” of vital resources. A synthesis of the literature that documents assemblages both inside and outside territories revealed a number of common patterns. Erect filamentous algae often dominate territories, whereas low-lying crustose coralline and prostrate algae characterise adjacent areas. Furthermore, territories consistently support a greater biomass, productivity and species richness of algae than undefended areas. Experimental studies suggest that damselfishes modify regimes of disturbance and succession but the potentially different effects of feeding, farming and territorial exclusion suggest a more complex interaction of processes. There are also substantial differences between defended and undefended areas in coral species composition and densities of small, mobile organisms such as cryptofauna and juvenile fishes, whereas larger herbivorous fishes are excluded from territories. However, the larger-scale effects of these interactions on the ecology of “included” or “excluded” species has yet to be examined. Many of the above generalisations may be premature as the literature is clearly biased towards a few larger, more aggressive species that maintain conspicuous algal mats. Our review draws attention to the numerically more abundant and less aggressive herbivorous species whose effects appear to be less dramatic. Furthermore, the spatial and temporal variability in the structure of damselfish communities is largely unknown, further restricting our ability to make valid generalisations. While the effects of territoriality have been tested by damselfish removals, more sophisticated experimental work is needed to assess the relative contributions of selective feeding, reduced herbivory, weeding and other farming activities. These mechanisms will be clearer if we have a better understanding of the function of territoriality, the actual benefits of

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algal turfs to the damselfishes and the separate tasks involved with establishing and maintaining territories.

Introduction It is widely acknowledged that herbivorous fishes have a major influence on the structure of benthic communities on coral reefs (Choat 1982, Steneck 1988, Horn 1989, Glynn 1990, Hay 1991, Hixon 1996). Although herbivores usually comprise <25% of the total fish species diversity and biomass (Randall 1961, Ogden & Lobel 1978, Meekan & Choat 1997), this low percentage does not reflect their ecological importance relative to other trophic groups. Grazing activities appear to control the standing crops of many dominant reef algae (Wanders 1977, Carpenter 1986, Steneck 1988, Hay 1991, Pennings 1996, McCook 1996, 1997, Miller 1998, Russ & McCook 1999). Where large herbivores have been excluded or removed through over-fishing, macroalgae have been reported to overgrow reefs and reduce live coral cover (Wanders 1977, Hughes 1994, Hay 1997, reviews by Miller 1998, McCook 1999). High cover of algae appears to inhibit coral recruitment and in the absence of active coral growth, the reef framework is eroded. Thus, herbivorous fishes have been attributed a general role in maintaining the abundance and diversity of reef-building corals (Ogden & Lobel 1978, Pennings 1996). Numerically, the most important families of herbivorous fishes on coral reefs are the Acanthuridae (surgeonfishes), Scaridae (parrotfishes) Siganidae (rabbitfishes), and some members of the family Pomacentridae (damselfishes) (Choat 1991). Despite the presumed general role, these families differ markedly in their feeding mode, behaviour and the likely impacts on benthic communities (Steneck 1988, Horn 1989). The greatest effects of feeding are usually attributed to the first three families, which account for a large proportion of the herbivore biomass and can have a destructive feeding mode that is capable of excavating the reef matrix (Bellwood & Choat 1990). However, the relative importance of the different herbivorous fish taxa and the mechanisms by which they influence benthic communities are poorly understood. The actual algal species consumed and the effects on algal species composition are not known in detail (McCook 1999). The relationships between particular groups of herbivorous fishes, macroalgae, corals and other taxa need to be examined to test the validity of the above generalisations. Herbivorous damselfishes are a diverse and abundant component of coral reef fish assemblages whose ecological role has been a matter of much speculation (Ogden & Lobel 1978, Horn 1989, Wilson & Bellwood 1997). They do not reach the large sizes of other herbivorous taxa and have a low impact mode of browsing within relatively restricted areas (Choat 1991). This feeding mode creates an impression that the effects of their feeding on algae may be substantially lower than other herbivorous taxa. Contrary to this expectation, they have been attributed a “keystone” role in maintaining the structure of algal communities (Kaufman 1977, Williams 1980, 1981, Hixon & Brostoff 1983, 1996, Hixon 1996), determining patterns of zonation in coral communities (Wellington 1982), and modifying the grazing activities of other herbivorous fishes (Jones 1992). These far reaching effects may stem in part from their presumed ability to “farm” preferred algal species (e.g. Irvine 1980, Lassuy 1980, Horn 1989), their ability to kill corals (e.g. Kaufman 1977) and their conspicuous territorial aggression towards other herbivorous fishes and invertebrates (e.g. Robertson et al. 1976, Sammarco & Williams 1982). However, what are the actual affects of damselfishes on different species of algae, coral, mobile invertebrates and fishes? Do all 356

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species have such dramatic effects or are these generalisations based on a few high profile species? Herbivorous damselfishes have received more attention from researchers than the other families of coral reef herbivores with respect to their effects on benthic communities (Carpenter 1986, Hixon 1996). It might be expected, therefore, that there is sufficient information to formulate general models that predict their effects on different components of coral reef assemblages. To this end, the aim of this paper is to review the ecology of herbivorous damselfishes, evaluate the magnitude of their influence on different aspects of benthic communities and determine the key mechanisms responsible for these effects. First, we review the relevant aspects of their ecology that define the range of functional groups of herbivorous damselfishes and the explicit mechanisms by which they may impact on other organisms. We then review the documented effects of territorial damselfishes on communities of (1) algae, (2) corals and (3) mobile organisms, including fishes and invertebrates. In each case, we describe and evaluate the generalisations which have emerged regarding patterns in community structure and the key ecological processes responsible for them and assess to what extent generalisations are representative of different functional groups of herbivorous damselfishes.

Ecology and behaviour of herbivorous damselfishes In evaluating the role of territorial herbivorous damselfishes on coral reefs, a number of key aspects of their biology need to be addressed. First, it is necessary to define what and who territorial herbivorous damselfishes are in terms of their essential characteristics and taxonomic composition. Second, it is essential to examine where different species of damselfishes are found and determine whether there is enough of them to have more than just a localised affect on benthic communities. Third, the mechanisms by which they can potentially affect the distribution and abundance of other organisms need to be established.

What are territorial herbivorous damselfishes? For the purposes of examining their impact on algal communities, any species that removes algae from the substratum qualifies as a herbivore (Steneck 1988). In most cases this will involve those species consuming algae for food, although incidental removal of algae in the process of eating other foods and “weeding” of algae may also be important (Lassuy 1980). Algae may be the predominant mode of nutrition in some genera of the Pomacentridae but it is not ubiquitous. All species of Dischistodus, Stegastes, Hemiglyphidodon and Plectroglyphidodon are reportedly herbivorous (Meekan et al. 1995). The genera Pomacentrus and Chrysiptera contain some herbivores, whereas the genera Abudefduf, Amblyglyphidodon, Amphiprion, Chromis, Dascyllus and Neopomacentrus appear to be composed almost exclusively of zooplanktivores (Randall et al. 1997, Lewis 1997). Species of Pomacentrus and Neoglyphidodon have been observed to behave as omnivores, feeding on plankton and algae, or on benthic invertebrates and algae (Allen 1975, Meekan et al. 1995). The other defining characteristic is that most herbivorous damselfishes occupy territories 357

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which they defend from conspecifics and other potential competitors and egg predators (Clarke 1970, Low 1971, Ebersole 1977, Gronell 1980, Mahoney 1981, Robertson 1984, Hourigan 1986, Jones & Andrew 1990, Cleveland 1999). Levels of aggression and the degree to which individuals maintain exclusive areas vary considerably among genera and species (Gronell 1980, Robertson 1984, Lewis 1997, Cleveland 1999). The species most commonly recognised as territorial are the large aggressive Dischistodus and Stegastes species (e.g. Ebersole 1977, Potts 1977, Hourigan 1986, Foster 1987, Cleveland 1999). Smaller species of Pomacentrus and Chrysiptera are extremely site-attached and at least some appear to defend these areas from other species (e.g. Low 1971). Despite the uncertain taxonomic distribution of herbivory and territoriality within this group, there is clearly a wide diversity of damselfishes that have both of these characteristics throughout the coral reef regions of the world (Table 1). The list of herbivorous species in Table 1 is far from exhaustive because it only includes species that have received some attention in the literature. Many unlisted species of Pomacentrus, Chrysiptera and other genera browse or graze inside defended areas but very little is known about their diets or potential effects on benthic communities. There is an obvious taxonomic bias in the studies that have been conducted on herbivorous territorial damselfishes to date, with a lot of information on a few well-studied species and very little for the large majority (Fig. 1). Clearly, larger and more conspicuous species of herbivorous damselfishes (>13 cm) have been well-studied (e.g. Hemiglyphidodon plagiometapon, Stegastes planifrons), while relatively small species have tended to be overlooked (Table 1). In this review we will evaluate to what degree this bias affects the validity of the generalisations that have emerged. Lewis (1997) defined two major ecological categories or functional groups of herbivorous damselfishes. Territorial algal turf “farmers”, which maintain territories in which the algal community is distinctly different from that on the surrounding substrata, and territorial algal turf “grazers”, which defend a territory of apparently undifferentiated turf algae. This distinction refers to species that maintain conspicuous mats of algae and those that do not and should not imply a dichotomy in the mechanisms by which damselfishes influence algal communities. The degree to which they farm algae or are strict grazers has not been fully evaluated. The evidence needed to classify damselfishes into species with and without Table 1 Species of damselfishes currently recognised in the literature as herbivorous. Locations are broad geographic regions and refer to where the major studies on the species have been done, rather than their actual biogeographic distributions. *territorial algal turf farmers, # territorial algal turf grazers. Species are categorised as farmers or grazers only if they have been described as such in the literature and are based on the definitions provided by Lewis (1997). The maximum size of all Indo-Pacific species is from Randall et al. (1997), whereas the size of species from other localities was obtained from the relevant literature.

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Table 1 continued

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Figure 1 The number of studies done on damselfishes species that contain information about the effects of these species on components of the benthic community.

conspicuous algal mats is not available for all species but larger species are more likely to be referred to as “farmers” in this classification (Table 1). We suspect that the two groups are extremes of a continuum in terms of the magnitude of the effect that individual species have on algal biomass. The literature has primarily been concerned with one end of this continuum (species maintaining conspicuous algal mats) and may therefore overestimate the magnitude of the impacts of the group as a whole, while underestimating their abundance and distribution.

The distribution and abundance of territorial damselfishes: how much space do they occupy? Herbivorous damselfishes are widely distributed throughout tropical oceans (Allen 1975). They also occur on subtropical (Foster 1972, Montgomery 1980a,b, Ferreira et al. 1998) and temperate rocky coastlines (Kohda 1984, Jones & Norman 1986, Jones & Andrew 360

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1990, Jones 1992). A comprehensive study on the large-scale distribution patterns of herbivorous damselfishes remains to be done. On the Great Barrier Reef, the biomass of herbivorous damselfishes was estimated to be highest on outer-shelf reefs (Williams & Hatcher 1983). However, there are clearly major changes in species composition on this large scale (Russ 1984a). For example, Williams (1982) found that Pomacentrus wardi was common on inshore and mid-shelf reefs, Stegastes apicalis was most abundant on midshelf reefs and S. fasciolatus, Plectroglyphidodon lacrymatus and P. dickii occurred predominantly on outershelf reefs. Within reefs, herbivorous damselfishes are a numerically important component of reef flat and shallow reef slope habitats (Russ 1984b). Smaller-scale patterns of distribution within reefs and habitat-partitioning among herbivorous damselfish species have been documented for both the Great Barrier Reef (Sale 1974, 1976, 1979, Robertson & Lassig 1980, Meekan et al. 1995, Bay et al. pers. comm.) and the Caribbean (Itzkowitz 1977, Waldner & Robertson 1980, Gutierrez 1998). Most species are restricted to certain reef zones and depths, and there are major changes in species composition along reef gradients. For example, at Heron Island on the Great Barrier Reef, Pomacentrus wardi is the most abundant species, especially on the reef flat, crest, and outer crest, while P. chrysurus is also very abundant on the inner crest (Robertson & Lassig 1980). Two larger species, Plectroglyphidodon lacrymatus and Stegastes apicalis, are comparatively rare and occur primarily on the crest and upper reef slope (Sale 1974, Robertson & Lassig 1980). The high degree of habitat partitioning in herbivorous damselfishes appears to be determined by a combination of processes including habitat selection at settlement, adult habitat choice and competitive interactions among adults (Itzkowitz 1977, Lirman 1994, Robertson 1996, Gutierrez 1998, Bay et al. pers. comm.). These patterns suggest that the nature and magnitude of the impacts of herbivorous damselfishes will depend on the reef strata in question. To examine the degree of spatial variability in the distribution and abundance of herbivorous damselfishes on the Great Barrier Reef, we surveyed the fringing reefs of three islands on the Great Barrier Reef (Magnetic, Orpheus and Lizard) (Fig. 2). Species composition and patterns of abundance are extremely labile on this scale. However, in general, herbivorous damselfishes are abundant in all shallow reef zones and the species composition exhibits dramatic changes along the reef crest and slope habitats. Small species that do not appear to visibly change the algal communities inside their territories (e.g. Pomacentrus wardi) tend to be more abundant and widespread than large, more aggressive species that maintain conspicuous algal stands (see also Meekan et al. 1995). In contrast, large species with conspicuous algal mats (e.g. Stegastes apicalis, S. nigricans, Neoglyphidodon nigroris) are less abundant and exhibit more narrow distributions that are usually associated with the reef crest (Fig. 2). This difference in distribution patterns confirms that there is unlikely to be a uniform impact of herbivorous damselfishes across all reef zones. Clearly, the distribution and abundance of territorial damselfishes varies among species, but are they ever abundant enough to exert a major influence on benthic communities? Few workers have addressed this question. Gleason (1996) noted for the Carribean that the back reef specialist Stegastes nigricans forms groups of up to 80 individuals with contiguous territories, covering an area of many metres in diameter. Species found on the front reef and in deeper water, such as Plectroglyphidodon lacrymatus and Stegastes fasciolatus are solitary and defend individual territories <1 m in diameter. To examine the amount of space occupied by damselfishes in more detail we combined estimates of average abundance and territory size in the literature (Table 2). In some areas, more than half of the available substratum on 361

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Figure 2 Zonation of selected species of herbivorous damselfishes on the fringing reef flats of three islands of the Great Barrier Reef, Australia: Nelly Bay, Magnetic Island; Cattle Bay, Orpheus Island and Watson’s Bay, Lizard Island. All species present were used for Nelly Bay. For the remaining two bays, the species were selected if they occupied comparable niches and were relatively abundant (at least four individuals in any given reef zone). Zones across the reef flat were defined according to major characteristics of the substratum and are described as follows: Flat 1: rubble/sand; Flat 2: rubble/rock/ coral (<5% cover); Flat 3: inner hard coral zone; Flat 4: outer hard coral zone.

shallow reef flats is under the influence of one or two species of territorial damselfishes (Table 2). The proportion of space occupied by damselfishes varies for different species and on different study reefs, from ~11% for Stegastes acapulcoensis in the deep zone of Contadora Island (Wellington 1982) to over 70% for S. fuscus on a rocky reef in southeastern Brazil (Ferreira et al. 1998). There can also be considerable variation between reef zones. There was a 30% difference in the space occupation of S. apicalis and S. nigricans between the 362

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Table 2 Spatial extent of substratum occupation by herbivorous damselfishes. Authors and study location is given for each species. Where the information was available, reef zone was included. GBR, Great Barrier Reef; PNG.

fore-reef crest and back reef (Klumpp et al. 1987), and approximately a 25% difference for S. acapulcoensis between deep and shallow areas in Panama (Wellington 1982) (Table 2). The effects of the damselfishes may be greater than the actual space occupancy would imply, particularly if their effects extend beyond territory boundaries, by concentrating the foraging activities of other grazers in areas between territories.

How do territorial damselfishes directly affect benthic organisms? There is a range of mechanisms by which damselfishes may establish and maintain territories that are distinctly different from the surrounding substrata. These may be broadly categorised into those that may reduce the abundance of preferred food algae, and “farming” activities (sensu Irvine 1980, Lassuy 1980), defined as those that actively promote the establishment and growth of algal crops.

Feeding intensity and selectivity Damselfishes may reduce the abundance of certain algae through feeding activities and may modify algal composition through selective feeding (Jones 1992). Data on the exact diet are lacking for most species and even fewer have compared what is in the diet with what is available within territories. Hence, it is not clear to what extent they can be classified as either grazers or browsers. Most information is based on the observation of bite rates rather than gut content or assimilation analysis (Wilson & Bellwood 1997). Many species have flexible diets, for instance Pomacentrus amboinensis, P. nagasakiensis, Neoglyphidodon nigroris and most Abudefduf species feed on benthic algae and plankton, while 363

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Neoglyphidodon melas feeds on benthic invertebrates and algae (Allen 1975, Meekan et al. 1995). Wilson & Bellwood (1997) provide evidence that field observational studies on bite rates may prove misleading and that at least gut contents analysis is necessary to establish what is ingested. They argue that detritus may be more important than algae in the diet of many species. If true, the potential impact of the consumption of algae may be less important than previously thought.

Farming: weeding, preparing substratum, fertilising and herbivore exclusion Damselfishes may influence the abundance of other organisms and promote the establishment or productivity of preferred algae in at least four different ways. First, there is some evidence that damselfishes selectively remove unpalatable algae, leading to the view that some species may “weed” their territories, promoting the growth of their algal food crop (Irvine 1980, Lassuy 1980, Lobel 1980, Montgomery 1980a, Branch et al. 1992). Although damselfishes clearly remove certain types of algae without eating it, the exact species composition of weeded algae is unknown. While some believe that weeding is done to promote the growth of preferred food algae (Lobel 1980, Montgomery 1980b), others maintain that the algae serve the purpose of trapping hidden but important elements of their diets, such as detritus (Wilson & Bellwood 1997), invertebrates (Zeller 1988) or the eggs of other species that nest inside territories (Jan 1995). The second potential farming activity involves substratum preparation, which may involve killing coral and other activities. Damselfishes certainly have the ability to kill coral within their territories to establish new substrata for growing food algae (Potts 1977, Lobel 1980, Robertson et al. 1981, Wellington 1982). For example, Stegastes planifrons kills Monastrea annularis and Acropora cervicornis, two major reef-building corals in the Caribbean (Kaufman 1977). Dead coral appears to be converted into an algal lawn. Damselfishes may also remove sediment and keep bare rock surfaces clean for growing algae. Third, the growth of preferred algae may also be promoted by nutrient enrichment from waste products egested by resident damselfishes (Polunin & Koike 1987, Klumpp & Polunin 1989, Ferreira et al. 1998). This could only be construed as farming if they were actively defecating in areas to fertilise their algal crop but there is no unequivocal supporting evidence. In fact, Polunin & Koike (1987) suggest that defecation takes place in localised patches away from feeding areas. The final way in which herbivorous damselfishes may maintain farms of algae is by reducing herbivory by other organisms through active defence. The territoriality of herbivorous damselfishes may not only cause a reduction in grazing within their territories but also concentrate grazing in areas where damselfishes are less abundant (Doherty 1983). Interspecific territoriality by the more aggressive herbivorous damselfishes is known to affect the local distribution of grazing fishes such as scarids, siganids and acanthurids (Robertson et al. 1979, Hourigan 1986, Hixon 1996) and grazing invertebrates (Sammarco & Williams 1982). Experimental removals of damselfishes usually result in a substantial increase in feeding by roving grazers within territories, with a concomitant reduction in algal biomass (Mahoney 1981, Kohda 1984, Hourigan 1986, Foster 1987). Solitary grazers are often excluded from territories and may avoid areas where damselfish territories are dense (Doherty 1983). In contrast, schooling species may gain a foraging advantage by swamping territory owners and accessing defended food supplies (Robertson et al. 1976).

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Effects on benthic algal assemblages The most obvious impact of territorial damselfishes is on the benthic algal assemblage within their territories, to the extent that territory boundaries are often recognised by the distinct changes in algal assemblages. There is evidence for differences in algal biomass (standing crop), productivity, nitrogen fixation, species composition, diversity and successional patterns between territories and surrounding areas. Although the following sections review the available evidence for each of these effects separately, we emphasise that they are interrelated because each effect may contribute to, or be the consequence of, other effects.

Biomass Comparison of all published data shows that algal biomass was generally higher inside territories compared with adjacent undefended areas (Table 3) but that coverage is limited, including Table 3 Algal biomass measured inside and outside damselfishes territories. Ratios for exposed inside/ outside, caged/inside and caged/exposed comparisons are given. Studies were included only if an insideoutside comparison could be made. *Only one study found higher biomass outside territories than inside, and that was not from a coral reef. GBR, Great Barrier Reef; PNG, Papua New Guinea; n.a., not available.

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only eight species from four genera of damselfishes. Importantly, even within this limited dataset, estimated increases in biomass varied substantially, between 15% and 2800% (i.e. a 28-fold increase). Although Montgomery (1980a) found algal biomass to be higher outside territories, this study was not from a coral reef but a rocky reef (see also Jones 1992). Unfortunately it is difficult to compare actual biomass data among studies because different studies have used different measures (wet weight, dry weight and decalcified dry weight). Although experimental evidence for the causes of the increased biomass inside territories is very limited, available evidence suggests that the main mechanism is the reduced total herbivory due to territorial defence by the resident damselfish, but that other factors are also involved. Of the two coral reef studies that have experimentally removed damselfishes from their territories to measure effects on benthic communities (Brawley and Adey 1977, Mahoney 1981), both recorded a rapid reduction in algal biomass shortly after the removal of the resident damselfish. A number of caging studies have also shown that herbivore exclusion leads to increased biomass adjacent to territories (Sammarco 1983, Wilkinson and Sammarco 1983, Wilkinson et al. 1985, Hixon and Brostoff 1996). However, as Russ (1987) stated, enhanced biomass can arise either from enhanced production (“farming”) or reduced consumption. Neither caging nor damselfish removals distinguish between damselfish effects on herbivory (algal consumption) and on algal growth (production). Russ (1987) further suggested that, despite evidence of bite rates in other studies, actual tissue removal rates may be similar inside and outside damselfish territories. In one case (Sammarco 1983), biomass was higher within territories with resident damselfishes, than within complete herbivore exclusions. However, this pattern was observed early in the experiment, and algal biomass was later higher inside herbivore exclusion cages. The relative roles of reduced consumption by herbivores and increased productivity due to some farming activities in contributing to biomass within territories remain unclear. The considerable variability in effects on biomass, suggested by within/out biomass ratios that vary over several orders of magnitude (Table 3), probably reflects spatial, temporal and interspecific variation, both among damselfishes, and among algal floras, although again there is little conclusive evidence. Klumpp et al. (1987; also Montgomery 1980a,b for rocky reef) noted seasonal differences in algal standing crop both within and outside territories and Klumpp et al. (1987) also showed differences among species of Stegastes at different reefs and within the same reef. Preliminary data comparing algal abundance inside and outside territories on fringing reef of the central GBR (Fig. 3) provide clear evidence both of differences within species among zones and within zones among species. Although not from a coral reef, interspecific differences were demonstrated even more dramatically by Montgomery’s (1980b) study, in which two species of damselfishes had very different effects. In one case, Microspathodon dorsalis territories had much lower algal biomass than the area outside, whereas territories of Stegastes rectifraenum were not noticeably different to the surrounding algal mats. Both Montgomery’s (1980b) results and our own (Fig. 3) suggest the important differences in impacts among species with more or less distinct territories. Montgomery’s (1980a) exceptional finding of low inside to outside biomass ratio is interesting, because it appears to reflect the high biomass of non-territory algal mats on these rocky reefs, apparently due to low herbivory outside territories. In this system, removal of the damselfish amounted to a reduction in herbivory, and led to an increase in territorial algal biomass (cf. Brawley & Adey 1977, Mahoney 1981). This may indicate that damselfish behaviour is not necessarily directed at increasing biomass finding but at a particular optimum biomass or state, independent of the external assemblage. Thus, some of the variation in 366

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Figure 3 Percent cover of algal turf and encrusting coralline algae inside and outside the territories of three species of damselfishes on three reef flat zones and the reef crest in Nelly Bay, Magnetic Island, near Townsville Australia. Reef flat zones are defined according to the predominant substratum types as follows: Flat 1: rubble/sand; Flat 2: rock/sand; Flat 3: dead coral. Stegastes apicalis territories are clearly distinguishable by the visually distinct algal composition, whereas those of Pomacentrus wardi and P. tripunctatus are not easily recognised. The consistent effects of the last two species, although smaller than those of Stegastes apicalis, suggest that these less noticeable species may make potentially important contributions to the overall impacts of the guild. Cover data were estimated using a dissecting microscope on samples of substratum chipped or broken off; the microscopic scale of cover estimation makes these data a good proxy for biomass. Cover was estimated by recording taxa present every 2 mm along four random 4-cm long transects for each of five samples of substratum each from six territories (and adjacent non-territories) per zone, using sample means (thus data are mean ±S.E. of 120 transects).

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Figure 4 Productivity inside and outside territories of five species of damselfishes. a) Motupore Island, PNG, n=12 inside, 8 outside Klumpp et al. 1987; b) Davies Reef, GBR; n=8 April, 4 August, Klumpp et al. 1987; c) Myrmidon Reef, GBR, n=6 each, Klumpp et al. 1987; d) Davies Reef, GBR, n=4 each, Klumpp et al. 1987; e) Myrmidon Reef, GBR; n=48 each, Russ 1987; f) Gulf of California, Mexico (rocky reef); n=November inside 6, outside 10, January inside 14, outside 23, Montgomery 1980a.

biomass effects may reflect differences in algal standing crop and intensity of herbivory outside territories, rather than different territorial composition. The increases within territories may be significant at the whole reef scale. Extrapolation of data from Klumpp et al. (1987) indicates that damselfish territories may be potentially contributing as much as 25–35% of reef-wide biomass, enhancing total reef algal biomass by 5–20% (based on Fig. 4 and Table la in Klumpp et al. 1987, where territories covered ~22% of the study reef transects, algal biomass was 1.2–1.9 times larger inside S. apicalis and S. nigricans territories, and assuming that biomass ratios are consistent for territories and non-territories throughout the reef). Although from a rocky reef, not a coral reef, similar calculations for the study by Ferreira et al. (1998) in southeastern Brazil indicate that the presence of damselfish territories increased the overall biomass at the study site by about 44% to 65%, contributing 368

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82% of biomass (S. fuscus territories occupied more than 70% of the substratum; biomass inside territories was enhanced by 62.6% in winter and by 65.9% in summer). Although these values are extremely rough, and should be taken only as indications, they nonetheless suggest that the damselfishes may be having significant overall effects at scales beyond the areal cover of their territories. Furthermore, these estimates are based on damselfish species that maintain visually distinct territories and may therefore ignore the potentially significant contribution of species with less recognisable territories (Fig. 3).

Productivity Measurements of algal productivity associated with damselfish territories exist for only four fish species from three coral reef locations (Klumpp et al. 1987, Russ 1987) and one species from a tropical rocky reef (Montgomery 1980a), but in each of these cases, productivity was markedly higher within territories than outside (Fig. 4). Interestingly, Montgomery (1980a) and Klumpp et al. (1987) found that productivity was not only higher per unit area but also per unit algal biomass. That is, the higher productivity did not simply reflect the higher standing crop but enhanced productivity of the algae themselves. Three factors may contribute to this enhanced productivity (Klumpp et al. 1987): (a) maintenance of algae at a size which maximises growth rates; (b) enhanced productivity due to nutrient enrichment, resulting from enhanced nitrogen fixation (see next section) or from cycling of resident fishes faeces; (c) selective removal of low-productivity algae. There is very little evidence to distinguish between these factors. Montgomery (1980a,b) suggested that the grazing rate of Microspathodon dorsalis maintained algae at a small size, where growth was exponential. However, assuming that areal growth (i.e. per unit area) shows a sigmoidal response to abundance or size, then specific growth rates (i.e. per unit algal biomass) will be maximum at intermediate abundances or sizes (i.e. the first derivative of the areal rates). Thus if damselfish territories create herbivory regimes intermediate between the very high herbivory of coral reefs generally, and the low herbivory within cages (Hixon and Brostoff 1983, 1996) or on Montgomery’s (1980a,b) rocky reefs, then algae within territories may be maintained at maximal specific growth rates (Klumpp et al. 1987). However, there do not appear to be any direct measurements to test this hypothesis. Evidence exists for nutrient supplementation within territories by nitrogen fixation or by faeces-derived fertilisation, as discussed in the next section. However, there is very little evidence for the effect these supplements might have on productivity. Ferreira et al. (1998) found no direct effect of faecal fertilisation on algal communities inside rocky reef territories, but this may reflect insufficiently sensitive experimental design (due to insufficient power to detect small effects, or to incompletely effective or confounded experimental treatments). Similarly, selective “weeding” or “gardening” behaviour has been suggested to favour more productive algal species (Lassuy 1980, Klumpp et al. 1987, Russ 1987). However, there are no direct comparisons of productivity of algae that were “weeded” from the territories and those that were left to grow. Thus, explanations of the differential productivity inside and outside territories remain largely speculative. The effects of damselfishes on productivity appear to vary considerably among locations, seasons and species (Fig. 4 and references therein). Productivity outside territories is known to vary over gradients at different spatial scales, including depth (Nelson & Tsutsui 1981), locations within a reef (Hatcher 1981, Klumpp & McKinnon 1989) and different reefs 369

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across the continental shelf (Russ & McCook 1999). Presumably the impact of the damselfishes will depend on the extent to which the particular species modifies its territory (e.g. Montgomery 1980b). Damselfish territories may make significant contributions to reef productivity at larger scales. Extrapolation of the data in Klumpp et al. (1987) suggest that damselfish territories potentially enhance algal productivity by 28% to 66%, and contribute ~50% of total reef algal production (Klumpp et al. 1987, their Fig. 4 and Table 1a, calculations and assumptions as for biomass estimates in previous section).

Nitrogen fixation and fertilisation There is particularly little evidence available on the contributions and roles of damselfishes to nutrient dynamics, and none for any nutrients except nitrogen. Russ (1987) found nitrogen content of algal turfs in Stegastes fasciolatus territories to be higher than in adjacent areas, whether measured as areal nitrogen content, or as C: N ratios. This nitrogen could be derived directly from enhanced fixation of gaseous nitrogen, or from enhanced capture and cycling within the territory. Only two studies have directly measured nitrogen fixation inside and outside damselfish territories (Wilkinson & Sammarco 1983, Wilkinson et al. 1985) and both found areal fixation rates to be consistently lower inside Hemiglyphidodon plagiometapon territories than outside, despite considerable seasonal variation. Fixation rates were lower still inside caged areas. The only other indications of nitrogen fixation rates come from relative abundances of blue-green algae (Cyanophyta), which are the primary nitrogen fixers on coral reefs (Margue & Holm-Hansen 1975, Wiebe et al. 1975, Larkum et al. 1988). A number of studies (Table 4) have found abundance of blue-green algae to be higher inside damselfish territories (Lobel 1980, Russ 1987), whereas others have observed the opposite pattern (Montgomery 1980a, but see Montgomery 1980b, Sammarco 1983) or no difference (Ruyter van Steveninck 1984, Hixon & Brostoff 1996). The relative contributions of nitrogen cycling processes and availability have also been studied very little but it appears likely that territories serve to capture and retain organic nitrogen. In particular, it has been suggested that fertilisation by localised deposition of resident fishes faeces and dissolved ammonium may significantly enhance nitrogen levels within territories (Polunin & Koike 1987, Klumpp & Polunin 1989). The availability of this nitrogen to damselfishes or other grazing organisms is unknown.

