Advances in Ecological Research, Volume 3

Advances in

ECOLOGICAL RESEARCH VOLUME 3

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Advances in

ECOLOGICAL RESEARCH Edited by

J. B. CRAGG The Nature Conservancy, Merlwood Research Station, Grange-over-Sands, Lancashire, England

VQLUME 3

1966

ACADEAIIC PRESS London and New York

ACADEMIC PREYS INC. (LONDON) LTD. BERKELEY SQUARE HOUSE LONDON, W.l

U.S. Edition publishod by ACADEMIC PRESS INC. 1 1 1 F i m AVENUE,NEW YORK10003, N E W YORK

Copyright @ 1966 by Academic Press Inr. (London) Ltd.

All rights reserved NO PART OF THIS BOOK MAY BE REPRODUCED IN A N Y FORM BY PHOTOSTAT, MICROFILM OR A N Y OTHER MEANS, WITHOUT WRITTEN PERMISSION FROM T H E PUBLISHERS

Library of Congress Catalog Card Number: 62-21479

Printed in Great Britain by W. S. Cowell Ltd, at the Butter Market, Ipswich

Contri1)utors to Volume 3 MANFRED D. ENGELMANN, Department of Natural Science, Michigan State University, East Lansing, Michigan, U.S.A. €1. KLOMP, Department of Zoology, Agricultural University, Wageningen, Netherlands. J. E. G. RAYMONT, Depurtment of Oceanography, University of Southampton, England.

T. B. REYNOLDSON, Department of Zoology, University College of North Wales, Bangor, Caerns., Wales.

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Preface At the 1965 meeting of the British Association for the Advancement of Science Sir Peter Medawer said, in talking about the state of embryology: “There is no theory of development . . . there has therefore been little sense of progression or timeliness about embryological research. Of many papers delivered at embryology meetings . . . one too often feels that they might have been delivered five years before or deferred for five years without making anyone conscious of great loss.” Replace the word “embryology” by “ecology” and that statement expresses what many regard as a major problem in ecological science; how much of modern and riot so modern ecological literature helps to advance the subject. It is our hope that the special topics selected for review in this series will make a positive contribution to the development of ecology. As far as possible subjects and authors are selected to highlight important problems or fields of research, or to bring to bear on ecology the methods and outlooks of other sciences. Whilst it is important that ecologists strive to develop an adequate theoretical basis for their subject, the need for reliable quantitative information collected with a view to testing hypotheses or theories cannot be overstressed. In this number, the contributions of Dr. Reynoldson and Dr. Klomp demonstrate the type of painstaking and long-term studies which are necessary to provide the solid basis for a proper understanding of population ecology. The two other contributions are concerned with production studies which are of special significance in view of the emphasis which is being given to productivity investigations in the International Biological Programme. Dr. Engelmann has produced a stimulating review of certain aspects of ecosystem dynamics ‘in which he particularly stresses the need for constructing models which can be used as a basis for logical predictions. Professor Raymont has brought together an abundant amount of information on production studies of marine plankton. Much of what he has to say has a bearing on possible developments in other branches of ecology, because the subtle chemical factors which influence the grow-th and succession of plankton will have their counterparts in the interactions of microflora and fauna in terrestrial systems. vii

...

Vlll

PREFACE

It is important in the present state of ecological development that adequate attention is paid to methods. These should be described in a form sufficiently detailed to allow a reader to make an adequate judgement about their reliability. It is hoped that the attention to practical detail which is given in all four contributions, will be of value t o advanced students who are faced with the problem of designing certain types of research programmes. December, 1965 J. B. b ~ a a

Contents CONTRIBUTORSTO VOLUME 3 PREFACE -

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V

vii

The Distribution and Abundance of Lake-Dwelling Triclads - towards a Hypothesis

T. B. REYNOLDSON I. Introduction 11. The Taxonomy of the Triclads 111. The Pattern of Distribution and Abundance A. Introduction and Field Methods B. Results IV. Historical Aspects of Distributiqn and Abundance V. Determinants of Distribution and Abundance A. Weather B. A Place to Live C. Food D. Organisms of the Same Species E. Organisms of Different Species VI. The Explanation of Distribution and Abundance A. The Total Triclad Population B. The Individual Species VII. Conclusions and Summary Acknowledgments References -

1 4 6 6 12 20 28 29 30 34 40 43 63 63 66 62 63 64

Energetics, Terrestrial Field Studies, and Animal Productivity

MANFREDD. ENCIELMANN

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I. Introduction 11. Three Approaches to Energetics Studies 111. Historical Considerations IV. Physiological Studies which Yield Energetics Information V. Studies Concerned Primarily with Maintenance Metabolism of Populations in the Environment VI. Studies which Ernphaaize the Trophic Scheme Analysis of Communities A. Trophic Dynamic Analysis of the Salt Marsh Ecotone B. Trophic Dynamic Analysis of “Old Field” Communities C. Trophic StudiesinaSavttnnahCommunity

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ix

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73 74 78 84 87 96 96 98

103

CONTENTS

X

VII. Projection References -

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108 112

The Production of Marine Plankton

J. E. G. RAYMONT I. Introduction 11. Phytoplankton Production - . A. Methods of Estimating Primary Production B. Factors Affecting Primary Production C. Production - Temperature and Stratification 111. The Standing Crop of Phytoplankton IV. Phytoplankton Crop and Annual Production V. Grazing by Zooplankton - - VI. Zooplankton - A. Methods for Estimating the Standing Crop of Zooplankton B. Regional Crop Assessments of Zooplankton C. Rate of Zooplankton Production D. The Feeding of Zooplankton E. Alternative Food Sources for Zooplankton F. Zooplankton - Quantitative Food Requirements VII. Conclusion . References -

117 120 120 126 147 155 157 160 168 168 170 178 182 186 188 189 191

The Dynamics of a Field Population of the Pine Looper, Buplus piniarius L. (Lep., Geom.)

H. KLOMP I. Introduction A. The Area of Investigation B. The Lifecycle of the Pine Looper C. The Pine Looper as an Object for Population Studies 11. Methods of Meaauring Density A. Density of Eggs and Larvae B. Density of Nymphs C. Density of Pupae D. Density of Moths E. The Dispersion of Nymphs, Pupae, and Moths III. Annual Routine Rearings A. Rearingof Eggs B. Rearing of Larvae - C. RearingofPupae - D. RearingofMoths IV. Annual Variations of the Reproductive Rate A. The Variability of Fecundity Within One Generation B. The Variability of Fecundity Between Generations V. The Composition of Life Tables -

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207 208 209 211 211 211 220 223 229 233 233 234 237 240 240 240 242 268 267

xi

OONTENTS

VI. The Analysis of the Causes of Fluctuation A. The Pattern of Fluctuation B. Key-factor Analysis VII. The Analysis of the Causes of Regulat,ion A. The Incidence of Regulation B. Density Dependent Fecundity C. Density Dependent Mortality D. Delayed Density Dependent Mortality VIII. Final Considerations Acknowledgments References

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273 273 275 286 286 288 289 294 299 303 303

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307

SUBJECTINDEX

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The Distribution and Abundance of Lake-Dwelling Triclads - towards a Hypothesis T. B . R E Y N O L D S O N

Department of Zoology, University College of North Wales, Bangor, Ca,erns., Wales I. Introduction.. . . . . . . . . . ................. 1 11. The Taxonomy of the Triclads.. ........................................ 4 111. The Pattern of Distribution and Abundance.. ............................ 6 A. Introduction and Field Methods.. .... ............................. 6 B. Results ........................................................... 12 IV. Historical Aspects of Distribution and Abundance.. ....................... 20 V. Determinants of Distribution and Abundance.. ........................... 28 A. Weather . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29 B. A Place to Live. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30 C. Food ........................................... . . . . . . . . . . . . . 34 D. Organisms of the Same Species.. ..................................... 40 E. Organisms of Different Species.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43 V I . The Explanation of Distribution and Abundance - a Hypothr5is. . . . . . . . . . . 63 A. The Total Triclad Population.. . . . . . . . . . . . . . . . . . . . . 63 B. The Individual Species.. ............................................ 56 VII. Conclusions and Summary.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62 Acknowledgments .......................................................... 63 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I. INTRODUCTION One of the main objectives of the ecologist is the study of factors underlying the distribution and abundance of animals. These factors are numerous, often subtle in operation and interact in complex ways so that in practice research is usually restricted to include only those which experience or a priori reasoning suggests may be important. Many inconclusive studies may stem from examples in which the wrong factors have been selected for study. There is much to be said for tackling such projects with resources of manpower equivalent to those which have been successfully employed in t,he study of the spruce-budworm (Morris, 1963) but it remains important to avoid stifling the initiative and ideas of the individual worker (Lund, 1!)64). Andrewqrtha and Birch (1954) provided a great stimulus in this field of ecology and interest has been maintained in recent texts by Odum (1953) and Macfadyen (1963). But 1

2

T. B . REYNOLDSON

one of the main conclusions to be drawn from these works is the paucity of examples in which causative factors of distribution and abundance have been satisfactorily demonstrated. The majority of important studies relating to freshwater habitats such as those of Jewel1 (1935) on sponges, Edmondson (1944) on rotifere, Boycott (1936) and Macan (1950) on molluscs, Macan (1938, 1954) on corixids, Hynes (1954) on (Jammarus, Bennike (1943) and Mann (1966) on leeches and Williams (1962a, b) on Asellus are concerned mainly with descriptive aapects of distribution and although in many cases a pattern related to some basic feature of the environment has been demonstrated, how it operates remains to be determined. Although Williams’ preliminary studies (1963) on Asellus are a notable exception, there has been little testing of hypotheses by experimentation either in the laboratory or the field. The recent critical treatment of freshwater studies by Macan (1963) has made this starkly clear. It is this situation which has evoked the pleas of Varley (1967) and Cragg (1961) for more use of the field experiment, and McFadden (1963) has gone so far as to doubt the value of field work without it. The fist stage of the work on lake-dwelling triclads has been largely confined to the usual study of the distribution in the field of four main species and an attempt to fit the results into the framework o€ the physico-chemical properties of lakes as a beginning. This was based on the examination of more than two hundred separate habitats in several lakeland areas of northern Britain, Ireland and the western islands (Fig. 1); limited work has also been done in Fennoscania. S h e any pattern of distribution usually bears the stamp of historical events to some variable degree, this aspect has also been considered. I n fact, these triclads show in relation to water chemistry a well-marked pattern which is modified by their dispersal history. As the second stage in the programme, hypotheses based on correlations obtained from field data have been tested by field and laboratory experiments as part of an analysis t o determine the major factors involved. The planning of this stage has been adapted from Andrewartha and Birch’s (1964,1960) concept of environmental components as modified by Andrewartha and Browning (1961) and further amended to apply to freshwater habitats. Thus the influence of water chemistry (especially calcium) and temperature on life-cycles have been studied and tolerances determined. Food which is proving to be a key factor, has been considered in some detail and attention has also been given to predators, while competition especially between the different triclad species themselves and at the intra-specific level, has been investigated. Distribution and abundance have three main parameters, space, numbers and time. Detailed studies of the population biology of the four

LAKE DWELLING TRIULADS

SHETLAND 1s. .FAIR

*@ORKNEY

3

Is. IS.

FIQ.1. The arena in black a m thoae in which the main work haa been done: stippled ~ s ~ e p l thoee for whioh samples or reports have been provided by other workere. Ielands mentioned in the text are ale0 shown.

common species with emphasis on numerical aspects, have provided information on the mechanism of population regulation which is very . relevant t o the main objective of this work. From these various approaohes it has been possible t o f m u l a t e a hypothesis to account for the distribution and abuhdance of lakedwelling triclads in Britain, and this seems a suitable point at which to report progress. The adequacy of the hypothesis cannot finally be judged until the third stage of this programme, the testing of the hypothesis by laboratory and field experiments, has been completed.

T. B. REYNOLDSON

4

11. THE TAXONOMY OF THE TRICLADS The four species of triclad mainly involved in this work are Polycelis nigra (Miill.), P . tenuis Ijima, Dugesia lugubris (0. Schmidt) and Dendromelum lacteum (Miill.) (Fig. 2 ) . Phagocata vitta (Dug&) is also reported in the field work and although it has a characteristic distribution no further work on it has been done in Britain, but Gislh (1946) and Dahm (1949) have studied it in Sweden. Bdelloce.phala punctata (Pallas), Planaria torva (Mull.) and Dugesia tigrinu (Girard) have been recorded also but from too few lakes to provide any substantial clues to the factors concerned in their distribution. Crenobia alpina (Dana) and Polycelis felina (Dalyell)more typically stream species, have also been recorded from lakes in Scotland and while this^ was probably related to temperature in some way (Reynoldson, 1953),no further work on this aspect has as yet been attempted. There has been confusion over the taxonomic defhitions and identification of several of these species but the position has been greatly clarified during the last five years. Originally, Polycelis nigra and P . tenuis were confused but gradually from the work of Komarek (1927), Lender (1936), Lepori (1950, 1955), Reynoldson (‘1948, 1958a), Lender andMoigne (1960),Moigne(1962),Melander(1963),andBenazzi (1963a), these two species can now be recognized easily by penis structure.

Pp

.9m

Po&cefis nigra

Polycelis fenuis

Dugesia lugubris

Dendrocoelum /acfeum

Pbogocofo ViffO

FIQ.2. The five lake species of triclad; vertical linen show the relative, average size of adults.

L-4KE DWELLING TRICLADS

5

Benazzi (loc. cit.) has reported that they are able to interbreed in the laboratory but this is not our experience with British material. There can be no doubt that they are good species on morphological, cytological and ecological grounds. I n the numerous habitats where they occur together the populations remain distinct even to their epizoic fauna (Reynoldson, 1956a); M. Benazzi (private communication) has recently agreed to this view of the situation in nature. Melander et al. (1954) reported a new species Polycelis hepta closely related to P . tenuis but differing from it in the absence of adenodactyls* and in possessing a haploid chromosome number of 7 compared with 6 in P . tenuis. However, the recent work of Lender and Moigne (1960), Moigne (1962), and Benazzi (1963a), has shown conclusively that interbreeding takes place and the occurrence of adenodactyls is not related strictly to chromosome number. Therefore, P . hepta can no longer be regarded as a good species. How the ecology of the different karyotypes varies is not known. Confusion has also been rife over distinctions between Dugesia lugubris and Dug. polychroa (0. Schmidt). Funaioli (1951) on the basis of morphological examination concluded that they were the same species, with lugubris as the correct specific name. However, the extensive work of Benazzi (e.g. 1957) and his school has shown the complexity of the situation by recording several karyotypes in this species-complex and he recommended (1963b) that the distinction in Schmidt’s sense (1860) should not be retained. Dendrocoelum lacteurn has been a less controversial species and identification is straightforward. Undoubtedly there are several karyotypes in some of these species, but Dend. lacteum has been recorded only in the diploid condition (Dahm, 1961). Polycelis nigra occurs mainly in the diploid condition with 2n = 16 (Melander et al., 1954; Moigne, 1962),but Benazzi (1963a) has also recorded a triploid variety. Polycelis tenuis is more complex, possessing two haploid chromosome numbers of 6 and 7 with triploids built onto both (Lepori, 1955;Moigne, 1962;Benazzi, 1963a).Asummary of the karyotypes in Dugesia lugubris is given in Benazzi (1959) and this species seems the most complex of the Planariidae considered here. All the British material of this species which has been examined except one population from N. Ireland belongs to either Biotype B or C of Benazzi, a triplo-hexaploid (Magagnini, 1961; M.-Benazzi, private communication). The polyploid races of these three species generally reproduce by pseudogamic development of the oocytes, i.e. sperm from another individual is necessary to stimulate development of the egg but no fusion of chromosomes occurs. * Pear-shaped glandular structures opening into the genital atrium.

6

T. B . REYNOLDSON

This complex situation in the Planariidae raises problems in ecological work as was appreciated by Dahm (1958) who was dealing with stream-dwelling species which show similar conditions. Obviously, it is too laborious to examine the cytology of every individual or even a part of every sample. Nevertheless, it is likely that different karyotypes will show some contrast in their ecology as already demonstrated by Dahm (1955) for Dugesia tigrina and by Mirolli (1961) for Dug. Zugubris in Lake Maggiore. The latter concluded that the triploid races of this species were likely to replace the diploid as seems to have happened in P. tenuis (Melander, 1963). This is a problem common in ecological work and further complicated by the fact that the genetic complex of populations is changing all the time a t varying rates depending upon the species and the habitat. The only practical approach with our present meagre knowledge of triclad ecology is to ignore intra-specific differences for the time being until the main outlines of the ecology of the species themselves are known. Anomalies which have already appeared in distribution and may well stem from contrasts of this kind, can be examined more profitably a t a later date. The life-cycles of these four species are similar in outline and reproduction is only of the sexual or pseudo-sexual type. Although asexual reproduction by fission has been reported for some races of P. nigra this has not been observed in British populations to any marked degree. The young which hatch from cocoons attached to the substratum are some 2 to 4 mm long and replicas of the adult, except of course in their immaturity. The breeding seasons of these species overlap but each has a characteristic peak period, and the effect of temperature upon the life-cycles differs to a variable degree according to species (Reynoldson et aZ., 1965; Table V).

111. THEPATTERN O F DISTRIBUTION A N D ABUNDANCE A.

INTRODUCTION A N D FTELD METHODS

This facet of triclad ecology can be treated at several levels. Distribution among the various habitats to be found in most lakes is one approach which has been studied to some extent. A second is to compare triclad populations in lakes of varying type without regard to specific habitat, while a third method would be to study lakes of contrasted productivity and restrict the observations to one type of shore. Since the complexity of factors was likely to be formidable in any case, the last approach which reduced some of them, seemed most appropriate. Although lakes may be classified in different ways, one of the most fundamental is that based on the type of rock in the drainage area. Hard rocks give rise to chemically poor water and lakes of low

PL.~TE 1 . (a) Stoiiy shore typical of those used to obtain data on triclad distribution and abundaiire. (b) An upland unproductive lake (LIyn Idwal. ralciurn 1.5 iiig/litre) in t,he Siiowdonia area of Nort,h Wales whirh did not support a trirlud population. ((b) and ( r ) reproduced with permission of the Commit,tee for Aerial Pliot,ography, University of Cambridge.) [to face pl-ge 6

PLATE1. (c) Productive lakes (foreground Lake Feneinere. calcium 93 Ing/litre) in Shropshire supporting H. large and varied triclad population.

L A K E DWELLING TRICLADS

7

productivity, soft rocks to chemically rich water and lakes of high productivity (Mackereth, 1957) (Plate 1, b, c). This broad relationship is modified by other factors such as shape, depth, aspect (Gorham, 1958), and often by human activities which always complicate interpretation of field work. The preliminary work showed that all the triclad species required resting sites providing shade. They were also most numerous in shallow water, scarce or absent when the edge of the lake was undercut and leading directly into deep water. Sandy shores were unfavourable, probably due to abrasion. The basic requirements are best met either by a shore with semi-emergent vegetation such as Yellow Flag (Iris pseudacorus, Linn.), Potamogeton or Water Lily (Nymphaea sp.) etc. which would normally be found growing on a soft substratum or by a stony shore. While the presence of vegetation usually means a sheltered habitat, a stony shore may be either exposed or sheltered to a varying degree. Exposure is unsuitable for lake-dwelling triclads because of the danger of crushing by shifting of the substratum under wave action (Beauchamp, 1932); their food supply is limited in a similar way. The effect of shelter and exposure upon these triclads was shown clearly in a! large lake such as Windermere where an exposed stony shore yielded only single specimens of two species, while a sheltered stony shore harboured the four main species in large numbers. I n some small lakes the effects of exposure can be very apparent. For example, in Shaw Lough (County Armagh, N. Ireland) triclads were absent from the stony shore exposed to the prevailing wind, whilst a sheltered shore with stones yielded a population of 282 collected per hour comprising three species (Reynoldson, 1968a). Such examples could be multiplied. In deciding between a shore of emergent vegetation and a stony shore for routine sampling, the most important criterion was amenability to quantitative sampling, but availability of shores was also important. Stony shores of comparable type are characteristic of oligotrophic lakes and are to be found in about half of the eutrophic lakes, the opposite is roughly true of plant dominated shores. In amenability to sampling, stony shores are superior. The species composition and the concentration of plants vary and the vegetation cannot be so easily searched, features which complicate any standard sampling technique; also such shores are usually less accessible. For these reasons a moderately sheltered, stony shore was preferred as the standard type for routine sampling (Plate la). Before finally deciding on a stony shore the habitat had to be tested to see whether it would bias the data in favour of a particular species. During the preliminary field work both types of shore were sampled in a number of lakes. The results showed that none of the four species

8

T. B. REYNOLDSON

had any preference for either type; a single leaf, stem or stone was often found carrying the four species. These initial observations have been supported by all later sampling and the results of surveys made by other workers, e.g. Berg (1938). Mirolli’s data (1961) for the distribution of Polycelis nigra, Dugesia lugubris and Dendrocoelurn lacteum in Lake Maggiore have been analysed from this aspect. His main variations in conditions were between exposure and shelter, between muddy, sandy and stony substrata. He found triclads in general most abundant on relatively sheltered, stony shores. When the distribution of the various species was analysed by a x2 test incorporating Yates’ correction it was found that this differed very significantly from random (P < 0.001); all three species tended either to occur together or to be absent. A major contribution to the value of x was derived from one cell where the expected number of negative values was low, but those actually observed were fairly high. However, if the contribution from this cell is omitted, x2 still had a significant value (P < 0.01 >0.001). Such a result supports the observation that when these species of triclad are present in a lake they occupy the same habitat. In this sort of approach the larger the number and the greater the variety of lakes it is possible to include, the better is the chance of detecting pattern. This prohibited using a boat and meant restricting the sampling to shallow, littoral zones which could be reached from the shore. Actually, our experience suggests that shallow water up to a depth of about 1 f t (30-5 cm) is the optimal zone for all these species, especially on sheltered, stony shores. In exposed places they may be concentrated in deeper water. These triclads follow changes in water level quickly (Beauchamp, 1932; Taylor and Reynoldson, 1962), and I have observed both species of Polycelis on stones overlying grass several metres from the original level within 12 h of flooding. They do extend into deeper water as shown by Berg (1938) but not into the sub-littoral (Humphries, 1936; W. J. P. Smyly, private communication). Although the data for stony shores reveal that the four species occur at approximately the same depth and zonation is not pronounced, Chodorowski (1959, 1960) studying vertical distribution in a lake with a mud or sand substratum and a rich flora found some evidence of zonation related t o plant type. In selecting lakes for quantitative sampling, size is important for several reasons as Gorham (1958) has shown. Large water bodies such as Windermere and Loch Lomond not only provide more varied habitats than smaller lakes because of changes in soil type along the shore with accompanying changes in the flora, but there is also greater variation in severity of wave action and other factors. It is also more difficult to select the most appropriate shore without a lengthy search.

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L A K E DWELLING TRICLADS

For these several reasons data from large lakes are not included in the routine samples. In practice, the upper size limit of lakes for sampling was taken as approximately 640 acres (259 hect.) and large ponds were taken as the lower limit; Table I gives size data for most of the places included in the quaiit>itativesampling. Even in small ponds the abundance and species composition of the triclad fauna are not restricted as, for example, appears to be so for molluscs and leeches (see Macan, 1963). Thus all four were often found in abundance in ponds only a few m2 in area. But the shorter duration of small ponds may mean less opportunity for triclads to reach them and such faunas may have a greater element of chance in their composition than those of larger places. Lakes in use as reservoirs were avoided because of rapid changes in water level which can affect the whole fauna (Hynes, 1961). Recent, artificial water bodies were also disregarded although a few may not have been recognized as such and inadvertently included. T A B L EI The Range of Some Physical and Chemical Features Indicated by a Sample of 100 Lakes Included in the ~Yurve~y Acres

Size Hectares

Altitude lakes

~~~

<4

244

10-34 35-69 70-145 > 145

4-13 14-27 28-59 >59

33 -3 19.8 9 -4 13.5

Calcium concentration &: lakes mg/litre ~~

<2.5 2-6-5.0 5.1-10.0 10*1-20.0 20.1-40.0 >40-0

-

21.4 18.4 17.3 13.3 17.3 12.3

Metres

yo lakes

0-76 77-152 153-228 229-305 306457 458-610

42.4 26.8 17.1 7.1 4 -0 3.0

~~

< 10

-__

Feet 0-250 251-500 501-750 751-1000 1001-1500 1 501-2 000

Total Dissolved Matter mg/litre yo lakes

-.

&50 51-100 101-150 151-200 201-250 > 250

21.3 24.0 24.0 16.0 8 -0 6.7

In planning field work and selecting lakes for sampling, attention was paid not only to lake size and history but also to situation vis it vis soil type and altitude, to provide n range from low to high productivity (Plate 1 , b, c); accessibility wits also a practical consideration. The ideal collecting site was one in which the shore was reasonably sheltered, sloped gradually and had a substratum ofstones about 6 in (15 cm) diameter

10

T. B. REYNOLDSON

(Plate la). It is clear that no two lakes are identical in all these qualities and it was necessary to depart from this ideal to some extent otherwise too few lakes would have been available. However, if a moderately sheltered shore and shallow water less than 1 ft (30.5 cm) deep were absent or the stones were all very small ( <3 in, G7.5 cm), or very large ( 2 8 in, 2 2 0 cm), the lake was omitted from the quantitative work. Such lakes left out for these reasons were included in qualitative sampling if otherwise they provided a suitable habitat for triclads. The sampling method had to be simple, not requiring any previous visit or any complex bulky apparatus, applicable to limited variation in size of stone and able to provide an adequate number of triclads. After experimenting with various methods including trays, baiting and timed hand collections, the last was found to be most reliable. It enabled a wide area of shore to be examined which helped to even out local concentrations of triclads. The time of collecting could also be adjusted to population size so providing 50-100 specimens for analysis. A basically similar method has been used successfully in other investigations, e.g. by Macan (1950) for molluscs and by Mann (1955) for leeches. When triclads were scarce, collecting was continued up to a maximum of 1 hour and if none were found they were recorded as absent. For comparative purposes the data were converted into number collected per hour. Since much practice in this sort of collecting had been experienced prior to routine sampling, it is unlikely that the data were influenced by an improving rate of collecting-a common danger. However, the method suffered from some drawbacks. For example, as the actual population increases, relatively more time is spent transferring triclads from stone to jar. This is akin to the artificial predatorprey situation analysed by Rolling (1959) and a similar relationship was found between the real population and the number collected per hour, as Holling found between predation rate and prey number (Reynoldson, 1958a, Table 2). The divergence between an estimated triclad population and the real one became large when the collecting rate exceeded 400 per hour. However, the majority of the populations (90%) were below this value, most considerably below, so that the error from this source is not extensive. Other drawbacks arise from the fact that usually only one sample was taken from each lake thus no confidence limits can be calculated. Reproducibility was tested by taking three sets of samples from each of eight lakes in Anglesey during spring, summer and winter and examining rank correlation. It might be added that this was a stringent test since, apart from one lake of low calcium and total mineral content, the rest had fairly high values in the range where experience had indicated already that there would be no marked effect on the triclad population. The spring and summer samples showed a rank

L A K E DWELLING T R I C L A D S

11

correlation positively significant at the P = 0-02 level. The correlation between winter and eit,her spring or summer was l ~ s i t i v ebut not significant. The species composition of each triclad fauna was identical in each season. Lakes in Snowdonia have also been sampled several times and given comparable estimates of population size and the species composition has always been the same. A further potential drawback with a single sample is possible variation in the size of the population over the year. This was minimized by restricting routine sampling to the summer months and in any case seemed to be an unlikely source of large error because study of the population dynamics of the planariid species (Reynoldson, 1980, 1961a; Taylor and Reynoldson, 1962) has shown that annual changes from births and deaths were around 50%; they were larger in Dendrocoelum lacteum however, up to 500%. This argument was supported by the data from Anglesey lakes which showed only small variation in amplitude from season to season. It seems reasonable to conclude that this simple method of estimating populatioii size and species composition in triclads was adequate for the purpose of examining trends in distribution and abundance. Clearly, it is insufficiently sensitive to compare individual lakes, especially those close together on the chemical spectrum and it has not been used for this purpose. During the search for triclads, other organisms found on the stones were noted or collected for identification. Samples of water for chemical analysis were taken at the same site lts the triclad sample. Again, only single samples were taken and what has been said about the reliability of the triclad method applies here but there is no doubt that the chemical samples have a narrower range of variability as the Anglesey data showed (Reynoldson, 1958a). It has also been possible to compare our measurements of various ions with those of other workers (e.g. Gorham, 1957, on the Shropshire meres) and there was reasonable agreement. Further, the data of Tucker (1958) and Olsen (1955)indicated that the range of values over a season would not substantially alter the ranking of lakes within a season. Of the several analyses, calcium and total dissolved matter have been most illuminating. I n considering anomalies it has sometimes been useful to look a t other chemical features such as for example, magnesium, chloride, oxygen uptake from permanganate. An indication of the range in chemical qualities of the lakes is given in Table I. Under favourable conditions five or six lakes could be sampled in one day and still leave time for examination of material in the evening; triclads were generally identi6ed on the day of collection. Dugesia lugubris, Dendrocoelumlacteum and Phagocuta vitta are identifiable by eye or lens, but with Polycelis species the large specimens had to be squashed and

12

T . B . REYNOLDSON

the penis examined under the microscope to separate tenuis and nigra. Sma.11 specimens of Polycelis were allocated to species according to colour pattern. Of t'he numerous P. nigra populations which have been collected only one has been found in which the colour was sufficiently mottled to confuse with P. tenuis and this lived in brackish conditions near Cullercoats, Northumberland. Mostly P. tenuis are mottled though several uniformly black populations, indistinguishable from P. nigra externally, occur in the more northerly parts of Britain.

B.

RESULTS

The data from areas showing a restricted triclad fauna have been omitted from immediate consideration since they could be misleading in both the qualitative and quantitative contexts. Thus the proportion of lakes occupied by a particular species would be affected and any competitive element absent or reduced. In addition, size differences in the adults would influence quantitative relations. The three main areas sampled with such a restricted fauna were the islands of Anglesey off the Welsh coast, Islay off the west Scottish coast, and the extreme north of Scotland beyond the Highland Fault (Caledonian Canal) (Fig. 1). The results from the lakes in these three areas and from the two large lakes of Windermere and Lomond are used to illustrate special aspects (pp. 27, 30).

1. The Distribution of the Species Data from 107 lakes considered here are derived mainly from midand north Scotland (34),N. Ireland (19), the Snowdonia area of N. Wales (29), Shropshire (12), the Lake District (11) and two Y'orkshire lakes. They show a wide range of physico-chemical properties from high lakes in Snowdonia to lowland lakes, from those with hardly a trace of calcium to those with large amounts (Plate l , b, c). The distribution of these lakes based on calcium content of the water is shown below: Calcium mg/litre

No. of lakes ~~

G2.5 2.51- 5.0 5.1 -10.0 10.1 -20.0 >20.0

33 12 20 1.2 30

In analysing the triclad data special attention was given to calcium because of the many studies of the distribution of other organisms in relation to this ion (see Macan, 1963). Total dissolved matter could have

13

L A K E DWELLING TRICLADS

been used equally well, and from some aspects is more suitable. Figure 3 presents species distribution in relation t o the amount of calcium present in the water and a distinctive pattern emerges. There were some 12% of the lakes without triclads, and all had a calcium content less than 5.0 mg/litre and most were less than 2 - 5 mg. Of the five species, Phugocatu vitta had the most striking distribution since i t was confined to lakes with less than 2.5 mg/litre of calcium and occurred in only 26% of these. One characteristic feature of lakes supporting this species was that they were usually fringed with wet areas containing Sphagnum. Indeed, Ph. vitta is almost terrestrial, in the sense that it occurred in large numbers in wet peaty soil and did not require the presence of surface water (H. B. N. Hynes, private communication; GislBn, 1946). The factors underlying the distribution of Ph. vitta in lakes have yet to be studied, but Dahm (1949) has discussed lotic habitats of this species. The distribution of Polycelis nigru contrasts with that of Phqocata. It was the most widespread of the five species in relation to calcium concentration, occurring in lakes with as little as 0.6 mg/ to those with over 100 mg/ litre. The distribution of Polycelis tenuis was similar to that of P. nigra except that i t did not extend into such calcium-poor waters. The lowest 0.25

0.50

I

Phogocata vitta

i

I Ill

Po/uce/is nigro

rh'

I.00 I

2.50 I

5.00 I

I Ill I l l 1IlI

10.0 I

20.0 I

100.0

50.0 I

I RI I II I 1I II I 1I rlllolrlllll~lllllIIlllln1A11111 I I

II

I

I1

I i I I I i~ IIIIIIIiIIIlIi II II IIIIII IIIIII II 1111

Po/uce/is fenuis

I II Ill II I I111111llI I I 11111

Dugesia /ugubris

Dendrocoelurn lacteum 0.25

I 0.59

1

1-00

I 2.50

I

I II I1 u I I 1I11UI 11111 I 11111 I

I

5.00 10.0 20.0 Calcium mg / litre - logarithmic scale

I 50.0

J

100.0

Fro. 3. The distribution of triclads in relat,ion to calcium. hach v e r t i c a l l i n e represents one lake; broken lines indicate the occurrence of Polycelia tenuia in lakes where P . n@ra was not found.

14

T. B. REYNOLDSON

limit recorded was 1.6 mg/litre whilst only 5% of total occurrences were below 5 mgllitre compared with 22% for P. nigra. The distributions of Dugesia lugubris and Dendrocoelum lacteum were so similar that they can be considered together. Both species were absent from lakes low in calcium. Only a single occurrence was found below 5 mg/litre, at 4.8 mg/ in Newton Mere, Shropshire, and this may be exaggerated since Gorham (1957) recorded 7.4 mg/litre. Eighty per cent of the records were from lakes with more than 10 mg/litre; comparable figures for P. nigra and P. tenuis were 30% and 40% respectively. When the distribution of these triclads was examined separately in the four main areas they showed the same pattern except that each presented a less complete picture (Reynoldson, 1958b). For example, most of the Snowdonia lakes fell into the range with a calcium value less than 5 mg/litre while the Shropshire meres lay a t the upper end of the range. Table I1 presents the data in summary form from a slightly different approach, showing the proportion of lakes occupied by the various species in particular calcium ranges. Polycelis nigra is seen to occupy a gradually increasing proportion of lakes reaching a peak of 94% in the calcium range 5-1-10.0 mg/litre but above this its incidence declines and it occurs in only 72% of the lakes in which calcium exceeds 20 mg. In contrast, P. tenuis although starting off at a lower level of incidence continues to increase until in the richest lakes it is universally present. Dugesia lugubris and Dendrocoelum lacteum both tend to occur in a higher proportion of lakes as the calcium increases but their maximal incidence is about 70%, i.e. neither is quite so well dispersed as the Polycelis species, even in the most favourable lakes. TABLEI1 Percentage Distribution of Triclads in Relation to Ca,lciunz Concentration of Water Calcium mg/litre

Species Absent Phagocata vitta Polycelis nigra Polycelis tenuis Dugeaia lugubris Dendrocoelum lacteum Total lakes

<2.5 26% 26% 44% 6% 0%

0%

33

2.6-5.0 36 %

5*1-10.0

64% 27% 9% 9% 12

94% 82% 29% 24% 20

0%

0% 0Y O

10.1-20.0

0% 0%

82% 91% 36% 36% 12

>20.0 0 0% 72%

looyo 69 % 66% 30

Total lakes 13 9 68 58 30 28 107

Calcium has been selected as a convenient framework within which to describe the distribution of these triclads, but an equally convincing pattern also emerges in relation t o ttotal dissolved matter.

LAKE DWELLING TRICLADS

15

2. The Abundance of l’riclads A stricter selection of lakes was necessary to maintain comparability of collecting sites. This reduced the original number of 107 to 68 of which 22 were located in Mid-Scotland, 6 in N. Scotland extending to the Highland Fault, 18 from N. Ireland, 16 from Snowdonia and 6 from Shropshire. The samples measured the standing crop of triclads, and since the Total Dissolved Matter (abbreviated later to T.D.M.) is a more reliable indication of productivity (Larkin and Northcote, 1958; Rawson, 1960) than calcium, this parameter has also been related to triclad abundance. Data for T.D.M. were available for only 44 of the 68 lakes which were about equally divided between Mid-Scotland, N. Wales and N. Ireland. The ranges of the physico-chemical properties of the lakes used here were similar to those already outlined in considering distribution. i. The Total Population. Scatter diagrams in which total numbers of triclads collected per hour are related to calcium and T.D.M. are shown in Fig. 4 and 5. The regression coefficients measuring both relationships are highly significant (P < 0-OOl),nevertheless it is apparent that these chemical factors only account for a part of the variance (especiallywith calcium) and other factors apart from sampling errors, are important. This is not surprising in view of the complex of factors involved. These may be regarded as operating at three levels, basic physico-chemical factors, primary production and secondary production, all of which can be expected to influence organisms like triclads which are at or near the apex of a food chain. While T.D.M. will be usually closely related to productivity of the littoral zone there may be exceptions since as Margalef (1958) pointed out, it is phosphate and nitrate which normally determine primary productivity and these form only a small part of T.D.M. There is also some evidence that very dystrophic conditions are related to low triclad populations independently of calcium and T.D.M. Consideration of some of the more striking exceptions to the trends shown in Fig. 4 and 5 indicates some of the contributory factors. For example, there is a group of lakes at the lower calcium and T.D.M. levels which either do not support a triclad population at all or only R relatively small one. These are mainly lakes at the higher altitudes, nnd clearly such adverse factors as low winter and spring temperature and a short summer are reinforcing the effect of low productivity. Newton Mere (Fig. 4 ~ is) also exceptional not only in supporting a relatively high populat,ion but also in containing Dugesia lugubris and Dendrocoelum lacteum although the calcium content is only 5 mg/litre. This lake, on slightly higher ground than the others, was surrounded by good agricultural land with a thin belt of deciduous trees along one

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T. B . R E Y N O L D S O N D

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FIQ.5. The relationship between the total triclad population 4nd the Total Dissolved Matter content (TDM) of the water; the regression line is also shown. Unfilled circles refer to lakes >500 f t ( > 152 m) above sea-level. E, Loch Camilla; F, Loch Kinghorn; other letters as in Fig. 4. Location of lakes shown in Fig. 2, Reynoldson (1958a).

LAKE DWELLING TRICLADS

17

margin, but the calcium content was surprisingly low compared with surrounding nearby lakes, e.g. The Mere, Ellesmere with 32 mg/litre calcium. Gorham (1957) who recorded 7 - 4 mg/litre of calcium suggested geological and hydrological reasons for tthe low mineral content of this lake. It is probable that plant and animal material from the terrestrial zone increases the productivity of the littoral zone so that it is higher than would be judged on water chemistry alone. Lakes Lurgan, Marlacoo, and Lowry (Fig. 4, B, c, D ) all in N. Ireland also support an exceptionally high population; indeed the Irish lakes nearly all tend to have a high population relative to the other areas especially Scotland, suggesting that it is perhaps unrealistic t o group them together (Reynoldson, 1958a). However, even within the Irish area, these three lakes have higher than average numbers of triclads, especially measured against calcium. The first, of these was undoubtedly enriched by organic waste from the township of Lurgan, while the other two had farm buildings near the shore from which nutrient-rich water drained into the lakes without noticeably increasing calcium or T.D.M. ;increased productivity from such sources is well known (Hasler, 1947; Mundie, 1957; Berg, 1958). The reasons for exceptionally low populations at high calcium and T.D.M. levels are not obvicus, but the two most striking examples (Fig. 5, E, F) are both in the Scottish area surrounded by land which was noL intensively farmed. When the main areas are considered separately in the present context they all show highly significant relationships between the standing crop of triclads and calcium, T.D.M. and altitude (Table 111). There is of course an obvious reason for the relationship with altitude since high ground usually means hard and insoluble rocks (Mackereth, 1957). This is made clear in Table I I I b where the regression coefficients between T.D.M. and altitude are shown to be negative and highly significant except for the N. Wales area. The latter result is explained by the circumstance that most of the lakes a t lower altitudes occur in narrow valleys flanked by high ground and have a resultant low T.D.M. It will be difficult to separate the influence of two such intimately connected factors as altitude and water chemistry upon the distribution and abundance of triclads, but the results from the low-lying lakes of Islay showed that calcium and T.D.M. per se can be related to triclad abundance (Reynoldson, 1958a). The adverse effect of altitude in the presence of high calcium was indicated by the relatively small triclad population restricted to P . nigra, found in Malham tarn (W. Yorks) at 1 2 5 0 f t (381 m) with 48.8 mg/litre calcium. ii. The Populations of the Individual Species. 117 analysing the changes in population size of the individual species, the 68 lakes have been grouped into categories based on calcium content and the population of

TABLEI11 (a) Regression Coeficients for the Relationship between Triclads, Calciwn, Total Dissolved Mutter, und Altitude Scotland

Reg. coeff. S.E. of R.C. Probability

AltiCa T.D.M. tude 10.00 1.090 -2.240 2.25 0.189 0.256 <0*001 <0*001 <0*005 >0*001

N. Ireland

Ca

7.78 2.93 <0*01 >0*005

AltiT.D.M. tude 3.400 -9.30 0.554 1-22 <0-001 <0.001

N. Wales

Ca

17.90 4.29 <0*005 >0*001

T.D.M.

2.051 0.626 <0.01 >Om006

Total Altitude 0.709 0.244 <0-02 >0*01

Ca 5.82 1.03 <0*001

(b) The Relationship between Altitude and Total Dissolved Matter ~~

Reg. coeff. S.E. of R.C. Probability

Scotland

N. Ireland

N. Wales

- 1-140

-2.552 0.293

-0.162 0.105 >0*1

0.365

<0-01

>0*002

<0*001

T.D.M. 1.881 0-272

<0*001

L A K E D W E L L I N G TRICLADS

If)

FIG.6. The average abundance of the individual triclad species and the total population related to the calcium content of the water. Dotted lines represent samples for a single lake.

each species averaged. Figure 6 shows the arithmetic means (examination of the data on a logarithmic basis showed no important difference) and indicates that in lakes with less than 5 mg calcium/litre Polycelis nigra was the most abundant species, P. tenuis was able to maintain a foothold with small populations in a few lakes (cp. Fig. 3) whilst Dugesia and Dendrocoelum were absent with the exception of the unusual Newton Mere”in Shropshire. Above 5 mg calcium/litre, there was a dramatic change in the distribution of the Polycelis species. Instead of following the general trend of increase in population, P. nigra was overtaken and substantially passed by P. tenuis which showed a fourfold increase. Dugesia and Dendrocoelum were able to maintain small populations in this range. With calcium between 10 and 20 mg the total population increased markedly mainly because of larger numbers of P. tenuis, although the other species contributed, especially Dugesia and Dendrocoelum. F’rom 20 mg/litre upward P. nigra showed a decline in numbers which was paralleled by the occupation of a smaller proportion of lakes (Table 11),whilst the other species increased both in numbers and the

20

T. B . R E Y N O L D S O N

proportion of lakes occupied. To summarize, a t low calcium levels Poly celis nigrrr m:iint:iined the highest population, whilst ; I t intermediate levels and higher, I‘. ten& was nndoubtedly the dominant species numcrically. 1)icyesirr lirguhris and 1)endroco~lumlacteuru only formed a numerically important component when calcium exceeded 20 mg/litre. This analysis is based upon numbers, but as adult Dugesia and Dendm coelum arc several times larger than adult Polycelis, in terms of biomass the former two species would form a larger part of the total population and together would sl)proximately equal the biomass of the Polycelis species in the highest calcium lakes. Also, whilst the total number of triclads reached a maximum a t 20-40 mg/litre of calcium, in terms of biomass a continuing upwtird trend would be shown throughout the entire range (Fig. 6 ) . iii. Conclusions and Summary. It has been showu that the standing crop of triclads became larger as the calcium and T.D.M. concentrations of lakes increased. I n lakes with calcium concentrations of 20 mg/litre and upwards, all four species regularly coexisted, but as the concentration declined below 20 mg, Dugesia lugubris and Dendrocoelum lacteum occurred in fewer lakes and in smaller numbers; below 5 mg they were usually absent. Polycelis tenuis was the most abundant species from the highest range down t o 5 mg/litre of calcium and persisted in a few lakes below 2 - 5 mg/litre. At 5 mg/!itre and lower, P. nigra was numerically the dominant species. An explanation of this natural pattern is the main purpose of this account. The pattern differs from that of many other organisms in showing the co-existence of several species a t one end of the series, whilst as the other end is approached, all the species are gradually eliminated. Most other natural distributions within a restricted habitat, whether of vertebrates or invertebrates, terrestrial or aquatic, usually depict only one of these situations (Andrewartha and Birch, 1954; Hutchinson, 1961; Macan, 1963).

I V . HISTORICAL ASPECTSO F DISTRIBUTION A N D ABUNDANCE I n considering the factors which underlie any pattern of distribution, it is necessary to ask the question, how far it reflects opport’unity for dispersal and how far it is the outcome of interaction among the physico-chemical and biotic factors of the environment,. This is especially pertinent for lake faunas where habitats tend t o be more isolated and temporary than most others so that dispersal may be relatively more important. Talling (1951) with reference t o ponds, reached the general conclusion that physical barriers “do not modify Nature’s habitual abhorrence of the ecological vacuum”. His view is similar t o that

LAKE

n WE LLI N G

TR I C L A D S

21

expressed earlier by Gurney (1916), Boycott (1936), Macan and Worthmgton (1951) and latterly reiterated by Macan (1963). However, the point must also be made that the rate of dispersal of any species will be characteristic of and determined by its particular ecology. All are agreed that species may be absent from a suitable habitat simply through chance. Moon (1957) has suggested that chance has played the most important part in the distribution of Asellus in the north of England but his argument has been refuted (Reynoldson, 1961b; Williams, 1962a). Another aspect which must be considered is that a species or a group of species may be extending their range and any discernible pattern may be only a temporary phase determined largely by historical rather than ecological events. In a sense, this is true of all organisms if the time scale is of geological dimension, but here we are considering a lesser scale, which can be termed “ecological” time. Some evidence of what is happening in lnke-dwelling triclads can be obtained by comparing the faunas of the western islands and the extreme north of Scotland with those of the mainland of Britain and of Ireland. I n producing what may be regarded as a typical fauna, the data for those areas known to contain all four species have been lumped together (i.e. the faunas of lakes bhown in Fig. 3). Obviously, in any comparison of this averaged fauna with that of another area, the proportion of lakes in the various categories based on water chemistry will influence the data, as seen from Table 11. To overcome this, lakes have been d:vided into two groups, those with G7.5 mg/litre of calcium, which might be expected to support mostly Polycelis species, and those with > 7.5 mg/litre calcium which might be expected to support the four species. Table I V compares the percentage occurrence of the triclad species in a typical fauna and the combined data for the similar faunas of Anglesey off the North Wales coast and Islay off the west Scottish coast. Also shown are corresponding data for an area north of the Highland Fault. I n the island lakes with <7-5 mg/litre calcium it is apparent that Polycelis tenuis is under-represented; the apparent over-representation of P. nigra is due to the fewer low-calcium, high-altitude lakes in these islands. This trend of scarcity of P. tenuis is made abundantly clear in lakes with >7.5 mg/ litre calcium. Dugesia and Dendrocoelum are also under-represented in the higher calcium lakes of Anglesey and Islay, being altogether absent in the former and represented by a single specimen found in Loch Finlaggin on Islay. This scarcity of species other than P. nigra was amply confirmed from the examination of lakes and ponds on other, smaller western islands. For example, in a total of seventeen lentic habitats containing triclads on Skokholm, Bardsey, Isle of Man and Lismore (Fig. l),most with 2 1 0 mg/litre calcium, all records referred to P.nigra. When details of the six lakes, two on Anglesey, four on Islay, which B

22

T. I3. R E T N O L D S O N

TABLEI V d Tgp'icul Y v i c l d E'uicnu C'onipwr~dwith thosc of Auglcsey plus Isla?/,and Scotlad lVorlh of the Fwult (CaledoniarL Canal) Lakes with > 7.5 mg/litre calcium Typical Anglesey & Islay N. Scotland

Species

_ _ _ ~ - ~

Absent Polycelis rcigra Polycelis tenuis Dugesia lugubris Dendrocoelum Euctrii ?ti Total lakes -