Taxonomic composition A number of studies have documented differences in taxonomic composition of algal communities inside damselfish territories and those found in surrounding areas (Table 4). In general, algal assemblages found inside damselfish territories appear to be dominated by filamentous rhodophytes (red algae) and cyanophytes (blue-green algae), and relatively fine corticated rhodophytes, whereas outside territories tougher, thicker algae were more abundant, often including both upright and encrusting calcified taxa (references in Table 4). Several algal taxa appear to be common to territories of several fishes species across a number of geographic locations. For example, Polysiphonia spp. (Rhodophyta, Ceramiales, Rhodomelaceae) were common in the territories of Hemiglyphidodon plagiometapon in Yap, Eupomacentrus lividus in Guam (Lassuy 1980), Microspathodon dorsalis in the Gulf of 370

Table 4 A summary of studies that have described algal species composition inside and outside damselfishes territories. Only the few most abundant or proportionally dominant species of algae are recorded here, with blue-green algae marked in bold letters. #, in some studies, settlement plates were used to quantify algal taxonomic composition. DAMSELFISHES AND BENTHIC COMMUNITIES ON CORAL REEFS

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California (Montgomery 1980a), Stegastes apicalis (Klumpp & Polunin 1989) and S. fasciolatus (Russ 1987) on the Great Barrier Reef, and S. apicalis in the Gulf of Thailand (Kamura & Choonhabandit 1986). The morphologically similar Centroceras clavulatum (Rhodophyta, Ceramiales, Ceramiaceae) was one of the dominant species in the territories of Eupomacentrus lividus in Guam (Lassuy 1980), Hemiglyphidodon plagiometapon (Sammarco 1983) and Stegastes apicalis (Klumpp & Polunin 1989) on the Great Barrier Reef, and S. fasciolatus in Hawaii (Hixon & Brostoff 1983, 1996). The closely related and morphologically very similar Ceramium flaccidum (Rhodophyta, Ceramiales, Ceramiaceae) was common in Stegastes fasciolatus territories on the Great Barrier Reef (Russ 1987). The fine corticated Gelidiopsis (Rhodymeniales, Rhodymeniaceae) was common in the territories of Hemiglyphidodon plagiometapon in Guam, Eupomacentrus lividus in Yap (Lassuy 1980), E. planifrons in Florida (Ruyter van Steveninck 1984), and Stegastes apicalis on the Great Barrier Reef (Klumpp & Polunin 1989) and in the Gulf of Thailand (Kamura & Choonhabandit 1986). Despite these similarities, there is also evidence that the effects of particular damselfish species on algal composition can vary between geographical locations (Brawley & Adey 1977). Table 4 provides comparison of algal composition for S. fasciolatus in Hawaii (Hixon & Brostoff 1981, 1983, 1996) and on the Great Barrier Reef (Russ 1987), for Hemiglyphidodon plagiometapon in Yap (Lassuy 1980) and on the Great Barrier Reef (Sammarco 1983), and Stegastes apicalis for the Gulf of Thailand (Kamura & Choonhabandit 1986) and the Great Barrier Reef (Klumpp & Polunin 1989), although these comparisons would be confounded by numerous other potential sources of variation. In each case, species and genus composition differed notably between locations, both within territories and outside territories. A preliminary study done in Nelly Bay, Magnetic Island, Australia, suggests that the taxonomic composition of algae in different species’ territories varies between the zones of a single reef flat (Fig. 5). Furthermore, the same species appears to affect the algal community differently in each reef flat zone. It therefore follows that generalisations made about the taxonomic preferences of even a single damselfish species must be made with caution. Overall then, many territorial damselfish species may have similar preferences in algal composition of their territories but that the expression of these preferences is dependent on the “background” pool of available species. The available data are insufficient to suggest general interpretations of preferences against this background variation. Most studies offer only a snapshot of the composition of the algal community in time and space, because most were done at one geographic location and at one time, and most provide no indication of spatial variation in algal composition within territories for comparison with outside areas. While there are clearly effects at the scale of individual territories, whether larger-scale patterns in the distribution of algae are affected by damselfishes remains unexplored. Several mechanisms have been proposed to explain the distinct algal flora of damselfish territories, including non-selective grazing at intermediate intensities that provides competitive advantages to the dominant species (Montgomery 1980a, Hixon & Brostoff 1983), selective consumption of other species such as larger macroalgae, or from “weeding” behaviour, which selectively removes other species without consumption (Lassuy 1980). It is also likely that fertilisation would favour particular groups (McClanahan 1997). Although Lassuy (1980) and Irvine (1980) have documented “weeding” of larger macroalgae, there is very little evidence to distinguish between these mechanisms, or to demonstrate their sufficiency as causes. Furthermore, the interpretation of the effects on algal composition is

372

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Figure 5 Percent cover of most abundant algal taxa inside and outside the territories of three species of damselfishes on three reef flat zones and the reef crest in Nelly Bay, Magnetic Island, near Townsville Australia (see Fig. 3 caption for methods). Taxa are, roughly in order from delicate to tough: 1) Polysiphonia, 2) Leveiella, 3) Gelidiopsis, 4) Laurencia, 5) Jania, 6) Amphiroa, and 7) crustose coralline algae. Most algal taxa are more abundant inside territories than outside, except for crustose coralline algae, which exhibit a higher cover outside in most Pomacentrus wardi territories and all Stegastes apicalis territories. Also in the territories of these species there is a rough trend for delicate algae to be more abundant inside territories and tougher taxa to be predominant outside.

hindered by the lack of experimental evidence about the value or purpose of the differences in algal composition, such as increased productivity.

Diversity and damselfishes territories as a test of the intermediate disturbance hypothesis

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Figure 6 A comparison of: a) algal species richness, b) diversity and c) evenness inside and outside the territories of damselfishes. 1: Eupomacentrus partitus, Florida Keys, Ruyter van Steveninck 1984; 2a: E. planifrons, Ruyter van Steveninck 1984; 2b: E. planifrons, Puerto Rico, Hinds & Ballantine 1987; 3a: Hemiglyphidodon plagiometapon, Britomart Reef, GBR, Sammarco 1983; 3b: H. plagiometapon, Yap, Lassuy 1980; 4a: Stegastes fasciolatus, Hawaii, Hixon & Brostoff 1981; 4b: S. fasciolatus, Hawaii, Hixon & Brostoff, 1996; 5: S. lividus, Guam, Lassuy 1980.

Despite the relatively limited data on species compositions, algal communities within damselfish territories are widely considered to be more diverse than surrounding algal turfs (Lassuy 1980, Hixon & Brostoff 1983, Ruyter van Steveninck 1984, Hinds & Ballantine 1987, Hixon 1996). A comprehensive review of the literature confirms that algal species richness was higher inside territories in most cases (Fig. 6a), and this was true despite large variations in the absolute number of algal taxa found within territories at different geographic locations. However, in contrast to species richness, there were no consistent patterns in diversity 374

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and evenness indices of the algal communities (Fig. 6b,c). Diversity (H’) was higher inside the territories of Stegastes lividus in Guam (Lassuy 1980) and S. fasciolatus in Hawaii (Hixon & Brostoff 1981, 1996) than in undefended areas, but not in the territories of Hemigliphidodon plagiometapon in Yap (Lassuy 1980). Species evenness (J’) was only higher in the territories of Stegastes fasciolatus, and only in the latter part of Hixon & Brostoff’s (1996) study. Lassuy (1980) provides results of caging experiments conducted in Guam and Yap. In Guam, diversity and evenness were lowest in caged territories of S. lividus, and highest in caged areas adjacent to damselfish territories. In Yap, diversity and evenness were also highest in caged areas outside the territories of Hemiglyphidodon plagiometapon, but they were lower in uncaged than in caged territories (Fig. 6b,c). Thus, no simple conclusions can be drawn on the effects of damselfish territories on algal diversity, perhaps because the different measures of diversity may be affected by different mechanisms (Rosenzweig 1971, Routledge 1983) As diversity is a derived property of the species composition, the lack of evidence on the causes of patterns in taxonomic composition (as discussed above, p. 370) also amounts to a lack of evidence for the causes of any effects on diversity. Thus, although often assumed to result from intermediate grazing intensities within territories, it remains possible that selective feeding, weeding or fertilisation effects are also involved. Hixon & Brostoff (1983) were the first to attempt to explain patterns of algal diversity in relation to damselfish territoriality, using damselfish territories as an elegant experimental test of Connell’s (1978) intermediate disturbance hypothesis (IDH). This hypothesis predicts that diversity is highest under a disturbance regime of intermediate frequency and intensity and declines when disturbance declines or increases in intensity and frequency. Damselfish territories are considered to be intermediate in grazing intensity between the intense grazing of undefended reef substratum, and the minimal grazing in caged areas (Hixon & Brostoff 1983, 1996, Ferreira et al. 1998). Interpreting grazing by herbivorous fishes as a form of disturbance of benthic communities (Lubchenco & Gaines 1981, Carpenter 1986), Hixon & Brostoff (1983) showed that algal assemblages within the territories of Stegastes fasciolatus in Hawaii suffered intermediate bite rate densities compared either with turfs protected from grazing in cages or with those exposed to natural levels of herbivory. Algal diversity was highest in the damselfishes territories, thus conforming to the predictions of the IDH. However, there are several limitations to these results as a test of Connell’s predictions. Although the results are consistent with the IDH, their experimental design did not distinguish between intermediate herbivory and other factors that may contribute to diversity. Intensity of herbivory (as measured by bite rates) may be intermediate in territories, but damselfishes have more complex effects (selective feeding, weeding and fertilisation) which may confound the effects of herbivory, and damselfishes do not feed in the same manner as the general roving herbivores found outside their territories (Choat 1991). Furthermore, Russ (1987) suggested that if the biomass of algae removed per bite is higher in territories, then bite rates may not be an accurate indication of herbivory levels. Finally, although diversity was increased in Hixon & Brostoff’s (1983) study, this was not a general pattern, so that damselfish territories in general would not seem to provide support for the IDH, depending on other sources of physical or biotic disturbance(S, H’ or J’; Fig. 6). At larger spatial scales, it is clear that the presence of damselfish territories increases the overall spatial heterogeneity in the algal communities, suggesting that they would enhance overall diversity. In particular, Hixon & Brostoff (1996) found that S. fasciolatus territories constitute a distinctly different assemblage in multivariate species space, thus increasing 375

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the overall diversity of the system. The algal flora of territories may not necessarily represent a subset of the non-territorial species pool but may contribute a substantial part of the overall species pool. Given the more intense herbivory outside territories which limits most algae to relatively small size, and vegetative growth, refuges such as damselfish territories may provide important opportunities for many taxa to achieve the larger size needed for reproduction and population maintenance. Finally, it should be recognised that the relatively low number of species outside territories may be scale dependent and a result of the low biomass. The overall low algal abundance will mean that small sampling areas will not necessarily accurately represent the overall diversity of the zone or reef.

Damselfish territories as tests of herbivore effects on successional trajectories Several authors have considered damselfish effects in terms of successional processes (Montgomery 1980a, McClanahan 1997). In a particularly elegant application of their data on S. fasciolatus territories, Hixon & Brostoff (1996) compared successional trajectories of algal communities on settlement plates in their three treatments (territories, outside territories and caged). Using multivariate analysis (detrended correspondence analysis) of the changes in species composition through time, they found that developing algal communities in territories followed a remarkably similar successional trajectory as complete herbivore exclusions but only followed the trajectory partway. In contrast, heavily grazed non-territorial plates followed another trajectory. Thus, over the year of the experiment, the developing algal assemblage in complete herbivore exclusions was initially dominated by filamentous green and brown taxa, which were replaced by filamentous red algae, and ultimately by more robust, thick filaments and “blades”. Damselfish territories developed very similar assemblages of filamentous green and brown algae, and later filamentous red algae, but the progression was slower than on caged plates and did not develop the thicker and more robust algal forms. Plates exposed to background herbivore intensities outside territories developed directly from filamentous green and brown algal assemblages to a distinctly different assemblage, dominated by algal crusts and mats. Hixon & Brostoff (1996) applied these results to models of herbivore impacts on successional change, in which herbivore feeding preferences (or weeding behaviour) are considered in combination with the roles of target algal taxa as early or late successional taxa, and as facilitating, tolerating or inhibiting subsequent colonists (see also Lubchenco & Gaines 1981, Farrell 1991, Glenn-Lewin & van der Maarel 1992, Sousa & Connell 1992). Herbivores can have three different effects on successional trajectories: 1) Deceleration of successional rate occurs when herbivores prolong an intermediate successional stage, and inhibit the establishment of later species; 2) Acceleration takes place when early species are inhibited to the benefit of later species; 3) Deflection occurs when herbivores cause early species to be replaced by others absent or rare in ungrazed systems. Hixon & Brostoff (1996) suggested that successional patterns in the damselfishes’ territories demonstrate deceleration of the ungrazed trajectory, with intermediate herbivory prolonging 376

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an intermediate successional stage, whereas the heavily grazed condition demonstrates “deflection”, in which the succession followed a distinctly different pathway in species composition. Thus their results not only demonstrate the importance of herbivory to succession, but the potential for very different effects. The interpretation of changes in damselfishes territories are still confounded to some extent by the more complex effects of damselfishes on algal composition but the very strong similarity between trajectories in ungrazed cages and in territories suggests that these effects are minimal. These results also demonstrate the value of considering successional trajectories in terms of the trade-offs in life-history traits of plant species (Huston & Smith 1987, McCook 1994, McCook & Chapman 1997) because the ability of different algal groups (fleshy macroalgae versus filaments versus crusts) to maintain populations in the face of different intensities of herbivory was apparently crucial to the successional pathway that occurred.

Effects on corals Damselfishes have been attributed an important role in determining the distribution and abundance of corals in one study. Wellington (1982) proposed that damselfishes play a key role in determining the depth zonation of massive and tightly branching corals in Panama. High damselfish densities increased the mortality of massive corals in shallow water, facilitating the settlement of branching Pocillopora spp. In deeper water, the lack of topographic complexity limited the damselfish population, allowing massive Pavona gigantea colonies to achieve greater abundance. This indicates that effects on corals vary with coral species and morphology. Wellington (1982) quantified mortality of P. gigantea colonies inside and outside Eupomacentrus acapulcoensis territories on a fringing reef in the Gulf of Panama. Approximately 90% of colony mortality occurred inside damselfish territories in shallow water, and almost 100% in deep water. There are no other studies to suggest that damselfishes have a general effect on the broad scale zonation of corals, despite 20 further years of study. However, they clearly influence the abundance and diversity of corals on the scale of individual territories, potentially accounting for local-scale patchiness in coral distributions. There are at least six different mechanisms by which damselfishes may either directly or indirectly affect coral recruitment or abundance. Some of these may reduce coral abundance whereas others may facilitate recruitment and growth of certain species. First, because the territories of many species are sites of increased algal biomass, this increased biomass interferes with the settlement, survival and growth of hermatypic corals through algal overgrowth or increased sedimentation (Vine 1974, Potts 1977, Lobel 1980, Sammarco et al. 1986). In an experiment to test the survivorship of Acropora palifera inside and outside the territories of Dischistodus perspicillatus, Potts (1977) found that the colonies were adversely affected only by the presence of the algal mats within the territories. The coral did not display lesions from fishes bites and was reportedly unharmed by direct overtopping or smothering by the algae. Instead, the algal mat and sediment trapped within it damaged the basal tissues of the corals, affecting the growth rate and survivorship of the colonies. Second, many damselfishes actively remove coral recruits and kill areas of coral to establish new substrata for algal growth (Kaufman 1977, Robertson et al. 1981, Wellington 1982). Wellington (1982) observed that in order to enlarge their territories, individual 377

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Stegastes (Eupomacentrus) acapulcoensis killed portions of the adult corals surrounding their territories by biting the live tissue at the edges of the colonies. Robertson et al. (1981) noted similar behaviour in the Caribbean damselfish S. planifrons. However, the actual area of coral killed by damselfishes and the influence on coral growth and mortality is unknown. A third mechanism by which damselfishes can reduce coral abundance is by facilitating the settlement of internal bioeroders onto dead or living coral (Kaufman 1977, Risk & Sammarco 1982, Sammarco et al. 1986, Letourneur et al. 1997). Bioerosion is known to influence the maximum size of coral colonies and weakens their structure, making them more susceptible to physical damage (Hein & Risk 1975, Risk & Sammarco 1982). Differences in internal bioerosion of corals inside and outside Hemiglyphidodon plagiometapon territories were examined at Britomart Reef, on the Great Barrier Reef (Risk & Sammarco 1982). The density of internal bioeroders inside territories was increased by ~22% with respect to areas outside territories. Therefore, although territories in the study site received almost half of all coral recruits, adult colonies inside territories were affected by 86.6% of the internal bioerosion in that area. In a fourth mechanism, Lobel (1980) suggested that the presence of territories weakens the structure of the reef framework itself because damselfishes exclude crustose coralline algae and thus inhibit the cementation of loose rubble. Other activities of damselfishes may enhance the abundance of corals. Territorial defence by damselfishes can reduce bioerosion caused by scraping scarids (Sammarco et al. 1986, Letourneur et al. 1997). The recruitment and survival of some coral species has been found to be higher inside damselfish territories (Gleason 1996), particularly species otherwise rare in the habitat (Sammarco & Carleton 1981, Sammarco & Williams 1982). The enhancement of rare species in territorial patches has the effect of increasing overall coral diversity (Sammarco & Carleton 1981). Sammarco & Carleton (1981) calculated that H. plagiometapon territories take up 14% of the study site on Britomart Reef, which consisted of an area behind the reef crest. Success of coral recruitment was five times higher inside damselfish territories than outside (70/600 cm2 inside, 14/600 cm2 outside), suggesting that nearly half (45%) of coral recruitment in that area occurs in damselfish territories. The “importance” of the territories therefore exceeded the proportion of the substratum their territories occupied. The last way in which damselfishes may enhance corals is through the exclusion of specialised corallivores, which are often prevented from feeding on live coral growing near or within territories (Wellington 1982, Glynn & Colgan 1988). Of particular importance may be the finding that the corallivorous starfish Acanthaster planci, which can occur in outbreak proportions, is often attacked by damselfishes. Their territories may therefore serve as coral refuges, which help the re-population of damaged reef areas (Glynn & Colgan 1988, Done et al. 1991). There has been no study designed to measure the relative importance of the above mechanisms on the distribution and abundance of corals. Although there are individual examples of some corals increasing and some decreasing within territories, the overall effect on coral assemblages awaits further consideration.

Effects on mobile invertebrates and fishes Damselfishes have the potential to facilitate and compete with a range of other mobile organisms associated with coral reef habitats, including invertebrates and other fishes. 378

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Changes in abundance may be caused by habitat modification induced by damselfishes. The density of small invertebrates (sometimes referred to as cryptofauna) is often higher inside territories of species maintaining a high biomass of turfing algae (Lobel 1980, Zeller 1988, Klumpp & Polunin 1989, Hixon & Brostoff 1996, Ferreira et al. 1998). High standing crops of algae inside territories may create refuges and enhance food supplies for cryptofaunal communities (Zeller 1988). In turn, these invertebrates are thought by some to remove a significant proportion of the algal productivity within territories (Brawley & Adey 1981, Klumpp et al. 1987, Klumpp & Polunin 1989). However, the ecological role of algal-dwelling invertebrates is poorly understood (Carpenter 1986, Hay et al. 1987). Herbivorous sea urchins, such as Diadema antillarum and Echinometra viridis, are treated as potential competitors and aggressively excluded from damselfish territories (Sammarco & Williams 1982, Kamura & Choonhabandit 1986). In areas where Diadema spp. and Echinometra spp. are abundant, damselfish territories may represent refuges from the destructive scraping of the sea urchins. Damselfish territories may represent important recruitment sites for some reef fishes. Green (1992, 1996, 1998) found that at least three species of reef fishes (Coris schroederi, Halichoeres melanurus and Scarus spp.) recruit in greater densities in damselfish territories than adjacent areas. The dense algal mats appear to offer recruiting fishes shelter from predation and supply greater amounts of food, whether the fishes eat algae or small invertebrates. Recruitment of potential competitors may be reduced inside territories. There is some evidence that some species of damselfishes aggressively exclude recruits of conspecifics and competing species from their territories (Ohman et al. 1998, Bay et al. pers. comm.). Risk (1998) found that Stegastes leucostictus reduced the settlement and the post-settlement persistence of Acanthurus bahianus. However, other species do not appear to exclude juveniles from territories and do not appear to influence their distribution and abundance (Booth & Beretta 1994, Gutierrez 1998). Hence, it is unclear whether herbivorous damselfishes can be ascribed a general role in determining fish recruitment patterns. Damselfishes are known to exclude many large herbivorous or predatory invertebrates from their territories through active defence (Sammarco & Williams 1982, Glynn & Colgan 1988). Likewise, many larger grazing fishes and potential egg predators are excluded through territorial aggression (e.g. Low 1971, Ebersole 1977, Itzkowitz & Slocum 1995). While territorial behaviour clearly influences the local distribution of subordinate species, the full extent of the effects of these interactions is uncertain. Long-term removal experiments indicate that aggressively dominant species of damselfish can reduce the abundance of other damselfishes (Robertson 1996). However, similar experiments have not been carried out to determine whether damselfishes have competitive effects on grazers from other taxa. Shortterm damselfish removals show that excluded species can rapidly exploit the high algal biomass found in territories of certain species (e.g. Mahoney 1981, Hourigan 1986) but it is not known whether this results in a long-term increase in food availability.

General discussion Although some herbivorous damselfishes have been ascribed keystone species status (Williams 1980, Hixon & Brostoff 1983) and their biology has been considered well known (Carpenter 1986), our review highlights the paucity of data on which the generalisations 379

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have been based. Certainly, some conclusions appear to have stood the test of time. As far as algae are concerned, biomass, productivity and species richness are generally higher in territories than surrounding areas. Also, territories tend to harbour filamentous red and bluegreen algae, as opposed to other algal groups. Delicate corticated red algae are commonly found inside territories, whereas crusts and upright calcareous species usually typify the surrounding areas. Most territories have the effect of reducing herbivory by other large grazing fishes, a factor that clearly contributes to the local-scale effects on algal communities. Some corals that are targeted by the damselfishes appear to decrease in abundance inside territories, while for others, territories may constitute a refuge from coral-feeding organisms. But do these patterns apply to all species? Of all the ways in which damselfishes can potentially affect communities, which are the most important? And what are the long-term demographic consequences for other organisms? In this review we have merely scratched the surface and found that many of the underlying questions remain unanswered.

Can we really generalise? We have grave concerns as to whether these generalisations apply to all herbivorous damselfishes. Not only has the research been limited to a few species, it has been biased towards particular species that maintain distinct algal mats (e.g. Hemiglyphidodon plagiometapon and Stegastes planifrons) (Fig. 1, p. 360). The fact that these species have an effect on the scale of individual territories is not surprising, as they were chosen because of their aggressiveness and the visually distinct algal mats within their territories. They may not be representative of other speciose genera, such as Chrysiptera, Plectroglyphidodon and Pomacentrus, which are often less aggressive and may have more subtle influences on benthic communities. These fishes make up a larger proportion of the community than the larger territorial species, and are more broadly distributed (Sale 1974, Robertson & Lassig 1980, Meekan et al. 1995, Lewis 1997). If these fishes also affect algal communities, then the impacts of herbivorous damselfishes on reef processes may not only be greater but also qualitatively different than presently assumed. Even if we ignore possible biases, other factors restrict our ability to make valid generalisations. The literature is also based on relatively few geographic locations (e.g. Great Barrier Reef, Caribbean). There is a lack of information on the spatial and temporal variability in both the damselfish community and benthic assemblages. Few studies were done at more than one place or time, and of those that were, a large degree of spatial and temporal variability was evident (Lassuy 1980, Klumpp et al. 1987, Ferreira et al. 1998). While we know that there are distinct distributions of species across typical shallow reef zones on coral reefs (e.g. Klumpp et al. 1987, Meekan et al. 1995), studies on impacts are usually restricted to a single habitat (Lobel 1980, Sammarco & Carleton 1981, Sammarco 1983). With such limited focus, effects that are characteristic of a particular zone could be unintentionally ascribed to the species as a whole.

How good are the data? Many feeding effects have been interpreted in the absence of data on actual diets and the degree of feeding selectivity (Wilson & Bellwood 1997). It is not possible to predict effects 380

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on the assumption that some damselfishes are grazers (non-selective feeders), while others are browsers (selective feeders). We do not know where most species sit in this continuum, or indeed, whether many are strictly herbivores at all. Arguments that damselfishes are grazers, based on gut contents or feeding observations, are potentially erroneous (Galetto & Bellwood 1994). A taxon contributing to only 1% of the composition within territories would take minimal selectivity to maintain but could easily go undetected in gut content analyses or feeding observations. There are few rigorous studies that indicate exactly what effects damselfishes have and how they have them. The potential roles of the four different “farming” mechanisms we identified (weeding, substratum preparation, fertilising and crop protection) have not been distinguished. There are several problems with simply comparing inside and outside territories, as many studies have done (Montgomery 1980a,b, Sammarco 1983, Klumpp et al. 1987, Hixon & Brostoff 1996). Differences are potentially the outcome of many different activities of damselfishes inside territories and other grazers which are excluded. Some studies assume these differences are due to differences in herbivory alone (e.g. Sammarco 1983, Wilkinson & Sammarco 1983, Hixon & Brostoff 1981, 1996). However, even when quantitative differences in feeding rates inside and outside territories are demonstrated, these differences do not preclude other mechanisms. Also, inside/outside comparisons are confounded by the fact that fishes choose where to establish territories in the first place. They are unlikely to set up territories on a random basis. Therefore, we may expect differences a priori, aside from any created by the fishes. Finally, these comparisons depend on what is outside territories. Most research appears to have been done on heavily grazed reefs, where the standing crop of macroalgae outside territories is relatively low (e.g. Sammarco 1983, Klumpp et al. 1987, Russ 1987, Hixon & Brostoff 1996). Most of the experimental studies that have been carried out are too simplistic to measure the relative importance of the different mechanisms. Experimental removals of damselfishes clearly implicate the role of territorial defence, as algal crops are often rapidly reduced by the influx of grazers (Brawley & Adey 1977, Mahoney 1981). However, these experiments do not have the necessary controls to isolate the direct effects of the damselfishes themselves. That is, where damselfishes are removed, an increase in feeding by other herbivores is confounded with the cessation of damselfish activities. Likewise, cages that are used to exclude both damselfishes and all other grazers (e.g. Brawley & Adey 1977, Mahoney 1981) do not allow their effects to be distinguished, without an orthogonal manipulation of the damselfishes. To measure damselfish effects, it is necessary to add an additional treatment in which other herbivores are caged out but direct access by damselfishes is permitted. Thus it is difficult to categorically interpret the role of herbivorous damselfishes within the constructs of succession or disturbance theory (see Hixon & Brostoff 1983, 1996), even though this may be important. There are many selective ways in which they may enhance or destroy algae or corals within territories and affect foraging by other potentially selective feeders.

Are there larger-scale effects? Most observations and experiments have been undertaken at the scale of individual territories. The larger-scale demographic consequences for species promoted or excluded by territorial behaviour, including algae, corals, invertebrates and fishes, are unknown. At a scale of individual territories, it is possible to conclude that some damselfishes exert 381

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a strong influence on benthic communities and affect the small-scale patchiness in their environment. Once damselfishes have selected preferred patches of substratum, they may further increase spatial heterogeneity through algal-farming activities (Sammarco & Carleton 1981). On the scale of a whole reef, such increased patchiness may increase diversity (Sammarco & Carleton 1981), and in doing so, play a key role in the maintenance of benthic diversity (sensu Levin & Paine 1974). Algae in territories may constitute a significant pool of species in the habitat (see diversity section). However, these largerscale roles need to be more fully assessed.

How do damselfishes benefit from their behaviour? A better understanding of the impact of damselfishes will come not only from a better distinction of mechanisms (disturbance, selective feeding, farming), but a clearer idea of the “purpose” and relative “benefits” of damselfish territoriality. Very little work has actually addressed the notion of purpose or function of different behaviours, whether aggression, weeding, killing coral and even eating algae. If the goal is to maintain a relatively high biomass filamentous turf, then the effects relative to areas outside territories will depend on what is actually outside. This goal may be a decrease in biomass, if fleshy macroalgal beds dominate the surrounding areas (e.g. inshore reefs) or an increase on reefs that are heavily grazed (e.g. offshore reefs). If it is the absolute biomass or productivity of algae that is important, inside/outside comparisons will miss the point completely. It is not clear whether the key function of damselfish territoriality is to increase biomass, productivity or alter the species composition of algae. The main benefit of territoriality will determine which variable is of fundamental importance and how they are related to one another. We can assume that fishes do not consciously aim to achieve derived properties such as successional trajectory or diversity. If the goal is to create a highly productive territory, it is probably productivity that dictates algal species composition, which grazers are excluded from territories, and so on. Perhaps the goal is to produce a sufficiently productive territory of algae of a certain nutritional quality or palatability. In this case, damselfishes may be manipulating both productivity and species composition. Biomass is not likely to be of critical importance because long-term survival and growth is not dependent upon how much food is present but how fast new food is available. Indeed, high biomass could be a liability because it attracts other herbivores. It is more likely that high biomass arises, either because productivity per unit area is maximised at higher biomass or that maximum biomass is set by preferred species composition. It must also be recognised that enhancing algae may not be a critical function at all. For example, Wilson & Bellwood (1997) showed that Hemiglyphidodon plagiometapon fed mainly on detritus sieved from the algae in its territory, while Zeller (1988) found that the guts of Stegastes apicalis contained a nutritionally significant amount of animal material. Thus damselfishes may be selecting and promoting species that are more efficient detritus collectors or invertebrate refuges.

How do damselfishes establish territories? Another distinction that is overlooked is the difference between the activities required to “establish” as opposed to “maintain” territories. Most of the research has concentrated on 382

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the latter and we do not have a clear idea how younger individuals acquire new territories or produce new algal mats. The relative importance of selective feeding and different farming activities is likely to change during this process, with substratum preparation more important in the early stages and territorial defence becoming increasingly necessary as higher quality resources are established. Clearly, the temporal dynamics of the algal and coral communities within damselfish territories must be investigated to resolve this issue. One of the common themes of this review is that all measured characteristics of the algal community, including biomass, productivity, diversity, and successional stage, were temporally variable. Monitoring must be coupled with studies on ontogenetic changes in the behaviour of damselfishes. Many reef fishes, including damselfishes, undergo a shift in habitat preference (Waldner & Robertson 1980, Lirman 1994, Tolimieri 1995, Danilowicz 1997) and diet (Letourneur et al. 1997) as they grow. One of the most widely studied species, Eupomacentrus (Stegastes) planifrons, undergoes an ontogenetic shift in habitat preference (Lirman 1994, Tolimieri 1995) but it is not clear whether individuals establish or inherit territories as adults.