Absent Polycelis nigra Polycelie tenuis Dugesia lugubrie Dendrocoelum lacteum Total lakes

24Yo 56% 2OYO

21% 79% 0Y O

4Yo

0% 0Y O

7%

54 _

50 Yo 10%

40YO 0% 0% 10

14

Lakes with > 7 *5mgjlitre calcium

_

0% 74% 94% 52 %

52 % 50

_

~ 0 YO

~

87 % 26% 0Y O

75 % 0 YO 25 % 0%

23

12

4%

0%

supported P.tenuis are examined, we find that they are all well-known trout-fishing lakes which have been stocked from time to time with mainland trout. The four Islay lakes have not only been stocked frequently (Reynoldson, 1958a) but also they lie close together, within a radius of 2 miles. The data for the extreme north of Scotland give an entirely different result. Here, in lakes with G7.5 mg/litre calcium the outstanding feature is the large proportion of lakes which did not contain triclads, and this was even more pronounced in the calcium-richer lakes where 75% lacked a population. It might be emphasized at this point that the same criteria for lake selection were used here as already described (p. 8). The other equally striking feature of these northern lakes is that in the small proportion (seven lakes) which did contain triclads, P . tenuis was the species recorded, a reversal of the situation on the western islands. As noted for the islands, several of the lakes containing P . tenuis are noted trout-fishing places, e.g. L. Heilin (Caithness); L. Hempriggs (Caithness); L. Ussie (Ross and Cromarty); and furthermore the other four are grouped closely around L. Garve (Ross and Cromarty). This evidence for the scarcity of triclads from the extreme north of Britain was supported by data from islands of corresponding latitude. For example, lake-dwelling species were scarce on Rhum, where one lake had a small population of P.nigra and another a population of P.tenui8. None were

LAKE DWELLING TRICLADS

23

found on N. Uist and Harris (R. C. Connolly, private communication); none in several lakes of the more northerly Shetlands (A. Milne, private communication). It seems unlikely that all these lakes were so unproductive that they were unable to support P. nigra a t least. Although details of water chemistry are available for only a few, several had calcium values exceeding 10 mg/litre. Any hypothesis advanced to explain the present-day distribution of triclads must be consistent with the following facts. First, the scarcity of triclads in the extreme north shows that these organisms have not yet occupied to anything like the full extent, the suitable habitats available, and are presumably still extending their range northwards. This is a similar situation to that found for several other common freshwater species, as shown for Gammarus pulex (Reid, 1951; Hynes, 1954); for Asellus species (Williams, 1962b); for gastropods (Hunter, 1957) and for a fresh-water mite (Efford, 1962). Second, it must explain the similarity of the British mainland fauna and that of Ireland; finally, it must account for the restriction of the more southerly western islands to virtually one lake species. Before detailed arguments are attempted, it is necessary to consider the mode of dispersal in triclads. Ullyott (1936) has denied the role of natural transport such as birds, although Thienemann (1950)reported some examples of this and also inferred from the distributions of Crenobia alpina and Pulycelis felina that birds may hare aided dispersal. Arguments for and against birds were also presented by Klie (1926)and Arndt (1924)respectively. The recent studies of Maguire (1963)on dispersal do not offer much support for transport of organisms like triclads by other animals. It appears that the balance of evidence, especially the clear-cut patterns discussed above, is against birds being an important factor in dispersal although they may have been responsible for some introductions (p. 24). It would appear that triclads mainly achieve dispersal by their own activities (Gislbn, 1946; Dahm, 1949); although the latter attributed some importance to passive transport. The most significant feature of the geographical distribution of lakedwelling triclads in the British Isles is the similarity of the Irish and mainland faunas, and also the fact that eight of the nine species comprising the entire British fauna are found also in Ireland (Southern, 1936; Reynoldson, 1958a). Bdellocephala punctata is the only absentee. The origin of the Irish fauna, especially the Lusitanian element, has been critically reviewed by Corbet recently (1962) who discussed three main theories to account for it: (a) survival in southern Ireland during the last glacial phase or from an earlier time, (b) post-glacial migration to Ireland via land connections, (c) introduction by man’s trading activities.

24

T. B. REYNOLDSON

Of these (b) is the least likely on present-day evidence of the extent, duration, condition and position of land bridges between Ireland and the mainland. Corbet favoured (c) to account for the Lusitanian fauna. Water for drinking purposes must have been transported often and in quantity by travellers, and triclads, especially the spring-dwelling species, may have been spread to some extent in this way. Fish stocking has undoubtedly contributed also in recent times and probably earlier. Bilge water of ships may be concerned in the dispersal of some aquatic animals (Williams, 1962b)but is unlikely to have been of importance for such delicate organisms as triclads. However, the widespread distribution and large number of species in Ireland argues forcibly against introduction in these accidental ways particularly in view of their slow dispersal on the mainland and the rarity of several species here, although i t is appreciated that they may not always have been ra.re. An important argument against this method of introduction is the fact that both P. nigra and P. felina have not succeeded in reaching Sweden, although both occur nearby on the mainland of Denmark and in Germany (Thienemann, 1950): the commerce across this narrow sea must have always been very heavy. This hypothesis also fails to account for the restricted fauna of Anglesey which lies on one of the trade routes between the mainland and Ireland. Anglesey also furnishes a very convincing demonstration of the ineffectiveness of birds in spreading triclads, since the island is separated from the mainland, where all four species occur, by a strip of seawater only some 300-400 m wide, a separation which has existed since early post-glacial times (Greenly, 1919). Only two lake species, P. nigra which is widespread and P. tenuis found in two lakes, have succeeded in crossing the narrow barrier; the former probably by its own movements before separation, the latter via troutstocking. Furthermore, if this type of introduction is important, Dugesia gonocephala should have been able to cross the Channel and establish itself in Brit,ain, since as Ullyott (1936) pointed out, the climatic and ecological setting i s similar on both sides. But this species has not been confirmed in Britain (Dahm, 1955; Reynoldson, 1956~).I n contrast it might be mentioned that Dugesia tigrina (Girard) has succeeded in establishing itself in some half-dozen places at least in Britain, probably as the result of trade in freshwater fish for aquaria between Britain and the Americas. However, if a narrow belt of seawater such as the Menai Straits between the Welsh mainland and Anglesey is an effective barrier, this raises the problem of how triclads have crossed the main watersheds. If not transported by the activities of birds or man, this leaves their own movement as the most likely explanation. It may be that triclads have crossed the watersheds in the plains where continuity is more likely and then dispersed up river. It is also possible that there have been

25

L A K E D W E LLIN 0 TRI C LA D S

shifts in the direction of How of rivers and correlated changes in watersheds which have permitted dispersal in directions which today appear improbable. But it must be admitted that, as for many other problems of zoogeography, we do not know the answer. Any hypothesis which suggests the survival of organisms in the icefree areas of southern Ireland and England during the last glacial phase must take cognizance of the climatic conditions which prevailed and the ecology of the organisms concerned. I t seems likely (Corbet, 1962;Efford, 1962)that on the edge of the glaciated areas, tundra conditions prevailed with summer temperatures around 9" C! (Ullyott, 1936). This climate would enable the survival of Polycelis nigra, P . tenuis and Dendrocoelum lncteum which can complete their life-cycles over a temperature range of3.5-5.0" C up to 15-20" C (Table V).A!though by comparison Dugesia is a genus more associated with warmer water, Dug. lugubris can breed at a temperature of 10" C and upward (Reynoldson et al., 1965), also it is found in Finland and in Russia near Leningrad (Luther, 1961) with their long, severe winters. It is possible that it could have survived in small numbers a t the extreme southern limit where conditions were probably less severe. In fact, survival of all these triclads may have depended more on the presence of suitable food organisms than on temperature. I n their ability t.0 tolerate low temperature triclads differ markedly from the Lusitanian fauna, and persistence during the last glacial period is much more €easible. Survival of P. felina and Crenobia alpina in Southern Ireland was also the basis of O'Rourke's argument ( 1 946) in refuting Ullyott's (1936) hypothesis concerning t,he use of

TABLEV Temperature Limits in "C of tlbe Various Stages and of the Complete Life-cycle in Dendrocoelum lacteum, Pol ycelis nigra, P. tenuis and Dugesia lugubris (Reproduced with permission from Reynoldson et al., 1965) Deiadrocoelum Polycelis lactezim dgra

Stage

Polycelis tenuis

Duge ai a lugubris

Cocoon production Lower Upper

1-5 18.5

3 -5 18.5

5 *O 20.0

10.0 23 -0

Egg development

Lower Upper

1.5 23.0

1.5 23.0

3 -5 23.0

5 .O 23.0

Maturat,ion

Lower Upper

3 -5 15.0

3-59 18.5

5.0 20.0

10.0 23 -0

Life-cycle

Lower Upper

3.5 15.0

3.59 18.5

5 *0 20.0

10.0 23.0

26

T. B . REYNOLDSON

these species to determine the climatic conditions at the time Britain was separated from the continent. The evidence from lake-dwelling species supports O’Rourke. The other fact which must be fitted into the hypothesis is the virtual restriction of the western island faunas to P. nigra. Accidental introduction may be discounted; the arguments against have already been stated, and to these can be added the uniformity itself, which suggests a natural phenomenon. This means that either P . nigra survived glaciation in these small islands, extending as far north ;t9 Islay, an unlikely event in view of the fact that its limit today is just a little farther north, or that it dispersed more quickly than the others and reached the islands before they were cut off from the mainland by the sea. There is no obvious reason from structure or life-cycle why P. ?zigra should have such an advantage, but if it is supposed that this species was mme widespread and abundant south of the glaciation than the others, just as it is in Britain today especially in harsh habitats (Fig. 3, Table 11),then it may have been able to follow the retreat of the ice more quickly. This would be enhanced by its ability to occupy streams more readily than the others (Reynoldson, 1956b); a view contradictory to that of Beauchamp (1932). Such an argument seems to be the only one which ean be advanced to account for this characteristic distribution and provides support for regarding the present-day pattern as a valid expression of the ecological ranges of these species. The argument developed here presupposes that the western islands concerned (p. 21) were a11 linked to the mainland at one stage after the retreat of the ice, and geological evidence suggests that this is likely except for the Isle of Man; here opinions are divergent (see Williams, 1962b).Such an explanation of the distribution of P. nigra is supported by that of the stream-dwelling Crenobia alpina and Polycelis felina. Both of these are more tolerant of severe climate and poor habitats (Reynoldson, 1961c),and on the same argument might be expected to follow the retreat of the ice even more closely and quickly than P . nigra, so extending farther north. They may even have been able to exist farther north than other species during glaciation and Crenobia alpina has often been regarded as a glacial relict species (Whitehead, 1922; Carpenter, 1928). Their present-day distribution supports such an argument for they occur not only on the western islands supporting P. nigra but one or both also occur on islands slightly farther north such as Mull, Rhum, Canna and Sanday (Bertram, 1939) and on the main Orkney Island and Fair Isle. They have not been recorded from the more outlying islands such as Lewis (Elton, 1936; R. C. Connolly, private communication), N. and S. Uist (R. C. Connolly, private communication) or the Shetlands (A. Milne, private communication). However, C . alpina was found on St. Kilda (J.B. Cragg-

L A K P DWELLING TRICLADS

27

private communication) while P. felina (and P. nigra) was recorded from the Outer Hebridean Island of Barra (Forrest et al., 1936)but the latter identification needs confirming based on the new taxonomy. There are also some records of Crenobia alpina in the Faroes, and Steinbock (1931) very tentatively suggested that it may have been transported to the island on icebergs, but this seems very doubtful. The presence of these populations cannot be explained satisfactorily at present. Triclads appear to be absent from Iceland (Steinbock, 1948). This general scarcity in the outlying islands is interesting since it appears that they have had no connection with the mainland since the last glacial phase (see Corbet, 1961). There are some striking resemblances between the distribution of Asellus (Williams, 1962b) and lake-dwelling triclads in the British Isles which deserve elaboration. The northern extension of both groups is similar in their scarcity north of the Highland Fault; the few occurrences of both organisms are probably due to trout stocking. The Highland Fault is mentioned only as a convenient landmark and it is not suggested that it has operated as a barrier. The most likely obstacle to northward spread is the Grampian Mountains to the south of the Fault which leave only narrow coastal plains on the east side. Another important brake on this movement is the general east-west flow of the main rivers in Britain. The distribution of A . meridianus is very similar to that of Polycelis nigra, each being the only representative on most of the western islands (e.g. Skokholm, Bardsey, Isle of Man) and the common species on Anglesey. It does not however extend so far north as P. nigra, being absent for example from Islay. Williams (ibid.) attributed this distribution to either the survival of the species in southern Ireland and England during the last glacial phase and its dispersal to the islands while land connections still existed by closely following the or to its edge of the retreating glaciers, i.e. as postulated for P. reaching Ireland from the mainland by land connections following retreat of the glaciers. As indicated (p. 24) the latter seems doubtful and unnecessary. Asellus aquaticus resembles the rest of the triclads in having a more restricted distribution which Williams attributed to its later arrival. He expressed the view that it was accidentally transported both to England and Ireland by man. Here events seem to differ from those suggested for triclads where cogent reasons have been advanced against man being primarily involved. The apparently more rapid spread of A . aquuticus compared with trricladsin recent times, probably reflects its greater resistance to desiccation and mechanical damage compared with triclads. A striking contrast to triclads in rate of dispersal is also afforded by the more suitably equipped Hydrobia ( = Potamopyrgus) jenkinsi which has been reported on by Hunter and Warwick (1957).I n general, the distributions of AseZlus, triclads and certain mites

28

T . B . REYNOLDSON

(Efford, 1962), suggest that they have been influenced by the same historical events and physiographical barriers, and they provide evidence of survival of freshwater organisms in Britain during the Ice age, in contradiction to the views of Ullyott (1936) and Thienemann (1950) who argued that Britain was re-colonized from the Continent via land connections after the last glacial period. The difficulties of accepting this have been outlined (p. 24) but the absence of Dug. gonocephala from Britain needs further consideration. It would appear that this species either never reached Britain at any time or failed to survive glaciation. Beauchamp and Ullyott (1932) have suggested that it is competitively superior to C. alpina and P . felina only when summer temperatures exceed 16" C. It is possible therefore that it was eliminated during a glacial period and never succeeded in re-colonizing, but until we know more about the basis of the supposed competition such an argument cannot be taken further. This historical approach, although unavoidably speculative, supports the view that the presenbday pattern of distribution in those areas containing all four species is the outcome of varied ecological attributes and represents a stable condition measured in ecological time. The fact that Dugesia and Dendrocoelum only occupy 70% of the most favourable habitats on the mainland (Table 11)is evidence that even here triclads are still extending their range and conceivably the pattern might alter. However, in N. Ireland where there are no important physiographic barriers, triclads seem to have dispersed more completely and Dugesia has for example occupied all the fully favourable habitats without in other ways altering the pattern. Admittedly this is based on few data, and more extensive sampling especially in Southern Ireland would be instructive. Further support for the reality of the pattern can be derived from triclad distribution in a large lake such as Windermere. Here there is a range of habitats from relatively sheltered, productive bays lined by deciduous trees with a correspondingly richer fauna supporting all four triclad species, to less productive, more exposed places supporting mainly Polycelis species. Thus we see the same pattern in a, single lake, produced by ecological and not historical events.

V. DETERMINANTS OF DISTRIBUTION A N D ABUNDANCE All environmental factors which influence the survival and reproduction of the individual are involved in any explanation of distribution and abundance, they differ only in degree. Andrewartha and Birch (1954) produced a classification of such factors which although criticized provides an orderly approach to the problem and their initial ideas have been further discussed and amended by Browning (1962). This author has classified the environment into five components: wen ther,

L A K E DWELLING T R I C L A D S

-..)

()

resources, numbers of the same species, numbers of other species and hazards. The component “resources” now includes the “food” component, and part of the component, “a place in which to live” of Andrewartha and Birch’s original scheme. While Browning’s arguments for doing this have much to commend them, in the particular treatment of the triclad environment adopted here, it seems more appropriate to use the original classification. The main reason for doing so is that in the quantitative work sampling was restricted to sheltered, stony shores. This was an attempt to eliminate any differential effect of the resource “substratum))and to reduce certain “hazards” in the sense considered by Browning. Under these circumstances five components are dealt with; weather, a place to live, food, other organisms of the same species and of different species.

A. WEATHER This factor is from some aspects less complex in aquatic than in terrestrial environments mainly because humidity is not involved, but also because the extremes of temperature are less and change is not so rapid. Indsed, temperature is the main variant for aquatic organisms although rainfall may have indirect effects mainly by altering the water level of lakes and the ionic composition of the lake water. Wind can also be important but, as already indicated, variations in this factor were reduced to a considerable extent. A detailed comparative study of the tolerance of the four triclad species to temperature and its effect upon the life-cycle has shown contrasts among them. The temperature ranges for the complete life-cycle are shown in Table V and while this factor has a differential influence, all the species would be able to breed in British lakes if temperature were considered in isolation. The species most affected by low temperature is Dugesia lugubris which is unable to breed at 7.5” C and below. Water temperatures in our highest lakes would seem to permit breeding of even this species (Reynoldson et al., 1965). For example, it is able to breed in southern Finland and Leningrad (Luther, 1961) where winter temperatures are severe, although summer temperatures may be higher than in Britain. While breeding experiments suggest there is some parallel between altitude and the distribution of the Polycelis species afid Dug. lugubris which involves temperature, this factor cannot alone account for the pattern, as shown clearly by the distribution of Dendrocoelum lacteum. This latter species is the most active breeder at the lowest temperatures, yet in Britain it is almost restricted to the warmer, more productive, lowland lakes. Temperature may prove to be a factor in distribution and abundance, but only in conjunction with other more important factors. Although rainfall may cause some rapid changes in the chemistry of lake water, B*

30

T . B . REYNOLDSON

especially the proportions of t’he ions (Macan, 1950) the magnitude of thesc in relation to the range found between lakes is small. Such a factor would appear unlikely to be directly concerned in the pattern, and experiments described on p. 31 confirm this. The other effect of rainfall, change in water level, does not differentiate between the species from what we know of their reaction. Extension of the level is certainly exploited by them in feeding on drowned terrestrial organisms; lowering of the level by evaporation is normally such a slow process that few will be stranded. Bearing in mind the restriction of sampling to favourable stony shores it is reasonable to conclude that weather does not have a direct bearing on the characteristic pattern of distribution and abundance of these four triclad species.

B.

A PLACE TO LIVE

A primary requirement of triclads is a firm substratum of leaves or stones, preferably in shallow water, which provides shaded resting sites. The sampling restrictions reduced variations from this source and also such hazards as abrasion from moving sand; effects of wave action have already been mentioned. Therefore, such physical attributes of the habitat as these are unlikely to be involved. The chemical properties of the lake water may be regarded as an aspect of (‘a place in which to live” and as we have seen, they show a relationship to distribution and abundance. The first problem to be examined here is the nature of the correlation, whether it is direct or indirect. Macan (1963) reviewing the relationships between calcium and freshwater organisms concluded that a direct effect was unlikely except in special cases like Procerodes ( = Gunda, Pantin, 1931) but each case requires testing; a similar conclusion would apply for the T.D.M. relationship. It is obviously preferable to test the ability of the various triclad species to survive and reproduce in lakes with low calcium and T.D.M. by retaining the natural conditions as far as possible during the experiment. This is best achieved by keeping the organisms in a suitable lake in cages which allow exchange of water between cage and lake. This avoids or reduces greatly the possibility of unnatural conditioning of the water, shown to be important for survival in some circumstances (Alee, 1951); it also permits the natural temperature regime to operate. For these several reasons triclads were kept in polythene cylinders 10 cm long and 5 cm internal diameter, closed a t each end with bolting silk of mesh fine enough to exclude organisms such as planktonic Crustacea. The cylinders>were clamped on to a metal frame by Terry clips and the apparatus kept in a sheltered part of the shore at a depth of about 30 cm. Lake Ogwen was selected for the experiments since it has a low calcium content ( 0 - 5 mg/

LAKE DWELLING TRICLADS

31

litre) and supports only Phagocata vitta, although it had the disadvantages of being popular with summer visitors and of suffering rapid changes of water level from time to time by withdrawal of water for local industry. Ten adults of each species collected from habitats with a moderately high calcium content were kept in separate cages and fed on earthworm slices a t approximately fortnightly intervals; the water temperature was read at each visit. Three experiments of this type were made, the first lasted 54 days from 30 October to 9 December 1957, when a sudden fall in water level killed all species except P. tenuis. A second using the original P. tenuis, ran for 113 days from 23 December to 22 April 1958, when visitors wrecked the cages; a third with new specimens lasted 112 days from 22 October 1958, to 10 February 1959. The experiments ran through two winters and temperatures were below 5" C and the lake ice-covered for long periods. Survival of the species is shown below: P. P. D. D. nigra tenuis lugubris lacteum 10 9 8 Expt. 1 54 days 0ct.-Dec. 1957 9 Expt. 2 113 days Dec.-Apr. 1958 5 8 10 10 Expt. 3 112 days 0ct.-Feb. 1959 10 10 6 8 Totals 24 28 25 26 All species survived in good condition and in large enough numbers to show that the chemical features of the water did not affect them adversely. Thus Dugesia and Dendrocoelum which are not usually found in unproductive, low-mineral lakes survived as well as P. tenuis and P. nigra which are characteristic of such lakes. The low number of P. nigra in Expt. 2 was partly due to the accidental squashing of two specimens during feeding. It was noticeable that the Polycelis species fed better than Dugesia when the lowest temperatures (1-3" C) prevailed. During such periods several of the Dugesia secreted a mucilaginous envelope around themselves. This is a general reaction to unfavourable conditions and has been recorded in the laboratory in water of high calcium content. I n the Ogwen experiment it was probably a reaction to low temperature. I n a further experiment the survival of these triclads in water of low calcium and T.D.M. without food was also tested using these cages in Lake Ogwen. Five specimens of each species except Dendrocoelum, not available at the time, were kept in the lake for 3 w ~ k during a May 1959. They all remained normal in appearance and behaviour and also produced cocoons during the period. The untimely end of the longer experiments meant that the main breeding season had been missed so that an additional experiment was made during April-May 1959 in which ten specimens of each species

32

T. B. R E Y N O L D S O N

were kept in the cages in Lake Ogwen and observed for cocoon production; these triclads were fed regularly. During a period of 30 days P. nigra produced two, P . tenuis twenty, Dugesia five and Dendrocoelum eleven cocoons. The majority of these proved fertile in the Ogwen water showing that these species are not only able to tolerate such conditions but are also able to breed under them. The growth and development of t'he young of each species except P . nigra was followed in the laboratory under a standard feeding and temperature regime in Lake Ogwen water, for comparison with similar experiments in water of higher calcium content (20 nig/litre, see Young, 1963 for details). Progress was similar in both types of water, culminating in the production of fertile cocoons in all species. Dendrocoelum lucteum took a little longer in the calcium-poor Ogwen water where the average maturation period was 217 days with limits of 188-232; in calcium-rich water it averaged 180 days (S.D. 19) at 10" C. The conclusion to be drawn from these various experiments is that the chemical nature of lake water plays no direct part in determining the pattern of distribution; Dugesia and Dendrocoelum are as capable of living in calcium and T.D.M. poor water as are the Polycetis species, nor were either of the Polycelis species specially fitted for life under such conditions. The occurrence of several freshwater organisms in large lakes normally outside their usual range as measured by edaphic factors has always been puzzling, and various interpretations have been offered (e.g. Macan, 1950; Tucker, 1958; Williams, 1962a). I n the case of triclads it is clear that the presence of Dugesiu and Dendrocoelum in Lake Windermere with 5.0 mg/litre calcium and in Loch Lomond with 3-0mg need not be explained in terms of physiological races as the Ogwen experiments showed. Nor is lake size necessarily involved, since both are found in the small Newton Mere with 5.0 mg calcium, while Dendrocoelum also occurs in the small Llyn Mair with only 2.4 mg/litre. This ability of the four species to tolerate equally well such a wide range of calcium and other ions, while of much interest to physiologists, lies outside the context of the present ecological problem. There are of course many other variables such as pH and dissolved oxygen which have not been considered, but there was no indication in the field work that they are relevant to distribution. Apart from some dystrophic lakes on Islay, low pH values have not been encountered and it is unlikely that dissolved oxygen becomes limiting in the littoral zone of stony shores. There was some indication (Reynoldson, 1958a)that in lakes with comparable water chemistry, those dystrophic in character supported a smaller population, but more work is needed to substantiate this view.