Concluding remarks Some herbivorous damselfishes are of considerable importance in structuring the benthic communities within their territories and promoting spatial heterogeneity on coral reefs. However, the mechanisms responsible for these effects and the underlying reasons for them remain obscure. Clearly, the feeding biology and behaviour of a wider variety of damselfish species must be assessed. Herbivorous damselfishes can no longer be treated as a homogeneous group, either in terms of their behaviour or ecological role. They are a diverse familial guild and the few species that have been studied do not do justice to their variety in terms of their diets, feeding modes, agricultural activities and levels of aggression. Whether the generalisations we have identified survive in the long term will depend on the outcome of more sophisticated experiments that delve deeper into the functions of their unique patterns of behaviour.

Acknowledgements This manuscript benefited from discussions with L.Bay, A.Lewis and D.Klumpp. It was supported by an Australian Research Council Grant (to G.P.J) and funding from the Cooperative Research Centre for Reef Research (to L.J.M.).

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389

AUTHOR INDEX

References to complete articles are given in bold type; references to bibliographical lists are given in italics; references to pages are given in normal type.

Abades, S., 120; 149 Abbot, D.P. See Morris, R.H., 91 Abdel-Gawad, A.M. See Mona, M.H., 91 Abe, N., 13, 22, 23, 28, 47, 50, 77; 78 Abello, P. See Gili, J.-M., 84 See Ramón, M., 160 Able, K.W. See Heck Jr, K.L., 297 See Rountree, R.A., 290; 301 See Sogard, S.M., 282, 283, 285; 301 See Szedlmayer, S.T., 284, 285, 291; 302 See Wilson, K.A., 303 Abraham, M.J. See Paul, M., 93 Acosta, C.A., 326; 341 Adal, M.N., 183, 193; 199 Adams, C.A. See Carr, W.E.S., 280; 295 Adams, S.M., 273, 274, 280, 281, 282, 290; 293 See Thayer, G.W., 302 Adey, W.H. See Brawley, S.H., 365, 366, 371, 372, 379, 381; 384 Adkins, B.E. See Harbo, R.M., 155 Agassiz, A., 47; 78 Agrenius, S. See Rosenberg, R., 266 Aharon, P., 131; 149 Åkesson, B., 213; 229 Alcaraz, M., 335; 341 See Saiz, E., 335; 351 Aldrich, F.A. See Morris, C.C., 127; 159 Allard, D.J. See Jones, D.S., 156 Allen, B.J. See Padilla, D.K., 234; 266 Allen, G.R., 357, 360, 364; 383 See Randall, J.E., 387 Allen, J.A. See Turekian, K.K., 164 Allen, M.J., 11, 22, 26, 75; 78 Allmon, W.D., 131; 149 See Jones, D.S., 137; 156 Al-Ogily, S.M., 13, 22, 44, 53; 78 See Knight-Jones, E.W., 87 Al-Roumaihi, E.M.H. See Richardson, C.A., 161 Alvariño, A., 51; 78 Alvsvåg, J. See Jennings, S., 230

Al-Wahaibi, D. See Shepherd, S.A., 162 Ambler, R.P. See Canete, J.I., 15; 79 Ambrose, W. See Jones, D.S., 156 Ambrose, W.G. See Ólafsson, E.B., 266 Ambrose Jr, W.G. See Gee, J.M., 230 See Irlandi, E.A., 297 Amft, J. See Wenner, E., 353 Anderson, D.T. See Andrews, J.C., 9, 18, 26, 27, 37, 54; 78 Anderson, E.E., 290, 293; 294 Anderson, J.D., 322; 341 Anderson, P.T. See Marsden, J.R., 18, 35, 37, 44, 45, 47; 89 Andreasson, F.P., 133; 149 Andrew, N.L. See Jones, G.P., 358, 361; 385 Andrews, J.C., 9, 18, 26, 27, 37, 54; 78 Aneer, G. See Jansson, B.O., 297 Ansari, Z.A., 287, 288; 294 Ansell, A., 104; 149 Ansell, A.D., 169, 190, 194, 195; 199 See Hughes, D.J., 264 Antoine, L., 105; 149 Anwar, N.A., 107, 113, 114, 147; 149 Ap Gwynn, I., 25; 78 Appeldoorn, R.S. See Granna-Raffucci, F.A., 122; 154 Arkhipkin, A., 126, 127, 128; 149 Arkhipkin, A.I., 127; 149 See Bizikov, V.A., 128, 129; 150 Armstrong, D.A. See Palacios, R., 159 Arnold, C.R. See Holt, S.A., 297, 346 Arnold, G.P., 306, 314, 315, 322, 323, 330, 334; 341 See Greer Walker, M., 345 See Harden Jones, F.R., 346 See McCleave, J.D., 348 See Metcalfe, J.D., 349 Arnold, W.S. See Jones, D.S., 156 Arrivillaga, A., 281, 282; 294 Arthur, M.A., 136; 150 See Bice, K.L., 150 See Jones, D.S., 156

391

AUTHOR INDEX

Aruna, C. See Mohan, P.C., 3; 91 Ashton, T.T., 18; 78 Aspden, K.R.H. See Seliger, H.H., 351 Atapattua, D. See Tait, N.N., 97 Atema, J. See Karnofsky, E.B., 298 Atkinson, R.J.A., 244, 258; 263 See Hughes, D.J., 250; 264 See Nash, R.D.M, 265 See Nickell, L.A., 265 Attrill, M.J., 287, 288; 294 See Jackson, E.L., 269–303 Augener, H., 43, 63; 78 Austin, A.P. See Dasgupta, S., 7, 8, 77, 78; 81 Avalos-Borja, M. See Shepherd, S.A., 121; 162 Azariah, J. See Whitin, N., 33; 100 Azuma, M. See Tanaka, M., 352 Baba, K., 61; 78 Babbage, P.C., 25, 77; 78 See King, P.E., 87 Bach, S.D., 281; 294 Bachelet, G., 104; 150 Baer, J.G., 62, 63; 78 Bagaveeva, E.V., 57, 76, 77; 78 Baglivo, J.A. See Brousseau, D.J., 110; 151 Bailey, J.H., 40; 78 See King, P.E., 87 Bailey-Brock, J.H., 9, 43, 61, 63; 79 See Vine, P.J., 51, 61; 99 Baird, D. See Hanekom, N., 283; 297 See Melville-Smith, R., 348 Baker, S.M., 170; 199 Balch, N., 126; 150 Balguerías, E. See Raya, C.P., 160 Ballantine, D.L. See Hinds, P.A., 371, 373, 374; 385 Balson, P.S. See Hickson, J., 155 See Johnson, A.L.A., 156 Baltazar, M. See Gutiérrez, D., 264 Baltz, D.M., 285; 294 See Arrivillaga, A., 281, 282; 294 Bamber, S. See Moore, A., 349 Barans, C. See Wenner, E., 353 Barbary, M.S. See Mona, M.H., 91 Barber, V.C., 179, 180, 181, 185, 192, 193; 199 Barbin, G.P., 323, 332; 341 Barbin, V., 107, 141, 144; 150 Bard, E. See Cornu, S., 152 Barker, M. See Chia, F.-S., 24; 80 Barker, R.M., 115, 117; 150

Barnes, R.D., 238; 263 Baross, J.A. See Jumars, P.A., 265 Barrett, R.L. See Southward, A.J., 267 Bartels, M. See Hardege, J.D., 85 Bartolini, M. See Jordan, F., 298 Barton, R. See Ap Gwynn, I., 78 Bartsch, J., 313; 341 Bauer, R.T., 289, 290; 294 Bauer, S. See Bricelj. V.M., 199 Bax, N.J., 275, 276, 279; 294 Baxter K.N. See Fore, P.L., 318; 344 Beal, B.F. See Peterson, C.H., 159 Beardsley, G.L., 318; 341 Bech, I.M. See Rosenberg, A.A., 162 Beck, P. See Hurley, G.V., 124; 155 Beck, P.C. See Perez, J.A.A., 159 Becker, K., 52; 79 Beckmann, M., 55; 79 Beckmann, T. See Hardege, J.D., 85 Beckwitt, R.D., 25, 76; 79 Bedaux, J.M. See McCleave, J.D., 348 Begon, M., 256; 263 Behrens, E.W., 57; 79 Bell, A.L., 178, 192; 199 Bell, J.D., 269, 270, 273, 276, 277, 278, 279, 283, 284, 285, 286, 287, 288, 291; 294 See Ferrell, D.J., 281, 282, 283, 291; 296 See Gray, C.A., 291; 296 See Middleton, M.J., 299 See Worthington, D.G., 303 Bell, J.L., 122; 150 Bell, S.S. See Robbins, B.D., 286, 289; 300 Bellwood, D.R., 356; 383 See Galetto, M.J., 381; 384 See Wilson, S., 356, 358, 359, 363, 364, 380, 382; 389 Bemis, B.E. See Geary, D.H., 154 Ben-Eliahu, M., 6; 79 Ben-Eliahu, M.N., 6, 11, 41; 79 Benfield, M.C. See Forbes, A.T., 321, 333; 344 Benham, W.B., 6; 79 Beninger, P.G., 185; 199 Bennett, J.T., 132; 150 Bennett, W.A. See Kimmerer, W.J., 347 Bentley, M.G. See Hardege, J.D., 23; 85 Bérard, H., 105, 106; 150 Beretta, G.A. See Booth, D.J., 379; 383 Bergan, P., 4, 5, 22, 23, 24, 59, 77, 78; 79 Berge, J.A., 336; 341 See Gee, J.M., 230

392

AUTHOR INDEX

Berger, W.H. See Killingley, J.S., 131, 136, 137; 157 Bergman, M.J.N., 309; 341 Bergmans, M., 213; 229 Bernal, P.A., 133, 139; 150 Bernard, F.R., 179, 186, 187, 195; 199 Bertine, K.K., 145; 150 Bett, B.J. 213; 229 Bettencourt, V., 125, 134, 140; 150 Betzer, P.R. See Grossman, E.L., 154 Beukema, J.J., 318, 319; 342 Bhaud, M., 51, 69, 70; 79 Bianchi, C.N., 58; 79 Bice, K.L., 134, 135; 150 Bidder, A.M. See Mangold, K.M., 124; 158 Biggley, W.H. See Seliger, H.H., 351 Bizikov, V.A., 128, 129; 150 See Arkhipkin, A.I., 125, 126; 150 Blaber, S.J.M., 274, 283; 294 Blaber, T.G. See Blaber, S.J.M., 283; 294 Black, K.P. See Jenkins, G.P., 297, 298 Blackburn, T.H. See Kristensen, E., 245; 265 Blackwelder, B.W. See Ragland, P., 160 Blair, N. See Levin, L., 265 Blair, N.E. See DeMaster, D.J., 263 See Levin, L.A., 265 Blake, J.A., 261; 263 Blanc, A., 277; 294 Blanton, B.O. See Hare, J.A., 346 See Luettich Jr, R.A., 348 Blanton, J. See Wenner, E., 353 Blanton, J.O. See Churchill, J.H., 343 Blaxter, J.H.S., 333; 342 Blegvad, H., 233, 238; 263 Blondel, D. See Forward Jr, R.B., 345 Bock, K.W. See Stecher, H.A., 163 Bock, M.J., 235, 248, 249; 263 See Miller, D.C., 265 Boehlert, G.W., 306, 324, 325, 326, 327, 330, 332, 334; 342 See Olney, J.E., 277, 279; 299 Boesch, D.F., 271, 285; 294 Boggs, J.A. See Seliger, H.H., 351 Boicourt, W.C., 309; 342 See Roman, M.R., 337; 350 Bolton, T.F., 35, 37; 79 Bonnet, P. See Sire, J.Y., 121; 162 Bonsdorff, E., 234, 239, 243, 253, 254; 263 See Boström, C., 277, 281; 294 See Rumohr, H., 266

Bookhout, C.E. See Costlow Jr, J.D., 319, 337; 343 Booth, D.J., 379; 383 Borg, A., 282, 283; 294 Boring, L. See Paulay, G., 93 Bos, A.R., 325; 342 Bosch, H.F., 308; 342 Bosch, I. See Rivkin, R.B., 94 Bosence, D.W.J., 61; 79 Bossey, S.J. See Jackson, E.L., 269–303 Boström, C., 277, 281; 294 Boudreau, B.P., 245; 263 Bouquegneau, J. See Dauby, P., 295 Bourget, E. See Bérard, H., 150 Bourgoin, B.P., 141, 145, 146; 150 Bourne, G.C., 176; 199 Bousfield, E.L., 309; 342 Boutilier, R.G. See Tupper, M., 270, 273, 279, 291; 302 Bowden, N. See Knight-Jones, P., 76; 87 Bowen, V.T. See Goldberg, E.D., 154 Boyden, C.R., 104; 150 Boyle, P.R. See Stephens, P.J., 194; 204 Boynton, W.R. See Lubbers, L., 299 Boysen-Jensen, P. See Petersen, C.G.J., 269; 300 Branch, G.M., 364; 383 Brand, A.R. See Ramsay, K., 160 Brandt S.B. See Mason D.M., 283; 299 Brasil, L., 62; 79 Braun, R., 173, 181; 199 Brawley, S.H., 365, 366, 371, 372, 379, 381; 384 Breen, P.A., 110; 151 See Harbo, R.M., 155 See Schiel, D.R., 121; 162 Bregazzi, P.K. See Knight-Jones, E.W., 87 Bretos, M., 121; 151 Brewer, D.T. See Blaber S.J.M., 294 Bricelj, V.M., 194; 199 See Pohle, D.G., 300 Brieske, T.A. See Geary, D.H., 154 Britayev, T.A. See Rzhavsky, A.V., 4, 13, 18, 22, 23, 57, 58, 59, 60, 75; 95 Bromley, R.G., 243, 244; 263 Brook, H.A. See Weinstein, M.P., 291; 302 Brook, I.M., 274, 280, 281; 295 Brookins, K.G., 318, 319, 320, 337; 342 Broom, D.M., 316; 342 Broom, J.G. See St. Amant, L.S., 351 Broom, M.J., 105; 151

393

AUTHOR INDEX

Brostoff, W.N. See Hixon, M.A., 356, 359, 365, 366, 369, 370, 371, 372, 373, 374, 375, 376, 378, 379, 381; 385 Brousseau, D.J., 104, 108, 110; 151 Brown, B. See Dawson Shepherd, A.R., 230 Brown, J.A. See Gotceitas, V., 277; 296 Brown, M.R. See Johnson, A.L.A., 156 Browne, R. See Tait, N.N., 95 Bruce, B.D. See Thresher, R.E., 302 Bruland, K.W., 144; 151 Bryan, G.W., 145; 151 Bryan, P.J., 44, 45, 53, 54, 55, 56; 79 Buchardt, B., 135; 151 Buchsbaum, R. See Epstein, S., 153 Buckel, J.A., 273, 275; 295 Bunn, S.E. See Loneragan, N.R., 298 Burau, J.R. See Kimmerer, W.J., 347 Burchmore, J.J. See Middleton, M.J., 299 Burfitt, A.H. See Ekaratne, K., 82 Burhenne-Guilmin, F. See Glowka, L., 230 Burke, J.S., 325, 328, 329, 332; 342 See Forward Jr, R.B., 344, 345 Burnett, D.S. See Furst, M., 154 Burrows, M.T., 275; 295 See Ansell, A.D., 199 See Gibson, R.N., 296 Burton, E.A., 142, 151 Bustamante, R.H. See Branch, G.M., 383 Butler, A., 284; 295 Butler, J., 128; 151 Butler IV, M.J. See Acosta, C.A., 341 Butman, C.A. See Snelgrove P.V.R., 234, 248, 257; 267 Caddy, J.F., 187, 289, 290; 199, 295 Cadée, G.C., 250, 258; 263 Cadenhead, A.D. See Levy, D.A., 323, 324; 348 Cai, D. See Margosian, A., 158 See Tan, F.C., 163 Cai, Y.Y. See Bernard, F.R., 199 Caillouet, C.W., 321; 342 Calafiore, N. See Costanzo, G., 80 Calbet, A. See Alcaraz, M., 341 Caley, M.J. See Ohman, M.C., 387 Callaerts, P. See Halder, G., 200 See Tomarev, S.I., 204 Campana, S.E., 127; 151 See Secor, D.H., 162 Campbell, D.C., 188; 199 Canete, J.I., 15; 79

Capps Jr, O. See Shabmann, L.A., 269, 275, 293; 301 Carell, B., 141, 146; 151 Carleton, J.H. See Sammarco, P.W., 363, 378, 380, 381, 382; 388 Carollo, T. See Vitturi, R., 99 Carpenter, R.C., 356, 357, 375, 379; 384 Carpenter, S.M. See Young, P.C., 321; 353 Carpizo-Ituarte, E., 10, 32, 45, 55; 79 See Holm, E.R., 86 Carr, M.H., 279; 295 Carr, M.R. See Somerfield, P.J., 237 Carr, W.E.S., 280; 295 Carrasco, F. See Gutierrez, D., 264 Carrier, R.H. See Perron, F.E., 64; 93 Carriker, M.R., 140, 141, 142, 145, 321, 322; 151, 342 Carter, J. See Sedberry, G.R., 284, 286; 301 Carter, J.G., 140, 141; 151 See Campbell, D.C., 199 Casanova, L., 29, 47, 77; 79 Castagna, M. See Lutz, R.A., 110; 158 Castel, J., 308; 342 Castonguay, M., 322, 323; 342 Castric, A., 61; 79 Castric-Fey, A., 4, 32, 51, 58, 59; 80 Cattaneo-Vietti, R. See Ansell, A.D., 199 Caullery, M., 62; 80 Ceccarelli, D.M., 355–389 Cerrato, R.M. See Thorn, K., 163 See Turekian, K.K., 164 Cespugilo, G., 131; 152 Chadwick, H.C., 61; 80 Chamberlain, J. See Ward, P., 129; 164 Chamberlain Jr, J.A. See Landman, N.H., 157 Champalbert, G., 334; 342 Chaplin, G. See Mattila, J., 299 Chapman, A.R.O. See McCook, L.J., 377; 387 Chapman, C.J. See Nash, R.D.M., 265 Charles, G.H., 167, 169, 173, 178, 190, 192; 200 Chatfield, C., 316; 342 Checa, A., 113; 152 Chen, M. See Wu, B.-L., 9; 100 Chenery, S. See Johnson, A.L.A., 156 Chenery, S.R.N. See Richardson, C.A., 161 Chester, A.J. See Thayer, G.W., 276; 302 Chia, F.-S., 24, 60, 70; 80 See Bryan, P.J., 79 See Cowden, C., 80

394

AUTHOR INDEX

See Martel, A., 69; 90 See Pennington, J.T., 38; 93 See Young, C.M., 11, 32, 35, 37, 38, 74; 100 Chiantore, M. See Ansell, A.D., 199 Chick, R.C. See Gray, C.A., 296 Chimenz Gusso, C., 51; 80 Choat, J.H., 356, 375; 384 See Bellwood, D.R., 356; 383 See Meekan, M.G., 356; 387 Choe, S., 124, 129; 152 Choonhabandit, S. See Kamura, S., 371, 372, 379; 386 Chow, T.J., 146; 152 Christensen, A.M., 61; 80 Christensen, B., 7, 8; 80 Christensen, P.B. See Rysgaard, S., 266 Christiansen, F.B., 64; 80 Christy, J.H., 317, 318, 320, 326; 342 Church, J.A. See Rothlisberg, P.C., 351 Churchill, E.P., 337; 343 Churchill, J.H., 314; 343 See Forward Jr, R.B., 344 See Luettich Jr, R.A., 348 Claparède, E., 4, 21; 80 Clark, J. See Provenzano Jr, A.J., 350 Clark, R.B., 7, 23; 80 Clark II, G.R., 105; 152 See Lutz, R.A., 110; 158 Clarke, K.R., 216, 217, 218, 219, 220, 221, 222, 227, 228; 229 See Dawson Shepherd, A.R., 230 See Gray, J.S., 230 See Rogers, S.I., 231 See Warwick, R.M., 207–231; 208, 210, 214, 216, 222; 231 Clarke, M.R., 124, 125; 152 Clarke, T.A., 358; 384 Clayton, G.R. See Murawski, S.A., 349 Cleland, M.G. See Robertson, D.R., 388 Cleveland, A., 358; 384 Cliche, G., 194; 200 Clough, L.M., 248; 263 Cochran, J.K., 132, 140; 152 See Landman, N.H., 157 Cochran, J.K. See Turekian, K.K., 164 Coen, L.D. See Morgan, S.G., 349 Colby, D.R., 316; 343 Cole, C.F. See Murawski, S.A., 349 Cole, H.A., 172; 200 Coleman, P.H. See Ponder, W.F., 203

Colgan, M.W. See Glynn, P.W., 359, 378, 379; 384 Collins, S.A. See Richardson, C.A., 161 Colman, M.H. See Ponder, W.F., 203 Colwin, A.L., 10, 21, 25, 73; 80 See Colwin, L.H., 25, 73; 80 Colwin, L.H., 25, 73; 80 See Colwin, A.L., 10, 21, 25, 73; 80 Conacher, C. See Blaber, S.J.M., 294 Conacher, C.A. See Loneragan, N.R., 299 Conan, G., 104; 152 Conley, D.J. See Josefson, A., 239, 242, 249; 265 Conlin, B.E. See Hunte, W., 86 See Marsden, J.R., 90 Connaughton, V.P., 37, 38; 80 Connell, J.H., 375; 384 See Sousa, W.P., 371; 388 Connolly, R.M., 270, 274, 276, 281, 284, 285, 287, 288; 295 Cook, J.C. See Voglis, G.M., 352 Cook, J.M. See Richardson, C.A., 161 Cook, P.A. See Erasmus, J., 153 Cook, P.H. See Arnold, G.P., 322, 323; 341 Coombs, S. See Bartsch, J., 313; 341 Cooper, M. See Martin, F.D., 287; 299 Coote, G.E., 141, 143; 152 Corbató, C.E. See Hall Jr, C.A., 155 Cordell, J.R. See Morgan, C.A., 349 Cornu, S., 134; 152 Costanza, R., 208; 230 Costanzo, G., 62; 80 Costlow, J.D. See Queiroga, H., 350 Costlow Jr, J.D., 319, 337; 343 Cotter, A.J.R. See Jennings, S., 230 Coughlan, J., 104; 152 See Ansell, A., 149 Counts III, C.L. See Carriker, M.R., 151 Coutinho, R. See Ferreira, C.E.L., 384 Couturier, C. See Hurley, G.V., 155 Cowan Jr, J.H. See Lyczkowski-Schulz, J., 348 Cowden, C., 38, 60, 74; 80 Cragg, J.B., 4, 25; 80 Cragg, S.M., 170; 200 Craig, G., 104, 105, 152 Craig, H., 130; 152 Crame, J.A. See Skelton, P.W., 204 Crawford, M.K. See Ropes, J.W., 110; 162 Crean, P.B., 313; 343 Crescenti, N. See Costanzo, G., 80 Cresp, J., 2; 81

395

AUTHOR INDEX

Creutzberg, F., 309, 324, 325, 332, 335; 343 See Venema, S.C., 333; 352 Crisp, D.J., 10, 52, 77, 121, 122; 81, 152 See Ekaratne, K., 82 See Ekaratne, S.U.K., 121, 122; 153 See Richardson, C.A., 161 Crisp, E.L. See Dodd, J.R., 141, 143; 153 Crisp, M., 18, 26, 32, 35, 37, 45, 47, 54, 57; 81 Cronin, L.E., 308; 343 Cronin, T.W., 308, 309; 343 See Forward Jr, R.B., 309; 344 Crosby, S.P. See Reid, R.G.B., 193; 203 Crossley, A.C. See Grant, N.J., 18; 84 Crowder, L.B. See Churchill, J.H., 343 See Forward Jr, R.B., 344 Cuerdo-Barcelo, J. See Cornu, S., 152 Cummings, V.J. See Turner, S.J., 302 Cunliffe, J.E., 111, 112, 115; 152 Cuq, F. See Glémarec, M., 296 Curry, G.B. See Mitchell, L., 158 Cushing, D.H., 322; 343 Cutter, G.R. See Diaz, R.J., 264 Daan, N, 322; 343 Dafni, J. See Ben-Eliahu, M., 6; 79 Daguzan, J. See Blanc, A., 277; 294 Daiber, J.C. See Cronin, L.E., 343 Dakin, W.J., 166, 178, 179, 180, 181, 183, 184, 185, 186, 192, 195, 196; 200 Dales, R.P. See Knight-Jones, P., 88 Dall, W., 306, 321; 343 Daly, J.M., 12, 18, 22, 23, 24, 25, 32, 58, 59, 60; 81 Dando, P.R., 242; 263 See Southward, A.J., 267 See Spiro, B., 267 Daniel, A., 51; 81 Daniel, P. See Klumpp, D.W., 386 Daniel, P.A. See Robertson, A.I., 300 Danilowicz, B.S., 383; 384 Dare, P. See Richardson, C.A., 161 Dare, P.J., 106, 138; 152 D’Arge, R. See Costanza, R., 230 Darnell, R.M. See Lochmann, S.E., 348 Darwin, C., 166, 167; 200 Dasgupta, S., 7, 8, 77, 78; 81 Daswell, M.J. See Parsons, G.J., 159 Dauby, P., 281; 295 Dauvin, J.-C, 209, 216; 230 See Thiebaut, E., 352

Dauwe, B., 241, 246, 247, 256, 257, 258, 259, 261; 263 Davies, C.C., 63; 81 Dawe, E.G., 126; 153 See Hurley, G.V., 155 See Lipinski, M.R., 158 See Perez, J.A.A., 159 Dawkins, R., 166, 167, 187; 200 Dawson Shepherd, A.R., 210; 230 Dayton, A.E. See Done, T.J., 384 Dayton, P.K. See Done, T.J., 384 Dean, H.K., 111; 153 Dean, J.M. See Secor, D.H., 162 DeCoursey, P.J., 327; 343 Decrouez, D. See Barbin, V., 150 Deelder, C.L., 336; 343 De Groot, R. See Costanza, R., 230 Deith, M.R. See Dare, P.J., 106, 138; 152 De long, D.J. See De Jonge, V.N., 270, 276; 295 De Jonge, V.N., 270, 276; 295 Del Carmen, K.A. See Walters, L.J., 100 DeMaster, D. See Levin, L., 265 DeMaster, D.J., 261; 263 See Levin, L.A., 265 Deming, J.W. See Jumars, P.A., 265 Den Hartog, C., 272, 292; 295 See Short, F.T., 301 Denman, K.L. See Platt, T., 316; 350 Denton, E.J., 187; 200 Depledge, M.H. See Forbes, T.L., 264 De Silva, P.H.D.H., 12, 13, 22, 23, 32, 36, 46, 52, 54, 57, 59, 77, 84; 81 De Troch, M., 287; 295 Deubler, E.E. See Williams, A.B., 326; 353 Deuser, W.G. See Jasper, J.P., 131, 139; 156 de Veen, J.F., 322, 323; 343 de Vlas, J. See Beukema, J.J., 318, 319; 342 De Vries, M.C., 311, 317, 320, 326, 328, 332, 333, 334, 337, 338; 343, 344 See Forward Jr, R.B., 344, 345 Dew, B., 51, 57; 81 De Wilde, P.A.W.J. See Witbaard, R., 164 De Wolf, P., 309; 344 Diana, J.S., 274; 295 Diaz, R.J., 261, 262; 264 See Blake, J.A., 261; 263 See Pardieck, R.A., 300 Dibden, C.J., 169, 195; 200 Dickie, L.M. See Stevenson, J.A., 104; 163 Di Grande, F., 7; 81

396

AUTHOR INDEX

Dimitriou, D.E. See Jones, A.V., 347 Dimmlich, W.F., 126; 153 Dirnberger, J.M., 34, 36, 52, 53, 78; 81 Ditchfield, P.W., 135; 153 Dittel, A.I., 309, 318, 320, 337; 344 Dixon, D.R., 4, 7, 9, 17, 22, 43, 73; 81 Dixon, P. See Robertson, A.I., 300 Dodd, J.R., 141, 142, 143; 153 See Malone, P.G., 141; 158 Dodson, J.J. See Henri, M., 346 See Laprise, R., 308, 309; 347 See McCleave, J.D., 348 Doherty, P.J., 364; 384 See Sale, P.F., 301 See Worthington, D.G., 303 Dollase, W.A. See Hall Jr, C.A., 155 Done, T.J., 359, 378; 384 Donner, B. See Kalberer, M., 156 Donner, J., 135; 153 See Kuisma-Kursula, P., 157 Dons, C., 9, 18, 41, 43, 59; 82 Donval, A. See Beninger, P.G., 199 Dorresteijn, A.W.C., 10, 26; 82 Doucet, P.G. See McCleave, J.D., 348 Douglas, W.A. See Sale, P.F., 301 Doyle, R.W., 36, 77; 82 See Mackay, T.F.C., 53, 77; 89 D’Ozouville, L. See Help, C., 230 Dreibelbis, D. See Thompson, I., 163 Duarte, C.M. See Richardson, C.A., 161 Dubrow, D.L. See Tabb, D.C., 352 Duchene, J.-C. See Bhaud, M., 51, 69, 70; 79 Dudley, W.C. See Grossman, E.L., 154 Duffy, J.E. See Hay, M.E., 385 Dugas, R.J. See Caillouet, C.W., 342 Duggins, D.O., 51, 52, 60; 82 See Eckman, J.E., 57; 82 Duineveld, G.C.A. See Witbaard, R., 110, 114; 164 Dunbar, R.B. See Grossman, E.L., 154 Duncan, P.B. See Peterson, C.H., 159 Durholtz, M.D., 143; 153 See Lipinski, M., 158 Dwarte, D.M. See Grant, N.J., 25; 84 Eakin, R.M., 174; 200 Eastman, M.P. See Pingitore, N., 142; 160 Ebersole, J.P., 358, 359, 379; 384 Eckelbarger, K.J., 8; 82 Eckman, J.E., 57, 277, 278; 82, 295 See Duggins, D.O., 82