33

L A K E DWELLING T R I C L A D S

One further aspect of the habitat suggested itself as a possible determinant of distribution, namely the biological quality of water, which may also differ as shown by Wilson (1051) for sea water. Were Dugesia and Dendrocoelum in the course of dispersal selecting water characteristic of productive lakes and avoiding that of unproductive lakes? This possibility was tested by choice experiments in an apparatus which allowed waters of different origin to be tested (for details; Young, 1963). Usually fifty triclads of each species collected from a calcium-rich habitat were used in each test. Observation showed that the triclads explored the experimental habitat before settling down. Eight such tests were made with P. tenuis and in seven there was no significant difference between the numbers settling in each water. I n one a significantly higher number was found in the calcium-poor water, but overall there was no selection. A similar result was obtained with Dugesia (Table VI). Dendrocoelum however behaved differently and in fifteen tests this species selected the calcium-rich water each time in significant numbers (P < 0.001). The specimens were then kept in Ogwen water for 5 weeks and tested again in five experiments with a similar result. They were kept for a further 7 months in Ogwen water, being fed a t regular intervals on Asellus. A further seven tests were made and this time the Dendrocoelunz showed a preference for Ogwen water, not so marked as the original preference for calcium-rich water, but nevertheless significant (P .= 0.05 > 0.02) (Table VI). It appears that this species can become conditioned to some property of the water of its habitat. However, if triclads disperse by their own locomotory activity (p. 24) it seems unlikely that such conditioning can play an important part in producing a pattern of distribution because normally changes in the TABLEVI The Distribution of Triclads between Calcium Rich and Calcium Poor Water in the Laboratory; ( a ) after no conditioning, (b) after 5 weeks, (c) after 7 m o n t h conditioning in calcium poor water Species (a)Polycelis tenuis ( a ) Dugesia lugubris ( a ) Dendrocoelum lacteum ( b )Dendrocoelum lacteum ( c ) Dendrocoelum lacteum

Ca poor water CE rich water No. expts. (0.5 mng/litre) (24.0 mg/litre)

Significance

8 8

146 114

133 117

none none

15

87

302

P < 0.001

5

47

110

P < 0.001

7

103

'73

P < 0.05

> 0.02

34

T. B. REYNOLDSON

chemical properties of water are gradual. Support for this interpretation is given by the wide distribution of Dendrocoelum lacteum in Feniioscania (Reynoldson, 1958c) where it had a pattern corresponding to that of P. nigra in Britain. It seems reasonable to conclude that a biological property of water per se does not determine the distribution of these triclads.

c. FOOD I n the present context we are not concerned so much with scarcity and abundance of food but rather with the kinds taken by the four triclad species as indicating the degree of overlap in their requirements. Food has been found to be a key resource in deciding the ability of ecologically similar species to co-exist, and has often been implicated in determining pattern. This aspect has been studied most thoroughly in birds (Lack, 1954; MacArthur, 1958); it has been less well studied for invertebrates, but work on gastropods (Kohn, 1959), and on tsetse flies (Weitz, 1964) using a serological technique, is an example of what can be achieved. No detailed study of the food of triclads occurs in the literature, and certainly none that would provide the kind of information which is required to determine the extent of overlap among the four species in nature. Hyman (1951) has stated that triclads do not feed on plants or decaying organisms (cp. Popham, 1955) and this has been confirmed by our studies. She also expressed the view that one species may feed upon another and that cannibalism may be extensive, as it seems to be for some strains of Dugesia tigrina (Root, 1960; Armstrong, 1964). Both aspects have been tested in our laboratory in various ways and the results showed (Reynoldson and Young, 1963)that neither phenomenon is common in these British species. Only two defbitive observations of predation have been noted, both by Dugesin lugubris, one upon Polycelis nigra and the other upon P. tenuis; in the latter instance the pharynx of the P . tenuis “ate” its way through the body wall of Dugesia within a few minutes of being ingested. No successful attack of one specimen upon another of the same species has been observed, but a few isolated examples of this have been reported (e.g. D. Clegg-private communication) again for Dugesia lugubris. It can be concluded that interactions of this sort are not important in nature and play no part in determining distribution and abundance. The behaviour-patterns which cause predation and cannibalism among triclads would appear to be subtle and have not been studied yet. The literature suggests that triclads as a group feed on small aquatic annelids, crustaceans and insect larvae, and they also take terrestrial organisms trapped in water, but the observations are too incidental to

35

L A K E D W E L L I N G TRICLADS

construct any sort of picture. This problem has been tackled in three main ways : (a) by examination of squashes of triclads recently collected from the field for the remains of prey. This method has the disadvantage that results may be biased in certain directions, especially towards oligochaetes, which are more likely to be detected on account of their setae. (b) laboratory experiments in which selected prey were exposed to triclads starved for a uniform period (Holling, 1963). This approach has two obvious disadvantages, the range of prey is restricted compared with natural conditions, and the normal behaviour of either prey or predator may be interfered with. The latter was probably reduced in the experiments by the provision of cover for both organisms. (c) the use of a serological technique for detecting prey in squashes of field specimens. This is the most reliable approach but it has only been used to a limited extent so far. The results from the examination of field specimens, both young and adult, are shown in Table VII. The main conclusions are that various TABLEVII Food Organisms Found in the Guts of Triclads Collected from the Field. (Reproduced with permission f r o m Reynoldson and Young, 1963.) Expressed as percentage of total identifications Polycelis . Dugesia Deiadrocoelum ri igrc, I’ dermis lugubris lacteuin, Adult Total . . ....-- -

Oligochaot,a Lumbriculus variegatus Naididae TubXicidac * Lumbricidae

28 -6 31.4 5.7

2.8

Arthropoda Insecta Asellus Others

14.3 Nil 11.4

Mollusoa t Lym.naeu sp. Hydrobia j enki mi Ancylus lacustris

X il Nil Nil

Others

5 *7

35.0 11.6 46.5 Nil

14.3 21.4 10.0 5.7

404 20.0 Nil Nil

Nil 78-6 3.6 Nil

70-6 29.4 Nil Nil

1.4 Nil 1.4

Nil Nil

5.7

Nil 18.6 2.3

5.0

3.6 Nil 10.7

Nil Nil Nil

Nil Nil Nil

Nil Nil Nil

15-7 11-4 1.4

Nil 35.0 Nil

Nil Nil Nil

Nil Nil Nil

Nil

1.4

Nil

3.6

Nil

40.0

2 -8

31.4 8 -6 2a 8 2 -8

5 *7

* May include Enhy!meidae. t Based on radulae only.

36

T . B . REYNOLDSON

oligochaetes appeared to be the main diet of all species except Dugesia which also fed extensively on gastropod molluscs; arthropods seemed to be of lesser importance in all four species. The food range of young was similar to that of adults and because communal feeding occurred on large prey, the size-ranges of the food of young and adults also overlapped (Young, 1963). When these results are compared with those from laboratory experiments (Table VIII) based on summation of data where single species were exposed, and data where several were exposed together (Reynoldson and Young, 1963)) the main conclusions based on squashes are confirmed for P. tenuis and Dug. lugubris, but in the case of P . nigra it was surprising how few oligochaetes were eaten. Dendrocoelum showed a very different result; in the laboratory it fed extensively on both arthropods and oligochaetes, in the field specimens only the latter were detected. When both Asellus and the oligochaete Lumbriculus were exposed to this species the former were all eaten in 3 days, the latter not until eight days had elapsed. The greater emphasis on arthropods in the laboratory shown by all species, although only slight for P. tenuis and D u g . lugubris, was undoubtedly due in part to the difficulty of detecting triclads which had fed on this sort of prey in the TABLEVIII

The Kinds a d Number of Organisms Eaten by Triclud.s in Laboratory Experiments. (Reproduced with permission f r o m Reynoldson and Young, 1963.)

Prey

I’olycelia iaigra.

No. oaten by Diigesin Deridrocoelum 1’. teri rcis lucpbris lncteum

Oligochaeta Lumbriculus variegatus

2/90

17/90

22/90

54/60

Arthropods, Asellus meridianus Gammarus p u k x Cloeon dipterum Diura bicaudata Chironomus sp. larvae Total Arthropoda

81150 0150 0160 9/50 6/50 13

11/150 0150 0150 4/50 6/50 21

20jl.50 0150 0150 3/50 3/50 26

100/100

Mollusca H?jdrobia jer ik ir 1 s i Lymiucea pereger Tot a1 Molliiwa

0/50

01150 0

1 /a0 1/150 2

15/60

1 Fi/15O

Bo

35/50 47/50 50150 45/50 277

0150 o/ 100

0

37

L A K E DWELLING TRICLADS

TABLEI X Positive Reaction to Rabbit anti-Asellus Serum by Squashes of Field Specimens of Triclads. (Reproduced with permission frowi Young et al., 1964.)

Species

The Mere Cole Mere No. NO. tested %+ve tested %+ve

Newton Mere No. tested %+vr

Beaumaris Reservoir No. tested %+ve

Dendrocoelurn lacteum

50

100

50

68.0

50

8.0

-

-

Dugesia Eugubria

56

5-4

48

0

12

0

-

-

Polycelis tenuis

52

9.6

48

48

8.3

-

-

Polycelia nigra

-

-

-

__

__

36

2.0

8.3 .-

field by the squash method. These experiments confirmed that gastropods are not important in the diet of any species except Dugesia. The results from the serological approach (Young et al., 1964) showed conclusively that Dend. lacteum fed much more on Asellus (Table IX) and probably arthropods in general, than the planariid species. They support the laboratory data and indicate that bias occurred in the results from the squashes. These various approaches to a study of the food of trirlads show that there is considerable overlap in the type of prey eaten by the four species. However, the Polycelis species take a larger proportion of oligochaetes than of other prey, Dugesia alone feeds on gastropods, and Dendrocoelum eats a greater proportion of arthropods, especially Asellus. An outstanding feature of the laboratory approach is the contrast between the planariid species and Dendrocoelum in the number of prey eaten. The behaviour patterns of the former seem to be such that they do not react very markedly to the presence of intact prey behaving normally. Although these triclads had been starved prior to the experiment and fed readily afterwards on punctured animals, they largely failed to recognize intact organisms a s potential food; a total of 1531840 only were eaten. I n contrast Dendrocoelum devoured 331/510 prey; if gastropods are excluded this becomes 331/360. Further experiments were made to study the behaviour of the triclads when damaged animals from which the body fluids had leaked were exposed to them, and in the case of the planariid species, to organisms trapped in vaseline. In

38

T. B . REYNOLDSON

the former (Table Xa), the planariid species showed a preference for oligochaetes with arthropods second choice, while gastropods were relatively unattractive ; Dendrocoelum showed a preference for arthropods (Asellus).When the rate of attraction was measured, again the planariid species reacted more quickly especially to oligochaete material (Table Xb). The reaction of the planariids to various prey trapped in vaseline TABLEX Triclads Feeding on Damaged Prey. (Reproduced with permission f r o m Reynoldson and Young, 1963.) Attractiveness of various prey exposed simultaneously Prey organism Asellus L y innaea Triclad species Earthworm meridianus pereger a.

Polycelis nigra P. tenuis Dugesia lugubris Dendrocoelum lacteum Total

14 25 19 6 64

0 0

11 9 9 10 39

Total 25 34 30 16 105

2

0

2

b. Rates of attraction t o t w o types of prey Earthworm Gammrus -

T i m e Polycelis ( m i n ) nigra 5 10 15 20

8

11 12 15

P. tenuia 3 7 10 11

DendroDugesia coelum lugubris lacteum 5 12 16 20

0 3 4 4

P. Polycelis n@ra tsnuis 5 10 12

-

7 13 17

-

DendroDugesia coelum lugubris laoteurn 8 13 18

-

2 9 13

but undamaged, was also illuminating (Table XI) and showed conclusively that organisms behaving abnormally are attacked with high frequency . These results not only confirm the differences in tho feeding behaviour of the several species, but also illustrate the considerable degree of overlap. While Polycelis species and Dugesia feed rather more on oligochaetes than arthropods, the reverse is true of Dendrocoelum; Dugesia alone attacks gastropods. A difficult problem, so far unresolved is whether or not P. nigra and P. tenuis take different foods. Scrut,iny of the data certainly shows some differences but the evidence is so far insufficient for reliable conclusions to be drawn, The planariid species do not seem to be primarily hunters attacking undamaged organisms, but feed more

TABLEXI AVumberof Prey Eaten when Fastened in Petroleum Jelly, Fastened and Allowed to Free Themselres, and under Nornial Conditions. (Reproduced with permission from Reynoldson and Young, 1963.) Twenty-five prey and twenty triclads used in each regime.

No. eaten by P . tenuis

Polycelis nigra Prey Asellus meridianus Cloeon dipterum LymnaecL pereger Hxdrobja jEnkinsi _ _

Fixed 18 4

~ -

Freed

I

1

-

Control 1

0

-

-

Fixed 19 11 -

Dugeaia lugubris

Freed

Control

-

-

9 5

3 0 -

Fixed 19 14 13 7

Freed 11 2 -

Control 0 0 2 8

40

T. B . R E Y N O L D S O N

on damaged individuals or those behaving abnormally, e.g. struggliug in mucus, trapped in the water film, or perhaps damaged by other predators. Dendrocoelum is an active hunter of small organisms and uses ail envelopment technique aided by its anterior sucker t o attack prey. While the role of mucus produced by triclads in ensnaring prey has been described by Jennings (1957) for P. felina, we have seen no evidence that it is important in the lake species of Planariidae; but mucus probably helps Dendrocoelum to catch prey, a t least under laboratory conditions.

D.

O R G A N I S M S O F THE S A M E S P E C I E S

The isolation of the intra-specific events which are considered here is entirely artificial and their influence upon the distribution and abundance of the several triclad species is indirect. However, this approach affords background information on the conditions under which the triclads are living and may indicate the important types of interaction occurring among the species in nature. During the ten years of observation there has been no hint in the field or in the various experiments that co-operation between individuals, of the type described by Allee (1938), determines the pattern of distribution of these triclads. It has already been shown that cannibalism is a rare phenomenon (p. 34). This leaves intraspecific competition as the main focus (sensu Milne, 1961). The population dynamics of the four species have been studied in some detail (Reynoldson, 1960; 1961a; Taylor and Reynoldson, 1962; Young and Reynoldson, in press), and while they all show basic similarities, there are interesting differences (for example in life-span) between the Planariidae and the Dendrocoelidae which influence events. Apart from differences in the time of year a t which breeding commences, which although slight probably influence distribution, the population biology of the three planariid species is similar. They all have a low birth rate and recruitment to the population is only about 50% of its pre-breeding size under natural conditions; in the laboratory with ample food the birth rates are several times greater. The low recruitment is due to the gradual development of a condition of food shortage after the initial hatching of young; this puts a brake upon and finally stops breeding. A t the same time the individuals decline in size because of food scarcity, and this is accompanied by some mortality which readjusts the population to its food supply. This cycle is repeated each year and represents a self-regulatory system operated by intra-specific competition for food. The more obvious operation of this homeostatic system compared with most natural populations arises from two properties of these triclad species. First, their capacity to remain alive under conditions of food shortage for long periods by resorbing their tissues and shrinking in size. Laboratory observations have shown that an adult

41

LAKE DWELLING TRICLADS

Polycelis tenuis of 8-9 mm length can live up to 8 months without food, in the meantime shrinking to 0.5 mm length; similarly Dugesia lugubris can shrink from 14 mm to 2 mm; the accompanying change in biomass is of course much greater. Such tenacity has not been observed in the field but shrinkage to 2-3 mm in both species has been noted. Furthermore, such field specimens are able to grow and breed again when fed, showing high resistance to senescence. Thus, triclads react initially to food shortage by a considerable change in biomass; they are more resistant to change in numbers. Secondly, these triclads appear to have no important predators or parasites in the stony, littoral zone of lakes (p. 44) and therefore intra-specific competition is able to exert a maximal effect. This hypothesis has been tested by field experiments in which the amount of food per individual has been increased artificially both by adding food and by reducing the triclad population. Also, newly created habitats have been studied in which the prey was initially numerous relative to the triclads (Reynoldson, 1964). Such populations showed an increased birth rate and recruitment, while shrinking was delayed and its extent reduced (Table XII). It seems evident that natural populations are under some restraint both in growth of the individual and in fecundity for a considerable period of each year, and that t,hey show great numerical stability which provides optimal conditions for survival (Martin, 1959) to which their longevity will also contribute (Hutchinson, 1957). They show to a high degree the population homeostasis which forms a key part of Wynne-Edwards’ hypothesis (1962), even to the extent that those individuals which fail to breed in a particular year may form a strategic breeding reserve. But in these simple organisms there is no evidence of social organization which could result in selfregulation, and in competing for food they show what Nicholson, (1054) TABLEXI1 Effect of Increasing the Food Supply upon Total Recruitment and Proportion of Adults during the Climax Month. (Reproduced with permission from Reynoldson, 1964.) Triclad species Polycelis tenuia (College pond) P . tenuis (New pond) Dugesia lugubria Polycelia nigra

Total recruitment,

Normal Increased food

Percentage adults Normal Increased food

(%I

(%)

50

350

4-3

55.2

50

175

4 -3

13.5

38 90

137 500

2.2 -

36.9

-

42

T. B . REYNOLDSON

describes as the scramble type. It is perhaps significant that as a group they appear to be inefficient predators and suffer from a shortage of food, absolute rather than relative (Andrewartha and Browning, 1961; Birch, 1962). Recently, MacArthur (1961) and Pimentel (1961, 1963) have emphasized the fact that predators can only feed on the “interest” and not the “capital” of their prey populations if they are to survive. The planariid triclads seem to be a good example of this, indeed their special properties make it imperative that some safety valve should be built into their biology. They have avoided over-exploitation of their prey by the evolution of a behaviour pattern which restricts their feeding largely to damaged organisms or to those behaving abnormally (p. 38). This may have evolved by the genetic-feedback mechanism now being explored by Pimentel, provided some degree of population isolation occurs; aquatic,populations are probably isolated to a much greater extent than terrestrial populations. On the other hand, one would expect considerable selective pressure in favour of increased predatory efficiency. I n my view, this mechanism which Pimentel assumes to have evolved by natural selection and which is supported by experimental evidence (Pimentel et al., 1963), sets the limits within which a population normally oscillates, i.e. it functions as a coarse adjustment, while the fine adjustment is achieved by a proximate (Baker, 1938; Lack, 1954) density governing factor (sensu Nicholson, 1954). Orians (1962) and Bakker (1964) have discussed the inter-relations of ultimate (evolutionary) and proximate (ecological) factors. I n the case of triclads the proximate factor is intra-specific competition for food. This can be clearly seen in tricleds by comparing rates of reproduction under natural conditions and under adjusted field conditions (Table XII).A genetic mechanism has too great a lag period, especially in those species with a long generation time, to operate speedily enough. Lack (1954) believed clutch size, an indication of birth rate, to be adjusted directly to food supply by natural selection, but as MacArthur (1961) pointed out, even in birds the problem is often more complex than this. If a population is to survive, the birth rate must also be adjusted to take into account the hazards the species has to meet, and the apportionment of nutriment between the needs of the parent for survival and the production of young (Fisher, 1930; Birch, 1960) will vary among the different species for this reason. For example, triclads have few natural hazards and when food becomes scarce after limited breeding they soon divert it from reproduction to maintenance of the individual; blowflies have to face more hazards among which is dispersal of their food and when this resource is short they convert as much food as possible to reproduction and sacrifice size of the individual to some extent; internal parasites with extreme hazards to meet are virtually egg-laying machines.

LAKE DWELLING TRICLADS

43

In Dendrocoelum lacteum the position is altered to some degree by the fact that a considerable proportion of the population are annuals and die after breeding (Yoiing and Iteynoldson, in press). As a result, when the young are hatching a food crisis is postponed because adults are dying a t the same time. This is shown by characteristic differences in the population size-structure of Dendrocoelum and the planariid species. Also stemming from the contrast in longevity is both a higher birth rate in Dendrocoelum (6-7 per adult compared with 1 in the planariid triclads), and a higher recruitment, 350% compared with 50-1000/. This means that the amplitude of population fluctuations is several times greater in Dendrocoelum during an annual cycle. It is also significant that Dendrocoelum is a more efficient predator than the planariid species and seems to cause a detectable reduction in the population of its main prey Asellus (p. 40)but other factors such as variation in severity of inter-specific competition are also involved. Although the mechanism of population regulation seems particularly evident in these triclads, Maguire (1962) has suggested in the case of Cura ( = Curtesia)formanni that some control on reproduction is exerted by ectocrine substances. Thers are some puzzling features of his data which suggest that the phenomenon he describes is more likely to be a physiological effect of laboratory crowding in a lotic species and is not applicable to field conditions. From the viewpoint of distribution and abundance, the important feature of intra-specific relationships is that serious food shortage occurs periodically in all species and it is against such a background that interspecific relationships must be considered.

E.ORGANISNS

OF DIFFERENT SPECIES

Here we are concerned with the effects of predators and parasites of triclads and the competitors for resources, all of which theoretically are capable of influencing the pattern of distribution and abundance. These are treated under two heads.

1. Predators and Parasites Predators may influence not only the abundance but also the distribution of their prey, but little is known of this factor among aquatic invertebrates (Macan, 1963). The literature suggests that some animals such as newts, sticklebacks and certain carnivorous insect larvae eat triclads (Whitehead, 1922; Bolen, 1938), while Hyman (1951) maintains that they are rarely eaten. The relative immunity of such soft-bodied organisms is attributed to their unpleasant taste, Fnd Jennings (1957) has produced experimental evidence of this. However, no substantial observations have been reported on which to assess the extent of

44

T. B. REYNOLDSON

predation. In the present programme Taylor (1960) confirmed that dragonfly and damselfly larvae fed extensively on Polycelis nigra and there was some indication that Erpobdella sp. ate a few. These experimeiits were taken further by Young and Reynoldson (1965) who tested a series of potential predators against young and adult P. nigra, P. tenuis, Dugesia lugubris and Dendrocoelum lacteum. The results (Table XIII) show that of nineteen invertebrates selected over a range of phyla, only adults of Dytiscus marginalis and the Odonata larvae took triclads in any numbers, and in these cases young rather than adult triclads were eaten. Fish, especially rudd (Scardinius erythrophthalmus) ate them to some extent. All these predators took approximately equal numbers of the four triclad species but the experimental regime did not offer a choice. There are several reasons for suggesting that such restricted predation is likely to be even less in the stony, littoral zone of lakes. First, those invertebrates which attacked the triclads occur most commonly in heavily weeded habitats with a muddy substratum. Second, it was evident that apart from rudd, only one or two individual fish fed upon the triclads, despite their evident unpleasant taste. This would account for Taylor’s ( 1 960) conclusion that minnows did not eat P. nigra. In nature, with alternative food it is unlikely that many triclads are eaten. Third, rudd are so sparsely distributed in Britain that they cannot influence triclad distribution; furthermore, fish with similar feeding habits are found precisely in those lakes where triclads are so numerous and diversified. Finally, triclads are so slow-moving or immobile that they will not attrart fish to the same degree as when both are confined in a dish with limited cover. Indirect evidence from the study of the population dynamics of the individual triclad species (p. 40) also suggested that predation was insignificant. However, before this factor can be dismissed altogether it will be necessary to examine feeding on triclads by some method applicable to field conditions such as the serological technique used successfully by Dempster (1960). Parasites of triolads can be dismissed quickly, since of the several thousands exanlined by squash techniques (Reynoldson and Young,

1963)jess than ten were found to harbour a trypanosome and less than

twenty populations were infected by a species of Sporozoa. I n the latter case, such populations were usually found in polluted regions of lakes. There is no evidence of the extent to which the triclads (all species) were harmed, if at all, by the sporozoan but the populations were not obviously reduced.

2. Competitors The two main resources for which inter-specific competition usually occurs are adequate living space and food (Nicholson, 1954; Milne,

TABLEXI11

The Number of Adult ( A )and Young ( Y ) Triclads Eaten by Predators in Laboratory Experiments. ( p ) = Portions Eaten. (Reprdueed with permission from Young and Reynoldson, 1965.)

Predator COELENTERATX Hydra oligactis Pallas HIRUDIKEA Helobdella stagnalis (Linn.) Erpobdella octocuulata (Linn.) COLEOPTERA adults of ~4gabzl8dirlyn~us(oliv.) A . paludosw, (Fab.) Colymbetea fuscw, (Linn.) Ilybiua fuliginosw, (Fab.) Rhantw, bistriatw, (Bergst.) Deronectes sp. (adults) Dermectea sp. (larvae) DytiscuB marginalis (Linn.) (adults) Dytiscw, marginalis (larvae) Haliplus ~ p (adults) . Haliplus sp. (larvae)

No. of predators used

No. of each size of triclad sp. used

20

50

@

20 20

50 50

0 1

10 10 10 10 10 10 10

50

0

5 5 10 10

25 25 50 50

50 50 50 50 50 50

No. of triclads eaten P . tenuis D. lugubrk A Y A Y

P . nigra A Y

1400

2

0

5

0

6

16

0

0 0

0 5

0 0

0 3

0

0

0 30

4

2 0 0 0 0 0 0

0 0 0 0 0 0 0

1 0 0 0 0 0 0

0 0 0 0 0 0

0 0 0 0 0 0

13 3 0 0

11

16 0 0 0

7

0 0 0 0

0 0 0 0

10 0 0 0

12 2 0 0

11 0 0 0

0

Total eaten

0

3

0 0 0 0 0 0 0

0

D . lucteum A Y

0 0

* 9Sj200 t 10,'200

0

UP)

0 0

4

95* 10t 0 0

TABLEXI11 - continued No. of Predator HEMIPTERA Notonecta gluuca (Linn.) N e p cinerea (Linn.) TRICHOPTERA Polycen tropw jlavomaculatus (Pictet) ODONATA Coenagrion puella (Linn.) Aeuhna cyunea (Mueller) PISCES CTaaterosteus aculeatus (Linn.) Phoxinus phoxinw (Linn.) Salmo trutta fonna fa& (Linn.) Scardiniw erythrophthdmw (Lh:) AMPHIBIA Triturua helveticus (Razoumowski)

predators used

No. of each size of triclad sp. used

10 10

50 50

0 0

0 0

10

50

_

_

10

50

10

50

P. nigra A Y

8+ 26 19(P) 45 42

No. of triclads eaten P. tenuis D . lugubris A Y A Y ___

0

0

0

0

_

_

14+ 31 WP) 44 40

0 0

3+

21(P)

49

0 0

_

D. lacteum A Y 0 0

0

32 43

0 0

lo+ 3(P)

@+ 35+

W P ) 6(P)

41+

46

5(P) 10 10 10

50 50 50

11 7 13

15 12 12

10 14 9

17 13

10

50

25

32

10

50

1

5

Total eaten 1400 0 0

lo+ (P) 149 +(P) 350 (P)

+

18 9 15

9 8 11

16 14 18

109

16

13 9 14

26

38

24

26

19

35

225

0

4

0

7

0

8

25

86

108

L A K E DWELLING TRICLADS

47

1961). Within the range of population size observed in this work, living space does not appear to be critical. Although it is shared by a large number of other organisms such as Cammarus, leeches of several species, oligochaetes, molluscs and various insect larvae, the requirements are usually not specific and living space as represented by the undersurface of non-bedded stones does not usually restrict the size of the littoral fauna of lakes. I n this connection Macan and Mackereth (1957) have discussed the possibility of jostling in overcrowded conditions causing Cammarus to be exposed to current and predation in streams but this does not occur in triclads. It has been shown (p. 40) that the food of triclads is in short supply especially during the 2-3 months after breeding, and it is reasonable to assume that triclads are sensitive to any inroads which may be made upon this resource. Depletion may result from the feeding activities of a wide range of animals, from those closely related to those only related in the sense that both are aquatic animals. For example, Asellus may be eaten by several species of fish, molluscs by leeches, oligochaetes by insect larvae and so on. The effects of such predation will be several and complex. For example, reductions in food supply will lower the overall triclad population or a specific part of it, depending on the type of food. It will also increase the intensity of any inter- and intra-specific competition in triclads and its timing. But the evidence, admittedly meagre, suggested that timing ;vas largely the result of intra-specific activities (Reynoldson, 1964). Generally it can be assumed that the more distantly related the predators using a food resource, the less intense and prolonged the ensuing competition. This follows because the more contrasted the ecology, usually but not always a function of taxonomic relationship, the less likely are peak demands to coincide and the more likely the availability of alternative food. Therefore the main pressure from inter-specific competition is likely to come from other triclad species. However, occasionally unrelated species may exert an influence sufficiently powerful to restrict distribution (Harper, 1964) but we know insufficient about this aspect of triclad ecology to indicate its prevalence. Leeches, because of their abundance in the littoral zone (Mann, 1955) and because they show appreciable overlap in food with triclada (Mann, 1962), are likely to be the most important component of the fauna in this respect and should be the tirst to be studied. Reliable evidence of inter-specific competition among triclads, almost certainly for food, in view of the demonstrated shortage (p. 40) and overlap (p. 38), has been obtained from several sources. It is most clearly demonstrated between Polycelis nigra and P . tenuis by comparing the size of the P. nigra populations in Anglesey where the species occurs mostly alone, with that of the mainland where it occurs with

48

T A B L EX l V a. The Size of Polycelis nigra Populatioiis i/i the Absence (Anglesey Lakes) and Presence (Mainland Lakes) of P . tenuis

t5.0 _

_

~

5*1-10*0

~-

Ca mg/litre 10.1-20.0 20.1-40.0

- -

>40*0 __

..-

P . nigra alone

17

-

P. nigra in presence of P. tenuio

42

49

76

40

38

P. n e r a

53

136

226

209

322

+ P. tenitis

173

140

179

b . Size of Polycelis nigra Populutiori in Two Anglesey Lakes C'ontaining also P . tenuis ~

P. nigra P. n e r a

+ P . tenuis 2 j P. nigra IP. nigra + P. tenuis

__

.

~

-

-

-

-

-_

-

-

--

__

35 213

-

_..

86 234 -.

-

-~

-

-

__

Triclad populations recorded as number collected per hour averaged for lakos in each calcium category; a dash means no lakes in that rategory.

P . tenuis and other species. It, is clear froin 'Fable XIV that P . tenuis has a markedly depressive effect upon the size of the P . nigra population. It seems unlikely that the environments of Anglesey and the niainland are sufficiently different to account for this. Indeed, this argument is destroyed by comparing the P . nigra populations o f two lakes on Anglesey (Llygerian and Coron, Table XIV, b l , b2) which a!so contain P . tenuis, with the rest: they show a P. nigrn population reduced to mainland proportions. It is interesting to note that while the total Polycelis populations of Anglesey and the mainland are of the same order, the latter tend to be slightly larger. This aspect will be discussed when considering the effect of inter-specific competition (p. 61).A further striking illustration of the effect of inter-specific competition on population size is afforded by the Ialay lochs (Fig. 7 ) . Here the species involved are mainly P. nigra and P . felina but in a few cases P. teriuis is also concerned. The same sort of result is apparent, a reduction of t
49

L A K E DWELLING T R I C L A D S

300

1

50 I

100

Size of

triclad

150

200

population

250 I

I

I

I

0-0

Polycelis tenuis

.. ..

C--l-.-l

I00

rn

..: ..... .,.... .. :.:. ....

IlClII 1121131141

Loke

300

350 .

400

I

450 1

I...D-. 1

,_..I.-.!...I

m

m

FIG.7. The species populations of lochs on Islay in ascending order of total population to illustrate the influence of Polycelis nigm, P . lenuia, and P . f e l i n a upon one another. (Reproduced with permission from Reynoldsoii, 1958a).

species. The low-calcium lakes in which P. tenuis is found occur in areas (Northern Scotland, artificial tarns of the Lake District) where P. nigra is absent. Evidence of another sort was obtained when the P. tenuis population in the College Pond was depleted by removing large numbers for experiments on the peritrich Urceolaria which is epizoic on this species (Reynoldson, 1957); lesser numbers of P. nigra were removed. These removals are referred to subsequently as "predation". Changes in the proportions of the three species in the pond are shown in Table XVI. During 1950-52 large numbers of P. tenuis were removed and by 1952 the proportions had altered considerably. From 1952 to 1956 no TABLEX V Distribu,tion of Polycelis nigra a i d P. tenuis in Lakes of Low Calcium Content <2*5

P . nigra alone P . nigra & P . tenuis P . tenuia alone Total lakes

13 0 6 19

Calcium mg/litre 2.6-5.0 14 2 6

22

6-1-7.5

6

5 2 13

T. B . R E Y N O L D S O N

50

TABLEX V I Changes in the Proportions of Triclad Species du,e to Artijcial Predation on Polycelis tenuis Percentage of total population Sample size

_ _ _ ~ _ _ ~

Before predation After predation (1948-1952)

Polycelia tenuia

.- -.

-

_. .

P. nigra

Dugeaia lugubris

__

-

>500

63

10

13 33

25 67

630 440 400 420 720 400

17 30 41 57 70 55

35 38 28 15 14 15

47 32 31 28 16 30

400

Recovery period (1952-

1954 1955 1956 early 1956 middle 1956 late 1957

“predation” occurred and the species gradually re-adjusted to the initial proportions. Unfortunately it was not possible to measure changes in absolute numbers, so that interpretation must be cautious. It could be argued that the data show nothing more than the recovery of the P. tenuis population without reference to the other species. However, this cannot be so because from 1952 to 1955 both species of Polycelis increased: if it was simply a matter of proportional change due to recovery of P. tenuis, P. nigra would decline persistently. The apparent more rapid response to “predation” on P. tenuis by Dugesia may be explained partly as an artefact due to the use of proportions and partly due to the potentially higher fecundity of Dugesia (Reynoldson, 1961a). Such changes are most satisfactorily explained by the hypothesis that P. nigra initially increased its numbers when competition was less severe as a result of the removal of P. tenuis. When P. tenuis was allowed respite from “predation” after 1952, both species increased at first, but ultimately P. tenuis was able to do so more effectively. The original proportions were reached 4 years after “predation” on P. tenuis ceased. Dugesia reacted in a similar manner. Apart from providing evidence of competition these data are of particular interest since they indicate, for a particular habitat, the period of time necessary for equilibrium to be reestablished among the three species. Further circumstantial evidence of competition was obtained by introducing species into natural habitats. Llyn Teryn is a high altitude

L A K E DWELLING TRICLADS

51

lake oiily 6 acres (2.5 hect.) in area with a relatively large population of P. nigra (72/h). In January 1956, 2 500 Y.tenu,is were introduced into this lake and collections of triclads have been made from it at intervals since. Up to 1063 no P. tenuis had been recovered and it appears as if this species has been unable to establish itself. It may be that the numbers of P . tenuis introduced were too few in relation to Y.nigra to enable it to succeed in this harsh habitat, or, less likely, it has not had sufficient time to build its numbers high enough to be detected. The second experiment of this sort was made in a small springfed pond with a restricted fauna (p. 61) 4 m2 in area in the College grounds. Baiting over 8 days showed that this small pond initially supported about 5 000 P. tenuis. Of these, 1 500 were returned together with 400 P . nigra. Subsequent sampling showed that P . nigra failed to establish itself under these initially favourable conditions; only a few were found 2 years after introduction and these have disappeared since. A similar but smaller introduction of Dugesia lugubris was successful and the implications of this are considered later (p. 61). The final evidence of competition between these two species relates to reproduction. Taylor and Reynoldson (1962) showed that in a habitat containing only P . nigra this species was able to achieve two peaks of breeding, in early spring and late summer. I n a habitat also containing P. tenuis and Dug. lugubris the second peak did not occur. Evidence of competition for food between triclad species belonging to different genera is not so striking, and this may have several causes. Competition is probably not so intense as between congeneric species because the overlap in food is less (p. 38) and it is therefore not so clearly demonstrable. There are no productive lakes which lack Polycelis and yet contain either Dugesia or Dendrocoelum so that any numerical restriction due to the presence of Polycelis cannot be measured. There are lakes containing Polycelis with and without the other two species, but these do not provide such a useful comparison since Polycelis is so dominant numerically whenever it occurs. Also, the fewer lakes containing Dugesia and Dendrocoelum make the comparisons less valid. However, the considerable degree of overlap in food between the species of different genera (p. 38) and the shortage of this resource (p. 40) would be expected to lead to competition at the inter-generic and inter-family levels, and there js some evidence of this. I n presenting such evidence it has been necessary to lump together the data for Dendrocoelum and Duqesia since they are so few taken separately. Table XVIIa compares the increase in total number of Polycelis species with that of Dugesia plus Dendrocoelum over the full range of lakes; and it is clear that the increase in size of the Polycelis population is halted at the point where the numbers of Dugesia plus Dendrocoelum become

TABLEXVII a. A Comparison of the Increase in Pdycelis Numbers with those of Dugesia lugubris plus Dendrocoelum lacteuni b. The Numbers of Polycelis in the Pnesence and Absence of Dug. lugubris plus Dend. lacteum.

.

a

Calcium mg/litre Species Total Polycelis Dug& Dendrowelum

+

Total Po1ydi.a when alone Total Polyw1i.a when others present

<2*5 30.7 0

-

-

2+5-0 104.7 5 *6

b

-

5.1-10.0

10.1-20.0

20.1-40.0

136.3 36.5

250.0 46.4

209.0 141.6

198 68

289 213

224 190

Triclad populations recorded aa number collected per hour averaged for lakes in each calcium category; a dash means no lakes in that category.

__

>40*0 222.3 144.2 222.3

LAKE DWELLING TRICLADS

53

substantial, i.e. within the calcium range of 20-40 mg/l. This suggeststhat the latter two species are curtailing further increase in Polycelis numbers. Table XVIIb compares the sizes of Polycelis populations in the presence and absence of Dugesia plus Dendrocoelum and it is apparent that in all cases Polycelis occurs in smaller numbers when the other species are present. Unfortunately, the few lakes providing data of this kind do not permit statistical analysis to measure significance but the results are in the right direction in each case. The only other evidence of competition relates to a comparison of fecundity in the laboratory and in the field for the planariid species. Both P . nigra and P . tenuis show fecundity in the field amounting to about 5 % of the laboratory value, but in Dugesia the corresponding value is about 2%. Such a contrast is probably explained by the fact that Dugesia is the last to breed and does so under more severe conditions of food shortage following breeding in the Polycelis species. It seems reasonable to conclude that these triclad populations live under a condition of severe food shortage and that competition for this resource occurs not only at the intra-specific level but also at the interspecific and inter-generic levels. This could play a decisive role in determining their distribution and abundance. OF DISTRIBUTION AND VI. THEEXPLANATION ABUNDANCE - A HYPOTHESIS

The four triclad species considered here show many similarities in their ecology such as habitat, feeding mechanism and life-cycle, so that it is convenient to consider the total tricled population as a unit initially and then to treat the individual species and their inter-actions.

A. THE TOTAL TRICLAD POPULATION A relation has been demonstrated between the size of the triclad standing crop in lakes and both the calcium and total dissolved matter of the water. Similar relations based on more qualitative data have been suggested for other littoral organisms such as gastropods (Boycott, 1936; Macan, 1950), leeches (Bennike, 1943; Mann, 1955), Asellus (Reynoldson, 1961b; Williams, 1962a) and tubificids (Kennedy, 1964). However, the phenomenon is even more widespread, extending to other lake communities. Thus bacteria and productivity have been correlated (Hayes, 1961), while Rawson (1960) has demonstrated the importance of the dissolved mineral content of lake water in relation to productivity. Larkin and Northcote (1958) have shown that significant correlations exist between this chemical feature and the amount,of plankton, biomass of benthic animals and fish. While these trends are unmistakable, nevertheless the individual features of a lake may be over-riding and 0

54

T. B. REYNOLDSON

give rise to exceptions based on any single edaphic measurement as emphasized by Larkin and Northcote (Zoc. c i t . ) and several examples of this in regard to triclads have been discussed (p. 15). The evidence already presented shows that the relation between water chemistry and the distribution of triclad species is indirect, which is not surprising for organisms at or near the apex of the food chain. These would be more immediately dependent on the kinds and numbers of their prey, and a closer, more direct relation between biomass and variety of littoral organisms and triclads would be anticipated. It is surprising that such comparative measurements of the littoral fauna are scarce, although Tucker (1958) has shown that the variety and numbers of littoral organisms are greater in calcium-rich, eutrophic ponds. Two sets of such data have been obtained for strongly contrasted lakes, one in North Wales, the other in the Loch Lomond area of Scotland. Both represent crude measurements of the standing crop in the spring and summer seasons respectively. Although Macfadyen ( 1963) has rightly pointed out the limitations of standing crop as an indication of productivity, in this case it is not likely to be grossly misleading since only macroscopic organisms were measured with life-cycles of comparable length. Standing crop is also influenced by the amount of predation on it. However, since predation is likely to be greater in minerally rich lakes, any correction for this would further emphasize the contrast in productivity between chemically poor and rich lakes. The North Wales data refer to five lakes and represent the pooling of independent estimates by nine students. They were obtained in two ways; by removing all the animals from five stones of fist size and by five-minute collections in the shallow littoral. Table XVIIIa shows clearly the relation between calcium, triclad numbers, biomass and numbers of the total littoral fauna. The variety of the fauna in the chemically richer lakes is less striking, but key secondary production such as Gammarus,Asellus and Lyrnnaeapereger was much greater in the minerally richer lakes. The Scottish data were obtained by Dr. J. 0. Young and the author by making a fifteen-minute collection in the stony, shallow littoral zone. The results (Table XVIIIb) show a clear relation between the standing crop of the littoral organisms (excluding triclads) expressed as biomass and the size of the triclad population. The regression coefficient is highly significant (b = 17.5, P < 0.02 >0.005) but this cannot be pressed since only twelve lakes were sampled. It is interesting that this relation is stronger than that between calcium and the triclad population. Rusky is an interesting lake in showing a much larger triclad population than the low calcium value would suggest. But this is matched by a comparably high littoral biomass, although Gummarus, a species not regarded as potential food of planariid triclads unless damaged

TABLEXVIII Comparison of hmbers and Biomass of the Littoral Fauna with Calcium and Triclud Numbers. For method see text

Lake Open Mymbyr Teryn Hendref Coron

Lake Arklett Con Ross *Lochan X Ard ArdGan Mentieth Dougalston +Pond Y Caldarvan

Rmky

Bardowie

Cangllitre

Triclads/hour

0 -4 1.1 0 -4 18.7 !6*5

0 30 72 160 299

a. Five lakes in N. Wales Biomass (gm.) Timed 5 stones 0.02 0.76 0-47 8-69 34-16

0.02 0.40 1-23 3.38 15-73

Number Timed 5 stones 2 46 41 208 650

2 34 29 97 317

Species Timed 5 stones 2 12 13 16 15

2 11 13 12 15

b. Lakes in Mid-Scotland (1963) arranged in ascending order of triclad numbers Caw Triclads Bioaass (gm) Dominant groups lire per h. Species per h. No. Species Biomass Number (8 16 12 20

58 :2 €0 2(8 E4 2 16

40 1f4

0 0 10 56 64 160 164 210 220 300 340 350

0 0 1 1 2 4 2 4 3 4

1 4

0.38 1.52 0 -54 3 -82 4-90 4.60 6 -05 6.45 3.04 6.60 7 -96 6.12

8 41 18 96 85 121 116 83 60 68 95 54

2 5 6 9 13 10 10 10 14 11 9 9

* h h a n X 3 miles (4.8 lon) N. of Drymen. Pond Y

1 mile (1.8km) 9. of Strathbhne.

Ephemeroptera Ephemeroptera Ephemeroptera Eph. Plecoptera Hirudinea Asellus Gastropoda Hirudinea Hirudinea Hirudinea Qammrua Hirudinea

+

Ephemeroptera Ephemeroptera Ephemeroptera Eph. Plecoptera Plecoptera AseUus Chironomus sp. AseUwr Asellus Hirudinea

+

Clammarus

Hirudinea

56

T. B. REYNOLDSON

(Reynoldson and Young, 1963), is numerically dominant. This briclad population is also exceptional in showing an increase since it was sampled 12years ago (Reynoldson, 1958a)when a population of 88/h was recorded compared with 340 in 1962. This was due to an increase in P. tenuis. Apart from the poorest calcium lakes the increase in number of littoral organisms is not marked, the increase in biomass being due to the prevalence of larger species. A similar conclusion applies to the variety of species but the key organisms alter; Plecoptera and Ephemeroptera of poor lakes give way to gastropods and Asellus in richer lakes. Leeches which probably compete with triclads for food, also dominate the richest lakes especially in biomass, along with triclads. Apart from Loch Rushy mentioned above, the variety of triclad species increases with standing crop. The conclusion which seems permissible from these results is that triclad numbers are related to the potential food supply in the littoral zone, and from what has been said earlier, are limited by this resource.

B. PZi? ZRazTzaZkz SPXCZZ# Before considering complex causes of distribution one obvious explanation of the co-existence of the four species in productive lakes must be dealt with, namely the possibility of vertical stratification of micro-habitats. If each species had an optimum micro-habitat a t a slightly different depth which still allowed mixing in the shallow littoral zone, it might not be detected by the sampling method used. However, apart from Chodorowski’s (1959,1960) work in rather different habitats there is no indication of this from the literature (Humphries, 1936; Berg, 1938). Proof that these four species are able to co-exist in the shallow littoral zone of productive habitats is given by their occurrence for upwards of 20 years in several small ponds around Bangor (N. Wales) with depths no greater than 1-2 f t (25-50 cm). Zonation would also fail to account for the reduction in species as lakes become less productive. I n Section V the major components of the triclad environment have been examined and the only factor which seems to be eligible as a determinant of the observed field distribution is inter-specific competition. The evidence of intra-specific competition for food, the overlap in range of food among the four species, the larger population size of species in isolation compared with mixed populations, the scarcity of predators and the resistance to senescence all indicate with reasonable certainty that food is the resource in short supply. This conclusion seems permissible despite the justified view of Mundie (1957) that the influence of single factors tends to be overstressed when they are considered separately and despite the ample demonstration (e.g. Elton and Miller, 1954) of the complex inter-action of organism and environment.

LAKE DWELLING TRICLADS

57

Competition in the narrower sense (Birch, 1957) is often regarded as including two facets, “exploitation” and “interference” (Brian, 1956; Park, 1962). There was no evidence from field or laboratory observations that “interference” is important in these triclads. Since the “exploitation” type of competition enters largely into this discussion some comment on definitions is necessary. Klomp (1961) has recently discussed competition from both the historical and definitive viewpoints, and my reading of his paper is that Birch’s (loc. cit.) and Milne’s (1961) definitions emphasizing a resource in short supply and Klomp’s clear enunciation of the role of a common regulatory factor are all acceptable since they reduce to the same essential. Pontin’s (1963) reluctance to accept Milne’s definition is misleading since he was dealing with the result of a process, Milne with the cause. DeBach and Sundby (1963) have suggested that competition occurs whenever a resource is used by two or more organisms, even when it is abundant. This is a matter of definition, but their view that competitive exclusion (or displacement, as they prefer) can take place when all resources are abundant, is misleading (cp. Solomon, 1957). Their supporting experiments suggest that “local” food shortages (Andrewartha and Browning, 1961) developed; in addition, their technique appeared to incorporate an artificial densitydependent factor. Deternination of distribution (and abundance) by inter-specific competition leads on to this concept of competitive displacement about which a great deal has been written since Darwin. At one extreme we have the improbable (Gilbert et al., 1952; Klomp, 1961) or absurd (Pontin, 1963) situation of different species with identical ecology; such species, if they existed, could not be differentially influenced by any ecological process. At the other, species which as a result of their evolutionary history are so different ecologically that they never compete. Between these extremes are all grades of severity of competition and outcome which may for convenience be reduced to three main categories. There are those situations in which one species will always eliminate another in a particular environment, those in which co-existence is usual, and those where intermittent co-existence is common. Although a mathematical approach to this problem with special reference to Tribolium populations has produced the same three cabgories (Park et al., 1964), the underlying causes may be dissimilar since co-existence in the field is usually associated with special circumstances as indicated below (cp. Pontin, 1961). It is interesting that Park et al. (loc. cit.) were unable to establish conditions for co-existence of T . castaneum and T . confusum in their experiments although a few populations came near to this. Examples from nature of elimination are usually inferred from patterns of distribution in space or time, but as Park (1948) and more recently Klomp (1961) and Hairston (1964) have pointed out,

’

58

T. B. REYNOLDSON

this is not conclusive and needs to be supported by experiment. Displacement by competition has been reasonably established for the special case of sessile animals (e.g. Connell, 1961) and plants (e.g. de Wit, 1960), and recently in the parasitic insect genus Aphytis (DeBach and Sundby, 1963). But the frequent reference in ecological texts to competitive displacement in stream-dwelling triclads (Beauchamp and Ullyott, 1932) a study unsupported by experiments, is symptomatic of the paucity of sound evidence on this matter, especially for invertebrates. In theory, co-existencedepends on one of several possible circumstances. There may be seasonal reversal of competitive superiority for the resource in short supply (Hutchinson, 1948, 1957) which Klomp (1961) has shown to demand density-dependent reaction; overlap in resource may be temporary as suggested by Lack (1946) for birds of prey, or it may be incomplete e.g. Kohn (1959) on gastropods. I n the latter case Andrewartha and Birch (1960) have pointed out the frequent need in laboratory experiments to provide a special niche (space resource) for one of the species if co-existence is to occur, although Utida (1957) was able to achieve this without such manipulation. Intermittent co-existence may occur when the average population level of one species at equilibrium is so low that periodically elimination occurs, for example during a “low” in the course of natural fluctuation; an aspect often overlooked in this context. Here, dispersal will re-establish the less successful species from time to time (cp. Skellam, 1951). Comparable examples illustrating these several categories were discussed for plants by Harper et al. (1961). With this short summary of competition and co-existence as a background we can now consider the special case of lake-dwelling triclads, bearing in mind that any hypothesis must explain exclusion a t one end of the habitat series and co-existence at the other. Study of the food of the four triclad species has shown that while there is considerable overlap in prey organisms nevertheless species representative of the three genera show some distinct contrasts. Thus Dendrocoelum lacteum is a more active hunter than the others and is able to capture Asellus so that in any competition which may develop for this prey it will be at an advantage. Dugesia lugubris alone feeds on gastropods to a considerable extent and this type of prey therefore provides a “food refuge” for it. Polycelis sp. tend to feed more on oligochaetes than the other species but they do not appear to have any special “food refuge” and indeed may not have been under any selective pressure to develop one since they are the most successful triclads. Thus each of these triclads would be expected to co-exist in habitats which provided sufficiently large populations of the more specific prey organisms. Correspondingly,if one or more of these “food refuges” are absent or too small then competition might be expected to proceed to elimination.

59

L A K E DWELIdINO TEICLADS

TABLEX I X The Distribution of Two Main Pwy Or
a. Lymnaea and Hydrsbia together (:a (mgllitre) t5.0 5.1-10.0 -~~

N. Ireland Mid-Scotland N. Wales Shropshire Total

014 3/11 2/14

N. Ireland

014 011 1 2/14 111 3/30

111 6/30

> 10.0

114 515 111 111 8111

8/11 13/15 9/12 11/11 41/49

114 415 111 111 7/11

711 1 11/15 12/12 11/11 41/49