Edgar, G.J., 270, 272, 273, 274, 275, 282, 290; 295 Eekhout, S. See Branch, G.M., 383 Eggleston, D.B. See Lipcius, R.N., 298 Ehrich, S. See Jennings, S., 230 Eilers, M.R. See Mattila, J., 299 Eissa, S.H.H. See Mona, M.H., 91 Ekaratne, K., 2; 82 See Richardson, C.A., 161 Ekaratne, S.U.K., 121, 122; 153 Elgin, R.H. See Karnofsky, E.B., 298 Eltink, A.T.G.W. See Creutzberg, F., 343 Emerson, L. See Greer Walker, M., 322, 323; 345 Emerson, L.S. See Arnold, G.P., 341 Ennis, G.P., 334; 344 Epifanio, C.C. See Garvine, R.W., 345 Epifanio, C.E., 309, 318, 319, 320, 326, 337; 344 See Brookins, K.G., 318, 319, 320, 337; 342 See Connaughton, V.P., 80 See Dittel, A.I., 309, 318, 320, 337; 344 See Garvine, R.W., 345 See Lambert, R., 318; 347 See Little, K.T., 320, 326, 337; 348 See Rowe, P.M., 325, 332, 333; 351 Epstein, S., 130, 135; 153 Erasmus, J., 121; 153 Erasmus, T. See Wooldridge, T., 308; 353 Erlenkeuser, H., 131; 153 Esnault, G., 257; 264 Evans, E.M. See Barber, V.C., 199 Evans, J.W., 115, 119; 153 Ewald, J.J. See Jones, A.V., 347 Ewart, J. See Carriker, M.R., 151 Ewart, J.W. See Carriker, M.R., 151 Fahay, M.P. See Heck, Jr, K.L., 297 Fairbridge, R., 306; 344 Fairweather, P.G. See McNeill, S.E., 286; 299 See Moran, M.J., 97 Faith, D.P., 212; 230 Fallick, A.E. See Mitchell, L., 158 Fandry, C.B. See Rothlisberg, P.C., 357 Fankboner, P.V., 182, 188; 200 Farber, S. See Costanza, R., 230 Farrell, T.M., 376; 384 Farrington, J.W. See Goldberg, E.D., 154 Farrow, G.E., 104, 115, 117, 118, 120; 154 See House, M.R., 115; 155

397

AUTHOR INDEX

Fauchald, K., 13, 233, 239, 242, 251; 82, 264 See Jumars, P.A., 239, 242; 265 Faulkner, G.H., 6, 7, 8, 41, 59, 63, 73; 82 Fauvel, P., 2; 82 Feder, H.M., 61, 104, 244; 82, 154, 264 Feller, R.J. See Stancyk, S.E., 206, 309; 351 Fenchel, T.M. See Christiansen, F.B., 64; 80 Fenical, W. See Hay, M.E., 385 Fenton, G.E., 280; 296 Féral, J.-P., 227, 242; 230, 264 Ferdández-Núñez, M. See Raya, C.P., 160 Fergusson, J.E. See Purchase, N.G., 145; 160 Ferreira, C.E.L., 359, 360, 362, 363, 364, 368, 369, 371, 375, 378, 380; 384 Ferrell, D.J., 281, 282, 283, 291; 296 See Bell, J.D., 294 See Worthington, D.G., 303 Fewkes, J.W., 28, 47, 49, 77; 82 Fiege, D., 75; 82 Finley, R.R., 36; 82 Fischer, A. See Dorresteijn, A.W.C., 26; 82 Fischer, G. See Kalberer, M., 156 Fischer-Piette, E., 18, 43, 73; 82 Fisher, J.S. See Fonesca, M.S., 278; 296 Fitzhugh, K., 2; 82 See Rouse, G.W., 71; 94 Fleeger, J.W. See Baltz, D.M., 294 Fletcher, E.A. See Robertson, D.R., 388 Flowerdew, M.W. See Ekaratne, K., 82 Fonesca, M.S., 278; 296 Fonseca, J.R.C. See Strathmann, R.R., 97 Fontenot, B.J. See Caillouet, C.W., 342 Forberg, S. See Carell, B., 151 Forbes, A.T., 321, 333; 344 Forbes, T.L., 241; 264 Forbes, V.E. See Forbes, T.L., 264 Ford, T.B. See St. Amant, L.S., 351 Ford, W.B. See Prince, J.D., 160 Fordy, M. See Knight-Jones, P., 38, 40; 87 Fore, P.L., 315; 344 Fornes, W. See Levin, L., 265 Forster, S. See Huettel, M., 264 See Zeibis, W., 267 Fortier, L., 308, 309; 344 See Koutsikopoulos, C., 347 Fortin, M.J. See Meekan, M.G., 387 Forward, R.B. See Hare, J.A., 346 Forward Jr, R.B., 305–353; 278, 309, 314, 317, 325, 326, 327, 328, 329, 330, 333, 334, 336, 337, 338, 339; 296, 344, 345

See Churchill, J.H., 343 See Cronin, T.W., 309; 343 See De Vries, M.C., 343, 344 See Late, M.I., 331, 338; 347 See Tankersley, R.A., 328, 329, 333, 337, 340; 352 See Welch, J.M., 353 Foster, M.S., 360; 384 Foster, S.A., 358, 364; 384 Fowler, A.J. See Worthington, D.G., 303 Fox, H.M., 59; 82 Føyn, B., 3, 10, 57, 58, 59, 70; 82 Fraenkel, G.S., 334; 345 Francour, P., 270, 273, 277, 285, 291; 296 Frankel, D.A.Z. See Forward Jr, R.B., 296 Franklin, L.E., 25; 83 Franzén, A., 8, 9, 10, 11, 12, 13, 15, 16, 20, 21, 77, 78; 83 Fraser, D.F., 295; 296 Fraser, S. See Gotceitas, V., 296 Fréchette, M. See Bérard, H., 150 Fretter, V., 122; 154 Fritz, L.W., 117; 154 Fry, B., 281; 296 Fuchs, H.M., 3, 83 Fuentes, L., 126; 154 Fuiman, L.A. See Rooker, J.R., 300 Fulcher, C.W. See Luettich Jr, R.A., 348 Fulcher, M. See Metcalfe, J.D., 349 Fuller, C.M., 245; 264 Fuller, D. See Butler, J., 151 Funnell, G. See Turner, S.J., 302 Furlani, D.M. See Thresher, R.E., 302 Furst, M., 143; 154 Gabriel, C. See Breen, P.A., 151 Gagne, J.A. See Koutsikopoulos, C., 347 Gaikwad, U.D., 12; 83 Gaines, S.D. See Lubchenco, J., 375, 376; 386 Galetto, M.J., 381; 384 Galinou-Mitsoudi, S., 110; 154 Gallardo, V.A. See Gutierrez, D., 264 Galzin, R. See Letourneur, Y., 386 Gamble, E. See Goldberg, E.D., 154 Ganssen, G. See Witbaard, R., 164 Garbarini, P., 22, 23, 32, 77; 83 Garcia-Esquivel, Z. See Pohle, D.G., 300 Garland, E.D. See Mullineaux, L.S., 54; 91 Garrison, L.P., 317, 318; 345 Garvine, R.W., 313; 345 Gaspar, M.B., 112; 154

398

AUTHOR INDEX

Gaten, E. See Johnson, M.L., 201 Geary, D.H., 131, 136, 137; 154 Gee, J.H.R. See Giller P.S., 233; 264 Gee, J.M., 12, 17, 22, 23, 24, 25, 32, 36, 44, 52, 57, 58, 63, 77, 213; 83, 230 See Nelson-Smith, A., 63; 91 Gehring, W. See Tomarev, S.I., 204 Gehring, W.J. See Halder, G., 200 George, J.D., 6; 83 Germano, J.D. See Rhoads, D.C., 259; 266 Gerry, L.R. See Weinstein, M.P., 352 Ghiselin, M.T., 64, 70; 83 Ghobashy, A.F.A., 45, 54, 59, 73, 77; 83, 84 Giangrande, A., 64, 69; 84 Gibson, R.N., 271, 277, 285, 289, 306, 327, 329; 296, 345 Giere, O., 242; 264 Giguere, M. See Cliche, G., 200 Gilbert, D. See Castonguay, M., 322, 323; 342 Gili, J.-M., 59; 84 Gilkinson, K.D., 111; 154 Gillanders, B.M., 280, 289; 296 Giller, P.S., 233; 264 Gilliam, J.F. See Fraser, D.F., 275; 296 Gilmore, R.G., 291; 296 Gilmour, T.H.J., 168; 200 Gjøen, I. See Føyn, B., 3, 10, 57, 58, 59, 70; 82 Gleason, M.G., 361, 378; 384 Glémarec, M., 289; 296 Glenn-Lewin, D.C., 376; 384 Glowka, L., 207; 230 Glynn, P.W., 356, 359, 378, 379; 384 Goldberg, E.D., 145; 154 See Bertine, K.K., 145; 150 See Koide, M., 157 See Daly, J.M., 12, 25; 81 Gonçalves, J.E.A. See Ferreira, C.E.L., 384 Gonor, J.J. See Johnson, G.E., 318, 320; 347 Goodell, H.G. See Pilkey, O.H., 142; 160 Goodrich, D.M., 326; 345 Goodwin, L. See Shaul, W., 110; 162 Gorman, A.L.F., 186; 200 Gosselin, L.A., 37, 60; 84 Gotceitas, V., 270, 276, 277, 280, 282, 284, 291; 296 See Langton, R.W., 298 Goto, T. See Tanaka, M., 352 Gotto, R.V., 61, 62, 63; 84 Gould, S.J., 186; 200 Govoni, J.J. See Hare, J.A., 346

Graf, G., 241, 242, 246, 249, 250; 264 Graham, A. See Fretter, V., 122; 154 Graham, J.J., 309; 345 Graham, S. See Kirchman, D., 87 Granna-Raffucci, F.A., 122; 154 Grant, A., 64; 84 Grant, N.J., 9, 18, 20, 21, 25, 26, 28, 47; 84 Grant, T.R. See Moran, P.J., 33, 57, 58; 91 Grassle, J.F., 208; 230 See Grassle, J.P., 213; 230 See Humes, A.G., 63; 86 See Turekian, K.K., 164 Grassle, J.P., 213; 230 Grasso, M. See Costanza, R., 230 Grave, B.H., 56, 57, 58, 59; 84 Gravier, C., 43, 63; 84 Gray, A.L., 141; 154 See Jarvis, K.E., 156 Gray, A.P., 118, 120; 154 Gray, C.A., 276, 281, 282, 289, 290, 291; 296 Gray, J.S., 59, 74, 210; 84, 230 See Lønne, O.J., 120; 158 See Pearson, T.H., 266 Green, A.L., 379; 384, 385 Green, J., 104; 154 Green, M.D. See Forward Jr, R.B., 344 Greenberg, D.A. See Werner, F.E., 353 Greening, H.S., 290; 296 Greenstreet, S.P. See Hall, S.J., 220; 230 Greenstreet, S.P.R. See Jennings, S., 230 Greenwald, L. See Ward, P., 164 Greenwood, P.B. See Spiro, B., 267 Greer Walker, M., 309, 315, 322, 323; 345 See Arnold, G.P., 341 See Harden Jones, F.R., 346 Grémare, A. See Medernach, L., 59; 90 Grizzle, R.E., 107, 117, 278; 154, 296 Groepler, W., 26; 84 Gronell, A., 358; 385 Gros, P. See Santarelli, L., 121, 131; 162 Grossman, E.L., 130, 139; 154 See Romanek, C.S., 131; 161 Gruffydd, L.D. See Thomas, G.E., 186; 204 Gruffydd, L1. D., 105; 154 See Richardson, C.A., 161 Grundelius, E. See Carell, B., 151 Guerra, A. See Bettencourt, V., 125, 134, 140; 150 Guidetti, P., 270, 273, 281, 291; 297 Guillou, M., 270, 273; 297 Gündling, L. See Glowka, L., 230

399

AUTHOR INDEX

Gunn, D.L. See Fraenkel G.S., 334; 345 Gunn, J.S. See Thresher, R.E., 302 Günther, C.P. See Ansell, A.D., 199 Gupta, S., 308; 345 Gutierrez, D., 241, 256, 257, 259, 261; 264 Gutierrez, L., 361, 379; 385 Gutt, J. See Piepenburg, D., 231 Haderlie, E.C., 61; 84 See Morris, R.H., 91 See Smith, S.V., 57, 59, 72; 96 Hadfield, M.G., 46, 54; 84 See Carpizo-Ituarte, E., 10, 32, 45, 55; 79 See Holm, E.R., 86 See Unabia, C.R.C., 54; 99 See Walters, L.J., 100 Haedrich, R.L. See Gilkinson, K.D., 154 Halder, G., 196; 200 See Tomarev, S.I., 204 Hall, A. See Taylor, J.D., 163 Hall, D.J. See Werner, E.E., 275; 303 Hall, S.J. 220, 236, 244, 250; 230, 264 Hall Jr, C.A., 108, 109; 154, 155 Hallam, A., 141, 142; 155 See Craig, G., 104, 105; 152 See Price, N.B., 143; 160 Halliday, I.A., 280; 297 Hamai, I. See Kato, Y., 111; 156 Hamamoto, K., 53, 60; 84 Hamanaka, Y. See Kuwahara, A., 347 Hameedi, J.M. See Feder, H.M., 264 Hamer, P.A. See Jenkins, G.P., 298, 347 Hamilton, P.V., 194, 196; 200 Hanekom, N., 283; 297 Hanks, J.E. See Turner, H.J., 17, 98 Hannan, J.C., 277, 278, 286; 297 Hannon, B. See Costanza, R., 230 Harbo, R.M., 110; 155 Hardege, H.D. See Hardege, J.D., 85 Hardege, J.D., 23; 85 Harden Jones, F.R., 306, 314, 322, 323, 330; 346 See Greer Walker, M., 345 Harder, T., 54, 55; 85 See Beckmann, M., 79 Harding, D., 322; 346 See Houghton, R.G., 322; 346 Hare, J.A., 313; 346 Hargis Jr, W.J. See Wood, L., 321, 322; 353 Harmelin-Vivien, M. See Letourneur, Y., 386

Harmelin-Vivien, M.L. See Bell, J.D., 286; 294 Harper, E.M., 168, 173, 186, 195; 200, 201 See Skelton, P.W., 204 Harper, J.L. 208, 210, 227; 230 See Begon, M., 263 Harris, J.M. See Branch, G.M., 383 Harris, T., 12, 14, 15, 60, 78; 85 Hartline, H.K., 186; 201 Hartwick, E.B. See Robinson, S.M.C., 124, 125; 161 Harvey, E. See Francour, P., 296 Harvey, G. See Goldberg, E.D., 154 Haskins, H., 322; 346 Hasler, A.D., 323; 346 Hassessian, H. See Marsden, J.R., 34; 90 Haswell, W.A., 41, 63, 64; 85 Haszprunar, G., 185; 201 Hatcher, A.I. See Williams, D. McB., 361; 389 Hatcher, B.G., 369; 385 Hatfield, E.M.C. See Rodhouse, P.G., 124; 161 Hatschek, B., 31; 85 Hatton, D.N. See Jenkins, G.P., 298 Haven, D.S. See Fritz, L.W., 117; 154 Havenhand, J.N., 67, 71; 85 See Bolton, T.F., 35, 37; 79 Hawksworth, D.L. See Harper, J.L., 208, 210, 227; 230 Hay, M.E., 356, 379; 385 Hearn, W.S. See Shepherd, S.A., 121; 162 Heath, D.J., 70; 85 Heaton, T.H.E. See Hickson, J., 155 See Johnson, A.L.A., 156 Heck, K.L. See Mattila, J., 299 See Morgan, S.G., 349 See Orth, R.J., 299 See Wilson, K.A., 303 Heck Jr, K.L., 274, 275, 276, 279, 280, 281, 282, 283, 284, 287, 288; 297 See Spitzer, P.M., 302 Hecker, B. See Rhoads, D.C., 261; 266 Hedley, R.H., 46, 50; 85 Hein, F.J., 378; 385 Heip, C., 207, 208; 230 Heip, C.H.R. See Dauwe, B., 263 Helfferich, C. See McRoy, C.P., 292; 299 Hellman, B. See Rosenberg, R., 266 Helm, N.E., 105; 155 Hempelmann, F., 62, 77; 85

400

AUTHOR INDEX

Hench, J.L. See Churchill, J.H., 343 See Luettich Jr, R.A., 348 Henderson, S.M., 117; 155 Hendry, J.P., 136; 155 Henri, M., 309; 346 Henrikson, L. See Carell, B., 151 Herman, P.M.J. See Dauwe, B., 263 Hermans, C.O. See Rosen, M.D., 203 See Schroeder, P.C., 43; 95 Hernández-González, C.L. See Raya, C.P., 124; 160 Hess, H., 11, 13, 15, 16, 17, 70; 85 Hesse, R., 173, 178, 179; 201 Hettler, W.F., 289, 290; 297 See Churchill, J.H., 343 See De Vries, M.C., 343, 344 See Forward Jr, R.B., 344 Hewitt, J.E. See Turner, S.J., 302 Hiatt, R.W., 61; 85 Hickson, J., 131; 155 Hickson, J.A. See Johnson, A.L.A., 156 Hidu, H. See Newell, C.R., 299 Highsmith, R.C., 69; 85 Hill, A.E., 312, 313; 346 Hill, B.J. See Dall, W., 343 Hill, M.B., 9, 51, 56, 58, 73; 85 Himmelman, J.H. See Stokesbury, K.D.E., 194; 204 Hindell, J.S., 275, 291; 297 Hinds, P.A., 371, 373, 374; 385 Hines, A.H. See Ruiz, G.M., 307 Hirano, R. See Kinoshita, H., 17; 87 Hirschberg, D.J. See Landman, N.H., 157 Hixon, M.A., 356, 357, 359, 364, 365, 366, 369, 370, 371, 372, 373, 374, 375, 376, 378, 379, 381; 385 Hoagland, K.E., 43; 85 Hobbs, G. See Gray, J.S., 230 Hobbs, K.L. See Harbo, R.M., 155 Hodson, R.G. See Weinstein, M.P., 352 Hoedt, F.E. See Dimmlich, W.F., 126; 153 Hoefs, J., 133; 155 Hoekstra, K.J. See Campbell, D.C., 199 Hoffman, S.G. See Robertson, D.R., 387 Höglund, L.B., 30, 31, 34, 47; 85 Hoisaeter, T., 61; 86 Holford, B.H. See Arnold, G.P., 341 See Metcalfe, J.D., 349 Holland, H.D., 142; 155 Holloway, M.G. See Jenkins, G.P., 298 Holm, E.R., 56; 86

Holmes, N.J. See Coughlan, J., 104; 152 Holm-Hansen, O. See Margue, T.H., 370; 386 Holmquist, J.G. See Sogard, S. M, 301, 302 Holt, G.J. See Holt, S.A., 346 See Rooker, J.R., 300, 301 Holt, S.A., 270, 275, 284, 287, 309, 315, 325; 297, 346 See Rooker, J.R., 300, 301 See Tolan, J.M., 302 Horn, M.H., 356; 385 Hörstadius, S., 17; 86 Hosmer, D.W., 317; 346 Hosomi, A., 104; 155 Hoss, D.E., See Burke, J.S., 342 See Forward Jr, R.B., 344 See Hare, J.A., 346 Hough, A.R., 308, 309; 346 Houghton, R.G., 322; 346 Houk, R.S. See Jarvis, K.E., 156 Hourigan, T.F., 358, 364, 379; 385 House, M.R., 115; 155 Hoven, H. See Grizzle, R.E., 296 Howard, R.K. See Klumpp, D.W., 298 Howd, P.A. See Welch, J.M., 353 Hsieh, J. See Marsden, J.R., 26, 36; 90 Huettel, M., 250; 264 See Zeibis, W., 267 Hughes, D.A., 318, 321, 328, 329, 332, 333, 335; 346 Hughes, D.J., 244, 250, 258; 264 See Nickell, L.A., 265 Hughes, T.P., 356; 355 Huh, S.H., 287; 297 Hui, L. See Thompson, I.S., 163 Hulberg, L.W. See Oliver, J.S., 266 Humes, A.G., 63; 86 Humphries, C.J., 211, 214; 230 See Vane-Wright, R.I., 231 See Williams, P.H., 211; 231 Hunt, O.D., 61, 238; 86, 264 Hunte, W., 52; 86 See Marsden, J.R., 90 See Tupper, M., 279; 302 Hunter, J.R. See Blaxter, J.H.S., 333; 342 Hurlbert, E.M. See Cronin, L.E., 343 Hurley, G.V., 105, 124, 125, 126; 155 See Balch, N., 150 See Dawe, E.G., 153 Huston, M., 377; 385 Hutchings, J.A. See Gilkinson, K.D., 154 Hutchings, P.A., 86

401

AUTHOR INDEX

Huxley, T.H., 4; 86 Hylleberg, J., 246; 265 Ibarrola, I. See Richardson, C.A., 203 Ibelings, B.W. See Short, F.T., 301 Ide, J. See Watanabe, N., 100 Idyll, C.P., 318; 346 Igic, L., 51; 86 Iglesias, J. See Fuentes, L., 154 Inestrosa, N.C. See Rodriguez, S.R., 94 Ingham, R.J. See Richardson, C.A., 203 Iribarne, O.O. See Schwindt, E., 51; 95 Irlandi, E.A., 270, 276, 284, 286, 287; 297 Irvine, G.V., 356, 363, 364, 372; 385 Isaac, M.J., 63; 86 Itzkowitz, M., 361, 379; 385 Ivanoff, P.P., 26, 73; 86 Iversen, E.S. See Idyll, C. P, 346 Ives, M. See Moore, A., 349 Ivin, V.V., 8, 13, 18, 22, 23, 58; 86 Izsak, C. 220; 230 Jablonski, D., 139; 155 Jablonski, D.C. See Lutz, R.A., 158 Jackson, E.L., 269–303 Jackson, G.D., 124, 125, 126, 127, 128, 147; 155, 156 Jackson, J.B. C, 61; 86 Jacob, W., 173; 201 Jacobs, D.K. See Jones, D.S., 139; 156 Jacobs, R.P.W.M., 289; 297 Jager, J.C. See McCleave, J.D., 348 Jager, Z., 325; 346, 347 Jägersten, G., 71; 86 Jahn, T.L. See Strathmann, R.R., 97 James, R.J., 52; 86 Jamieson, B.G.M., 11, 20, 21; 86 Jan, R.-Q., 369; 385 Jansen-Jacobs, M.J. See Ten Hove, H.A., 74; 97 Jansson, B.O., 283; 297 Jarre-Teichmann, A. See Jennings, S., 230 Jarvis, K.E., 141; 156 Jasper, J.P., 131, 139; 156 Je, J.G. See Khim, B.K., 157 Jearld Jr, A. See Ropes, J.W., 104, 107; 162 Jellyman, D.J., 324, 326; 347 Jenkins, G. See Connolly, R., 295 Jenkins, G.P., 270, 276, 277, 279, 283, 287, 291, 325; 297, 295, 347 See Hindell, J.S., 299 See Shaw, M., 281, 283; 301

Jenness, M.I. See Witbaard, R., 164 Jennings, S., 227; 230 Jernakoff, P. See Butler, A., 284; 295 Jewett, S.C. See Feder, H.M., 264 Jirkov, I.A. See Kupriyanova, E.K., 2; 88 Johannes, R.E. See Wiebe, W.J., 389 Johannessen, P.J. See Pearson T.H., 266 Johannesson, K., 69; 86 Johnels, A. See Carell, B., 151 Johnson, A.L.A., 135; 156 See Hickson, J., 155 Johnson, C.C. See Carriker, M.R., 151 Johnson, D.F. See McConaugha, J.R., 348 See Provenzano Jr, A.J., 350 Johnson, G.E., 318, 320; 347 Johnson, H.P., 3; 86 Johnson, M.L., 187; 201 Johnson, W.R. See Feder, H.M., 264 Joll, L.M., 105, 168, 187, 194; 156, 201 See Dibden, C.J., 169, 195; 200 Jones, A.C. See Roessler, M.A., 350 Jones, A.E. See Tabb, D.C., 352 Jones, A.M., 104; 156 Jones, A.V., 318; 347 Jones, C.B. See Rosenberg, G.D., 141; 162 Jones, D.S., 107, 109, 110, 114, 115, 130, 131, 136, 137, 138, 139; 156 See Allmon, W.D., 149 See Arthur, M.A., 150 See Krantz, D.E., 157 See Romanek, C.S., 162 See Ropes, J.W., 162 See Thompson, I., 163 Jones, G.A. See Weidman, C.R., 107, 130, 131, 132, 136, 137, 138; 164 Jones, G.P., 271, 279, 356, 358, 359, 361, 363, 366; 298, 385, 386 See Ceccarelli, D.M., 355–389 See Ohman, M.C., 387 Jones, J., 234; 265 Jones, M.B. See Jackson, E.L., 269–303 Jones, P.C.T. See Ap Gwynn, I., 25; 78 Jong, J.T.L. See McCleave, J.D., 348 Jönsson, E. See Andreasson, F.P., 149 Jordan, F., 272, 274, 280; 298 Jørgensen, B.B. See Zeibis, W., 267 Josefson, A., 239, 242, 249; 265 Joyeux, J.C., 289, 290, 325; 298, 347 Juanes, F. See Langton, R.W., 298

402

AUTHOR INDEX

Jumars, P.A., 239, 242, 247; 265 See Fauchald, K., 233, 239, 242, 251; 264 See Yager, P.L., 267 Jyssum, S., 7, 8; 86 Kachurak, K.A. See Tankersley, R.A., 352 Kaiser, M.J. See Ramsay, K., 160 Kajihara, T. See Miura, T., 10, 18, 22, 26, 35, 57; 91 Kalberer, M., 131, 139; 156 Kalin, R.M. See Hendry, J.P., 136; 155 Kamura, S., 371, 372, 379; 386 Karlsen, H.E. See Sand, O., 330; 351 Karnofsky, E.B., 273; 298 Karpenko, A.A., 194; 201 Kato, Y., 111; 156 Katz, A., 142; 156 Kaufman, L., 356, 364, 377, 378; 386 Kawaguti, S., 182; 201 Kawahara, T. See Knight-Jones, P., 88 Keeling, M.J. See Price, A.R. G., 231 Kellaway, D.M. See Loneragan, N.R., 298 Kelly, J.C., 316; 347 Kemp, W.M. See Lubbers, L., 299 Kendall, M.A. See Williamson, P., 121; 164 Kennedy, D., 167, 172, 188; 201 Kennedy, H.A. See Richardson, C.A., 161 Kennedy, I.R. See Larkum, A.W.D., 386 Kennedy, P. See Richardson, C.A., 161 Kennedy, V.S., 321; 347 Kennedy, W.J. See Taylor, J.D., 163 Kennish, M.J., 109, 111, 113, 115, 117; 156, 157 See Cunliffe, J.E., 111, 112, 115; 152 Kenny, R., 122; 157 Kenyon, R.A. See Loneragan, N.R., 299 Keough, M.J., 54; 86 See Hindell, J.S., 297 See Jenkins, G.P., 297, 295, 347 Kerr, J.D. See Blaber, S.J. M., 294 Ketchum, B.H., 308; 347 Key, D. See Richardson, C.A., 161 Kharkar, D.P. See Turekian, K.K., 164 Khim, B.K., 131; 157 Khomsi, A. See Dauby, P., 295 Kikuchi, T., 269, 271, 272, 273, 280, 289; 298 See Nishi, E., 92 Killingley, J.S., 131, 136, 137, 139, 140; 157 See Wefer, G., 130, 131, 140; 164 Kimmerer, W.J., 308; 347 Kincheloe, K. See Mense, D.J., 349

Kindblom, L. See Grizzle, R.E., 296 See Newell, C.R., 299 King, B.D., 318; 347 King, P.E., 4, 5, 7, 77; 87 See Babbage, P.C., 25, 77; 78 Kinoshita, H., 17; 87 Kinoshita, I. See Burke, J.S., 342 Kirby, M.X., 110; 157 Kirby-Smith, W.W. See De Vries, M.C., 344 Kirchman, D., 54, 55, 75; 87 See Mitchell, R., 54; 91 Kirk, J.T.O., 187; 201 Kirsipu, J.S. See Holland, H.D., 155 Kiseleva, M.I., 13, 16, 18, 28, 77; 87 Kishinouye, K., 181; 201 Kitting, C.L. See Holt, S.A., 297 Kleckner, R.C. See McCleave, J.D., 324, 327, 332, 336; 348 Klein, R. See Witbaard, R., 112; 164 Klein, R.T., 145; 157 Klöckner, K., 33, 35, 51, 54, 57, 60; 87 Klumpp, D.W., 274, 363, 364, 365, 366, 368, 369, 370, 371, 372, 378, 379, 380, 381; 298, 386 See Polunin, N.V.C., 359; 387 Knight-Jones, E.W., 12, 13, 14, 16, 23, 31, 32, 33, 34, 35, 36, 38, 40, 44, 46, 53, 61, 75, 76, 77; 87 See Al-Ogily, S.M., 13, 22, 53; 78 See Gee, J.M., 12, 36, 52; 83 See Harris, T., 12; 85 See Knight-Jones, P., 12, 13, 15, 21, 38, 53; 87, 88 See Thorp, C.H., 98 Knight-Jones, P., 12, 13, 14, 15, 16, 21, 38, 40, 53, 70, 75, 76; 87, 88 See De Silva, P.H.D.H., 12, 13, 46, 52; 51 See Knight-Jones, E.W., 87 See Rzhavsky, A.V., 16, 40; 95 See Thorp, C.H., 98 Knott, D. See Wenner, E., 353 Knowlton, N., 213; 230 Ko, Y. See Matuso, R., 10, 58; 90 Koch, K.M. See Hamilton, P.V., 194, 196; 200 Kohda, M., 361, 364; 336 Kohn, A.H. See Pernet, B., 63; 93 Koide, M., 145, 146; 157 Køie, M., 62; 88 Koike, I. See Polunin, N.V.C., 364, 370; 387 Kos, L. See Tomarev, S.I., 204 Koutsikopoulos, C., 305; 347

403

AUTHOR INDEX

Krantz, D.E., 131, 136, 138, 144, 145; 157 See Jones, D.S., 156 See Romanek, C.S., 162 See Stecher, H.A., 163 Krebs, C.J., 233; 265 Kreider, J.L. See Bryan, P.J., 79 Kristensen, E., 245; 265 Kristensen, T.M., 124, 127; 157 Krog, C. See Støttrup, J.G., 302 Kronick, A.T. See Krantz, D.E., 157 Ku, T.K. See Grossman, E.L., 130; 154 Kudenov, J.D., 245, 250; 265 Kuhl, W., 18, 25; 88 Kuisma-Kursula, P., 141; 157 Kulczycki, G.R., 284, 287, 288; 298 Kunkle, D.E., 322; 347 Küpfer, M., 173; 201 Kupriyanova, E.K., 1–101; 2, 74; 88 Kuwahara, A., 321; 347 Kyser, T.K. See Muhs, D.R., 135; 159 Lacalli, T.C., 9, 11, 18, 22, 26, 31, 33, 34, 36, 37, 47; 88 Lacroix, G.L., 324; 347 LaCroix, M.W. See Bach, S.D., 294 See Thayer, G.W., 302 Lambert, R., 318; 347 See Esnault, G., 264 Lammens, J.J., 104; 157 Lament, P. See O’Connor, R.J., 61; 92 Land, M.F., 167, 168, 169, 181, 185, 186; 201 See Barber, V. C, 181; 199 Lande, R., 208; 230 Lander, K.F. See Ansell A., 149 Landman, N.H., 129, 132; 157 See Cochran, J.K., 132; 152 Langheld, C. See Giere, O., 242; 264 Langton, R.W., 292; 298 Lankester, E.R., 62, 74; 88 Laprise, R., 308, 309; 347 Larkum, A.W.D., 284, 292, 370; 295, 386 Lasserre, P. See Grassle, J.F., 230 Lassig, B. See Robertson, D.R., 359, 361, 380; 387 Lassuy, D.R., 356, 357, 359, 363, 364, 369, 370, 371, 372, 373, 374, 375, 380; 386 Latz, M.I., 331, 338; 347 Lau, S.C.K., 53, 54, 56; 88 Lawton, P. See Langton, R.W., 298 Le Campion, J. See Champalbert, G., 342 Lee, D.S. See Koide, M., 157