b. Asdlus

Mid-Scotland N. Wales Shropshire Total

It would appear therefore that the key to understanding the distribution of these triclad species is LO be sought in the faunas of the lakes, and these have been examined from data collected a t the same time as the triclad observations. Table X [Xrecords the distribution of the two main types of prey providing “food refuges” in relation t o calcium. Although presence and absence cannot be pushed too far on such brief searches, the pattern shown for A s e h s (Reynoldson, 196lb) has been confirmed by Williams (196%~). These data show that as lakes become less productive the main “food refuges” of D.lncfeum and Dug. lugubris become fewer; fiirthermore the populations probably become smaller before disappearance. Thus Hunter ( 1957) has stated that although Lymnaea pereger occurs in the less productive north basin of Loch Lomond it is several times more iL5undant in the more productive lower basin; similar examples of this could be quoted from our own observations. It is clear from Table X LX that there is a broad parallel between the distribution of a particular ti-iclad species and its “food refuge”. The case of Dendrocoelum and Asellus has been analysed more fully (Young, 1963). The results (Tablo X S ) show conclusively (P < 0.001) that Dendrocoelum is usual y f m n d only in lakes containing Asellus. The few occurrences of Asellues without Dendrocoelum may be attributed to either the shortcomings of the data, the incomplete distribution of the triclad even in the most f s v o ~ r a b l habitats t or the small size of the Asellus population. Records of Dcndrocoelum in lakes without Asellus, all from N. Ireland habitats, may mean that under certain conditions it can co-exist with other triclad species in the absence of Asellus

60

T. B. REYNOLDSON

TABLEXX The Comparative Distribution of Asellus sp. and Dendrocoelum lacteum Asellus Present Absent Total

Dendrowelum Present Absent 31 7

38

7

41 48

but is more likely to be an artefact due to limitations of the data. The hypothesis that the occurrence of Dendrocoelum in the presence of the other triclad species is dependent on Asellus as a “food refuge” is also supported by consideration of the anomalous lakes in the relationship between triclad distribution and calcium. These are the artificial LIyn Mair (N. Wales) with 2.4 mg/litre calcium and Newton Mere with 5 mg/ litre. Among the large lakes the occurrence of Dendrocoelum in Loch Lomond with 3 mg/litre and Lake Windermere with 5 mg/litre come also into this category. Since Asellus occurs in these lakes also outside its normal calcium range in Britain it would provide the necessary “food refuge” for Dendrocoelum. The more frequent penetration of Dendrocoelum into low-calcium lakes in Fennoscania (Reynoldson, 195%) is again paralleled by a similar penetration by Asellus (Reynoldson, 1961b in Discussion). Some recent work by Mr. I. R. Ball on the triclads of streams and ponds in Cambridgeshire and nearby counties supports this view. He has found (private communication) that of thirteen localities with a triclad fauna, the eight which contained Asellus in numbers also supported Dendrocoelum usually with other triclad species. Of the remaining five, one contained a few Asellus, the rest none. This close link between the triclad and main prey raises the question whether we are dealing with a specific dependence on Asellus or a non-specific one. Consideration of the food of Dendrocoelum which includes a wide range of organisms (Reynoldson and Young, 1963) supports the latter view, and here it is assumed on the basis of both similarity in food and feeding mechanism that if one species of triclad can maintain a sizeable population in a particular lake, then any of the others can do likewise in isolation, but field experiments have not been completed to test this. Differential temperature effects may demand some qualification of this generalization but not in the case of ~ e ~ r o coelum (Repoldson et al., 1965) which is the most tolerant Of low ternperatures. Dugesia lugubris also occurs in Newton Mere, Loch Lomond and Windermere outside its normal calcium range and this is also

L A K E DWELLING TRICLADS

61

paralleled by the presence of snails. The importance of this type of prey was nicely illustrated by a simple field experiment. Previously (p. 51) reference was made to the failure of Polycelis nigra to establish itself in a small P . tenuis habitat ‘which contained largely Asellus meridianus, Hydrobia ( = Potamopyrgus)jenkinsi and Luwi,briculus variegatus. When the comparable experiment was done with Dugesia, although the initial numbers introduced were smaller than in the #caseof P . nigra, 250 compared with 400, it had no difficulty in establishing itself and this is attributed to the presence of Hydrobia in lslrge numbers. The broad relationship suggested between the distribution of gastropods and Dugesia is also supported by the work of Boycott (1936), Macan (1950), and Hunter (1957) on snail distribution, but it is worth mentioning at this point that the rapid spread of Hydrolrict in Britain (Hunter and Warwick, 1957) may well influence the futurls distribution of Dugesia, because this snail is more tolerant of unproductive habitats than the common species Lymnaea pereger. This may make less productive habitats available to Dugesia. The overall picture presented here suggests that as lakes become less productive the total hriclad population declines and ultimately disappears because of food shortage. The parallel restriction of species, ultimately to Polycelis wigra, is due to the lesser numbers and variety of prey so that “food refuges” become smaller and eventually disappear, forcing the triclads to compete for the same food resource to an increasing degree. An explanation of the co-existence of Polycelis nigra and P. tenuis is more difficult although evidence of competition between them is more obvious, both features resulting from the c1oc:e taxonomic relationship. The elimination of P . tenuis a t low calcium levels and the reduction or elimination of P. nigra at high levels is almost certainly due to competition for food; their co-existence in lakes of intermediate type suggests incomplete overlap of food. This was not demfonstratedconvincingly by the study of feeding, but it is to be expected because of close taxonomic relationship that any difference might be slight and difficult to detect. In this connection it is interesting to note that P. nigra fed more extensively than P. tenuis on Plecoptern (Reynoldson and Young, 1963), a group characteristic of unproductive lakes, but this needs further testing. A second point is that lakes containing only P. nigra seem to have a rather smaller population than those containing P. tenuis in addition (Table XIVa), suggesting that the two species together are able to tap a wider food source. A third point is that co-existence seems to be more difficult in the most, productive lakes, for example in Shropshire P.nigra was not recorded in 5/12 meres. Here the faunas are likely to depart farthest from those of unproductive lakes and therefore would suit P. tenuis more. Although some aspect of their ecology other than C*

62

T. B . REYNOLDSON

food might be involved, this seems unlikely in view of their similar biology; but Harper (1964) has made the point that biology is not always an adequate basis on which to forecast ecological interactions. This work started from a correlation established between the chemical condition of lakes and their triclad faunas. We now know that this is a very indirect relation which nevertheless was detectable through a food chain of at least three trophic levels, a fact which illustrates the over-riding influence of the physico-chemical background of the environment. It follows that for a complete understanding of the distribution of triclads it will be necessary to follow the food chains back to the primary producers. Again, looking beyond the hypothesis suggested here which is now being tested experimentally in the laboratory and the field, it will be ultimately necessary to consider the reasons why a particular species is successful or unsuccessful in the struggle for existence. It is at this level of inter-action that other modifying factors of the environment such as temperature and water chemistry may operate differentially. AND SUMMARY VII. CONCLUSIONS

The four main lake species of triclad, Polycelis nigru (Mull.), P . tenuis Ijima, Dugesiu lugubris (0.Schmidt) and Dendrocoelum lacteum (Mull.) all occupy the shallow littoral zone and feed on other organisms found there. The feeding mechanisms of all are similar and there is wide overlap in the type and size of prey eaten by them and also by the young and adults of the same species. At the species level, triclad populations show restricted fluctuations in numbers and live under conditions of food shortage for long periods of the year. Numbers are regulated by intra-specific competition for food, which stems mainly from two biological properties: high resistance to death by starvation because of their ability to resorb and then regenerate tissues, and a high degree of immunity from predators. The triclad populations of lakes vary in size from complete absence to very high numbers and there is a general, positive correlation with both the calcium content and the total dissolved matter of the water. The pattern of species distribution is also related to these factors. The relation is indirect and triclad abundance is determined primarily by the amount of food available in the littoral zone, itself ultimately dependent on the water-chemistry. The distribution and abundance of the individual species of triclad are determined primarily by inter-specific competition for food. The outcome depends upon the pattern of distribution and abundance of certain numerically important types of prey because, despite the high degree of overlap, each triclad species feeds on a particular kind of prey

LAKE DWELLING TRICLADS

63

to a greater extent than the others, i.e. each lhas a “food refuge”. Thus Dug. lugubris alone feeds upon gastropod molluscs, Dend. lacteum captures Asellus most efficiently and Polyeelis species take more oligochaetes . It is suggested that because these import$iit food organisms become both less numerous and less varied in the littoral zone as lake productivity declines, the triclad species are forced to compete with increasing seventy. As a result, lakes of low productivit:r (minerally poor) support smaller numbers of triclads and fewer species than lakes of high productivity (minerally rich). Thus only P.nigru exists in the poorest lakes while all four species co-exist in the richest lakes. The basis of coexistence of P. nigru and P. tenuis in all but the poorest lakes has not been established, but it is probably due to a “food refuge” difficult to detect because of the very similar nature of %heirfood. It is important to emphasize that competitive displacement depends not only on the ecological properties of the organism but also on the properties of the habitat. For example, in unproductive lakes all the triclad species are effectively ecologically similar in their food, in productive lakes this is not so.

ACKNOWLEDGMENTS I wish to acknowledge the help of Dr. J. 0. Young who was my assistant for three productive years and also his permission to use the data on littoral organisms collected jointly. The following people kindly helped either by collecting and sending me triclads or making observations on their occurrence in the remoter places; Dr. M. Angel, Dr. R. Carrick, Mr. R. C. Connolly, Dr. Llyr Gruffydd, Mr. H. G. Lloyd, Miss S. MacLachlainn, Dr. A. Milne, Mr. P. Langton, Mr. R. J. Spittle, Mr. T. Warwick and Mr. D. R. Williams. I have also to thank Mr. F. J. Mackereth for providing some of the chemical data. I am grateful to Dr. A. G. Dahm and Dr. (3.B. Corbet who gave me the benefit of their advice on the historical aspects of distribution and to Dr. P. O’Donald who advised on the statistical analysis of Dr. Mirolli’s data. The manuscript was read for me by Mr. L. H. Jackson to whom I am grateful for several improvements. The Department of Scientific and Industrial Research have generously provided money for an assistant during the last three years and are continuing to do so. I am grateful to the Nature Conservancy and the Royal Society who financed a major pan; of the travelling incurred by the field work. I also wish to thank the Leverhulme Trust for the grant which enabled me to study triclads in Sweden and N. Ireland. Finally, I wish to thank Professor F. W. FCogers Brambell, F.R.s., for his encouragement and support at all times, *

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Young, J. O., Morris, I. G. and Reynoldson, T. B. (1964). Arch. Hydrobiol. 60, 366-373. A serological study of Asellus in the diet of lake-dwelling triclads. Young, J. 0. and Reynoldson, T. B. (in press). 0i.kos. A quantitative study of the population biology of Dendrocoelum lacteccm (Miill.) (Turbellaria, Tricladida). Young, J. 0. and Reynoldson, T. B. (1965). Hydrobiologia 26, 307-313. A laboratory study of predation on lake-dwelling triclads.

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Energetics, Terrestrial Field Studies,

and Animal Productivity M A N F R E D D. E N G E L M A N N

Department of Natural Science, Michigan State University, East Lansing, Michigan, 1J.S.A.

..........................................................

I. Introduction 73 11. Three Approaches to Energetics Studies.. ................................ 74 111. Historical Considerations.. ............................................. 78 IV. Physiological Studies Which Yield Energetics Infcmrmation. ................. 84 V. Studies Concerned Primarily with Maintenance Metabolism of Population8 in the Environment 87 VI. Studies Which Emphasize the Trophic Scheme Analysis of Communities. 96 A. Trophic Dynamic Analysis of the Salt Marsh Ekotone 96 B. Trophic Dynamic Analysis of “Old Field” Communities.. 98 C. Trophic Studies in a Savannah Community.. ......................... .lo3 VII. Projection ............................................................ 108 References ................................................................ 112

.................................................... .... .................. ...............

I. INTRODUCTION There is currently a feeling among ecologists that their science has reached maturity, and that the concepts and knowledge of this science are destined to shape the future of our burgeoning human population (Sears, 1964; Odum, 1964; Blair, 1964; Cole, 1964; and others). These scientists consider ecology to be a “respectable” science for reasons ranging from the fact that problems of ecology are concerned with practical considerations (such as atomic fallout, overpopulation, pollution, and pesticides) to the fact that the ecologisI;s are using models, both mathematical and verbal, to guide future experiments. I n this age of an accelerated pace of human events and immense social prmsures, a p p mium has been placed upon the directed approach and rightly or wrongly scientists are called upon to justify their studies and indicate their importance either to the body of knowledge called science or to human problems, or both. If ecology, then, is to be a part of the new trend and to be in the mainstream of science and human destiny, ecologists must 6 the human effort. justify their science and elucidate its importrince t The goal of this paper is to evaluate the growth and development of 73

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terrestrial energetics at this point in its history. The task is by no means a small one. Even though the accumulated literature a t present is rather limited, the studies that have been reported are recorded in many different journals covering diverse approaches to ecological research. In this article, the subject of field estimation of productivity will be approached in three ways: first, the historical and theoretical bases which undergird terrestrial productivity studies will be considered; second, the various works in the field will be reviewed, with particular emphasis upon the relationships of the papers to one another and the type of data each yields; finally, the progress of terrestrial energetic studies as a whole will be evaluated and areas wherein critical research is needed will be indicated. I must admit that I face some difficulty performing the task set before me with necessary thoroughness, especially with respect to the final point. However, I hope that my efforts will give others further insight into the problems in the field and thus enhance its progress.

11. THREEAPPROACHES TO ENERGETICS STUDIES There are probably three main approaches to the problem of field estimates of animal production. The preceding statement is qualified because the word productivity has various interpretakions. Not one of the definitions given in Webster’s Unabridged Dictionary would suitably characterize the highly specialized nature of “production” as used in the field of energetics. The cattlemen and farmers use the word to mean such measurements as number of head or bushels per acre, the biologist refers to number of individuals born per unit time as “production”. Most of the time, the ecologist also employs the latter meaning when constructing life tables or dealing with other aspects of population. However, when the term calorie is considered, the terms production and productivity take on more restricted meanings. The restricted meaning, moreover, was not immediately recognized, but evolved slowly through the 1930’s and 1940’s. Variations in the use of these terms by different authors are eloquently summarized by Macfadyen, 1963a, pages 160 and 161. His table, clearly demonstrates why the term productivity provokes a confused response from “production scientists”. To avoid many of the difficulties raised, I wish to sidestep the issue by stating the two definitions of productivity used in this paper. They are: (1) net productivity, the number of calories represented by the new individuals and the increase in weight of the population per unit of time; and, (2) gross productivity, the total number of calories expended by the population in maintenance, i.e. respiration, plus the calories represented by numbers produced and increase in population weight or biomass. In referring to the three main sources of productivity information, then, I

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am specifically referring to that portion of the literature which is concerned with caloric values and transfers. The first major source of information on energetics of natural communities has its origins in physiological studies dating from the investigations of Lavoisier in the late 18th century. They emphasize the homeostatic mechanisms of the organism, the iinvestigator exploring the individual’s response to an environmental stress. Some aspect of the animal’s metabolic rate is measured during the various stress situations. When respiration rate or heat production is used as the measure of response of the animal to stress, the data aro potentially useful in an energetics analysis. The stress studies themselves, however, are usually not sufficient for energetics analysis because field data on numbers or biomass are lacking. The studies of the physiological ecologist (or the ecological physiologist) are concerned primarily with the individual and form a tremendous and diverse reservoir of information, useful in making field estimates. The second major source of information on energetics of natural communities comes from analysis of maintenance energy by what I refer’ to as the “Bornebusch” approach, which is b,ased on the assessment of three key parameters -numbers of individuals, biomass, and oxygen consumption. When these parameters are known for different populations in the field or for different communities, the resulting data can then be used to compare the impact of the dijfferent populations on the community or the relative amounts of energy flow through the different communities. The key factor in a Bornebusch type study is comparison of the total metabolism of different populations as reflected by respiration rates. Respiration rates can be a sound means of comparing populations, because in most animals about 70% of the assimilated calories are used for maintenance and thus show up as respiration. From the community point of view, all of the calories captured aa radiant energy will eventually be dissipated as heat via respiration (exceptions are peat bogs and rapidly buried organic deposits). On the other hand, population or community analysis using species diversity or numbers presents great problems. Here we are comparing unlike elements and more or less objectively making them equivalent, i.e a species as a unit. The Bornebusch approach utilizes units which are common to all animals and plants, i.e. mass and respiratory metabolism. Thus, the comparisons are less subjective. The third approach to this subject of energetics of natural communities comes from the trophic-dynamic or Undeman school of community metabolism. The guiding principle in this type of study is the Lindeman (1942) model. It consists of a flow diagram of energy made up of the following components: A,, the energy coming into a trophic or feeding

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level of the system in the form of food or sunlight; A,, the energy found in the bodies of individuals which make up the trophic level, i.e. the standing crop energy; R,,the energy lost to the trophic level in respiration; D,, the energy lost to the trophic level by way of the decomposers; and Adl, the energy lost to the trophic level from consumption by the next trophic level (see diagram). The flow diagram is in turn based upon several laws and assumptions. They are as follows: (1) the laws of thermodynamics hold for plants and animals; (2) plants and animals can be grouped together into trophic levels according to their feeding habits; (3) there are at least three trophic levels (there may be more) which are: (a) producers (green plants) ; (b) herbivores (animals feeding upon the green plants); and (c) ca.rnivores (animals feeding upon the herbivores); and (4) the system is in equilibrium; and ( 5 ) calories are the basic units of the trophic scheme. From these assumptions, it can be deduced that: (1) each succeeding trophic level will have fewer calories than the preceding one, and (2) that there is a finite number of trophic levels. I n a steady state condition, A,, will equal the sum of R, D, Adl. For increasing or decreasing populations, A, will equal R, D , hdl AA,, where AA, is the increase or decrease in energy of the standing crop. However, the Lindeman model is not designed to

+ +

+ +

+

TO NEXT TROPHIC LEVEL

Fra. 1. Schematic representation of the Lindeman Model. The drawing depicts a single trophic level with the energy flow indicated by the arrows. For a complete representation of the trophic levels of an “old-field’’community see Engelmann, 1961, p. 236.

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handle situations of imbalance because of the equilibrium assumption. A very important point should be emphasized here, one that is most apt to cause confusion when discussing the Lindeman model. A body is made up of both matter and energy. The energetics approach is concerned only with energy, not the matter. The matter is recycled through the biosphere, being used again and again through successive ages. Energy is not recycled by the biosphere. Each time organisms transfer potential energy from one trophic ievel to the next, a portion of the energy is lost in the transfer, never to be regained by the system. Thus, when we speak of standing crop, we are concerned not with the matter this represents but with the amount of energy necessary to hold that matter together. The trophic dynamic approach to the problem, then, is concerned primarily with food relationships (i.e. the food of the community), the assignment of populations to food levels, and the total energy flow through an area or community. A complete analysis of this kind results in an energy balance sheet for the community and therefore should give a number of internal checks on the consistency of the various estimates of energies. If a model is to be a useful guide t o further research, it must have particular characteristics which result in logical deductions and predictions. Three important criteria for judging whether a model will result in useful information are as follows: ( I ) the internal consistency of the model; (2) the number of important testable hypotheses resulting from the model; and (3) the relevance of the inodel to existing concepts and hypotheses. How does the Lindeman model hold up under these criteria? Slobodkin (1962) has indicated that Lindeman’s model is more or less internally consistent and leads to testable hypotheses. This model immediately raises three testable questions, which are: (1) What is the maximum number of food links in an a,rea? (2) Is there a characteristic ratio between the calories contained in one trophic level and the calories contained in the succeeding level? and (3) Are there any consistencies between the ratios of the productivity of a species and that of its predators? Criterion three mentioned above (the clarification and integration of existing concepts and hypotheses) seems also to be met at this stage of our knowledge by Lindeman’s model. It fits logically with the concept of community. If the community is-real, then energy flow within community boundaries will be much greater than across community boundaries. Therefore, the tool for more certainly delimiting and defining communities may be within the ecologist’s grasp. It is very likely that the Lindeman model or some modification of it will give us a better understanding of the community concept. Other ecological concepts can be re-evaluated by use of the energetics a,pproach.For example, the

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subjectively determined, dominant, characteristic, influential, conspicuous, and rare species categories can be given a more objective basis using energetics criteria. A species with a large number of slow metabolizing individuals may be less important to the community than another species with fewer metabolically or reproductively active individuals. Finally, the Lindeman model depends heavily upon natural history observations, life tables, metabolic data, phenology, physiology, and, in short, the majority of the factual information accumulated from natural communities over the years. This model, though imperfect, can give a new dimension to the old concepts in ecology. There are, of course, other models in the ecological literature which are designed to define and characterize elements of certain ecological concepts (e.g.MacArthur, 1960; Hairston, 1959; Hairston et al., 1960; Patten, 1959; et cetera). All of these are of value in our present stage of knowledge. Some models may eventually have greater significance than do those based on energetics. Others may contribute much to the Lindeman model. Of course all of them are subject to a great deal of debate, and the resolution of the debate will come from a conclusive experiment or observation. As has been pointed out by Slobodkin (1962) and will be underlined again in this paper - the paucity of the data in the field of energetics at this time emphasizes the need for research rather than discourse.

111. HISTORICAL CONSIDERATIONS At first glance there is a parallel between the spread of the study of energetics in ecology and the evolution of the vertebrates. Both had their origins in fresh water and then spread to the sea, but only with reluctance did they clamber to the land. It required 20 years from the beginning of the productivity studies t o the enunciation of the guiding principles of those studies and it required another 20 years for those studies to spread to terrestrial situations. Although the work of Birge and Juday laid down the beginnings of productivity studies in 1922 and the trophic dynamic approach was proposed by Lindeman in 1942, the first major work on terrestrial systems did not appear in the literature until 1960 when Golley published a Microtus food chain analysis in the Lindeman tradition. The limnologists and oceanographers during the forties and fifties produced numerous works on freshwater and marine habitats. The terrestrial biologists were not completely inactive during this period, for Bornebusch (1930) did his classical study on beech forests in Denmark. He paid attention not only to the number of individuals in each species but also to their weights and respiratory rates. It was apparent to Bornebusch that the different rates of metabolism of the

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different species populations could alter their importance to the community. His methods, however, were not utiltced by others working on natural communities and his work remains a solitary landmark in the literature. To be sure, the engine-like nature of the living organism was elucidated by Lavoisier in 1777 and many workers through the years turned their attention to the bioenergetics of animals. All these works, however, were concerned with single individuals of either man or domestic species (Atwater and Benedict, 1903; Armsby, 1903; Brody, 1945).