Lee, E., 62; 88 Le Faou, Y. See Glémarec, M, 296 Leggett, W.C., 306; 348 See Fortier, L., 308, 309; 344 See MacKenzie, B.R., 335; 348 Leighton, K. See Robertson, D.R., 388 Lemeshow, S. See Hosmer, D.W., 317; 346 LeMessurier, M.H. See Evans, J.W., 115; 153 Leng, M., 144; 157 Leone, D.E., 8, 17, 57, 58; 88 See Zuraw, E.A., 10, 17; 101 Le Pennec, M. See Beninger, P.G., 199 Le Reste, L., 321; 348 Lessard, E.J. See Rivkin, R.B., 94 Letourneur, Y., 378, 383; 386 Levi, C. See Levi, P., 173; 201 Levi, P., 173; 201 Levin, L., 241, 246, 247; 265 Levin, L.A., 241, 246; 265 See DeMaster, D.J., 263 Levin, P., 277, 279, 282, 291; 298 Levin, S.A., 382; 386 Levinton, J.S. See Lopez, G.R., 242; 265 Levitan, D.R., 65, 68; 88 Levy, D.A., 323, 324; 348 Lewis, A.R., 357, 358, 359, 380; 386 Lewis, F.G. See Stoner, A.W., 287; 302 Lewis, G.F., 291; 298 Lewis, J.B., 22, 26; 88 Lewis, R.M., 325, 327, 329; 348 L’Hardy, J.-P., 12; 88 Liang, X.Y., 168; 201 Liao, C.M. See Lin, M.C., 145; 157 Light, J. See Warwick, R.M., 227; 231 Light, V.E., 172; 202 Limburg, K. See Costanza, R., 230 Lin, M.C., 145; 157 Lindh, U. See Carell, B., 151 Ling, R. See Southward, A.J., 267 Lipcius, R.N., 276, 279; 298 See Metcalfe, K.S., 349 See Pardieck, R.A., 300 See Pile, A.J., 300 Lipinski, M., 124, 125, 126, 127; 157, 158 Lipinski, M.R., 125; 158 See Durholtz, M.D., 153 Liret, C. See Francour, P., 296 Lirman, D., 361, 384; 386 Little, E.J., 321; 348 Little, K.T., 320, 326, 337; 348 See Epifanio, C.E., 344

404

AUTHOR INDEX

Liu, J.H. See Richardson, C.A., 121, 122; 161 Livingston, J.R., 286; 298 Livingston, R.J. See Greening, H.S., 290; 296 Lizano, O. See Dittel, A.I., 344 Llewellyn, L.C. See Knight-Jones, E.W., 87 Lobel, P.S., 359, 364, 370, 377, 378, 380; 386 See Ogden, J.C., 356; 387 LoBianco, S., 36, 43, 74; 89 Lochmann, S.E., 318, 319, 320, 330; 348 Loder, J.W. See Tremblay, M.J., 352 See Werner, F.E., 353 Lohmann, K.C. See Klein, R.T., 157 Loneragan, N. See Connolly, R., 295 Loneragan, N.R., 270, 273, 277, 281, 284, 287, 288; 298, 299 Longinelli, A. See Cespugilo, G., 152 Lønne, O.J., 120; 158 Lonsdale, D.J. See Gupta, S., 345 Loosmore, F.A. See Ansell, A., 149 Lopez, G.R., 242; 265 See Clough, L.M., 248; 263 Lord III, J.C. See Stecher, H.A., 163 Lorens, R.B., 142; 158 Lorenzen, S., 211; 230 Loudon, C. See Scheltema, R.S., 95 Lough, R.G. See Werner, F.E., 353 Low, R.M., 358, 359, 379; 386 Lowenstam, H.A., 141; 158 See Epstein, S., 130, 135; 153 See Furst, M., 154 Lu, C.C. See Jackson, G.D., 128; 156 Lubbers, L., 282; 299 Lubchenco, J., 375, 376; 386 Luetjens, C.M. See Dorresteijn, A.W.C., 10, 26; 82 Luettich, R.A. See Churchill, J.H., 343 Luettich Jr, R.A., 314; 348 See De Vries, M.C., 344 Luhrs, T.C. See Lipcius, R.N., 298 Luther III, G.W. See Stecher, H.A., 163 Lutz, R.A., 108, 110, 139, 141, 142; 158 See Grizzle, R.E., 107, 117; 154 See Jablonski, D., 139; 155 See Rhoads, D.C., 103, 107, 120, 127; 160 Lyczkowski-Schulz, J., 305; 348 Lynch, D.R. See Werner, F.E., 353 Lyster, I.H. J., 32; 89 MacArthur, R.H., 221; 230 MacClintock, C. See Pannella, G., 107, 111, 115, 116, 117, 120; 159

MacDonald, B.A., 104, 108, 110; 158 MacDonald, K.C. See Killingley, J.S., 157 MacGinitie, G.E., 11, 74; 89 MacGinitie, N. See MacGinitie, G.E., 11, 74; 89 Mackay, T.F.C., 53, 77; 89 MacKenzie, B.R., 335; 348 Maeda, T. See Burke, J.S., 342 Magnier, Y. See Ward, P., 164 Magurran, A.E., 208; 230 Mahoney, B. M, 358, 359, 364, 366, 379, 381; 386 Main, K.L., 275, 280; 299 Maiorca, A. See Vitturi, R., 99 Makino, S., 8; 89 Malaquin, A., 6, 7, 63; 89 Malone, J. See Levin, P., 298 Malone, P.G., 141; 158 Malouf, R.E. See Helm, N.E., 105; 155 Mangold, K.M., 124; 158 Mann, K.H. See Margosian, A., 158 Mann, K.O., 129, 142, 144; 158 Mann, R. See Baker, S.M., 170; 199 Manuel, J.L., 313, 316; 348 Marchand, J. See Champalbert, G., 342 Marelli, D.C. See Jones, D.S., 156 Margalef, R., 61; 89 Margolis, L., 62, 73; 89 Margosian, A., 131, 133, 138; 158 Margue, T.H., 370; 386 Marincovich Jr, L. See Bice, K.L., 150 Marinelli, R.L., 245; 265 See Boudreau, B.P., 245; 263 Maris, R.C. See McConaugha, J.R., 348 Marsden, J.R., 4, 11, 18, 22, 26, 34, 35, 36, 37, 44, 45, 47, 52, 54, 59; 89, 90 See Hunte, W, 86 Marshall, J.D. See Ditchfield, P.W., 153 Martel, A., 69; 90 Martin, C. See Levin, L., 265 Martin, C.M. See Levin, L.A., 265 Martin, F.D., 287; 299 Martin, J.H. See Goldberg, E.D., 154 Martin, W.E., 62; 90 Mason, D.M., 283; 299 Mason, J., 104, 105; 158 See Broom, M.J., 105; 151 Matjasic, J., 10, 26; 90 Matthews, T.R. See Acosta, C.A., 341 Mattila, J., 290 See Spitzer, P.M., 302

405

AUTHOR INDEX

Matuso, R., 10, 21, 58; 90 Mau-Lastovicka, T. See Robertson, R., 62; 94 Maxwell, J.G.H. See Ralph, R., 194; 203 May, H.M.A. See Jenkins, G.P., 298 May, R.M., 211; 230 See Nee, S., 210; 231 Mayer, L.M. See Jumars, P.A., 265 Mayor, S. See Gutierrez, D., 264 Mayr, E. See Salvini-Plawen, L.V., 166, 167, 169, 178, 190; 203 McAlice, B.J. See Newell, C.R., 299 McClanahan, T.R., 372, 378; 386 McCleave, J.D., 306, 316, 324, 327, 329, 332, 336; 348 See Barbin, G.P., 341 See Parker, S.J., 315, 323, 331, 336; 350 See Rommel Jr, S.A., 336; 350, 351 See Sheldon, M.R., 315, 324; 351 See Wippelhauser, G.S., 324, 329, 336; 353 See Zimmerman, M.A., 336; 353 McComb, A.J. See Larkum, A.W. D., 298 McConaugha, J.R., 326, 337; 348 See Provenzano Jr, A.J., 350 McConnaughey, T., 281; 299 McCook, L.J., 356, 377; 386, 387 See Ceccarelli, D.M., 355–389 See Russ, G.R., 356, 370; 388 McCurdy, P. See Lacroix, G.L., 324; 347 McDonald, L. See Richardson, C.A., 161 McEachran, J.D., 222; 230 See Lochmann, S.E., 348 McEdward, L.R., 65; 90 McElligott, D.J. See Gray, C.A., 296 McHugh, D., 64, 71; 90 McIntosh, W.C., 43, 62, 63, 73; 90 McIntyre, A.D. See Grassle, J.F., 230 McKelvey, L.M. See Tankersley, R.A., 352 McKeown, B.A., 306; 348 McKinnon, A.D. See Klumpp, D.W., 363, 369; 386 McMurry, J.T., 338; 348 McNeely, J.A. See Glowka, L., 230 McNeill, S.E., 286; 299 See Bell, J.D., 294 See Worthington, D.G., 303 McReynolds, J.S. See Gorman, A.L.F., 186; 200 McRoy, C.P., 281, 292; 299 See McConnaughey, T., 281; 299 See Phillips, R.C., 291, 292; 300 McShane, P.E., 121, 122; 158

Mead, T.A. See Moore, A., 349 Meadows, P.S., 54, 77; 90 Meco, J. See Cornu, S., 152 Medernach, L., 59; 90 Meekan, M.G., 356, 357, 358, 359, 361, 364, 380; 387 Mees, J. See De Troch, M., 295 Meeuwig, J. See Marsden, J.R., 52; 90 Melville-Smith, R., 315, 325; 348 Meñez, E.G. See Phillips, R. C, 271, 272, 284, 285; 300 Meng, L., 290; 299 Menge, B., 70; 90 Menon, N.R. See Paul, M., 93 Mense, D.J., 320, 326, 337; 349 Mergardt, N. See Jennings, S., 230 Merrill, A.S., 104, 105, 110; 158 Mesjasz-Przybylowicz, J. See Durholtz, M.D., 153 Mesnil, F. See Caullery, M., 62; 80 Metcalfe, J.D., 315, 322, 323, 330, 339; 349 See Arnold, G.P., 322, 323; 341 Metcalfe, K.S., 326; 349 Meyer, E., 31,47, 74; 90 Michael, T.M. See Hadfield, M.G., 84 Michel, C. See Guillou, M., 270, 273; 297 Middleton, M.J., 277, 284, 287; 299 Miles, S.G., 332; 349 Miller, D.C., 234, 235, 239, 240, 248, 249, 257; 265 See Bock, M.J., 235, 248, 249; 263 Miller, D.L. See Lipcius, R.N., 295 Miller, J.M., 327; 349 Miller, M.W., 356; 387 Miller, W.H., 180; 202 Milne, L.J., 166; 202 Milne, M.J. See Milne, L.J., 166; 202 Milner, N.J. See Moore, A., 349 Minello, T.J. See Rozas, L.P., 284, 285, 290, 291, 292; 301 See Thomas, J.L., 302 See Zimmerman, R.J., 284; 303 Mingazzini, P., 62; 91 Mitchell, L., 139; 158 Mitchell, R., 54; 91 See Kirchman, D., 87 Miura, T., 10, 18, 22, 26, 35, 57; 91 Miyake, T. See McEachran, J.D., 222; 230 Modin, J. See Gibson, R.N., 296 Mohammad, M.-B., 51, 61; 91 Mohan, P.C., 3; 91

406

AUTHOR INDEX

Moller-Racke, I. See Von Buddenbrock, W., 186; 204 Moltschaniwskyj, N.A. See Jackson, G.D., 125; 156 Mona, M.H., 8; 91 Monroy, A., 25, 73; 91 Monteiro, C.A. See Gaspar, M.B., 154 Montgomery, W.L., 359, 360, 363, 364, 365, 366, 368, 369, 370, 371, 372, 376, 381; 387 Moore, A., 315, 324; 349 Moore, C.G. See Bett, B.J., 213; 229 Moore, K.A., 289; 299 See Orth, R.J., 291; 299 Moran, M.J., 60; 91 Moran, P.J., 33, 57, 58; 91 Moreira, M.H. See Queiroga, H., 350 Morgan, C.A., 308; 349 Morgan, P.J. See Nash, R.D. M., 265 Morgan, S.G., 317, 326; 349 Morgan, T.H., 166, 195; 202 Morri, C. See Bianchi, C.N., 58; 79 Morris, C.C., 126, 127; 159 Morris, N.J. See Skelton, P.W., 204 Morris, R.H., 9; 91 Morrisey, D.J. See Turner, S.J., 302 Morton, B., 165–205; 167, 168, 169, 170, 171, 172, 173, 174, 175, 176, 177, 178, 179, 180, 183, 184, 185, 186, 187, 188, 189, 192, 193, 194; 202, 203 See Adal, M.N., 193; 199 See Bernard, F.R., 199 See Harper, E.M., 173, 186; 200 See Liang, X.Y., 168; 201 See Tan, K.S., 60; 97 Morton, R.M. See Pollock, B.R., 350 Moxica C. See Fuentes, L., 154 Mpitsos, G.J. See Bell, A.L., 178, 192; 199 Mueller, C. See Hardege, J.D., 85 Muhs, D.R., 135; 159 Mukai, H. See Hamamoto, K., 84 Mulder, H.P.J. See Jager, Z., 325; 347 Muller, W.J. See Larkum, A.W. D., 386 Mullineaux, L.S., 54; 91 Munday, P.L. See Ohman, M.C., 387 Mundy, B.C. See Boehlert, G.W., 306, 324, 325, 326, 327, 330, 332, 334; 342 Muñoz-Lopez, T., 121; 159 Munro, J.L. See Roessler, M.A., 350 Murawski, S.A., 108; 159 See Ropes, J.W., 162

Murty, T.S. See Crean, P.B., 343 Muschenheim, D.K., 250; 265 Mutvei, H. See Carell, B., 151 Muus, K. See Ockelmann, K.W., 242; 266 Myers, A.C., 244, 245, 262; 265 Naeem, S. See Costanza, R., 230 Naidu, A.S. See Feder, H. M, 264 Naimie, C.E. See Tremblay, M.J., 352 Nakanose, T. See Natsukari, Y., 159 Narciso, L. See Ré, P., 124, 129; 160 Nash, R.D.M., 258; 265 See Atkinson, R.J.A., 244; 263 Natsukari, Y., 127; 159 See Lipinski, M.R., 158 Naylor, E., 327, 329; 349 See Hough, A.R., 308, 309; 346 See Richardson, C.A., 161 See Zeng, C., 318, 319, 320, 327, 328, 329; 353 Nedved, B.T. See Holm, E.R., 86 Nee, S., 210; 231 Neill, W.H. See McCleave, J.D., 348 Neilson, J.D., 306; 349 See Campana, S.E., 127; 151 Neira, C. See Gutierrez, D., 264 Nekludova, N. See Arkhipkin, A., 124, 125, 127; 149 Nellbring, S. See Jansson, B.O., 297 Nelson, C. See Jordan, F., 298 Nelson, J.S., 222, 323; 237, 349 Nelson, S.G., 369; 387 Nelson, T.A., 289, 290; 299 Nelson, W.G., 53, 54, 75, 276; 91, 299 See Kulczycki, G.R., 298 See Zupo, V., 284, 287; 303 Nelson-Smith, A., 9, 63; 91 Nerini, M.K., 244; 265 Newell, C.R., 278; 299 See Grizzle, R.E., 296 See Muschenheim, D.K., 250; 265 Newman, W.A. See Killingley, J.S., 157 Nichols, J.H. See Harding, D., 346 Nichols, P.D. See Klumpp, D.W., 274; 298 See Thresher, R.E., 302 Nickell, L.A., 258; 265 See Gibson, R.N., 296 Nielsen, J.R. See Støttrup, J.G., 302 Nielsen, L.P. See Rysgaard, S., 266 Nighy, F.E. See Merrill, A.S., 158

407

AUTHOR INDEX

Nilsson, D.-E., 167, 168, 173, 174, 185, 191, 193, 196, 197; 203 Nilsson, H.C., 262; 266 See Rosenberg, R., 266 Nishi, E., 4, 5, 6, 9, 10, 11, 12, 13, 17, 18, 19, 20, 21, 22, 25, 28, 29, 41, 43, 47, 48, 59, 73, 75; 91, 92 See Kupriyanova, E.K., 1–101 Nishihira, M. See Nishi, E., 4, 5, 6, 9, 11, 17, 25,41, 59; 91 Nixon, K.C., 212; 231 Nixon, M., 124; 159 Norcross, B.L., 306, 308; 349 Nord, A.G. See Donner, J., 135; 153 Nordback, K., 8, 7, 25; 92 Norman, M.D. See Jones, G.P., 359, 361; 386 North Sea Task Force, 210; 231 Nott, J.A., 30, 31, 46, 47, 49, 50, 77; 92 Nowell, A.R.M. See Eckman, J.E., 277; 295 See Yager, P.L., 267 Nowikoff, M., 173; 203 Nozaki, Y. See Turekian, K.K., 164 Nybakken, J.W. See Oliver, J.S., 266 Oba, T. See Tanabe, K., 110; 163 Obrebski, S., 68; 92 O’Brien, C.J., 273; 299 O’Brien, J.W. See Valle, C.F., 302 O’Callaghan, C.J. See Price, A.R. G., 231 Ockelmann, K.W., 242; 266 O’Connor, R.J., 61; 92 Oda, K. See Natsukari, Y., 159 Odense, P.H. See Dawe, E.G., 153 See Hurley, G.V., 155 O’Donnel, M.A., 60; 92 O’Dor, R.K. See Dawe, E.G., 153 See Hurley, G.V., 155 See Manuel, J.L., 313, 316; 348 See Perez, J.A.A., 124, 128, 129; 159 Odum, W.E. See Rozas, L.P., 275, 276; 301 See Wood, E.J.F., 303 Ogden, J.C., 356; 387 Ohman, M.C., 379; 387 Ohno, T., 119, 120; 159 Ojeda, F.P. See Rodriguez, S.R., 94 Okamoto, K., 51, 56, 58; 92 See Watanabe, N., 100 Okuda, S., 13, 28, 29, 30, 36, 47, 49, 50, 77, 78; 92 Olafsson, E.B., 251; 266 Olenin, S., 255, 256; 266

Olive, P.J. W. See Clark, R.B., 7; 80 Oliver, J.S., 248; 266 See Nerini, M.K., 244; 265 Olla, B.L. See Sogard, S.M., 270, 280; 301 Olmi III, E.J., 320, 337; 349 Olney, J.E., 277, 279; 299 Olsen, G., 8; 92 Olsgard, F. See Somerfield, P.J., 231 Olsson, M. See Carell, B., 151 Olsson, R.K. See Kennish, M.J., 109, 117; 157 O’Neal, J.P. See Mattila, J., 299 O’Neill, R.V. See Costanza, R., 230 Onuf, C.P. See Tolan, J.M., 302 Orensanz, J.M. See Palacios, R., 159 Orlando, B.A. See Irlandi, E.A., 297 Orsi, J.J., 309; 349 Orth, R.J., 275, 276, 279, 284, 287, 288, 291; 299, 300 See Goodrich, D.M., 345 See Heck, Jr, K.L., 275, 284, 287, 288; 297 See Metcalfe, K.S., 349 See Pardieck, R.A., 300 See Pile, A.J., 300 See Ryer, C.H., 301 See van Montfrans, J., 352 Ortiz-Quintanilla, M. See Shepherd, S.A., 162 Osborn, T.R. See Rothschild, B.J., 335; 351 Oshel, P.E. See Gilkinson, K.D., 154 Otieza, R. See Abades, S., 149 Oviatt, C.A. See Raposa, K.B., 284, 286; 300 Oxburgh, U.M. See Holland, H.D., 155 Padilla, D.K., 234; 266 Page, F.H. See Tremblay, M.J., 352 See Werner, F.E., 353 Paine, R.T. See Levin, S.A., 382; 386 Palacios, R., 141, 142, 143; 159 Palmer, A.R., 67; 92 Palmer, J.D., 327, 329, 340; 350 Palmer, R.E. See Carriker, M.R., 151 Palmer, T.J. See Harper, E.M., 200 Pannella, G., 107, 111, 115, 116, 117, 120, 127; 159 See Rhoads, D.C., 107, 115, 116, 117, 120, 127; 160 Pantus, F.J. A. See Ten Hove, H.A., 73; 97 Papadopoulos, I. See De Troch, M., 295 Pardieck, R.A., 280, 285, 289; 300 Paris, J., 63, 74; 92 Parker, K.R. See Nott, J.A., 47, 50; 92 Parker, P.L. See Goldberg, E.D., 154

408

AUTHOR INDEX

Parker, S.J., 105, 315, 323, 331, 336; 159, 350 See Barbin, G.P., 341 Parkins, C. See Branch, G.M., 383 Parsons, G.J., 105; 159 Paruelo, J. See Costanza, R., 230 Parulekar, A.H. See Ansari, Z.A., 294 Patten, W., 167, 180; 203 Patterson, P. See Jordan, F., 298 Pätzold, J. See Cornu, S., 152 See Kalberer, M., 156 Paul, A.J. See Feder, H.M., 104; 154 Paul, M., 56; 93 Paul, M.D., 57, 58; 93 Paula, J., 318, 326; 350 Paulay, G., 32, 74; 93 Pawlik, J.R., 52; 93 See Toonen, R.J., 8, 54, 55; 98 Pearce, N.J. See Leng, M., 144; 157 Pearce, N.J. G. See Price, G.D., 141; 160 Pearse, J.S. See Rivkin, R.B., 94 Pearson, T.H., 213, 233, 238, 239, 243, 248, 251, 259; 231, 266 See Bonsdorff, E., 234, 239, 243, 253, 254; 263 See Rumohr, H., 266 Pease, B.C. See Middleton, M.J., 299 Peaucellier, G., 26; 93 Pechenik, J.A., 56, 68; 93 See Qian, P.Y., 24, 56, 58; 94 Peery, C.A. See van Montfrans, J., 352 Pelger, S. See Nilsson, D.-E., 167, 168, 193, 197; 203 Pelseneer, P., 169, 183, 184, 188, 192; 203 Pembroke, A.E. See Epifanio, C.E., 344 Pemerl, J., 26; 93 Penn, J.W., 312, 318, 321; 350 Pennings, S.C., 356; 387 Pennington, J.T., 38; 93 Pérès, J.M., 63; 93 Peret, A.C. See Ferreira, C.E.L., 384 Perez, J.A.A., 124, 128, 129; 159 Perkins, W., 146; 159 Perkins-Visser, E., 270, 274, 276, 279; 300 Pernet, B., 63; 93 Perret, W.S. See Caillouet, C.W., 342 Perron, F.E., 64; 93 Perry, R.I. See Neilson, J.D., 306; 349 See Werner, F.E., 353 Peters, D.S. See Forward Jr, R.B., 344 Petersen, C.G.J., 269; 300

Peterson, C.H., 107, 108, 117; 159 See Irlandi, E.A., 270; 297 See Olafsson, E.B., 266 See Summerson, H.C., 279, 283, 289, 290; 302 Petrik, R. See Levin, P., 298 Pfister, C.A. See Hay, M.E., 385 Philips, K.B. See Provenzano Jr, A.J., 350 Phillips, D.J.H., 145; 159 Phillips, R.C., 271, 272, 284, 285, 291, 292; 300 Pianka, E.R., 233; 266 Piatigorsky, J. See Tomarev, S.I., 204 Picard, A., 8, 12, 13, 14, 15, 25; 93 Piccinetti, C. See Cespugilo, G., 152 Picken, G.B., 121; 160 Pielou, E.C., 214; 231 Piepenburg, D., 220; 231 Pihl, L., 285; 300 See Borg, A., 294 See Gibson, R.N., 296 Pile, A.J., 280; 300 Pilkey, O.H., 142; 160 See Ragland, P., 160 Pillai, T.G., 2, 6; 93 Pingitore, N., 142; 160 Pirrie, D. See Ditchfield, P.W., 153 Plaia, G. See Levin, L., 265 See Levin, L.A., 265 Platt, H.M. See Warwick, R.M., 231 Platt, T., 316; 350 Podniesinski, G. See Newell, C.R., 299 Pohle, D.G., 270, 278; 300 Poiner, I.R. See Loneragan, N.R., 299 Polenz, A. See Wessing, A., 26; 100 Pollard, D.A. See Bell, J.D., 269, 270, 273, 276, 285; 294 See Klumpp, D.W., 298 See Middleton, M.J., 299 Pollock, B.R., 324, 326; 350 Polunin, N.V.C., 359, 364, 370; 387 See Klumpp, D.W., 364, 370, 371, 372, 378, 379; 386 See Robertson, D.R., 359; 388 Ponder, W.F., 188; 203 Pope, R.H. See DeMaster, D.J., 263 Portman, J.E. See Jones, J., 265 Posey, M.H., 234, 257; 266 See Mense, D.J., 349 See Ruiz, G.M., 301 Posgay, J.A. See Merrill, A.S., 158

409

AUTHOR INDEX

Potswald, H.E., 4, 5, 7, 8, 16, 21, 22, 23, 24, 25, 31, 40, 46, 47, 49, 50, 58, 77, 78; 93, 94 Potter, E.C.E. See Moore, A., 349 Potts, D.C., 358, 364, 377; 387 Powell, C.J. See Meng, L., 290; 299 Powell, G.V.N. See Sogard, S.M., 301, 302 Power, J.H., 313; 350 See McCleave, J.D., 336; 348 Powles, H. See Henri, M., 346 Prandle, D., 306; 350 Prévot, G., 62, 73; 94 Prezant, R.S. See Carriker, M.R., 151 Price, A.R.G., 220; 231 See Izsak, C., 220; 230 Price, G.D., 141; 160 Price, N.B., 143; 160 See Hallam, A., 141, 142; 155 Prince, J.D., 121; 160 Proud, S.V. See Richardson, C.A., 161 Provenzano, A.J. See McConaugha, J.R., 348 Provenzano Jr, A.J., 318, 337; 350 Przybylowicz, W.J. See Durholtz, M.D., 153 Pullin, R.S.V. See Atkinson, R.J.A., 258; 263 Purchase, N.G., 145; 160 Qian, P.-Y., 24, 56, 58; 94 See Gosselin, L.A., 37, 60; 84 See Beckmann, M., 79 See Bryan, P.J., 79 See Harder, T., 54, 55; 85 See Lau, S.C.K., 53, 54, 56; 88 See Pechenik, J.A., 56; 93 See Qiu, J.-W., 4, 17, 32, 37, 44, 51, 57, 59, 58, 60; 94 Qiu, J.-W., 4, 17, 32, 37, 44, 51, 57, 59, 58, 60; 94 Queiroga, H., 307, 318, 319, 320, 326, 327, 328; 350 Quievreux, C., 13, 14, 15; 94 See L’Hardy, J.-P., 12; 88 Quinlan, J.A. See Hare, J.A., 346 Quitmyer, I.R. See Jones, D.S., 109; 156 Rackocinski, C. See Baltz, D.M., 294 Radashevsky, V.I. See Ivin, V.V., 86 Radley, J.D. See Harper, E.M., 200 Radtke, R. See Romanek, C.S., 162 Radtke, R.L., 124, 134; 160 Ragland, P., 143; 160 Rahid Al-azri, A. See Shepherd, S.A., 162

Raimondi, P.T. See Keough, M.J., 54; 86 Räisänen, J. See Kuisma-Kursula, P., 157 Ralph, R., 194; 203 Ramani, P. See Ansari, Z.A., 294 Ramón, M., 104, 117; 160 Ramsay, K., 107, 110, 112; 160 Ramseyer, K. See Barbin, V., 150 Randall, J.E., 61, 356, 357, 358; 94, 387 Ranzoli, F., 3, 6, 73; 94 See Vannini, E., 6; 99 Raposa, K.B., 284, 286; 300 Raskin, R.G. See Costanza, R., 230 Rasmussen, E., 269, 289; 300 Rasmussen, K. See Støttrup, J.G., 302 Ray, G.C. See Grassle, J.F., 230 Raya, C.P., 124, 126; 160 Raynie, R.C., 315, 325; 350 Ré, P., 124, 129; 160 Reed, R.J. See Murawski, S.A., 349 Rees, H.L. See Jones, J., 265 Rees, W.J., 168, 186; 203 Regnart, H.C., 326; 350 Rehrer, R.C. See Roessler, M.A., 321; 350 Reid, A.M. See Reid, R.G. B., 193; 203 Reid, D.G., 71; 94 Reid, R.G. B., 193; 203 Reinsel, K.A. See Forward Jr, R.B., 344, 345 Reish, D. See Kirchman, D., 87 Reish, D.J., 51, 73; 94 Renard, M. See Rio, M., 161 Retière, C. See Esnault, G., 264 Reusch, T.B.H., 270; 300 Rex, M.A. See Killingley, J.S., 139, 140; 157 Reynolds, J.D. See Rogers, S.I., 231 Rhoads, D.C., 103, 107, 115, 116, 117, 120, 127, 244, 245, 259, 261; 160, 266 See Diaz, R.J., 264 See Lutz, R.A., 110; 158 Rice, A.L., 333; 350 Rice, S.A. See Franzén, A., 8; 32 Richardson, C.A., 103–164; 104, 105, 107, 110, 113, 114, 115, 116, 117, 118, 119, 120, 121, 122, 127, 131, 133, 146, 147, 148, 190; 160, 161, 203 See Abades, S., 149 See Anwar, N.A., 149 See Crisp, D.J., 152 See Gaspar, M.B., 154 See Henderson, S.M., 117; 155 See Ramón, M., 117; 160 See Ramsay, K., 160