Ecologists of the 1940’s and 1950’s presumably had the techniques and information available to carry out energetic studies on terrestrial communities. Why were not these studies carried out earlier? There is no certain answer to this question, but part of the explanation lies in the different characteristics of the two major envJronments (terrestrial versus aquatic), as well as in the elements of human whim and communication. The aquatic environment is easily definable with rather clear-cut boundaries. The majority of the physical components of the liquid environment can be measured by simple chemical tests. The portions of an aquatic environment stay relatively congtant during the die1 cycle and have a limited range of variation during the annual cycle. Last and by no means least, most aquatic environments have a biota which is taxonomically well defined and not tremendously complex. On the other hand, the terrestrial situation is very complex. For example, moisture variation from day to day and place to place has a tremendous influence on the biota of an area and poses a formidable measurement problem for the investigator. Moisture can precipitate in an area in the form of rain, snow, sleet, or dew, and can be lost in the area as run-off or evaporation. A single aspect of the moisture content of the air can be recorded as relative humidity, vapor pressure, saturation deficit, absolute humidity, specific humidity, and mixing ratio (Platt and Griffiths, 1964). The obvious variability of the physical terrestrial environment is one of the deterrents to a complete energetics study. The biological elements of this environment further complicate the matter. Many of the taxa important to terrestrial communities are poorly known. It has been stated in the literature that there are about 650 000 species of described insects in the world (Metcalf and Flint, 1939), and it is estimated that 2 500 000 species exist at this time. The insects are an important component of every terrestrial community, both from the standpoint of numbers and of ,activity. Thus, almost half the species present in the natural community are not as yet recognized by science. Taxonomically, the insects are well knQwn when compared to some other taxa such as mites or nematodes. Furthermore, the number of species present in any single area may be great. Evans (1964), for

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example, reported 1 700 species captured from the herb strata of an “old field” in Michigan. Two hundred and sixty of these species occur commonly and were believed to represent the resident fauna of that field. Hairston (1959) and Hairston and Byers (1954) recorded 271 species of arthropods found in the soil of the same “old field”. For this 15-acre field in southern Michigan then, nearly 2 000 species of arthropods have been recorded, of which about 320 are part of the normal resident fauna. The task of keeping the species categories separated during energetics analysis is formidable. The problems which made terrestrial communities less suitable for energetics studies in the 1940’s are still present. The need for making such studies is becoming more evident and more urgent, and thus these pioneer studies set forth the first crude guides to the methods necessary for such an endeavor and yield data which begin to define the limits of the problem. To make a complete energetics analysis we must have estimates on ingestion rates, assimilation rates, egestion rates, respiration rates, growth rates, death rates, numbers and biomass, and the calories represented by these figures. None of these parameters is directly measurable in the laboratory or field but must be calculated from several kinds of data. Paradoxically, a good portion of the data necessary for field estimates must come from laboratory studies. If energetics studies are to be properly evaluated, it is essential to understand the general procedures of obtaining the relevant data. Measurement of ingestion rates requires knowledge of the amount of food the animal consumes during a certain time period and the caloric value of the food consumed. If the amount ingested cannot be measured directly in the field, estimates must be made from ingestion data on animals in enclosures or in culture cages. Direct measurements of assimilation rate must be done in the laboratory, but this parameter can be estimated from an equation when ingestion and egestion rates are known. It should be noted that every rate estimated from an equation eliminates one of the internal checks inherent in the Lindeman system. The calories egested are not important to the particular population or trophic level which “produce” them, but the feces are important for the decomposer system since they make up part of the energy source of the decomposers. Energetically, feces contribute no calories to the population for performing work and require only that the organism expend energy to move them through the digestive tract. The animals which can move great quantities of non-utilizable material through the digestive tract with small amounts of energy would of course have some adaptive advantage, but present methods used in energetics studies are not sufficiently refined to answer such questions.

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The respiration rate represents the maintenamce portion of the energy budget, that portion of the assimilated food necessary to keep the organism together and functioning. Respiration can be estimated by measuring either oxygen consumption or carbon dioxide production. There are numerous devices which measure oxygen uptake, but they generally fall into three major types: the constant pressure, constant volume, and differential (Dixon, 1952). The most widely used apparatus in tissue culture study is the constant volume type represented by the Warburg respirometer. Yet in most of the energetic studies at present, some form of a constant pressure apparatus is employed. The major exception to this statement is found where very small organisms (mites, collembola, etc.) are concerned, and then the Cartesian diver apparatus (a constant volume type) is used. Several studies employ some method of estimating respiration rate by CO, production. This usually involves capturing the CO, in a standard basic solution, thus converting the base to a salt and then titrating the remaining base with an aoid standard. It must be kept in mind that in energetics studies the number of units of 0, respired is not so important to know as the number of calories represented by this respiration, because it is an estimate of the amount of heat the population loses in the process of maintenance. Conceivably, it should be possible to measure the heat production directly via calorimetry in the field. However, at present the technique required for direct field calorimetry has not yet been attempted. Growth rates are measured either in the 5eld or in the laboratory where the animals are kept in cages or culture,g.Each approach presents problems. I n the laboratory, growth rates ca2 be measured very accurately, but the conditions under which the animals are kept are not those of the field. Field studies, on the other hand, have the advantage of natural surroundings, normal activities, and usual diets, but present the problem of measuring and keeping track of the growth rates of particular individuals. Still another approach to the measurement of growth rates is that of deducing them from the numbers of individuals found in various size categories during successive field samplings. This approach is particularly useful for the meiofauna and the microfauna where marking, release, and recapture techniques have not yet been worked out. Data on death rates are obtained in the r3ame way as are data on growth rates. Cage or culture studies, however, yield only data on deaths resulting from physiological limitations, and the survival rate is higher than that found in field populations due to the absence of predation. The most reasonable approach at this time seems to be the construction of a life table (Allee ct al.,1949, page 265) from laboratory or enclosure data, and the adjustment of this table to field conditions. One of the most complete life tables we have for ,an animal other than man

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is that of the human louse, Pediculus humanus (Evans and Smith, 1952), yet no one has yet seen fit to work out the energetics of this animal. Complete life table data are very hard to obtain, but yield estimates of standing crop and turnover rates, these being far superior to the estimates derived from simple field counts. The entire field estimate depends ultimately upon the estimate of the numbers of individuals present in the area. A large amount of literature has accumulated concerning the many and varied techniques for sampling populations. The techniques vary with the type of terrain and the kind of animal being sampled. Dice (1952)and Macfadyen (1963a)among others have written good general chapters on sampling techniques. Each investigator, however, has his own modification of some existing technique made necessary by the kinds of animals and the terrain encountered as well as by the time, materials, and money available to him! Several other estimates (e.g. total numbers of individuals present during a period of time, biomass, standing crop, age and/or size classifications, and total respiration per annum) are derived directly from the number of organisms counted in the field sampling program. Thus, it is important that these counts be as accurate as possible. When field data on numbers are not accurate, as in the case of Bornebusch (Birch and Clark, 1953), the study loses a good deal of its usefulness. As previously stated, numbers of individuals, per se, are not useful’to the energetics analysis and, thus, conversion must be made to energy units. The information necessary for the conversion is: (1) the weight of each individual and (2) the calories represented by the weight. Weight or biomass, then, is the intermediate step between numbers and calories. Under certain circumstances, weights are assigned from graphs or equations relating some aspect of size to weight. Dry weight or live weight may be used, but dry weight is preferable because it eliminates the possible variation in water content of the individual. The weighed material must then be burned in a calorimeter to obt9in the equivalent calories. Lists of energy values for various animals and plants have been compiled by Golley (1961) and Slobodkin and Richman (1961). Average values derived from such lists are often used where direct calorimetry cannot be undertaken by the investigator. Aside from the techniques neceasary for making energy estimates, there are also several ratios or relationships which are useful in comparing different species, populations, or communities. Three such ratios appear to be important to the studies of energetics of terrestrial animals. The first,relationship is more or less characteristic of the individual, the efficiency of digestion. The efficiency of digestion can be calculated also for a population and, thus, can be used in a broader sense; however, it is ultimately based upon each individual’s ability to consume and assimilate food. The ratio is

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defined as follows: the efficiency of digestion ia equal to the number of calories assimilated divided by the number of calories ingested. This ratio is important because food consumption in the field is difficult to measure directly. If the investigator has information on either the amount of ingested material or the growth plus the maintenance amounts, then the formula for digestive efficiency can give him some estimate of the food ingested during the period of time in question. The second ratio of importance to energetics studies is the relationship between metabolic rate and weight of the animal. This is used also as a predictive tool in an effort to estimate respiratory rate or metabolic rate when only the weight of the animal is known. The general formula for this relationship is: M = aWb, where it1 represents metabolic rate, W is the weight of the individual, and a and b are constants. The value obtained for the constant b in a set of experiments can be used to compare the metabolism of two animals. Theoretically, a and b should be constant, and b should be equal to 0.67. However, this is not actually the case, and the formula for the weight mei;abolism relationship becomes a comparative as well as a predictive tool. The third ratio is one characteristic of the .Lindeman or trophic efficiency model. When this ratio was first proposed by Lindeman (1942) he called it “progressive efficiency” and defined it as A, divided by An-l times 100, where A, was the number of calories ingested by the organisms feeding on An-l, and An-l is the number of calories ingested by An-l. Hutchinson (Lindeman 1942) called this the “true productivity’’ of the energy level. Slobodkin (1960) recognizing the confusion surrounding this important ratio renamed it “eco!’ogicalefficiency”. Patten (1959) in his paper on cybernetics and energetics renamed this same ratio the “efficiency of transfer of ingested energy”; Davis and Golley (1963) called it “utilization efficiency”; while Wiegert (1964) pleading for uniformity in nomenclature and for names which outline the important features of the efficiency ratios, introduced the title of “gross efficiency of yield divided by ingestion”. The term “ecological efficiency” seems to me to be the most convenient and the least ambiguous and I shall use it when discussing the ratio of the number of calories removed by the predators (A,) divided by the number of calories ingested by the prey (An-l) times 100. Note that the ecological efficiency does not compare gross productivity of two successive levels, but rather compares the ingestion rates of the two successive levels. Ecological efficiency, then, is an important ratio when one community is compared with another, as well as when two trophic levels are compared. The ratio is primarily important to the Lindeman model rather than to any practical applications by man. There are other comparisons in the form of efficiency ratios, made by the trophic analysis, Patten (1959). It may

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be that through increasing knowledge one or more of these ratios will become more important to the ecologist studying the energetics of ecosystems as well as to the production manager. However, at this stage, the three relationships listed above seem to be the most important; discusion will be confined to them. Using the approaches and ratios listed above as a framework, we can now look at the research in the field in an effort to: (1) understand what has been done or attempted to date; (2) view data thus far accumulated on net and gross productivity in terrestrial communities and (3) evaluate the information in terms of theoretical and practical objectives.

IV. PHYSIOLOGICAL STUDIES WHICH YIELD ENERGETICS INFORMATION I have set a rather arbitrary limitation on my discussion of the physiological literature. I will consider chiefly papers which either have used another author’s field data, made estimates of field energies, or have provided physiological data used by other researchers in making field estimates. Several studies have reported oxygen consumption a t various temperatures: for a spider, Lycosa pseudoannulata (It6, 1964), the collared lizard, Crotaphytus collaris (Dawson and Templeton, 1963), crossbills, Loxia curvirostra sitkensis and L. 1. leucoptera (Dawson and Tordoff, 1964), the eastern cardinal, Richmondena cardinaZis (Dawson, 1958), the English sparrow, Passer d . domesticus (Kendeigh, 1944 and 1949) and Emberiza (Wallgren, 1954) and several rodents including Zapus, Eutainias, Microtus, and Glaucomys (Morrison and Ryser, 1951), Dipodomys and Citellus (Dawson, 1955). Other studies deal with food consumption in relationship to temperature (e.g. Sealander, 1952) or with food utilization and digestion (e.g. Waldbauer, 1964; Gere, 1956a, b; Van der Drift, 1958). Still others have done notable works compiling great areas of knowledge, such as the books or chapters by Brody (1945), King and Farner (1961). Several of the papers are worth particular note. It6 (1964) is one of the few whose writing concerned some aspects of the energetics of a predator. Using a microchemical technique for carbon dioxide production, It6 was able to estimate energy utilization of the spider which averaged about 35-81 g cal/g (live weight)/day, or about 150-94 g cal/g (dry weight)/day. Using these data and making assumptions on assimilation, he estimated that the spider required 73 g cal/g (live weight)/ day in food to maintain itself. This stud has most of the elements necessary for a field estimate and lacks only data on numbers present in a natural habitat. The book by Brody, “Bioenergetics and Growth”, deserves special

Y

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mention because of its importance as a standard reference on energetics. This work is concerned with domesticated farm animals and thus is useful in calculating farm productivities. However, many of the chapters are of a general nature and contain a wealth of information concerning such vital subjects as energetics and energy units ; energetic efficiencies of growth and work processes; nutrition, the principle of diminishing increments in efficiency; homeostasis and organismic theories; methods in animal calorimetry; and the energetic efficiencies of muscular work. For the most part, the book discusses such aepects as the processes of growth and metabolism. Marshall “Biology and Comparative Physiology of the Birds”, Vol. 11, contains much information on energetics. The chapter on energy metabolism, thermo-regulation, and body temperature contains information on calorimetry, met.a,bolicrates, energy metabolism and the variation in energy metabolism. The chapters on flight, long distance orientation, behavior, and bird populations also contain information which is potentially useful in making field energy estimates. The study undertaken by West (1960) on the tree sparrow, Spizella arborea, met all but one of the requirements of a complete field productivity study; field data are lacking on numbers of individuals. West’s primary concerns were: (1) the number of calories necessary to support the birds in their environment; (2) the caloric burden of migration and incubation. Food consumed and excrement produced (West used this term to mean egestion plus excretion) by the ;birds was measured both in the laboratory and in outdoor cages at Churchill, Manitoba, Canada (the birds’ breeding range) and a t Urbana, Illinois, U.S.A. (the wintering range). Values averaged around 4.4 kg cal fm the food and 3.7 kg cal for the feces. The energy consumption of the birds varied with the ambient temperature from 34-23 kcal/bird/day (1-64 kcal/g/day) at -30” C to 10.77 kcal/bird/day (0.49 kcal/g/day) at 30” C. Day length also caused variation in calorie requirements rmd caloric consumption. From these and other data West constructed a series of equations and a graph for the annual energy budget of an adult bird. The equation which related grow energy intake of the bird to temperature was GE = 25.89 kcal/bird/day-0.254 T o C. The equation which represented metabolizableenergy with relationship to temperature was M E = $9.05 kcal/bird/day-0-167 T o C. Each bird required roughly 7 460 kg cal each year to live, migrate and reproduce in the wild. West had no figures on the area necessary to provide these calories and, thus, no productivity figures per unit area for the population were given. The last paper of a primarily physiological nature I wish to discuss is that of Pearson (1960) which has many elements of the Bornebusch approach although emphasizing the homeostatic mechanisms of the harvest mice. Pearson considered oxygen consumption and its relationD

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ship to ambient temperature. The effects of nest, insulation of hair, huddling and exercise upon metabolism are investigated. Finally, Pearson turned to the bioenergetics of the mice and using data from several sources, calculated the oxygen consumption for an average mouse during an average June day and an average December day in California. He calculated energy estimates for the mice, assuming both diurnal and nocturnal activity patterns. These values equalled 1 370 cc and 1 782 cc of oxygen respectively, averaging 1 576 cc of oxygen per day and were equal t o 7.6 kcal/mouse/day for the nocturnal pattern. Using population data from another investigator, Pearson estimated that the mouse population dissipated on an average 91 kcal/day/acre which is about one-half to one yoof the daily energy stored by the plants on that acre. If Pearson's average daily estimate were used to calculate an annual respiration sum, it would equal 8.741 kcal/m2/ann. The final question in Pearson's paper concerned the cost of nocturnal activity of the mouse Reithrodontmys megalotis. Pearson estimated that nocturnal activity costs 420 g callday or the energy contained in three and one-half grains of wheat. This, then, is the price a mouse must pay to keep away from hawks and other diurnal predators. Comparison of these papers as a group with respect to their productivity significance is a difficult task, for the papers do not approach the problem of metabolism in the same manner. The data were inconclusive, in most cases, due to the lack of information about popuiation size and structure, lack of data on the temperature of the environment, and lack of information on the natural diet. We can compare respiration ratios (Table I),but this information will lead only to statements about the metabolic intensity of each species. Even the estimates of the annual population respiration totals by Pearson were unsatisfactory, for although we have estimates of the maintenance requirements of the mouse, we have no estimates of the calories produced in the form of new tissue. The value of the papers just discussed lies rather in the potential value of the data for field ecologists rather than in their direct contribution to the energetics field. TABLEI Comparison of Respiration Rates of Several Wild Animals Oxygen Consumed g cal/g animal/day

Temperature of Exp.

Common Name of Animal

Author

160.94 960 to 731 1 6 4 0 t o 490

Dec. t o June

29" C

Spider Mome sp8mOw

Itti 1964 Pearson 1960 West 1960

-30" to $30" C

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V. STUDIESCONCERNED PRIMARILY WITH MAINTENANCE IN T H E ENVIRONMENT METABOLISMOF POPULATIONS

I describe the studies discussed under this heading as the “Bornebusch school”, although most have gone one step further than Bornebusch in that they calculated the calories burned by the population rather than just the oxygen consumed by it. This approach can be employed at one of three different levels of organization: ( I ) the species population, (2) the higher taxon (e.g. order and class), and (3) the community. The work of Pearson (1960) could be considered under the Bornebusch approach as well as under the physiological approach, for the final portion of his paper deals with maintenance meta,bolismof the field population. Others dealing with maintenance metabolism of species populations in the field are McNab (1963), Nielsen (1!#61),O’Connor (1963), and Phillipson (1962). Berthet (1963) attacked the problem at the taxon level while Bornebusch (1930) and Macfadyeri (1963a, b) dealt with the community. McNab’s (1963) paper dealt witth three species of the field mouse Peromyscus. Star\ing with the physical and physiological elements which influence the metabolism of a mouse, McNab d.erived a series of formulae which eventually described the metabolic requirements of the mouse for a 24-h period. Using these formulae and information about environmental temperatures, size of animals, and numbers of individuals present in a tract of chaparral near Berkeley, California, and assuming 60% assimilation, McNab came to the following conclusions about the mouse populations. (1) Homiotherms have little energy available for work other than homeostasis. (2) The amount, of energy for activity has an Averse relationship with body weight. (3) Mouse populations consume only 2-5% of the primary productivity of the chaparral. P . manicuhtas was estimated to consume 14 kcal/day in June. Of the 14 kcals, it assimilated 8.37 kcallday. The total mous,e population of the three species of Peromyscus on the 26 acres of chaparral (32 P . maniculatus, 22 P . truei, and 13 P . californicus)during a typical June day consumed 24 kcal/acre. During a typical February day they dissipated 59 kcal/ acre in respiration and consumed 100 kcal/acre/day in food. Using another set of data on grassland, McNab estimated the “mice” (Reithrodontomys, Peromyscus, and Microtus) required 203 kcal/acre/day in summer and, thus, consumed 338 kcal/acre/day. McNab commented upon the estimates of Odum et al. (1962), noting that their 2.5 activity factor was arbitrary and too high, and recalculated the energy flow of the “old field” mice to 19.8 kcal/acre/day - a value which represented only 1.8 to 3.6% of the seeds produced on the old field. Nielsen (2961) also deals with the respiratory metabolism of field

88

MANFRED D . ENOELMANN

populations and adheres to the Bornebusch pattern in that oxygen consumption was estimated, but, the values were not converted to caloric equivalents. Nielsen obtained data on respiration rate of enchytraeid worms via Cartesian diver in the laboratory. Using field information, he calculated respiratory+values for field populations of both enchytraeids and nematodes. He took into consideration (1) environmental temperature, (2)activity, (3)oxygen tension, (4)drought or moisture content of the soil, and (5) mean body weight, in making the field estimate (see Table 11). If we make the assumption that the RQ of the animals is 0.85 (an average RQ for a mixed diet), then each litre of oxygen will yield 4.8 kcal of heat. TABLEI1 The Numbers of Individuals and Calories Respired by the Enchytraeid and Nematode Worms in a Permanent Pasture in Denmark. Data from Nielsen, 1961 Respiration Total Litres of Oa/ma/yr

Calories Released Yearly via Respiration kcal/ma/yrt

Taxon

Station

No. of Individuals x 10a/ma

Enchytraeidae

1 4 18

44 30 74

7 10 32

33.6 48-0 153.6

Nematoda

1 4 18

i x 104 5 x 103 1 x 104

43-63 3 1-46 71

2064-302-4 148+3-220.8 340-8

t Calculated by the present author using

4.8 kca1:L conversion factor.

Using the respiration figures and making some assumptions about the nature of assimilated food of the nematodes, Nielsen estimated that these animals required 800 kg of bacteria (live weight) and 320 kg of plant root cells (live weight) to satisfy the respiratory requirements indicated by his calculations. The diet of enchytraeids was assumed to be bacteria and the amount requireg to maintain the enchytraeids was estimated at 300-400 kg (live weight). Nielsen pointed out succinctly that knowledge of numbers of individuals alone is not sufficient to allow judgement of population. Data on the enchytraeids indicated that the site with the smallest numbers of individuals per meter square did not have the lowest respiratory metabolism. Presumably, then, the animals at “station 4” had a greater impact upon the environment than did those at “station 1”. However, the consumption of energy for body

89

ENERGETICS A N D ANIMAL PRODUCTIVITY

maintenance .is not the sole influence an animal can have upon its environment. O’Connor (1963) studied three species of enchytraeid worms from Epglish coniferous soils, obtaining information on (1) mean monthly population density in the field, (2) the numbers of individuals in each size category, (3) monthly age structure of the population as well as weights of the size categories, and (4) mean monthly field temperatures. From these data, he estimated that 14.33 x lo4 worms/m2 will weigh 10.794 g (dry weight), and respire 149.5 kcal. O’Connor also pointed out that the number of individuals alone can be unreliable as an indication of the importance of a species. I n Table III[ we see the relative rank each species holds with respect to a particulsx characteristic; first rank representing the largest value and the third rank representing the smallest value. Cognettia is the third in numbers present in the field when compared to the others, but first in the annual dissipation of calories. O’Connor compared his data obtained from the Douglas fir forest with the data Neilsen obtained from pasture soil. The figures from “Station 18” of Neilsen’s study yielded about the same values as O’Connor’s, both populations releasing about 150 kcal/m2/year. The physical factors of the two sites (Wales versus Denmark), were similar. TABLEIrI The Relative Rank held by Three Species of Ehchytraeidae when c m pared with one another. Original Data fiom O’Connor, 1963

Species ~~~

~

Numbers/m*

Biomass

Individual Total Calories Respira- Population Dissition pates Annually

~~

Hemihenleu cambrensis Achaeta ebeni Cognettia cognettii

~

First Second Third

First Third Second

Second Third First

~~