410

AUTHOR INDEX

See Robinson, R.F., 112; 161 See Seed, R., 162 See Thompson, I.S., 113; 163 Richardson, S.L. See Lyczkowski-Schulz, J., 348 Rijnsdorp, A.D., 325; 350 See Jennings, S., 230 Riley, J.D. See Greer Walker, M., 345 Rio, M., 137; 161 Rioja, E., 2; 94 Risebrough, R.W. See Goldberg, E.D., 154 Risk, A., 379; 387 Risk, M.J., 359, 378; 387 See Bourgoin, B.P., 141, 146; 150 See Hein, F.J., 378; 385 See Sammarco, P.W., 388 Rittschof, D. See Forward Jr, R.B., 326, 337, 338; 296, 344, 345 Ritz, B.A. See Fenton, G.E., 280; 296 Rivas, M. See Gutierrez, D., 264 Rivers, M.L. See Thorn, K., 163 Rivkin, R.B., 37; 94 See Seliger, H.H., 351 Rivonker, C.U. See Ansari, Z.A., 294 Rivosecchi Taramelli, E. See Chimenz Gusso, C., 51; 80 Robbins, B.D., 286, 289; 300 Robblee, M.B., 289, 290; 300 Roberts, C.M., 359; 387 Robertson, A.I., 278; 300 Robertson, D.R., 356, 358, 359, 361, 364, 377, 379, 380; 387, 388 See Waldner, R.E., 359, 361, 383; 388 Robertson, R., 62; 94 See Hoagland, K.E., 43; 85 Robertson, W. See Goldberg, E.D., 154 Robinson, J. See Warwick, R.M., 213; 231 Robinson, R.F., 112; 161 Robinson, S.M.C., 124, 125; 161 See Parsons, G.J., 159 See Sloan, N.A., 110; 163 Roche, W.L., 181; 203 Roddick, D.L. See Tan, F.C., 163 Rodhouse, P.G., 124; 161 Rodriguez, S.R., 50; 94 Roessler, M.A., 321; 350 Roff, J.C. See Parsons, G.J., 159 Rogers, H.M., 308; 350 Rogers, S.I., 218, 222, 223, 224; 231 Rollins, H.B., 136, 137, 145; 161 Rollins, J.C. See Rollins, H.B., 161

Roman, C.T. See Heck, Jr, K.L., 297 Roman, M.R., 337; 351 Romanek, C.S., 130, 131, 138; 161, 162 See Jones, D.S., 156 Rommel Jr, S.A., 336; 350, 351 Ronnback, P., 271; 300 Rooker, J.R., 270, 275, 276, 277, 278, 287, 289, 290; 300, 301 Ropes, J.W., 104, 107, 110; 162 See Bennett, J.T., 150 See Murawski, S.A., 158 Rosen, M.D., 184; 203 Rosenberg, A.A., 127; 162 Rosenberg, G.D., 103, 107, 120, 141; 162 Rosenberg, R., 258, 259, 262; 266 See Graf, G., 249; 264 See Nilsson, H.C., 262; 266 See Pearson, T.H., 213, 233, 239, 243, 248, 251; 231, 266 See Pihl, L., 285; 300 Rosenthal, H. See Klöckner, K., 87 Rosenzweig, M.L., 375; 388 Rothlisberg, P.C., 22, 23, 58, 77, 333; 94, 351 See Dall, W., 343 Rothschild, B.J., 335; 351 Rountree, R.A., 290; 301 Rouse, G.W., 9, 11, 20, 25, 26, 71; 94 See Jamieson, B.G.M., 11, 20, 21; 86 See McHugh, D., 71; 90 Routledge, R.D., 375; 388 Roux, M. See Barbin, V., 150 See Rio, M., 161 Rowden, A.A. See Attrill, M.J., 294 See Jackson, E.L., 269–303 Rowe, P.M., 325, 332, 333; 351 See Epifanio, C.E., 344 Rowlatt, S.M. See Jones, J., 265 Rozas, L.P., 275, 276, 284, 285, 290, 291, 292; 301 Rubin, J.A., 61; 94 Rudjakov, J.A., 338; 351 Ruiz, G.M., 285; 301 Rullier, F., 7, 9, 11,25, 56; 95 Rumohr, H., 255; 266 Runcorn, S.K. See Rosenberg, G.D., 103, 107, 120; 162 Runham, N.W. See Richardson, C.A., 161 Ruple, D.L. See Lyczkowski-Schulz, J., 348 Russ, G.R., 356, 359, 361, 366, 368, 369, 370, 371, 372, 375, 381; 388

411

AUTHOR INDEX

Ruyter Van Steveninck, E.D., 359, 370, 371, 372, 373, 374; 388 Rye, D.M. See Cochran, J.K., 152 Ryer, C.H., 270, 275, 289, 290; 301 Ryland, J., 54, 77; 95 Ryland, J.S. See Crisp, D.J., 52, 77; 81 Rysgaard, S., 245; 266 Rzhavsky, A.V., 4, 13, 16, 18, 22, 23, 38, 40, 57, 58, 59, 60, 75; 95 See Kupriyanova, E.K., 1–101 Sabelli, B. See Di Grande, F., 7; 81 Safrit Jr, G.W. See Peterson, C.H., 159 Saint-Joseph, A. de, 44; 95 Saiz, E., 335; 351 See Alcaraz, M., 341 Sakata, K. See Okamoto, K., 92 See Watanabe, N., 100 Sale, P.F., 277, 359, 361, 380; 301, 388 Salensky, W., 11, 28, 31, 36, 43, 76; 95 Salini, J.P. See Blaber, S.J.M., 294 Salvini-Plawen, L.V., 166, 167, 169, 174, 178, 190, 192, 193; 203 Sammarco, P.W., 359, 363, 365, 366, 370, 371, 372, 374, 377, 378, 380, 381, 382; 388 See Risk, M.J., 359, 378; 387 See Wilkinson, C.R., 365, 366, 370, 381; 389 Samstad, S., 8; 95 Samtleben, C. See Trutschler, K., 111; 163 Sand, O., 330; 351 Sanders, H.L. See Turekian, K.K., 164 Sandifer, P.A., 318; 351 Sandweiss, D.H. See Rollins, H.B., 161 Santarelli, L., 121, 131; 162 Sarnthein, M. See Hoefs, J., 133; 155 Sato, S., 111, 117; 162 Savilov, A.I., 238; 267 Savino, J.F., 275, 276, 279; 301 Sawada, N., 10, 21; 95 Schanning, M. See Gee, J.M., 230 Schein, E. See Barbin, V., 150 See Rio, M., 161 Scheltema, R.S., 10, 32, 37, 53, 54; 95 Schenk, S.L., 7, 74; 95 Scherbich, Z.N. See Arkhipkin, A.I., 128; 150 Schiel, D.R., 121; 162 Schively, M.A., 28; 95 Schmidt, T.W., 270, 273, 274; 301 Schmitz, B. See Andreasson, F.P., 149 Schneider, E. See Goldberg, E.D., 154

Schneider, J.A., 182, 188; 203, 204 Scholes, P. See Harden Jones, F.R., 346 Schreiner, K.E., 178; 204 Schroeder, P.C., 43; 95 Schuur, A. See Connaughton, V.P., 80 Schwindt, E., 51; 95 Scott, J.K., 287; 301 Scott, M. See Moore, A., 349 Seabergh, W.C., 313; 351 Sea-Fish Industry Authority, 270; 301 Seaward, D.R. See Turk, S.M. 228, 229; 231 Secor, D.H., 125; 162 Sedberry, G.R., 284, 286; 301 Seed, R., 104, 118; 162 See Anwar, N.A., 149 See Carter, J.G., 140; 151 See Richardson, C.A., 161 See Thompson, I.S., 163 Segl, M. See Kalberer, M., 156 Segrove, F., 3, 10, 18, 19, 26, 31, 35, 45, 47, 48; 95 See Thorp, C.H., 40, 78; 98 Seikai, T. See Burke, J.S., 342 Seliger, H.H., 309; 351 Selim, S.A. See Ghobashy, A.F.A., 45, 54, 59, 73, 77; 83, 84 Sellanes, J. See Gutierrez, D., 264 Sellers, T.L. See Prince, J.D., 160 Sentz-Braconnot, E., 2, 26, 47, 51, 52, 57, 73, 74; 95 Serchuk, F.M. See Murawski, S.A., 159 See Ropes, J.W., 162 Settle, L.R. See Hare, J.A., 346 Sewell, A.T. See Duggins, D.O., 82 Shabmann, L.A., 269, 275, 293; 301 Shafee, M.S. See Conan, G., 104; 152 Shanks, A.L., 306, 319, 324; 351 Sharp, B., 167, 171, 172; 204 Shaul, W., 110; 162 Shaul, W.J. See Bennett, J.T., 150 Shaw, C. See Edgar, G.J., 270, 272, 273, 274, 275, 282, 290; 295 Shaw, M., 281, 283; 301 See Jenkins, G.P., 298 Shaw, M.A. See Scheltema, R.S., 95 Shaw, R.F. See Norcross, B.L., 306, 308; 349 See Raynie, R.C., 315, 325; 350 Shearer, C., 26, 31, 73; 96 Sheilds, T.L. See Breen, P.A., 110; 151 Sheldon, J.M. See Robertson, D.R., 387 Sheldon, M.R., 315, 324; 351

412

AUTHOR INDEX

Shelton, P.M.J. See Johnson, M.L., 201 Shepherd, S.A., 121; 162 See Larkum, A.W.D., 298 Sheridan, P., 281; 301 Shirley, S.M., 334; 351 Shirley, T.C. See Shirley, S.M., 334; 351 Short, F. See Newell, C.R., 299 Short, F.T., 289; 301 See Grizzle, R.E., 296 Sichel, G., 25; 96 Sick, L.V. See Carriker, M.R., 151 Sigala, M.A. See Tankersley, R.A., 352 Simenstad, C.A. See Morgan, C.A., 349 Simpson, E.H., 214; 231 Sinclair, M.M. See Tremblay, M.J., 352 See Werner, F.E., 353 Sinis, A.I. See Galinou-Mitsoudi, S., 110; 154 Sire, J.Y., 121; 162 Sirois, A. See Balch, N., 150 Skelton, P.W., 194, 195; 204 See Harper, E.M., 168; 201 Sket, B. See Matjasic, J., 10, 26; 90 Slattery, M., 50; 96 Slattery, P.N. See Oliver, J.S., 266 Sloan, N.A., 110; 163 Slocum, C.J. See Itzkowitz, M., 379; 385 Smedstad, O. See Jennings, S., 230 Smith, C.M. See Hadfield, M.G., 84 See Walters, L.J., 100 Smith, K. See Seed, R., 162 Smith, M.G. See McShane, P.E., 121, 122; 158 Smith, N.P., 313; 351 Smith, R.J.F., 306; 351 Smith, R.S., 2, 11, 19, 22, 24, 26, 27, 28, 33, 34, 35, 45, 46, 47, 57, 59, 75; 96 Smith, S.V., 57, 59, 72; 96 Smith, T. See Huston, M., 377; 385 Snelgrove P.V. R., 234, 248, 257; 267 Snyder, C.B. See Chow, T.J., 152 Snyder, H.G. See Chow, T.J., 152 Sogard, S.M., 270, 271, 280, 282, 283, 284, 285, 286, 287, 288, 289, 290, 291; 301, 302 Soldatova, I.N., 51, 56, 57; 96 Somerfield, P.J., 222; 231 See Warwick, R.M., 231 Soniat, T.M. See Kirby, M.X., 157 Soto, A. See Gutierrez, D., 264 Soto, M.A. See Rooker, J.R., 301 Soulen, H.L. See Jordan, F., 298

Soulier, A., 8, 26, 74; 96 Soulsby, R.L., 306; 357 Sousa, W.P., 376; 388 Southward, A.J., 242; 267 See Dando, P.R., 242; 263 See Spiro, B., 267 Southward, E.C., 63; 96 See Southward, A.J., 267 Spero, H.J. See Kirby, M.X., 157 Spiro, B., 242; 267 Spitzer, P.M., 274, 275, 284; 302 Spratt, J.D., 124; 163 Srinivasagam, R.T., 33, 73; 96 Stachowitsch, M., 53; 96 Stagni, A., 4, 7, 8, 77; 96 Stam, A. See Bergman, M.J.N., 341 St Amant, L.S., 321; 351 Stancyk, S.E., 306, 309; 351 See Christy, J.H., 318, 326; 342 Staples, D.J., 318, 321; 351 See Dall, W., 343 See Loneragan, N.R., 299 Stasek, C.R., 168, 170, 182, 185, 188, 194; 204 See Rosen, M.D., 203 Stasko, A.B., 315, 323, 331; 352 Stebbing, A.R. D., 53, 54, 61, 77; 96 Stecher, H.A., 143, 145; 163 Steene, R.C. See Randall, J.E., 387 Steffe, A.S. See Bell, J.D., 294 Steger, R. See Done, T.J., 384 Stein, R.A. See Savino, J.F., 275, 276, 279; 301 Steneck, R.S., 356, 357; 388 See Langton, R.W., 298 Stephens, G.C., 242; 267 Stephens, P.J., 194; 204 Steven, A.D.L. See Meekan, M.G., 387 Stevens, K.F., 135; 163 Stevenson, J.A., 104; 163 Stewart, B.D. See Jenkins, G.P., 298 Stock, J.H., 61, 63; 96, 97 See Humes, A.G., 63; 86 Stokesbury, K.D. E., 194; 204 Stoner, A.W., 276, 280, 284, 287, 288, 290, 293; 302 See Buckel, J.A., 273, 275; 295 See Lewis, G.F., 291; 298 See Smith, N.P., 313; 351 Storeton West, T.J. See Metcalfe, J.D., 349 Støttrup, J.G., 279; 302 Strasburg, D.W. See Hiatt, R.W., 61; 85

413

AUTHOR INDEX

Strathmann, M.F., 9, 11, 18, 22, 27, 32, 43, 74; 97 See Strathmann, R.R., 70; 97 Strathmann, R.R., 21, 36, 37, 70, 71, 250; 97, 267 See Palmer, A.R., 67; 92 See Paulay, G., 93 Straughan, D., 2, 3, 4, 45, 52, 56, 57, 61, 73; 97 Stronach, J.A. See Crean, P.B., 343 Strong, J.A. See Attrill, M.J., 294 Stunkard, H.W., 62; 97 Sturesson, U., 145; 163 Sudo, H. See Tanaka, M., 352 Sulkin, S.D., 330, 333, 334, 337; 352 Summerson, H.C., 279, 283, 289, 290; 302 See Peterson, C.H., 159 Sutton, P. See Costanza, R., 230 Svärdström, K. See Carell, B., 151 Sveshnikov, V.A., 13, 21, 29, 34, 76, 77, 78; 97 Swan, E.F., 50; 97 Swan, J. See Johnson, A.L.A., 156 Swann, C.P. See Carriker, M.R., 151 Swanson, J. See Forward Jr, R.B., 345 Sweatman, H.P.A. See Robertson, D.R., 388 Sweijd, N. See Erasmus, J., 153 Swift, D.J., 245; 267 Synge, H. See Glowka, L., 230 Szedlmayer, S.T., 284, 285, 291; 302 Tabb, D.C., 318, 321; 352 Taira, K., 135; 163 Tait, N.N., 32; 97 Talbot, S.R. See Prince, J.D., 160 Talks, L. See Moore, A., 349 Tampi, P.R.S., 11, 19, 26, 28, 29; 97 Tan, F.C., 131; 163 See Margosian, A., 158 Tan, K.S., 60; 97 Tanabe, K., 110, 111; 163 Tanaka, M., 325, 326; 352 See Burke, J.S., 342 Tanaka, Y. See Burke, J.S., 342 Tanikawa-Oglesby, S. See Bricelj, V.M., 199 Tankersley, R.A., 317, 318, 320, 328, 329, 332, 333, 337, 338, 340; 352 See De Vries, M.C., 344 See Forward Jr, R.B., 305–353; 344, 345 Targett, N.M. See Connaughton, V.P., 80 Taylor, A.C., 104; 163 See Atkinson, R.J.A., 258; 263

Taylor, B.E., 140; 163 Taylor, J.D., 107; 163 Taylor, W.R. See Bosch, H.F., 308; 342 Temnyh, A.A. See Ivin, V.V., 86 Ten Hove, H.A., 2, 4, 6, 41, 53, 57, 61, 62, 63, 73, 74; 97, 98 See Ben-Eliahu, M.N., 6, 11, 41; 79 See Fiege, D., 75; 82 See Kupriyanova, E.K., 1–101 See Pillai, T.G., 6; 93 Thayer, C.W., 233, 243; 267 See Klein, R.T., 157 Thayer, G.W., 274, 276; 302 See Bach, S.D., 294 Thiebaut, E., 319, 321; 352 Thoman, T.A. See Heck Jr, K.L., 274, 275, 276, 279, 282; 297 Thomas, C. See Levin, L., 265 Thomas, C.J. See Levin, L., 265 Thomas, G.E., 186; 204 Thomas, J.G., 7; 98 Thomas, J.L., 284; 302 Thomas, M.L.H. See MacDonald, B.A., 104, 108, 110; 158 Thompson, I., 107; 163 See Jones, D.S., 156 Thompson, I.S., 113; 163 Thorn, K., 141; 163 Thorp, C.H., 22, 32, 40, 60, 75, 76, 78; 98 See Knight-Jones, P., 40; 88 Thorson, G., 9, 41, 43, 44, 52, 56, 59, 68, 77; 98 Thresher, R.E., 274, 280; 302 Thrush, S.F. See Turner, S.J., 302 Thurston, M.H. See Morton, B., 187; 203 Tolan, J.M., 277, 287; 302 Tolimieri, N., 383; 388 Tomarev, S.I., 196; 204 Tomiyama, M. See Tanaka, M., 352 Toonen, R.J., 8, 54, 55; 98 Townsend, C.R. See Begon, M., 263 Tremblay, M.J., 313; 352 See Hurley, G.V., 155 Trent, L., 318; 352 Trompetter, W.J. See Coote, G.E., 141, 143; 152 Trott, L.A. See Wilkinson, C.R., 389 Trutschler, K., 111; 163 Tsuruta, Y. See Yamashita, Y., 353 Tsutsui, R.N. See Nelson, S.G., 369; 387 Tsutsumi, H., 241; 267

414

AUTHOR INDEX

Tungate, D.S. See Harding, D., 346 Tupper, M., 270, 273, 279, 281; 302 Turekian, K.K., 111, 132, 138; 164 See Bennett, J.T., 150 Turk, S.M., 228, 229; 231 Turner, E.J. See Miller, D.C., 265 Turner, H.J., 17; 98 Turner, R.D. See Lutz, R.A., 158 Turner, R.E. See Boesch, D.F., 271, 285; 294 Turner, S.J., 284, 286; 302 Turpaeva, E.P., 233, 238, 249; 267 See Soldatova, I.N., 51, 56, 57; 96 Turpaeva, Y.P., 57; 98 Tweedy, J.H. See Jones, A.V., 347 Tyson, T. See Breen, P.A., 151 Uchida, H., 9, 10, 13, 21, 41, 43, 72, 76; 98 Ueno, M. See Burke, J.S., 342 Unabia, C.C. See Hadfield, M.G., 84 Unabia, C.R.C., 54; 99 Underhill, L.G. See Lipinski, M., 158 Underwood, A.J. See James, R.J., 52; 86 See Moran, M.J., 91 Urey, H.C., 130; 164 See Epstein, S., 153 Uschakova, O.O., 26; 99 Uwe, B. See Rollins, H.B., 161 Uysal, H. See Bryan, G.W., 145; 151 Vaišnys, J.R. See Turekian, K.K., 164 Valenti, C.C. See Epifanio, C.E., 344 Valentine, J.F. See Mattila, J., 299 Valle, C.F., 270, 276, 278, 279, 280, 284, 286, 289; 302 Vance, D.J. See Staples, D.J., 321; 351 Vance, R.R., 64; 99 Van den Belt, M. See Costanza, R., 230 Van den Hurk, P. See Ten Hove, H.A., 57; 98 Van der Borg, K. See Witbaard, R., 164 Van der Maarel, E. See Glenn-Lewin, D.C., 376; 384 Van der Steen, W.J. See McCleave, J.D., 348 Van der Veer, H.W. See Bergman, M.J.N., 341 See Rijnsdorp, A.D., 350 Vane-Wright, R.I., 211, 212; 231 See Humphries, C.J., 230 See Williams, P.H., 231 Van Heukelem, W.F. See Sulkin, S.D., 337; 352

Van Montfrans, J., 326; 352 See Goodrich, D.M., 345 See Metcalfe, K.S., 349 See Orth, R.J., 276, 284, 291; 299, 300 See Pile, A.J., 300 See Ryer, C.H., 301 Vannini, E., 4, 6, 9; 99 Van Noort, G.J. See Creutzberg, F., 343 Van Stralen, M. See Rijnsdorp, A.D., 350 Vásquez, C. See Gutierrez, D., 264 Vaughan, N. See Allmon, W.D., 149 Veale, L.O. See Ramsay, K., 160 Vedder, K. See Strathmann, R.R., 21; 97 Veiga, J. See Castel, J., 308; 342 Vella, P. See Stevens, K.F., 135; 163 Venema, S.C., 333; 352 Venn, T.J. See Taylor, A.C., 104; 163 Vermeij, G.J., 194; 204 Verwey, J., 318; 352 Vigneau, S. See Cliche, G., 200 Villanueva, R. See Gili, J.-M., 84 Vine, P.J., 14, 15, 16, 23, 51, 61, 377; 99, 388 See Knight-Jones, E.W., 87 Vinogradov, K.A., 61; 99 Virnstein, R.W. See Kulczycki, G.R., 298 Vitturi, R., 7, 8; 99 Vogel, S., 335; 352 Voglis, G.M., 315; 352 Von Buddenbrock, W., 186; 204 Von Drasche, R., 18; 99 Von Marenzeller, E., 63; 99 Voorzanger, B. See McCleave, J.D., 348 Voss, J. See Piepenburg, D., 231 Vuillemin, S., 7, 18, 21, 26, 32, 40, 47, 56, 58, 73, 77; 99 Wada, K. See Hamamoto, K., 84 Wada, Y. See Kuwahara, A., 347 Wägele, J.W., 64; 99, 100 Waldner, R.E., 359, 361, 383; 388 Walker, A.J.M. See Knight-Jones, P., 14, 15, 38; 88 Walker, G. See Thompson, I.S., 163 Walker, P. See Richardson, C.A., 107, 114; 161 Waller, T.R., 173, 174, 178, 185, 188, 192, 195; 204 Walsh, H. See Burke, J.S., 342 Walter, L.M. See Burton, E.A., 142; 151 Walters, L.J., 53, 55; 100 Wanders, J.B.W., 356; 389

415

AUTHOR INDEX

Wang, D.-P., 313; 352 See Gupta, S., 345 Wang, Z. See Thiebaut, E., 352 Ward, J.E., 61; 100 Ward, P., 129; 164 Ward, P.D. See Taylor, B.E., 140; 163 Warlen, S.M. See Forward Jr, R.B., 344 Warner, R.R., 70; 100 Warwick, R. See Help, C., 230 Warwick, R.M., 207–231; 208, 210, 213, 214, 216, 218, 221, 222; 231 See Clarke, K.R., 216, 217, 218, 219, 220, 221, 222, 227, 228; 229 Warwick, R.M. See Dawson Shepherd, A.R., 230 See Gee, J.M., 230 See Gray, J.S., 230 Watanabe, A. See Okamoto, K., 92 Watanabe, N., 55; 100 See Okamoto, K., 51, 58; 92 Watanabe, S. See Watanabe, N., 100 Watanabe, Y. See Watanabe, N., 100 Webb, D.G., 273, 274; 302 Webb, K.L. See Wiebe, W.J., 389 Webb, P.W. See Metcalfe, J.D., 349 Weber, F.L., 181, 182; 204 Wefer, G., 130, 131, 140; 164 See Erlenkeuser, H., 131; 153 See Kalberer, M., 156 Weidman, C.R., 107, 130, 131, 132, 136, 137, 138; 164 Weihs, D., 314, 315, 339; 352 Weinstein, M.P., 291, 306, 309, 324; 302, 352 Weiss, S.L. See Weinstein, M.P., 352 Welch, J.M., 331, 334, 335, 338; 353 See Forward Jr, R.B., 344, 345 Wellington, G.M., 356, 359, 362, 363, 364, 377, 378; 389 Wells, M.J., 185; 204 Welsford, D.C. See Jenkins, G.P., 347 Weng, H. See Pollock, B.R., 350 Wenner, E., 321; 353 Wenner, E.L. See Mense, D.J., 320, 337; 349 Wennhage, H. See Borg, A., 294 See Gibson, R.N., 296 Wenrich, D.H., 167; 204 Werner, F.E., 275, 313; 303, 353 See Churchill, J.H., 343 See Hare, J.A., 346 See Luettich Jr, R.A., 348 See Tremblay, M.J., 352

Wesenberg-Lund, E., 61; 100 Wessing, A., 26; 100 West, J.E. See Lacalli, T.C., 47; 88 West, T. See Mense, D.J., 349 Westermark, T. See Carell, B., 151 Westheide, W., 7; 100 Westoby, M. See Bell, J.D., 278, 279, 283, 284, 286, 287, 288; 294 See Worthington, D.G., 303 Wheatcroft, R.A. See Jumars, P.A., 265 Wheatley, M.J. See Jenkins, G.P., 298 Wheeler, A., 271, 282; 303 Wheeler, Q.D. See Nixon, K.C., 212; 231 White, J., 26, 75; 100 White, R.W.G. See Wolf, B.M., 194; 205 Whitin, N., 33; 100 Whitlatch, R.B., 241; 267 Whitledge, T.E. See Feder, H.M., 264 Whyte, M.A., 115; 164 Wiborg, K.F. See Rosenberg, A.A., 162 Wickins, J.F., 321; 353 Wiebe, W.J., 370; 389 Wieber, M.G. See Tankersley, R.A., 352 Wieghell, J.G. See Crisp, D.J., 152 Wiese, K.B. See Valle, C.F., 302 Wilcox, D.J. See Moore, K.A., 289; 299 Wildish, D.J., 241, 244, 249; 267 Wilkens, E.P.H. See Lewis, R.M., 325, 327, 329; 348 Wilkens, L.A., 188, 194; 204, 205 Wilkinson, C.R., 359, 365, 366, 370, 381; 389 Wilkinson, D.M., 210; 231 Wilkinson, M.R. See Turner, S.J., 302 Willfuhr, J. See Klöckner, K., 87 Williams, A.B., 321; 353 Williams, A.H., 356, 379; 389 See Sammarco, P.W., 357, 363, 364, 378, 379; 388 Williams, D.F. See Arthur, M.A., 150 See Jones, D.S., 156 See Krantz, D.E., 157 See Romanek, C.S., 162 Williams, D. McB., 361; 389 Williams, G.B. See Gee, J.M., 24, 25, 77; 83 See Meadows, P.S., 54, 77; 90 Williams, I.P. See Scheltema, R.S., 95 Williams, J.B., 36, 46, 52, 77; 100 Williams, P.H., 211, 212; 231 See Humphries, C.J., 230 See Vane-Wright, R.I., 231

416

AUTHOR INDEX

Williams, R.J. See Hannan, J.C., 277, 278, 286; 297 Williamson, P., 121; 164 Wilson, D.P., 31; 100 Wilson, E.O. See MacArthur, R.H., 221; 230 Wilson, K.A., 275; 303 See Heck Jr, K.L., 275; 297 Wilson, S., 356, 358, 359, 363, 364, 380, 382; 389 Wilson, W.H., 64; 100 Wiltschko, R., 330; 353 Wiltschko, W. See Wiltschko, R., 330; 353 Wippelhauser, G.S., 324, 329, 336; 353 See McCleave, J.D., 324, 329; 348 Wisely, B., 19, 26, 27, 35, 45, 46, 47, 73, 77; 100 Witbaard, R., 110, 112, 114, 115, 138; 164 Wkwabi, E.O. See De Troch, M., 295 Wolcott, D.L. See Perkins-Visser, E., 300 Wolcott, T.G. See Perkins-Visser, E., 300 Wolf, B.M., 194; 205 Wong, K.C. See Garvine, R.W., 345 Woo, K.S. See Khim, B.K., 157 Wood, E.J. See Dew, B, 51; 81 Wood, E.J.F., 281; 303 Wood, L., 321, 322; 353 Wooldridge, T., 308; 353 See Melville-Smith, R., 348 Word, J.Q., 234; 267 Worthington, D.G., 277, 278, 286, 291; 303 See Bell, J.D., 294 Wright, D.E. See Barber, V.C., 181, 185, 192; 199 Wu, B.-L., 9; 100 Yager, P.L., 250; 267 Yamada, H. See Yamashita, Y., 353

Yamashita, Y., 325, 326; 353 Yamasu, T. See Nishi, E., 4, 6, 9, 10, 11, 13, 17, 18, 19, 20, 21, 28, 29, 41, 43, 47, 48, 75; 92 Yaremko, M. See Butler, J., 128; 151 Yokel, B. See Idyll, C.P., 346 Yonge, C.M., 167, 168, 170, 184, 185, 187, 188, 192, 194, 195, 238; 205, 267 See Ponder, W.F., 203 Yoshioshi, K. See Matuso, R., 10, 21; 90 Young, C.M., 11, 32, 35, 37, 38, 74; 100 See Cowden, C., 80 Young, D.K., 61; 100, 101 See Rhoads, D.C., 244, 245; 266 Young, P.C., 290, 321; 303, 353 Zeibis, W., 244; 267 See Huettel, M., 264 Zeleny, C., 35, 45, 73; 101 Zeller, D.C., 359, 364, 378, 379, 382; 389 Zeng, C., 318, 319, 320, 327, 328, 329; 353 Zibrowius, H., 2, 9, 41, 43; 101 Zieman, J.C. See Robblee, M.B., 289, 290; 300 See Wood, E.J.F., 303 Zimmer-Faust, R.K. See Morgan, S.G., 349 Zimmerman, M.A., 336; 353 Zimmerman, R.J., 284; 303 See Thomas, J.L., 302 Zirovieva, R. See Tomarev, S.I., 204 Zolotarev, V.N., 108; 164 Zugmayer, E., 181; 205 Zuidema, D. See Bergman, M.J.N., 341 Zupo, V., 284, 287; 303 Zuraw, E.A., 10, 17; 101

417

SYSTEMATIC INDEX

References to complete articles are given in bold type; references to sections of articles are given in italics; references to pages are given in normal type. Abra, 252 alba, 247 nitida, 247 Abralia trigonura, 128 Abudefduf, 357, 364 Acaenomolgus protulae, 61 Acanthaster planci, 378 Acanthomysis, 308 Acanthopagrus australis, 324 Acanthuridae, 61, 356 Acanthurus bahianus, 379 Acartia longipatella, 308 natalensis, 308 Acmaea antillarum, 122 Acropora cervicornis, 364 palifera, 377 prolifera, 52 Actiniidae, 238 Adamussium colbecki, 194, 195 Aequipecten opercularis, 131, 135 Agonus cataphractus, 223 Alloteuthis subulata, 124, 126, 127 Amblyglyphidodon, 357 Ambonychiodea, 189 Ampharete, 252 Amphipholis squamata, 240 Amphiprion, 357 Amphiroa, 373 Amphitrite, 247 Amphiura, 247, 252 filiformis, 242, 253, 259 Amplicaria, 40 Amusium, 179, 186, 187, 192 balloti, 105, 168, 187, 194, 195 pleuronectes, 168, 179, 184, 187, 194 Amygdalum, 184 Anadara granosa, 112, 113, 117, 120 notabilis, 193 Anapagurus, 318 Anatina (=Laternula), 169, 183 Anchoa mitchilli, 325

Anguilla, 323 anguilla, 223, 309, 323, 324, 332, 335, 336 austrails, 324 dieffenbachii, 324 rostrata, 316, 322, 323, 324, 329, 332, 339 Anguilliformes, 223, 323, 324 Angulus, 252 Anomalodesmata, 165, 183, 188, 193, 197, 198 Anomia, 170 simplex, 142 Anomiidae, 165, 170, 184, 188, 192, 197 Anomioidea, 170, 176, 177, 188, 189, 190 Anomura, 318, 320 Anoplophyra spirorbis, 62 Anthrocosioidea, 189 Apomatolos simplex, 72 Apomatus, 73 globifer, 72 Aporocotyle simplex, 62 Area, 131, 169, 170, 173, 184, 185, 188 noe, 196 zebra, 196 Archanodontoidea, 189 Arcidae, 169, 187 Arcoida, 165, 166, 170, 173, 178, 184, 187, 188, 191, 193, 196, 197, 198 Arcoidea, 123, 173, 174, 185, 188, 189, 190, 192, 193 Arctacama proboscidea, 62 Arctica islandica, 106, 108, 110, 111, 112, 114, 115, 131, 132, 136, 137, 147 Arcticoidea, 189 Arenicola cristata, 240 marina, 258 Argopecten gibbus, 105, 145 irradians, 105, 194, 270, 276, 287 Arnoglossus imperialis, 223 laterna, 223 Arripis truttacea, 291 Arthropoda, 165, 173 Ascidia, 238 Ascophyllum, 53

418

SYSTEMATIC INDEX

Aspitrigla cuculus, 223 Astacus gammarus, 59 Astarte elliptica, 11 Asterias rubens, 186 Asteroidea, 61 Astropecten americanus, 240 Atrina, 168 Autobranchia, 196 Avicula (=Pteria), 169 Babinkoidea, 189 Balanus, 33, 252 amphitrite, 61 improvisus, 253, 255, 309 Balistidae, 61 Barbatia, 173, 174, 185, 190, 191 cancellaria, 173, 174, 196 virescens, 174, 192 Bathyarca pectunculoides, 187 Bathymodiolus thermophilus, 137 Bathyporeia pilosa, 255 Bivalvia, 103, 165, 167, 168, 169, 170, 184, 187, 188, 189, 190, 191, 194, 195, 196, 198 Blennius ocellaris, 223 Boccardia redeki, 253 Boonea, 62 Bothidae, 223 Brachyura, 318, 320 Brevoortia patronus, 223, 325 tyrannus, 325, 326, 329 Buccinum undatum, 121, 122, 123, 131 Buglossidium luteum, 223 Bugula neritina, 53 Bushiella, 3, 4, 15, 20, 22, 40, 75, 77 (B.) abnormis, 15, 75 (B.) evoluta, 53 (Jugaria) atlantica, 15, 17, 75, 76 (Jugaria) granulata, 15, 75, 76 (Jugaria) granulatus, 3 (Jugaria) kofiadii, 15, 38, 75 (Jugaria) quadrangularis, 3, 15, 75 (Jugaria) similis, 3, 15, 75 Callianassa, 247 californiensis, 318, 320 Callinectes sapidus, 269, 270, 317, 318, 319, 320, 326, 328, 335, 336, 340 Callista chione, 108 Calocaris macandreae, 253, 259 Calothrix, 371

Calyptogena, 131 magnifica, 137 Camptochlamys alaskensis, 135 Cancer irroratus, 194, 320 pagurus, 113 Capitella, 241, 248 capitata, 213 sp. 1, 241 Capros aper, 223 Capulidae, 63, 64 Caranx hippos, 274 Carchariniformes, 223 Carcinus maenas, 318, 319, 320, 326, 327, 329, 340 Cardiidae, 165, 169, 185, 188, 192, 193, 194, 196, 197 Cardioidea, 165, 181, 188, 189, 190, 193 Cardiomya, 193 Carditoidea, 189 Cardium (=Cerastoderma), 169 edule, 115 Caridea, 318 Cavolina longirostris, 133 Cellana toreuma, 112, 121, 122 Centroceras, 371 clavulatum, 372 Centrolabrus exoletus, 223 Cephalochorda, 238 Cephalopoda, 103 Cepola rubescens, 223, 258 Ceramiaceae, 372 Ceramiales, 370, 372 Ceramium, 371 flaccidum, 372 Cerastoderma, 184, 191, 196, 252 edule, 104, 108, 109, 115, 117, 118, 119, 120, 142, 147, 181, 188, 190, 192, 194 glaucum, 104 glaucum (=lamarckii), 255 Cercaria loossi, 62 Chaetoceros, 37 Chaetodontidae, 61 Chaetopterus, 247 Chaetozone setosa, 253 Chamelea, 252 gallina, 117 Chamoidea, 189 Chelon labrosus, 223 Chione (Austrovenus) stutchburyi, 145 subrugosa, 137, 145 Chirolophis ascanii, 223

419

SYSTEMATIC INDEX

Chironomidae, 253 Chitinopoma, 72 arndti, 9, 41, 72 occidentalis, 72 rzhavskii, 9, 41, 72, 73 serrula, 8, 9, 18, 20, 21, 36, 41, 43, 72, 73 Chlamys, 135, 192 gemmulata, 135 multistriata, 185 nobilis, 184 opercularis, 104, 105, 186, 194 varia, 104 Chondrichthyes, 223 Chondrus, 44 Chordata, 223 Chromis, 357 Chrysiptera, 357, 358, 380 biocellata, 358 Ciliata mustela, 223 Circeinae, 13, 31, 38, 39 Circeis, 13, 39 armoricana, 3, 18, 13, 18, 22, 23, 25, 58, 75 cf. armoricana, 4, 5, 28, 29, 30, 34, 36, 47, 49, 50, 53, 59, 75, 78 cf. armoricana A, 13 cf. armoricana B, 13 oshurkovi, 13, 75 paguri, 13, 22, 53, 75 spirillum, 7, 8, 22, 53, 75, 78 Cladophora, 282 Clavagella australis, 193 Clavagelloidea, 189 Clinocardium nuttalli, 118, 138 Cliopyramidata, 131, 139 Clupea harengus harengus, 308 Clupeiformes, 325 Coelothrix, 371 Conger conger, 223, 273 Congeria kusceri, 167 Corallina officinalis, 77 Corbiculoidea, 189 Cordilophora caspia, 255 Coris schroederi, 379 Corophium, 255 Coryphaenoides rupestris, 223 Cranchia scabra, 128 Crangon crangon, 253 Crassatelloidea, 189 Crassostrea gigas, 110, 143 virginica, 141, 145, 321

Crenilabrus melops, 223 Crenomytilus grayanus, 108 Crepidula fornicata, 121, 122, 142 plana, 142 Cresis, 131 acicula, 139 Crucigera, 24 irregularis, 9, 22, 72 zygophora, 9, 22, 36, 72 Crustacea, 238 Crustacea Decapoda, 318, 320 Ctenodontoidea, 189 Ctenoides, 165, 191, 198 excavata, 178 floridanus, 178, 179, 192, 197 Ctenolabrus rupestris, 223 Cucullaea, 173 Cuspidaria, 193 Cuvierina columnella, 139 Cyamiodea, 189 Cycloconchoidea, 189 Cyclopterus lumpus, 223 Cymbasoma filogranarum, 63 Cynoscion nebulosus, 274, 325 regalis, 38, 325 Cyrtodontoidea, 189 Dascyllus, 357 Dexiospira foraminosa, 19, 75 Diadema, 379 antillarum, 379 Diastylis rathkei typica, 255 Dicentrarchus labrax, 223 Dimyoidea, 189 Diopatra cuprea, 240 Diplecogaster bimaculata, 223 Diplodus annularis, 273, 277 Dischistodus, 357, 358 melanotus, 358 perspicillatus, 358, 360 prosopotaenia, 358, 362 pseudochrysopoecilus, 359 Ditrupa arietina, 8, 59, 72 Donax vittatus, 104, 117, 190 Dreissena polymorpha, 167, 171 Dreissenoidea, 189 Drilonereis, 63 Drosophila, 196 Dunaliella primolecta, 37 salina, 37 tertiolecta, 37

420

SYSTEMATIC INDEX

Echiichthys vipera, 223 Echinarachnius parma, 240 Echinocardium, 247, 252, 258 Echinodermata, 238 Echinoidea, 61, 238 Echinometra, 379 viridis, 379 Echinus, 252 Echiurida, 238 Ectocarpus, 371 Edmondioidea, 189 Eisothistos, 63, 64 Eledone cirrosa, 124 Emerita talpoida, 240 Enigmonia, 165, 184, 185, 191, 192, 193 aenigmatica, 176, 177, 188, 197 Ensis, 247 arcuatus, 112 directus, 146, 240 ensis, 109, 117 siliqua, 112, 113, 117, 145 Entelurus aequoreus, 223 Epilucinia californica, 135 Equichlamys bifrons, 194 Eulaeospira, 39, 77 convexis, 14, 56, 75, 77 Eupagurus bernhardus, 53 Eupomacentrus acapulcoensis, 377 lividus, 370, 372 planifrons, 372, 374, 380 Eurytemora affinis, 308, 309 Eutrigla gurnardus, 223 Fargoa, 62 Ficopomatus, 2, 21, 26, 61 enigmaticus, 2, 3, 7, 8, 9, 17, 18, 21, 22, 25, 26, 32, 36, 43, 45, 47, 51, 56, 57, 58, 59, 72, 73 miamiensis, 9, 36, 37, 72, 74 uschakovi, 2, 3, 4, 9, 22, 51, 56, 57, 58, 61, 72, 73 Filograna, 4, 8, 36, 63, 72 implexa, 8, 51, 59, 63, 72, 74 tribranchiata, 73, 74 Filograna/Salmacina complex, 4, 7, 9, 41, 64, 72 Filogranella, 6 elatensis, 6, 73 Filograninae, 2

Filogranula, 5, 6, 41 gracilis, 6, 73 rzhavskii, 72, 73 stellata, 63, 73 Fissurella crasa, 121 Floriprotis sabiuraensis, 9, 21, 43, 73 Foraminifera, 238 Fragiinae, 188 Fragum, 188, 196 erugatum, 188 unedo, 119 Fucus, 24, 53, 77, 282 serratus, 44, 52 vesiculosus, 282 Fulvia, 182 Gadidae, 223 Gadiformes, 223 Gadus morhua, 223, 270, 276, 322, 323, 336 Gaidropsarus mediterraneus, 223 vulgaris, 223 Gaimardioidea, 189 Galeolaria, 24, 26 caespitosa, 4, 9, 18, 20, 21, 22, 25, 26, 32, 33, 34, 35, 36, 37, 45, 47, 54, 62, 73 hystrix, 4, 9, 18, 19, 73 Galeomma, 168 Galeommatoidea, 189 Galeorhinus galeus, 223 Gammarus, 253 Gasterosteus aculeatus, 223 Gastrochaenoidea, 189 Gastropoda, 61, 62, 103, 166, 168, 190 Gelidiopsis, 371, 372, 373 Gelidium, 371 Geukensia demissa, 108, 110 (=Modiolus) demissa, 104 Giffordia, 288 Gilchristella aestaurius, 325 Glossoidea, 189 Glycera, 252 Glycymeris, 173, 174, 185, 190, 191 glycymeris, 107, 108, 109, 110, 112, 113, 175, 176, 192 Glyptocephalus cynoglossus, 223 Gobiesox strumosus, 325 Gobiidae, 223 Gobioidei, 325 Gobiosoma bosci, 325

421

SYSTEMATIC INDEX

Gobius gasteveni, 223 niger, 223 paganellus, 223 Gonatus fabricii, 127 Gracilaria, 371 Gracilariopsis, 371 Grapsidae, 318, 320 Gregarinidae, 62 Haemocera, 63 Haletta semifasciata, 270, 273 Halichoeres melanurus, 379 Halicryptus spinulosus, 255 Halimeda, 371 Haliotis corrugata, 121 Haliotis fulgens, 121 iris, 121 laevigata, 121 mariae, 121 midae, 121 rubra, 121, 122 Halodule, 272, 274, 290 wrightii, 272, 275, 276, 287 Halophila, 280 Haplosporidium marchouxi, 62 Harmothoe (=Antinoella) sarsi, 255 Hediste (=Nereis) diversicolor, 253, 255, 257 Helicosiphon, 39 biscoeensis, 14, 75 platyspira, 14, 75 Hemidonacidae, 188 Hemidonax, 188 Hemiglyphidodon, 357 plagiometopon, 358, 359, 360, 363, 365, 370, 371, 372, 374, 375, 378, 380, 382 Herposiphonia, 371 Heterodonta, 166, 188, 198 Heteromastus filiformis, 248, 253, 259 Heterosiphonia, 371 Heterozostera, 283 tasmanica, 272, 273, 282, 291 Hexapanopeus angustifrons, 320 Hiatelloidea, 189 Hinnites (=Crassoderma) multirugosus, 195 Hippocampus hippocampus, 223 ramulosus, 223 Hippoglossoides platessoides, 223 Hippoglossus hippoglossus, 223 Hippopus hippopus, 182 Hippuritoidea, 189 Histioteuthis macrohista, 125

Holothurida, 238 Homarus americanus, 273 Hyalopomatus claparedii, 63, 73 Hydrobia, 255 Hydroidae, 238 Hydroides, 18, 21, 24, 26, 31, 62 dianthus, 7, 8, 10, 17, 21, 25, 26, 32, 35, 36, 38, 45, 51, 54, 55, 56, 57, 58, 62, 73, 74 diramphus, 8, 73 elegans, 2, 3, 4, 8, 10, 17, 19, 20, 21, 24, 25, 26, 27, 32, 33, 35, 36, 37, 44, 45, 46, 47, 51, 53, 54, 55, 56, 57, 58, 59, 60, 62, 73, 74 ezoensis, 10, 18, 21, 22, 26, 35, 36, 55, 56, 57, 73 fusicola, 10, 21, 73 hexagonis/us, 73 norvegica, 2 norvegica/us, 73 norvegicus, 2, 7, 8, 21, 25, 73 pectinatus, 73 tuberculatus, 63, 73 uncinatus, 2, 73 Hydrolithon, 371 Hyperoplus immaculatus Idas argentus, 111 Idiosepius pygmaeus, 124, 126, 127 Idotea, 253 Illex, 125 argentinus, 127 gahi, 123 illecebrosus, 124, 125, 126, 127, 128, 129 Ilyanassa obsoleta, 240 Isochrysis galbana, 37 Isognomon, 170, 184, 185, 191 costellatus, 170 legumen, 173, 186 Isognomonidae, 173, 186, 190 Jania, 371 Janua, 40 pagenstecheri, 4, 7, 8, 13, 20, 22, 25, 30, 40, 53, 54, 57, 59, 62, 75, 77, 78 (Dexiospira) alveolata, 75 (Dexiospira) brasiliensis, 75 (Dexiospira) formosa, 75 (Dexiospira) lamellosa, 75 (Dexiospira) nipponica, 75 (Dexiospira) steuri, 75 (Fauveledora) kayi, 75 (Pillaiospira) trifurcata, 75

422

SYSTEMATIC INDEX

Januinae, 13, 31, 38, 40, 50 Josephella, 63, 73 marenzelleri, 6, 73 Kareius bicoloratus, 325 Labridae, 61, 223 Labrus bergylta, 223 mixtus, 223 Laevicardium, 185 Lagodon rhomboides, 272, 325, 328 Lamellibranchia, 238 Laminaria, 53, 59, 77, 252 digitata, 53 ochroleuca, 221 Lanice, 252 Laternula, 165, 184, 191 anatina, 184 cf. gracilis, 184 crecinna, 184 elliptica, 184, 196 rostrata, 184 truncata, 165, 183, 184, 193, 194, 196, 198 Laternulidae, 165, 166, 169, 183, 185, 190, 193, 194, 196, 197 Laurencia, 373 Leiostomus xanthurus, 324, 325, 328 Leitoscoloplos fragilis, 240 Leodora, 40 Lepidorhombus whiffiagonis, 223 Leptopecten latiauratus, 179, 186 Lesueurigobius friesii, 223 Leverella, 373 Liagora, 371 Libinia, 320 Lichomolgidae, 63 Lima, 168, 191, 192 (=Ctenoides) excavata, 178 excavata, 188 scabra, 178 squamosa, 178, 185 Limacina, 131 helicina, 133, 139 inflata, 139 Limanda limanda, 223 Limaria, 173 Limidae, 165, 188, 191, 192, 197, 198 Limoidea, 178, 179, 185, 188, 189, 190, 193 Limopsoidea, 170, 171, 173, 175, 176, 178, 185, 188, 189, 190, 192 Liocranchia reinhardti, 128

Liparis liparis, 223 Litharca, 173 Lithodomus (=Lithophaga), 170 Lithophaga lithophaga, 110 Lithothamnion, 44 polymorphum, 52 Littorina littorea, 121, 122, 123, 133 scabra, 122 Lobophora, 371 Loligo, 124, 125 chinensis, 128 forbesi, 124 gahi, 127, 128 opalescens, 128, 196 vulgaris, 125 vulgaris reynaudii, 125, 142 Loliolus noctiluca, 126 Lophiiformes, 223 Lophius piscatorius, 223 Lucinoidea, 189 Lumpenus lumpretaeformis, 223 Lutraria lutraria, 113 Lyngbya, 371 Macoma balthica, 104, 318, 319 Macrocallista, 131 Macropipus holsatus, 318, 333 Macruronis novaezelandiae, 280 Mactra chinensis, 131 isabelleana, 144 Mactroidea, 189 Maera loveni, 259 Maldane, 247, 252 sarsi, 253, 259 Malleus, 170, 184 Marenzelleria jonesi, 240 viridis, 255 Margaritifera margaritifera, 146 Marifugia cavatica 10, 26, 73 Maxmuelleria lankesteri, 258 Mediomastus, 248 Megalodontoidea, 189 Melanogrammus aeglefinus, 223 Meleagrina (=Pinctada), 170 Mercenaria, 287 mercenaria, 104, 107, 108, 109, 110, 111, 112, 114, 115, 116, 117, 143, 145, 240, 270, 287 Mercierella enigmatica, 73 Merlangius merlangus, 223 Merluccius merluccius, 223

423

SYSTEMATIC INDEX

Mesopodopsis slabberi, 308 Metalaeospira, 39 clasmani, 14, 75 pixelli, 15, 17, 75 tennis, 15, 38, 75 Metapenaeus, 281 Metavermilia cf. ovata, 10, 43, 73 Metazoa, 196 Meuschenia frycineti, 270, 273 Microchirus variegatus, 223 Microcoleus, 371 Microgobius, 325 Micropogonias undulatus, 325 Microprotula ovicellata, 10, 36, 41, 43, 73 Mi(c)roserpula inflata, 73 Microspathodon chrysurus, 359 dorsalis 359, 360, 365, 366, 368, 369, 370, 371 Microstomus kitt, 223 Microteuthis ingens, 124 Minnivola pyxidatus, 175, 186 Modiola (=Amygdala), 170 Modiolaria (=Musculus), 170 Modiolus modiolus, 107, 108, 113, 131, 133, 135, 139, 146, 147, 148 Modiomorphoidea, 189 Mola mola, 223 Mollusca, 238, 318, 321 Molva molva 223 Monastrea annularis, 364 Monocystis serpulae, 62 Monodonta lineata, 121 Monoporeia affinis, 253, 255 Morone saxatilis, 275 Moroteuthis ingens, 125, 128 robusta, 128, 129 Mullus surmuletus, 223 Musculus, 184 Mustelus asterias, 223 mustelus, 223 Mya, 172, 252 arenaria, 104, 107, 108, 110, 111, 113, 141 142, 143, 167, 172 (Arenomya) arenaria, 255 truncata, 110, 146 Myoidea, 189 Myriochele, 253 Mysella, 242 bidentata, 242 Mytilidae, 141 Mytiloidea, 170, 188, 189

Mytilus, 33, 141, 170, 184, 252 californianus, 131, 136, 145, 146 edulis, 62, 104, 105, 106, 107, 108, 112, 113, 114, 116, 117, 119, 131, 135, 141, 142, 143, 145, 146, 167, 253, 255, 270, 276, 278 edulis chilensis, 118 galloprovincialis, 104 trossulus, 117, 144 Myxocephalus scorpius, 223 Nacella (Patinigera) cancinna, 121 Nannochloris atomus, 37 Nassa mutabilis, 131 Nautilus, 124, 129, 132, 143 macromphalus, 140, 144 pompilus, 129, 132, 140, 144 scrobiculatus, 132 Neodexiospira, 29, 40, 57, 76, 77 alveolata, 13, 22, 28, 36, 47, 49, 50, 75, 76, 77 brasilensis, 4, 13, 25, 38, 53, 54, 55, 56, 57, 58, 59, 60, 75, 76, 77 cf. brasiliensis, 13, 18, 22, 23, 77 foraminosa, 13, 18, 75, 76 formosa, 14, 75, 76 kayi, 14, 75, 76 lamellosa, 14, 56, 75, 76, 77 pseudocorrugata, 14, 28, 40, 54, 59, 76, 77 steueri, 14, 75, 76 Neoglyphidodon, 357 melas, 364 nigroris, 359, 361, 362, 363 Neomonospora, 371 Neomysis mercedis, 308 Neopomacentrus, 357 Neosabellaria cementarium, 38, 73, 74 Nepthyidae, 64 Nereis, 62 Nidificaria, 40 nidica, 15, 17, 76 palliata, 15, 38, 76 Nucella lapillus, 121, 122 Nucula, 247 Nuculanoidea, 171, 189 Nuculoidea, 171, 189 Octopus, 126 dofleini, 124 vulgaris, 124, 126 Odostomia, 62

424

SYSTEMATIC INDEX

Okadaia elegans, 61 Omphalopoma stellata, 73 Oncorhynchus nerka, 323, 324 Ophiothrix, 252 Ophryotrocha, 213 Opistobranchia, 61 Opsanus beta, 274 Oscillatoriaceae, 371 Osmerus mordax, 308, 323, 324 Osteichthyes, 223 Ostrea, 170 edulis, 108, 110, 172, 185 virginica, 167 Ostreidae, 170, 172 Ostreoidea, 170, 188, 189 Ovalipes ocellatus, 320 Owenia, 247 Paguridae, 320 Pagurus longicarpus, 240 Palaemon, 318 Palaeotaxodonta, 185 Palinura, 321 Pandaroidea, 165, 188, 189 Panope abrupta, 110 generosa, 110, 132 Panopea zelandica, 110 Panopeidae, 318 Panulirus argus, 321 cygnus, 285 Paphies subtriangulata, 143 Parablennius gattorugine, 223 Paradexiospira nakamurai, 76 vitrea, 25 (Spirorbides) vitrea, 7, 8, 13, 23, 38, 47, 50, 76, 78 Paradiopatras quadricuspis, 253 Paralabrax nebulifer, 270 Paralaeospira, 39 levinseni, 14, 38, 76 malardi, 14, 25, 76, 77 parallela, 14, 76 Paralaeospirinae, 14, 31, 38, 39 Paralichthys, 324 albiguttata, 325 californicus, 278, 286 dentatus, 325, 328 lethostigma, 325, 328 olivaceus, 325 Paraprotis, 71 dendrova, 10, 17, 20, 21, 28, 36, 43, 73

Paraprotula apomatoides, 10, 41, 73 Parma victoriae, 359 Parophrys vetulus, 325 Patella, 146, 252 vulgata, 121, 122 Patinopecten, 191 yessoensis, 179, 180, 181, 194 Pavona gigantea, 377 Pecten, 192 diegensis, 105 irradians, 180 jacobaeus, 179, 184 maximus, 104, 105, 106, 107, 109, 139, 168, 179, 180, 183, 184, 185, 186 pusio, 180 (=Chlamys) pusio, 180 ziczac, 184 Pectinaria koreni, 319, 320 Pectinidae, 168, 169, 178, 183, 186, 187, 191, 192, 195, 196, 197, 198 Pectinoidea, 165, 166, 178, 180, 185, 187, 188, 189, 190, 192, 193, 195, 196, 198 Pectunculus (=Glycymeris, Limopsis), 169 Penaeidea, 318, 320 Penaeus aztecus, 281, 318, 321 duorarum, 318, 321, 328, 329, 333, 335 esculentus, 270, 273, 281 indicus, 321 japonicus, 321 latisulcatus, 312, 318, 321 merguiensis, 318, 321 plebejus, 280, 321, 333 semisculatus, 281 setiferus, 321 Penitella penita, 115 Perciformes, 223, 323, 324, 325 Percoidei, 323, 325 Petrolisthes, 318, 320 Phacosoma japonicum, 110, 111, 117 Philobrya, 170, 173, 184, 185, 190, 191 munita, 171, 175, 180 Pholadoidea, 189 Pholadomyoidea, 189 Pholis gunnellus, 223 Photololigo, 125 Phrynorhombus norvegicus, 223 regius, 223 Phyllospadix iwatensis, 53 Pileolaria, 40, 76 berkeleyana, 16, 22, 32, 60, 76, 77 daijonesi, 16, 76

425

SYSTEMATIC INDEX

dakarensis, 16, 17, 76 lateralis, 16, 76 marginata, 16, 76 militaris, 16, 18, 20, 76 cf. militaris, 28, 76, 77 moerchi, 76, 77 pseudoclavus, 16, 76 pseudomilitaris, 76 rosepigmentata, 76, 77 sp. 1 (connexa), 16, 76 sp. 2 (invultuosa), 16, 76 spinifer, 16, 38, 76 tiarata, 16, 76 (Duplicaria) zibrowi, 76 (Jugaria) atlantica, 76 (Nidularia) nidica, 76 (Nidularia) palliata, 76 (P.) granulata, 76 (Simplicaria) pseudomilitaris Pileolariinae, 15, 31, 38, 40 Pillaiospira, 40 trifurcata, 14, 75, 76 Pinctada, 170, 184 Pinna, 135 nobilis, 131, 133, 134, 135 Pinnidae, 168 Pinnixa, 318, 320 Pinnoidea, 189 Pinnotheres, 318, 320, 332 Pinnotheridae, 320 Piscicola geometra, 253 Pista palmata, 240 Placopecten, 186 magellanicus, 104, 105, 110, 131, 136, 138, 145, 167, 194, 313 Placostegus tridentatus, 8, 10, 21, 63, 73 Platichthys flesus, 223 Platilimaria, 178 Plectroglyphidodon, 357, 380 dickii, 359, 360, 361 lacrymatus, 359, 360, 361, 362, 365, 368 leucozona, 359 Pleuronectes flesus, 325 platessa, 223, 315, 322, 323, 325, 339 Pleuronectidae, 223 Pleuronectiformes, 223, 323, 324, 325 Plicatula, 195 Plicatulidae, 195 Plicatuloidea, 189 Pocillopora, 377 Podon polyphemoides, 308

Pogonophora, 242 Pollachius pollachius, 223 Polychaeta, 7, 8, 238, 321 Polyrhabdina serpulae, 62 Polysiphonia, 371 Pomacentridae, 356, 357 Pomacentrus, 357, 358, 380 adelus 359, 362 amboinensis 363 bankanensis, 359, 360 chrysurus, 359 flavicauda, 359 grammorhynchus, 359 nagasakiensis, 363 prosopotaenia, 362 tripunctatus, 362 wardi, 359, 361, 362, 367, 373 Pomatoceros, 3, 7, 18, 24, 26, 31, 32, 58, 252 lamarckii, 2, 3, 4, 8, 35, 51, 58, 73 strigiceps, 73 terranovae, 10, 73 triqueter, 2, 3, 4, 7, 8, 10, 18, 19, 25, 26, 32, 35, 36, 44, 45, 46, 47, 48, 51, 54, 57, 58, 59, 60, 61, 62, 63, 70, 73 Pomatoleios, 26, 45 kraussii, 4, 10, 18, 20, 21, 22, 26, 32, 35, 36, 45, 47, 51, 52, 54, 56, 57, 61, 73 Pomatomus saltatrix, 275 Pomatostegus actinoceras, 11, 73 stellatus, 63, 73 Pontonema, 213 Porifera, 238 Porites ramosa, 52 Poromyoidea, 189 Portunus pelagicus, 285 Posidonia, 283, 285, 286, 287 australis, 272, 285, 290 oceanica, 133, 272, 273, 277, 285, 291 Praecardioidea, 189 Praexogyra hebridea, 136 Priapulida, 238 Proctoeces maculatus, 62 Propeamussium lucidum, 187 Prostoma obscurum, 253 Protobranchia, 171, 196 Protolaeospira, 39 Protolaeospira eximia, 7, 8 striata, 25 (Dextralia) stalagmia, 15, 17, 76 (P.) canina, 76 (P.) eximia, 15, 76

426

SYSTEMATIC INDEX

(P.) pedalis, 15, 76 (P.) striata, 15, 76 (P.) tricostalis, 15, 76 (P.) triflabellis, 15, 76 Protoleodora, 40 uschakovi, 16, 53, 76 Protula, 19, 26, 29, 31, 36, 43, 71, 73 globifera, 8, 11, 21, 72, 73 intestinum, 61, 63, 74 meilhaci, 74 palliata, 11, 36, 74 sp. 1, 11, 28 sp. 2, 11, 28 tubularia, 11, 26, 36, 43, 47, 61, 62, 63, 72, 74 Pseudanthessius gracilis, 62 Pseudochitinopoma occidentalis, 11, 17, 41, 51. 52, 57, 59, 60, 61, 68, 70, 71, 72, 74 Pseudodiaptomus forbesi, 308 hessei, 308 Pseudovermilia, 11 conchata, 41, 74 occidentalis, 43, 74 cf. occidentalis, 41 cf. pacifica, 41 Psychroteuthis glacialis, 128 Psygmobranchus protensus, 74 Pteria, 170, 184, 185, 191, 197 brevialata, 170, 171, 173, 193 Pteriidae, 172 Pterioida, 165, 170, 184, 185, 188, 193, 196, 197, 198 Pterioidea, 170, 172, 173, 185, 188, 189, 190, 192, 193 Pteriomorphia, 188 Ptychodera flava, 33 Pycnodonte, 135 Pygospio elegans, 253, 255 Pyramidellidae, 62 Raja brachyura, 223 clavata, 223 microocellata, 223 montagui, 223 naevus, 223 radiata, 223 undulata, 223 Rajidae, 223 Rajiformes, 223 Raniceps raninus, 223 Rapana bezoar, 186

Rhinonemus cimbrius, 223 Rhithropanopeus harrisii, 308, 309 Rhodomelaceae, 370 Rhodophyta, 370, 372 Rhodopsis pusilla, 4, 6, 11, 17, 19, 21, 28, 36, 41, 43, 72, 74 Rhodymeniaceae, 372 Rhodymeniales, 372 Rhombosolea tapirina, 281 Romanchella, 39 pustulata, 15, 17, 77 quadricostalis, 15, 77 scoresbyi, 15, 38, 77, 78 solea, 15, 77 Romanchellinae, 14, 31, 38, 39 Ruppia maritima, 275 Sabella, 252 pavonina, 253 Sabellaria alveolata, 26, 74 cementarium, 74 Sabellariidae, 65, 73, 74 Sabellidae, 64 Sabelliphilus, 62 Saccoglossus kowalevskii, 240 Sagartia elegans, 253 Salmacina, 3, 4, 5, 8, 11, 20, 25, 63 aedificatrix, 4, 74 amphidentata, 11, 74 dysteri, 4, 5, 6, 11, 17, 19, 21, 28, 29, 43, 47, 48, 62, 63, 74 dysteri var. tribranchiata, 74 incrustans, 4 setosa, 63, 74 tribranchiata, 11 Salmo salar, 323, 324, 336, 339 trutta, 324 Salmoniformes, 323, 324 Sarpa salpa Scaridae, 356 Scarus, 379 Sciaenops ocellata, 274 Sciaenops ocellatus, 270, 290, 325 Scoloplos armiger, 255 Scomber scombrus, 322, 323 Scombroidei, 323 Scophthalmidae, 223 Scophthalmus maximus, 223 rhombus, 223 Scorpaeniformes, 223 Scrobicularia plana, 104, 145

427

SYSTEMATIC INDEX

Scyliorhinidae, 223 Scyliorhinus canicula, 223, 323 stellaris, 223 Selenidium, 62 caulleryi, 62 Semimytilus algosus, 120 Semivermilia aff. uchidai, 11, 41, 74 Sepia, 132, 140 esculenta, 129 hierreda, 126 officinalis, 124, 125, 129, 134, 270, 277 subaculeata, 129 Sepiella maindroni, 129 Sepioteuthis lessoniana, 126, 127 Serpula, 11, 20, 24, 26, 54, 74 columbiana 11, 18, 21, 22, 26, 32, 35, 36, 38, 59, 60, 63, 74 concharum, 2, 74 contortuplicata, 74 hartmanae, 63, 74 uncinata, 74 uschakovi, 11, 74 vasifera, 43, 63, 74 vermicularis, 7, 8, 11, 21, 62, 63, 74 vermicularis granulosa, 240 Serpulidae, 1, 2, 3, 7, 9, 28, 59, 66, 72 Serpulinae, 2 Siganidae, 356 Sillaginodes punctata, 269, 270, 325 Simplaria, 40 potswaldi, 4, 5, 7, 8, 16, 22, 24, 25, 46, 47, 49, 50, 58, 77 pseudomilitaris, 16, 25, 76, 77 Sinocalanus doerrii, 308 Sinonovacula, 184 Siphonaria gigas, 121, 122 Sipunculida, 238 Solea lascaris, 223 solea, 223, 322, 323 Soleidae, 223 Solemyoidea, 171, 189 Solen, 168, 172, 181 ensis, 169 vagina, 167, 171 Solenoidea, 184, 189 Spartina alterniflora, 281 Sphacelaria 371 Sphaerechinus granularis, 270, 273 Sphaeropomatus miamiensis, 74 Spio, 252 setosa, 240

Spiochaetopterus oculatus, 240 Spionidae, 64 Spiraserpula, 6 snellii, 6, 74 Spirobranchus, 24, 26, 31, 33, 36, 45, 46, 57 corniculatus, 11, 18, 21, 24, 26, 33, 35, 45, 47, 52, 63, 74, 75 cruciger, 74 gardineri, 63, 74, 73 gaymardi, 74 giganteus, 11, 19, 22, 26, 34, 35, 36, 52, 59, 63, 74 giganteus corniculatus, 20, 22, 74, 75 giganteus giganteus, 74 giganteus incrassatus, 74 latiscapus, 62, 73, 75 polycerus, 4, 11, 18, 22, 26, 33, 34, 35, 36, 54, 59, 75 polycerus var. augeneri, 4 spinosus, 33, 47, 75 tetraceros, 12, 63, 75 tricornis, 75 Spirorbidae, 1, 2, 3, 7, 12, 21, 35, 38, 40, 59, 64, 66, 75 Spirorbinae, 2, 12, 31, 38, 39 Spirorbis, 28, 39 alveolatus, 76, 77 ambilateralis, 77 argutus, 77 bifurcatus, 12 borealis, 25, 44, 77 borealis var. tridentatus, 77 convexis, 77 corallinae, 8, 12, 22, 23, 46, 54, 57, 59, 77 corrugatus, 77 cuneatus, 12 granulata, 3 granulatus, 75, 77 infundibulum, 12, 17 inornatus, 12, 25, 44, 53, 77 cf. inornatus, 52 lamellosa, 77 malardi, 77 militaris, 77 moerchi, 77 nipponicus, 77 pagenstecheri, 77 pusill/a(us), 77 pusilloides, 78 rothlisbergi, 12, 22, 23, 58 rupestris, 12, 17, 22, 25, 36, 44, 52, 57, 58

428

SYSTEMATIC INDEX

scoresbyi, 78 spatulatus, 12 spirillum, 2, 75, 78 spirorbis, 4, 5, 7, 8, 12, 18, 20, 22, 23, 24, 25, 26, 29, 32, 33, 34, 35, 36, 38, 44, 46, 49, 52, 53, 54, 57, 58, 59, 60 strigatus, 13 tridentatus, 8, 13, 22, 25, 30, 36, 52, 54, 57 vitreus, 78 (Dexiospira) spirillum, 78 (Janua) pagenstecheri, 77 (Laeospira) borealis, 77 (Laeospira) moerchi, 77 (Paradexiospira) vitreus, 78 (S.) bifurcatus, 77 (S.) corallinae, 77 (S.) cuneatus, 77 (S.) infundibulum, 77 (S.) inornatus, 77 (S.) rothlisbergi, 77 (S.) rupestris, 77 (S.) spatulatus, 77 (S.) spirorbis, 77 (S.) strigatus, 77 (S.) tridentatus, 77 (Spirorbella) marioni, 77 (Velorbis) gesae, 12, 77 Spisula, 136, 172, 247 sachalinensis, 111, 131 solidissima, 107, 110, 114, 115, 131, 136, 138, 143, 167 subtruncata, 119 Spondylidae, 178, 195, 197 Spondyliosoma cantharus, 223, 270, 273 Spondylus, 192, 195 gaederopus, 179, 186 Squaliformes, 223, 323 Squalus acanthias, 223 Stegastes, 357, 358, 366 (Eupomacentrus) acapulcoensis, 359, 360, 362, 363, 377 apicalis, 359, 360, 361, 362, 363, 365, 367, 368, 371, 372, 373, 382 diencaeus, 359 dorsopunicans, 359, 360 fasciolatus, 359, 360, 361, 365, 368, 370, 371, 372, 374, 375, 376 fuscus, 359, 360, 362, 363, 369, 371 gascoynei, 359 leucostictus, 359, 360, 379 lividus, 359, 360, 371, 374, 375

mellis, 359 nigricans, 359, 360, 361, 362, 363, 365, 368 partitus, 359, 360, 371 planifrons, 358, 359, 360, 363, 364, 365, 371, 377, 380 rectifraenum, 359, 360, 363, 365, 366, 371 variabilis, 359 Strombus, 131, 137, 140 bubonius, 134 costatus, 122 gigas, 122 graciloir, 137 pugilis, 137 Strongylocentrotus droebachiensis, 133 polyacanthus, 61 Styela gibbsii, 38 Styliola, 131 subula, 139 Syngnathidae, 223 Syngnathiformes, 223 Syngnathus acus, 223 Syngnathus rostellatus, 223 Syphraena barracuda, 270 Syringodium filiforme, 212 Taenioma, 371 Tagelus plebeius, 240 Tanypodinae, 253 Tapes phillipinarum, 108, 116, 119 Taurulus bubalis, 223 Tellinoidea, 189 Terebella rubra, 240 Terebellides stroemi, 253, 255 Terebra areolata, 138 Tetraodontiformes, 223 Tetraselmis suecica, 37 Thalassia, 272, 274, 275, 290 testudinum, 53, 272, 274, 276, 286, 287 Thalassiosira pseudonana, 37 Theragra chalcogramma, 270 Thoumaleus rigidus, 63 Thyasira, 247, 252 (Parathyasira) equalis, 253 callistiformis, 132 Tiostrea, 143 edulis, 110 Tisbe, 213 Tivela stultorum, 109 Todarodes sagittatus, 127 Torpediniformes, 223

429

SYSTEMATIC INDEX

Torpedo marmorata, 223 nobiliana, 223 Trachinus draco, 223 Trachycardium procerum, 137, 145 Triakidae, 223 Trichoptera, 253 Trichotropis cancellata, 63 Tridacna, 138, 184, 191 maxima, 131, 138, 162 tevoroa, 182 Tridacnidae, 165, 167, 182, 185, 188, 193, 194, 196, 198 Tridacnoidea, 189, 190 Trigla lucerna, 223 Triglidae, 223 Trigloporus lastoviza, 223 Trigonia, 135 Trigonioidea, 189 Trisidos semitorta, 187 Trisopterus luscus, 223 minutus, 223 Turbo setosus, 121 Turritella, 131, 252 apicalis, 137 gladeensis, 137 Uca, 318, 320, 328, 332 tangeri, 318 Udotea, 371 Ulva, 282 lactuca, 282 lobata, 54

Unionoidea, 189 Upogebia pusilla, 318 Urophycis floridanus, 274 Vayssiereidae, 61 Veneroidea, 189 Venus, 172 mercenaria, 167 Vermiliopsis infundibulum, 75 infundibulum-glandigera complex, 12, 75 Vinearia, 40 zibrowii, 16, 76, 78 Xanthidae, 318, 320 Xenia, 61 Yoldia thraciaeformis, 111 Zeiformes, 223 Zeugopterus punctatus, 223 Zeus faber, 223 Zoarces viviparus, 223 Zostera, 53, 273, 278, 281, 282, 283, 285, 287, 288 asiatica, 53 capricorni, 272, 273, 280, 281, 282, 286, 290 marina, 53, 269, 271, 272, 273, 274, 275, 276, 278, 279, 280, 281, 282, 283, 284, 286, 287, 290 muelleri, 272, 273, 274, 282, 287

430

SUBJECT INDEX

References to complete articles are given in bold type; references to sections of articles are given in italics; references to pages are given in normal type. Accessory sense organ, 165, 174, 175, 177, 178, 181, 182, 183, 184, 190, 193, 198 Acetate peels, 107, 108, 109, 112, 117, 119 Adriatic, bivalves, 131 Alaska, isotope records in fossil molluscs, 135 Algal communities, and damselfishes, 374, 376, 380, 382, 383 Algal mats, 358, 360 Algal productivity, and damselfishes, 369–70, 372 Alpha diversity, 219 Anadromous fishes, 323, 324 Antarctica, isotope records in fossil molluscs, 135 Antipredation, in bivalves, 168, 195 Arctic Ocean, isotope records in fossil molluscs, 135 Arctic, metal pollution, 146 starfish, 220 Argentina, serpulimorph polychaetes, 51 Artificial seagrass units (ASU), 276, 278, 279, 291 Atlantic Ocean, seagrass beds, 272 starfish, 220 Australia, damselfishes, 359, 367, 372, 373 Australia, seagrass beds, 269, 270, 272, 276, 281, 285, 287, 288, 291 serpulimorph polychaetes, 51 Average phylogenetic diversity (AvPD), 212, 214, 215, 227 Average taxonomic distinctness (AvTD), 212, 213–18, 222, 224, 226, 227, 228, 229 Average taxonomic diversity, 214, 215 Bahamas, larval transport, 313 Baltic Sea, benthic functional groups, 234, 253, 254, 255 seagrass beds, 270 Barbados, serpulimorph polychaetes, 22 Bay of Morlaix, biodiversity, 216 Bed flows, 234, 235, 237, 248 Behaviour underlying tidal transport, 326–36

Belgian Front, bioturbation, 247 Benthic boundary layer, 236, 237, 238, 244, 250 Benthic communities on coral reefs, effects of damselfishes, 355–89 Benthic-pelagic coupling, 236, 242 Bermuda, isotope records in fossil molluscs, 135 Beta diversity, 220 Biodiversity, marine, practical measures of, 207–31 measures based on taxonomic distance between species, 210–29 application of taxonomic distinctness measures, 220–9 environmental impact assessment, 221–7 geographical biodiversity comparisons, 220–1 surrogates for biodiversity estimation, 227–9 taxonomic distinctiveness, 207, 210, 211–13 phylogenetic diversity, 212–13 root weight, 211–12 taxonomic distinctness, 207, 211, 213–20 average taxonomic distinctness, 213–18 taxonomic dissimilarity between samples/areas, 219–20 variation in taxonomic distinctness, 218–19 species diversity, as a measure of biodiversity, 208–10 Bioerosion, by damselfishes, 378 Bioturbation, role in marine benthic functional group ecology, 233–67 Bivalve eyes, evolution, 165–205 Blue-green algae, 370, 371 Brazil, damselfishes, 359, 368, 377 Brillouin’s H, 209 Brittany, seagrass beds, 281 serpulimorph polychaetes, 32, 51 Burglar alarms, light sensitive, 168, 185 movement sensitive, 196

431

SUBJECT INDEX

Caging experiments with damselfishes, 365, 366, 368 California current, 133 California, bivalves, 109 isotope records in fossil molluscs, 135 seagrass beds, 270, 276, 278, 280, 286, 288 serpulimorph polychaetes, 51 squid, 128 Canada, metal pollution, 145 Cape Cod, seagrass beds, 283 Cape Hatteras, benthic macrofauna, 261 Caribbean, damselfishes, 359, 361, 365, 377 Catadromous fishes, 322, 333 Cathodoluminescence, 107, 144 Cephalopod beaks, 124 Chesapeake Bay, seagrass beds, 269, 282, 283, 284, 290 Chile, bivalves, 120 seagrass beds, 272 Chukchi Sea, isotope records in gastropods, 133 Cladogram, 211 Clyde estuary, biodiversity, 216, 221 Complementarity, 211 Conservation, of biodiversity, 210 of seagrass beds, 292–3 Convention on Biological Diversity, 207 Conveyor belt feeders, 245, 246, 247, 257, 258 Coral, effects of damselfishes on, 377–8 Coupled behaviour circulation models, 313 Critical shear velocity, 235, 240 Cryptofauna, 378, 379 Cuttlebones, 129 Damselfishes and structure of coral reef benthic communities, 355–89 ecology and behaviour, 357–64 definition, 357–60 distribution and abundance, 360–3 effect on benthos, 363–4 farming, 364 intensity and selectivity, 363–4 effects on benthic algae, 365–77 biomass, 365–9 nitrogen fixation and fertilisation, productivity, 369–70 taxonomic composition, 370–3 test of herbivore effects on succession, 376–7 test of intermediate disturbance hypothesis, 373–6 effects on corals, 377–8

effects on mobile invertebrates and fishes, 378–9 establishment of territories, 382–3 large-scale effects, 381–2 validity of data, 380–1 validity of generalisation, 380 Deposit feeding, 241, 242, 246, 248, 249, 251, 256 Dissolved free amino acids, 55 Dogger Bank, tidal stream transport, 322 Dumping at Sea Act, 147 Ekman currents, 337 Ekofisk oilfield, 222 El Niño, 137, 145 Electrical fields, 335–6 Electron probe, 125 Elemental records in mollusc shells, 140–7 Endogenous rhythms, 327–30, 334 Energetics of tidal migration, 314 English Channel, fish assemblages, 222, 224 tidal migration, 314, 322 Environment change, molluscs as archives of, 103–64 Environmental impact assessment, 221–7 Estuaries, tidal transport in, 305, 306, 307, 308, 309, 310, 311, 312, 313, 314, 315, 319, 322–4, 324–5, 328, 330, 332, 334, 335, 336, 337, 339, 340 Evolution of eyes in the Bivalvia, 165–205 eye structure in Bivalvia, 169–84 branchial (cephalic) eyes, 169–71 pallial eyes, 171–84 Evolutionary history, 210 Exe estuary, biodiversity, 216 Eyeless homeobox gene, 166, 196, 197, 198 Eyes, evolution in bivalves, 165–205 marginal, 169 pallial, 166, 167, 168, 169, 185, 186, 188, 189, 190, 193, 196, 197, 198 cephalic, 265, 167, 169, 184, 187, 188, 189, 196, 197 compound, 165, 173, 174 Eyespots, 165, 168, 175, 178, 182, 185, 192, 194, 197 Fal estuary, pollution, 221 Falklands, bivalves, 118 Farming, by damselfishes, 355, 358, 360, 361, 363, 364, 366, 381

432

SUBJECT INDEX

Feeding guilds, 248, 251, 253 Firth of Clyde, benthos, 259 Fishing, effects on bivalve shells, 111 Florida, damselfishes, 371, 374 mollusc isotope profiles, 137 seagrass beds, 270, 272, 274, 276, 288 Foraging, in seagrass beds, 273–4 France, seagrass beds, 270, 273 serpulimorph polychaetes, 62 Friday Harbor, serpulimorph polychaetes, 32 Friesian Front, bioturbation, 247 Functional group ecology in soft-sediment marine benthos, role of bioturbation, 233–67 benthic habitat, 243–6 benthic habitat processes, 236–7 biological constraints in layered space, 237 functional traits in benthic organisms, 237–51 functional analysis of feeding behaviour, 238–51 adaptive behaviour, 248–9 biodeposition and resuspension, 249–50 lability of food taken, 241–2 motility and habitat utilisation, 242–4 other functions for characterising groups, 250–1 sedimentary bioturbation, 244–8 trophic group analysis, 238–41 future development of concept, 261–2 multifunctional groups, 251–6 relationship between bioturbation and benthic infaunal productivity, 259–61 utility of functional groups, 256–9 Galapagos Rift zone, molluscs, 132 Gamma diversity, 219 Geotaxis, 330, 331 German Bight, bioturbation, 247 Grand Banks, bivalves, 111 Grazing, by damselfishes, 358, 360 Great Barrier Reef, damselfishes, 361, 362, 363, 365, 366, 368, 371, 372, 374, 378 Guam, damselfishes, 371, 372, 374, 375 Gulf of Bothnia, benthic functional groups, 254 Gulf of California, damselfishes, 359, 365, 368, 371 Gulf of Carpentaria, seagrass beds, 270 Gulf of Finland, benthic functional groups, 254 Gulf of Guinea, isotope records in fossil molluscs, 134

Gulf of Maine, bivalves, 110 Gulf of Mexico, seagrass beds, 270, 274, 276 Gulf of Panama, damselfishes, 359, 363, 377 Gulf of Thailand, damselfishes, 371, 372 Habitats Directive, 207 Hawaii, damselfishes, 365, 371, 372, 374 Heron Island, damselfishes, 361 Humic acids, 327 Hydrostatic pressure, 331, 333–4, 337, 338 Hypoxia, 253, 254, 255, 256, 261 Indian Ocean, damselfishes, 359 Intermediate disturbance hypothesis, and damselfishes, 373–6 International Seagrass Workshop, 281 Irish Sea, benthic communities, 251 fish assemblages, 222, 224 Island biogeography, 221 Isle of Man, bivalves, 112 Isles of Scilly, biodiversity, 221, 227, 228 Isotopic records in molluscs, 130–2, 133–40 Jamaica, damselfishes, 371 Japan, bivalves, 111, 119 serpulimorph polychaetes, 4, 58 Kamchatka, serpulimorph polychaetes, 23 Kattegat, suspension feeders, 249 Larval release, 317 Larval supply, to seagrass beds, 277 Laser ablation inductively coupled plasma spectrometry, 141, 146 Life-history patterns in serpulimorph polychaetes, 1–101 asexual reproduction, 5–6 correlation of small size and brooding, 70–1 covariates of body size, 69–70 development, 26–33, 68–9 comparative morphology of feeding and non-feeding larvae, 31 factors affecting larval development, 31–3 food, 32–3 light, 33 other invertebrates, 33 pollutants, 33 salinity, 32 temperature, 32 of feeding larvae, 26–8 of non-feeding serpulid larvae, 28

433

SUBJECT INDEX

of non-feeding spirorbid larvae, 28–31 overview, 26 direction of evolution of life history traits, 71 fertilisation success, 68 gametes, 7–21 eggs, 18–21 factors affecting gamete maturation and fecundity, 17–18 fecundity, 8–17 gonads and other gamete-producing organs, 7 morphology and composition, 18–21 oogenesis and spermatogenesis, 7–8 production and development, 7 sperm, 21 importance of life-history research, 3 juvenile growth and maturation, 56–8 growth, 56–8 factors affecting juveniles, 57–8 ontogenetic changes, 57 seasonal changes, 57 maturation, 58 larval ecology and behaviour, 33–8 larval defences, 37–8 larval feeding, 36–7 bacterivory, 37 distribution in the group, 36 mechanism, 36–7 preferred food, 37 rates, 37 larval swimming, 33–5 behaviour, 33–4 effect of salinity, 35 effect of temperature, 35 mechanism, 34 velocity, 34 photoresponse, 35–6 correlates of, 36 variability, 35–6 length of metamorphic competence stage and delay of metamorphosis, 44 longevity, 59 mortality, 59–64 age specific, 59–60 mortality factors, 60–4 competition, 61 parasites, 61–4 predators, 60–1 parental care of eggs and young, 38–44 serpulid brooding methods, 41–4

erroneous records, 43–4 in gelatinous masses, 43 in pockets of the thoracic membranes, 43 in tube ovicells, 41 inside the branchial crown, 43 tube brooding, 41 spirorbid brooding methods, 38–40 opercular brooding, 40 tube brooding, 39–40 phylogenetic position and taxonomic problems, 2–3 planktonic lecithotrophy, 65–8 settlement and metamorphosis, 44–56 chemical nature of conspecific inducers, 55–6 artificial induction or inhibition of settlement, 55–6 signalling pathways in metamorphosis, 56 factors affecting settlement and metamorphosis, 50–5 generic precondition settlement factors, 51–2 specific settlement factors, 52–5 morphological changes at metamorphosis, 47–50 in planktotrophic larvae, 47 of lecithotrophic larvae, 47–50 settlement behaviour, 45–7 of lecithotrophic larvae, 46–7 of planktotrophic larve, 45–6 sexuality patterns, 3–5 gonochorism and sequential hermaphroditism, 3–4 simultaneous hermaphroditism, 4–5 spawning and fertilisation, 21–6 environmental physical factors, 23 factors affecting spawning, 23–4 fertilisation, ecology of, 24–6 cytological aspects, 25–6 external, 24 in brooding species, 24–5 self-fertilisation, 25 frequency of spawning and length of breeding season, 22–3 morphological changes accompanying spawning, 21–2 spawning synchronisation, 23–4 trends in egg size and larval feeding modes, 64–5

434

SUBJECT INDEX

Limfjord, benthic communities, 238 seagrass beds, 279 Linnean classification, 211 Liverpool Bay, pollution, 222 Lunar cycles, 325–6 Margalef’s index, 208, 209 Maryland, bivalves, 110 Massachusetts, seagrass beds, 273, 280 Mediterranean, isotope records in bivalves, 133 isotope records in fossil molluscs, 134 seagrass beds, 270, 272, 291 serpulimorph polychaetes, 2, 8, 51, 62 Menai Straits, serpulimorph polychaetes, 8 Mesozoic Marine Revolution, 194 Metal pollution, 145–7 Molluscs as archives of environmental change, 103–64 elemental records in mollusc shells, 140–7 bivalves, 141–3 bivalves, strontium thermometry, 142–3 cephalopods, 143–4 combined isotope and elemental analyses, 144 metal pollution analysis, 145–7 upwelling, 144–5 future research goals, 147–9 isotope records and their use as records of environmental change, 133–40 ontogenetic changes, bivalves, 138–9 ontogenetic changes, cephalopods, 140 ontogenetic changes, gastropods, 139–40 temperature reconstruction, fossil molluscs, 134–6 temperature reconstruction, living molluscs, 133–4 thermocline development, 136–8 water depth estimations and upwelling, 130–2 isotopic records in molluscs, 130–2 general principles, 130 growth line studies, 131 radioisotopes, 132 sample preparation, 130 shell records, 130–1 surface rings and internal shell growth patterns, bivalves, 104–19 applications of the patterns, 113–15 disturbance rings, 105 disturbances to shell growth, 111 growth lines, 106–11 growth ridges and spines, 105–6

growth rings, 104–5 microgrowth patterns, air temperatures, 118 daily and tidal, 115–16 seasonal, 117–18 spring neap cycles, 120 tidal regime, 118–20 other effects, 111–13 surface rings and internal shell growth patterns, cephalopods, 123–30 beaks, 124 cuttlebones, 129 gladii, 128–9 growth patterns, 125–6 growth zones, 126–7 ontogenetic changes, 128 population studies, 127–8 spring neap cycles, 127 statoliths, 124–5 the Nautilus shell, 129 surface rings and internal shell growth patterns, gastropods, 121–3 growth rings, lines and ridges, 121–2 statoliths, 122–3 Monitoring, of biodiversity, 211 Natural selection, 166, 167, 168, 169, 194, 195, 197, 198 Negative feedback systems, 330, 331 Netherlands, seagrass beds, 284 New England, bivalves, 111 New Jersey, seagrass beds, 284 New South Wales seagrass beds, 272, 285, 286 New Zealand, metal pollution, 145 serpulimorph polychaetes, 51 seagrass beds, 272 Newfoundland, seagrass beds, 270, 280, 282 Nigeria, serpulimorph polychaetes, 58 Nitrogen fixation, by damselfishes, 370 North Atlantic, molluscs, 132 North Carolina, seagrass beds, 270, 281, 283 North Carolina Shelf, polychaete feeding, 241 North Pacific, upwelling, 242 North Sea, biodiversity, 210 bioturbation, 241, 246, 247 bivalves, 112, 114 fish assemblages, 220, 222 isotope records in fossil molluscs, 135 metal pollution, 147, 148 mollusc isotope profiles, 137 serpulimorph polychaetes, 57 tidal stream transport, 314, 315, 322

435

SUBJECT INDEX

North Wales, bivalves, 118, 119, 120 Northeast Atlantic, fish assemblages, 223 Northumberland, serpulimorph polychaetes, 23 Norway, bivalves, 118 serpulimorph polychaetes, 23 Norwegian Sea, 241 Nova Scotia, isotope records in bivalves, 133 Numerical models of tidal stream transport, 312–15 Optic nerve, bivalves, 170, 171, 176, 177, 178, 180, 181, 182, 183 Oregon, bivalves, 118 Organically polluted habitats, 213 Orkney Islands, bivalves, 112 Orthogenesis, 166, 195 Oslofjord, serpulimorph polychaetes, 8 Pacific Ocean, seagrass beds, 272 Pallial sense organs, 172 Panama, mollusc isotope profiles, 137 Papua New Guinea, damselfishes, 363, 365, 368 Persian Gulf, isotope records in gastropods, 133 Peru, mollusc isotope profiles, 137 Photoresponses, in polychaetes, 35–6 Photosymbionts, in molluscs, 138, 139 Phototaxis, 330, 331 Phylogeny of Bivalvia, 189 Pielou’s J’, 208, 209 Pigment cups, 165 Predator-prey relations, in seagrass beds, 275, 276 Puerto Rico, damselfishes, 370, 374 Puget Sound, serpulimorph polychaetes, 22 Queensland, seagrass beds, 280 Radioisotopes, for aging molluscs, 132 Residual currents, 306, 307, 309 Retention in estuaries, 307 Retinae, in bivalves, 166, 176, 177, 180, 181, 182, 183, 186, 187, 195, 196, 197, 198 Rheotaxis, 334–5 Ria de Arosa, isotope records in cephalopods, 134 Ross Sea, bivalves, 194 Sargasso Sea, tidal stream transport, 314, 322 Seagrass beds, importance for fishery species, 269–303

importance of scale, 283–91 spatial scales of variability, 283–7 temporal scales of variability, 288–91 limitations of sampling methodologies, 291–2 permanent residents, 271–3 recommendations for conservation, 292–3 relative value of seagrass to fishery species, 281–3 seagrass detritus as basis of coastal fisheries food chain, 280–1 temporary residents, 273–80 foraging, 273–4 larval supply, 277 larval transport, 277 nursery role, 276–80 post-settlement processes, 279–80 pre-settlement processes, 277–9 refuge from predation, 275–6 settlement, 278 spawning grounds, 277 Sediment Profile Imaging (SPI), 259, 262 Sedimentation, 249, 252, 261 Selective tidal stream transport of marine animals, 305–53 field studies, 315–25 detection and analysis, 315–17 ebb-tide transport of invertebrates, 317–19 estuaries—adult fishes, 322–4 estuaries and bays—fish larvae and postlarvae, 324–5 flood-tide transport of invertebrates, 319–22 offshore areas—adult fishes, 322 models for the blue crab, 336–9 numerical models, 312–15 coupled behaviour-circulation, 313–14 migration energetics, 315 vertical migration in tidal currents, 312–13 semi-lunar/lunar cycles, 325–6 tides and tidal currents, 306–12 underlying behaviour, 326–36 currents, 334–6 electric fields, 335–6 rheotaxis, 334–5 turbulence, 335 endogenous rhythms, 327–30 hydrostatic pressure, 333–4 olfactory cues, 322 responses to environmental cues, 330–6 salinity, 332–3 temperature, 334

436

SUBJECT INDEX

Semilunar cycles, 325–6 Settlement processes, seagrass beds, 277–80 Shadow-off reflex, 165, 167, 170, 185, 196, 198 Shannon’s H’, 208, 209 Sibling species, 213 Simpson’s index, 208, 209, 214 Skaggerak, benthic community structure, 259 benthic functional groups, 254 bioturbation, 247 Soft-sediment benthos, functional group ecology, 233–67 Southampton Water, bivalves, 114 Spain, serpulimorph polychaetes, 51 Stable carbon isotope analysis, 274, 280 Statolith, 147 bivalves, 122 cephalopod, 124, 125, 126, 127 Storms, effects on bivalve shells, 111, 112, 115 Striae, in bivalves, 105, 106 Strontium thermometry, 142–3 Suspension feeding, 239, 241, 248, 249, 251, 252 Swimming, in bivalves, 166, 168, 179, 184, 186, 187, 192, 194, 195, 196, 198 in polychaete larvae, 33–5 Tasmania, seagrass beds, 272 Taxonomic distinctiveness, 207, 210, 211–13 Taxonomic distinctness, 207, 211, 213–20 Territories, of damselfishes, 355, 356, 358, 363–4, 365, 366, 367, 368, 369, 370, 371, 372, 373–7, 378, 379, 380, 381, 382, 383

Texas Gulf, larval transport, 313 Texas, seagrass beds, 270, 281, 284, 290 Thermocline development, 136 Tides and tidal currents, 306–12 Tides, effect on bivalve growth, 115, 116, 118, 119, 120 Trophic Group Amensalism, 244 Trophic groups, in benthos, 233, 238–41, 242, 244, 253, 255, 257, 259 Turbulence, 335, 338–9 Ultrasonic tracking, 332 Upwelling, 144–5 Velocity shear field, 312 Vertical migration, 306, 308, 309, 310, 312, 313, 316, 329, 333, 337, 340 Virginia, bivalves, 110, 131 Wales, metal pollution, 146 Washington, seagrass beds, 270 Weddell Sea, starfish, 220 Weeding, by damselfishes, 355, 357, 364, 369, 372, 375, 381 Western Australia, larval transport, 312 Woods Hole, serpulimorph polychaetes, 58, 62 Yap, damselfishes, 371, 372, 374, 375 Zooxanthellae, 165, 167, 182, 188, 190, 192, 194, 197

437