~~~

Second Third First

Phillipson (1962) dealt with the populations of Mitopus morio and Oligolophus tridens (Phalangiidae). Using a continuously recording, constant pressure respirometer which automa ticnlly replaced the oxygen used, Phillipson obtained respiration values for all stages of the two species of harvestmen which showed that the day-night respiration rates of the animals differed as well as did daily respiration totals. Using a series of independent observations on food consumption and respiration requirements, he concluded that the animals were not utilizing the components of their diet (i.e. fat, proteins, and carbohydrates) in the same proportions as they occur in the food. Uniform absorption is

90

MANFRED D . ENQELMANN

widely assumed in energetic studies, but .Phillipsoncontended that there is differential absorption especially by the immaturc stages of the animals. Employing field data and biomass estimates from other studies, Phillipson estimated that the phalangids free from 1-34to 1-47 kcal/ma of ground layer in an English deciduous woods in a year. The daily respiration rates of the phalangids agreed closely with those of the lycosid spider (Table IV). However, though the harvestmen showed a decreasing respiration per unit size with increasing weight (a common relationship in animals), data on lycosids did not follow that pattern. The respiration rate of the lycosid was measured a t 29” C, while those of the harvestmen were measured at 16” C. If we assume a &Io of two, then the lycosids respired about 56 cal/g/day (dry weight). This is the expected value for an animal of that size (note Table 4 gives live weights for size comparison rather than dry weights). Phillipson’s paper is important because of the conclusions drawn about differential assimilation of food and the information gained on energy utilization by arthropod predators. TABLEIV Comparison of Respiration Rates of Xeveral Predatory Arthropods. (Data from Phillipson, 1962 and ItB, 1964.) Specie8

Cal Respired/ g dry wt/day

Live Wt Individuals (mg)

Mitopus morio Oligolophue tridena Lycosa pseudoannulata

85-95 120-130 150.9

3.7-56.1 3-1-17‘3 1-150

The study by Berthet (1963) also concerned with soil arthropods, was centered on herbivores or generalized feeders. He dealt with all the species of a particular taxon (the Oribatei) found in the soil layers of the Meerdael Forest, Belgium. The animals were removed from the forest soil to the laboratory, where their respiratory rate was measured in a Cartesian diver respirometer. The respiratory rates were measured at 1 5 O , lo”, 5”, and 0” C, respectively, during successive two-hour intervals. The respiration rate of the 16 oribatid species was related to temb X , where Y is the log to perature according to the equation Y = a the base 10 of the oxygen consumed x ml; X is the temperature; and “a” and “b” are constants, “b” being one-tenth the antilog of the &Io value. Values of the &Io ranged from 2.6 to 5.6 and averaged 3-9 for the 16 species tested at these temperatures. The relationship between daily oxygen consumption, weight of the individuals, and temperature was described by the formula Y = 18.059 0.7W - 0.4872, where Y

+

+

ENERGETICS A N D ANIMAL PRODUCTIVITY

91

equals the log 10 of the oxygen consumed x ml/individual/day, W equals log 10 rate of the individuals in pg, 2 equals 1 x lo4 divided by the temperature in degrees A. Using these formulae, data on numbers and biomass of the oribatid mites, and data on the annual temperature fluctuation of the forest soil, Berthet estim,%tedthat the oribatids respired a total of 4.488 L (oxygen)/m2/annum.(See Table v.) TABLEV The Numbers, Biomass, Respiration and Calorie Requirements of Oribatid Mites Found in Belgium Forest Soil. (Original Data from Berthet, 1963.)

Taxon Oribatei (46 SPP)

No. of Individuals x 103/me

Biomass

&m/me

Oxygen Consumption L/ma/yr

Calories Released kcal/m*/yrf

133.6

5.377

4.488

21.54

t Assuming 4.8 kcal/L Oxygen coilsumed.

Berthet, like Nielsen, did not calculate the caloric equivalents for the respiration figures. If we convert by the factor of 4.8 kcal/L oxygen, we find that 21.54 kcal were released by the population in one m2 during a year. The two authors who studied the problem of maintenance metabolism on the community level of organization were Bornebusch (1930) and Macfadyen (1963a, b). Bornebusch confined his calculations to the areas he sampled, while Macfadyen, in an effort to point out some norm or pattern of energy utilization, analyzed the data of other workers as well as his own. The analysis of the five Danish forest soils is summarized in Table VI. It has been claimed by various authors (Birch and Clark, 1953; Macfadyen, 1963b) that the density figures given by Bornebusch were low and, thus, that all of his calculations were deficient. This contention was supported by a comparison with the figures of Van der Drift (1951) on beech forest soils in the Netherlands. Even though comparison of Bornebusch’s figures with those of other authors was thus difficult, the significance of his conclusions is not altered. The efficiency of his extraction technique was probably the same for each of his sites and, therefore, the same magnitude of error was present in all of his calculations, thus, the data had comparative values. Bomebusch’s observations include the following: (1) The slower the decompositior, of the humus, the greater were the numbers of arthropods present and the rower was their total weight. (2) The weight of the forest soil fauna waa a more reliable index

M A N F R E D D . ENOELMANN

92

to their activity than was the number of individuals. (See Table VI.) The best index, however, was the oxygen consumption rate of the fauna. (3) Large earthworms were most important in rich mull soils, mixing and aerating the top layers. (4) In raw humus where earthworms are sparse, arthropods initiated the breakdown of the material to be decomposed. Bornebusch concluded with a statement which underlines the importance of the soil fauna to the soil building process, and he called the attention of the forester to this fauna and directed him to take heed of soil organisms, a directive which has, on the whole been disregarded or has passed unnoticed. TABLEVI Density, Biomass, and Respiration of the Fauna Found in Five Forest Soils. (Datafrom.Bornebusch, 1930.) Mean Density Soil Type

Oak Mull Beech Mull f 5 Beech #4, raw humus Spruce Mull Spruce, raw humus

#/m2 Rank 2978 4424 14163 10790 11 938

5

4 1 3 2

Mean Biomass g/m2 Rank 76-81 37-76 24-02 10.72 9.84

1 2 3 4 5

Respiration 13” C

-

mi3

Ol/hr/maRank 17-74 11-51 12.08 6.74 7.09

1 3 2

6

4

Macfadyen employed the maintenance metabolism of populations as a comparative tool, but his scope was much broader and his figures admittedly more approximate than those of other authors. The purpose of a study such as Macfadyen’s is creation of a framework, admittedly imperfect, in an effort either to reveal some pattern or principle which will be useful as a predictive tool, or to give a basis of organization which, as new data accumulate, may be modified into another more precise framework. I n his book, “Animal Ecology’’ (1963a, page 234), Macfadyen set forth the framework of a hypothetical grassland soil community, indicating the approximate relationship each taxonomic component should have to this community. I n the grassland soil, bacteria were more numerous and harvestmen were the least numerous. Plants (bacteria and fungi) accounted for 1 400 g/m2 of the soil biota, while animals accounted for only 225.9 g. In terms of metabolic activity, nematodes were the most important animal group, followed by earthworms, enchytraeids, and collembola. In Doeksen and Van der Drift (1963), Macfadyen sets forth a more

ENERGETICS A N D ANIMAL PllODUCTIVITY

93

comprehensive framework, comparing different communities (pages 8,

9) as well as components within the communities. He used data from

several authors in the compilation of this table. The table contained data from both forest (coniferous and deciduous) and grassland communities. In Table VII are listed the percentage of animals comprising each major trophic group as given by Macfadyen and the rank each group held with equivalent trophic groups of the other communities. I have used these data to compute a rough carnivore-herbivore ratio and several generalizations emerge: (1) There is a rather constant percentage (20 to 33%) of herbivores -this category includes anima@which reside in the soil and feed upon algae and roots of’green plants but not upon bacteria and fungi. (2) There is an inverse relationship between the percentages of predators and large decomposerig (sig. at the 5% level using Spearman rank correlation (Siegel, 1956,page 202) ). (3)It would appear that there is an inverse relationship between the percentages of large decomposers and small decomposers; however, the rs equals 0.5, which is not significant. Most of the deviation comw from a single observation (Spruce, R. H. (6) ). If this item were removed, the relationship between large and small decomposers would attain statistical significance at the 5% level (r, = 0.69), but since we have no justification for eliminating the data on the Spruce, R. H. (6) communil;y, the relationship remains doubtful. It is also important to note that in Madadyen’s data the predatorherbivore ratio was not constant and did not seem to correlate either directly or inversely with any other element of the community. Macfadyen (1963b) points out that, although the various taxonomic components vary considerably from community to community, the total picture of metabolism remains remark ably constant. Although in view of the adjustments and assumptions made, the figures thus derived must be considered as tentative. From information on bacterial respiration and field experiments with soil reupirshion, Macfadyen estimated that animal respiration represented from 10 to 20% of the total soil metabolism. He concluded that the soil fauna is important in its %atalytic” activity and control of the energy passing through the decomposition cycle. When the studies on maintenance met,abolism are reviewed as a group, at least three salient points emerge. First, annual maintenance metabolism is a better indication of the impmt of a population or group on an area than are numbers or biomass. However, it was pointed out by Phillipson, Macfadyen, and O’Connor that respiratory metabolism rates alone do not represent the full impact of the population. The eating habits, efficiency of digestion, and rate of reproduction can have D*

TABLEVII The C m p r k o n of % or Rank of Annual Calorie Dksiption and Predator-Herbivore Ratio of Different Trophic Groups Found in Nine Natural Communities on the British Isla and the i3uropeun Continent. (Datafrom Macfadyen, 1963b.) 1

community

2 Limestone Grassland Grass

Herbivore Rank Herbivore yo Large Decomposer Rank L. Decomposer yo Small Decomposer Rank S. Decomposer yo Predator Rank Predator yo €tank Total kcal/yr Ratio carnivoreFerbivore

7

3

Juncus Moor

4

Oak MUll

5

Beech RH

6

7

8

9

Beech MUll

Beech Mull

Spruce MUll

Spruce RH

(15)

(4)

(1)

(6)

5 28.36

1 32.91

8 22-29

25-65

3 31.77

4 30.85

9 20.36

6 27.25

2 32.08

4 27-36

1 55.54

8 1.21

2 33.49

5 8.42

3 31.24

6 3 a46

7 3.3

9 0.54

4 39.32 6 10.95

9 17.38 9 1.38

1 64.18 8 2-85

6 29-87 5.79

2 46.06 3 25.15

8 23.92 5 17-58

3 45.41 4 19.05

5 36-48 2 31-86

29.12 1 37.43

1

2

4

7

9

5

3

8

6

0.1232

0.0140

0.0293

7

0.0614

0-3360

0.2133

0.2353

0.4675

7

0.5981

ENERGETICS A N D A N I M A L PItODUCTIVITY

95

marked effect upon the community - effects which are not indicated in the Bornebusch type of analysis. Finally, it is of interest to note that the majority of the investigations were on soil animals or soil communities. This could be due either to tradition or to the fact that the soil provides many species and complex relationships readily accessible in small areas. The added fact that this system plays an important role in the economy of man probably also lends impetus to the pursuit of soil study.

VI. STUDIES WHICH EMPHASIZE THE TROPHIC SCHEME ANALYSISOF COMMU:YITIES This last group of studies gives us our best figures on animal productivity in natural communities. These studies are concerned not only with estimates of maintenance energies, but also with the incorporation of calories into new protoplasm. These growth calories can either fall prey to another trophic level, or increase the biomass of the population. The capacity of the population to produce these surplus calories determines the ultimate structure of the community as well as the usefulness of that community to man. With regard to this last point, we must bear in mind that the net productivit,y of a natural population is not equivalent to its yield useful to man. If man were to utilize the complete net production of a population, he would have to aasume the role of predator and decomposer for the entire population. Man begins to approach this relationship with his domestic animals, but the natural community presents a different situation. Investigators utilizing the trophic dynamic approach at the population level were: Golley and Gentry (1964), Odum and Smalley (1959), Odum et al. (1962), Petrides and Swank (1965), Smalley (1960), and Wiegert (1964). Only one author (Golley, 1960) has approached the subject of field energetics from the standpoint of energy flow through a food chain, while two investigators (Engelmann, 1961; Teal, 1962) have attempted some kind of analysis at the conimunity level. Three of the papers reported data on homiotherms (Golley, 1960; Odum et al., 1962; Petrides and Swank, 1965), while the remainder dealt with poikilotherms, particularly insects. Most of the investigators used field data to create complete energy budgets.

A. TROPHIC D Y N A M I C A N A L Y S I S O F THE SALT MARSH E C O T O N E Smalley (1960) working on the insects of a salt marsh has provided basic information utilized by other authow. His data for the grasshopper, OrchelimumJidicinium, were used in his own 1960 paper, the paper by Odum and Smalley (1959) and the paper by Teal (1962). His basic sampling tool was a sweep net, standardized against captures in a square meter cage placed randomly on the sampling area. With these

96

MANFRED D . ENOELMANN

tools, Smalley could collect data on numbers of individuals, and size categories of individuals. Weights were assigned to the size categories by weighing representative individuals from each size category. A simple constant pressure respirometer was used to measure respiration rates. Observations on caged individuals were used in making estimates of egestion rates. Calorific values for various biological materials were determined in a Parr bomb calorimeter. Ingestion was figured as the sum of respiration, “production” and defecation. “Production” in this case then refered to net production which included estimates of new nymphs produced and numbers of individuals lost to the population through death. Estimates were lacking on numbers of eggs produced by the population. Smalley calculated that a biomass equivalent to 10.8 kcal/m2respired 18.6 kcal of oxygen annually. Gross production by the population equaled 29.4 kcal/m2/year. Assimilation efficiency averaged 2’7.4% and ranged from 20.8 to 35.4%. Smalley estimated that the grasshoppers ingested 107 kcal of the 5 200 kcal produced annually on each square meter of the marsh. The grasshoppers consumed only 2% of the net amount produced by the flora available to them. It is of interest that the net productivity of this population was estimated entirely from the data on calories lost to the population via death. This population, as in the case of many insects, overwintered in the egg stage and, thus, the adults died off at the end of the season, their bodies going directly to the decomposer system. The net production estimate of the grasshopper, however, was still short, for Smalley did not have data on the number of deaths for every stage in the life cycle. The paper by Odum and Smalley (1959) summarized energetics data for grasshopper and snail populations living in the salt marsh on Sapelo Island off the coast of Georgia. The data for this study were collected by Smalley. The authors calculated that the grasshopper, Orchlimum, ingested 48 kcal/m2/year of Spartinu grass. Thirty-six per cent of the food ingested was assimilated. The gross production of the grasshopper was 28 kcal/m2/year. The snail (Littorina) feeding upon the decaying grass stems and algae, etc., was 45% efficient in assimilating its food and yielded a gross productivity of 290 kcal/m2/year.No ingestion figure was given for the snail. Since the organism was 45% efficient in assimilating food, it must have egested 55% of the material, or 354 kcal/m2/year. Thus, the Littorina population ingested annually a total of 644 kcal/m2. Littorim used only 14% of its assimilated energy for production of new individuals, while the grasshopper utilized 37% of its energy in reproduction. These figures can give us a minimal estimate of net productivity in the two species, but losses due to death were not stated in this paper. Net production in the grasshopper was 10.4 kcal/m2/year, and in the snail, 40.6 kcal/m2/year. The major point Odum and Smalley

ENERGETICS A N D ANIMAL PRODUCTIVITY

97

made was that even though numbers of individuals and biomass varied in the salt marsh “community” the energy jlow through the population remained relatively constant. It is also worth noting the difference between the figures used by Odum and Smalley (1959) and those used by Smalley (1960). First, there was a 1.4 kcal/m2/year difference in the figures on gross productivity in the two papers. Secondly, Odum arid Smalley used an assimilation figure of 36%, resulting in an estimate of 7 7 - 7 7 kcal/m2 ingested annually, while Smalley set the assimilation rate at 27.4 and the ingestion rate at 107 kcal/m2/year. I n the first CiiSe, the maximum assimilation rate was used. I n the second assimilation was an average rate. Thus, the first paper compared the average efficiency of the animal, while the second compared the maximum efficiency. The salt marsh is not typically a terrestrial community but is rather an ecotone. The fact that typically marine populations as well as terrestrial populations can be found at times in the same square meter plot tends to complicate analysis of this type of habitat. Allowances must also be made in the analysis for immigration and emigration of materials and populations, particularly if the inflow and outflow of energy is not equal. Teal (1962) attempted an analysis of the energetics of the salt marsh community. He employed data from several sources in making his estimates. A number of assumptions were used to give estimates where data were lacking. He stated production equalled 0.25 to 0.3 respiration; energy degradation was equal under anaerobic and aerobic conditions; the racoons had an assimilation equal to that of the Clapper rails; spiders and carnivorous birds took the same proportion of the prey as did the mud crabs, rails, and racoons which preyed upon detritus algae feeders. Some of these assumptions were supported by logic or circumstantial evidence; others, such as the last two listed, were not. The energy flow through the salt marsh system was summarized by Teal as follows: Input as light 6 x 106 E:cal/m2/year, loss in photosynthesis 563 620 kcal/m2/year, gross production of the producers 36 380 kcal/m2/year,respiration by the producers 28 175 kcal/m2/year, net production of the producers 8 205 kcal/m2/year, bacterial respiration 3 890 kcal/m2/year, primary consumer respiration 596 kcal/m2/ year, secondary consumer respiration 48 koal/m2/year. The total energy released by the consumers equaled 4 534 kcal/m2/ year or 55% of the net production of the pi-oducers, leaving 3 671 kcal/ m2/year to be exported by tides and other losses. This “community” contained a great number of marine and fresh wqter species. If we confined attention to terrestrial animals then his data on the grasshopper, Orchelimum, the plant bug, Prokelisia, and the nematodes should

98

MANFRED D . ENGELMANN

be considered. The data on the grasshopper were those of Smalley (1960). The gross productivity of 29.4 kcal/m2 was used by Teal. A gross productivity figure of 275 kcal/m2/yearwas reported for an average standing crop of 70 kcal/m2for Prokelisia, the plant bug. Teal calculated that the nematodes respired 64 kcal/m2/year, and he assumed production in the marsh to be 21 kcal/m2/year or 25% of the respiration rate. Teal did not calculate ecological efficiencies for the various trophic levels, although he did report efficiencies for the utilization of the Spartina standing crop by the insects 4.6%). If we use the formula by Engelmann (1961) which is correctlyreported by Slobodkin (1962, p. 98), an ecological efficiency of 6.8 can be obtained for the herbivore-carnivore trophic levels. Teal’s paper is important because it deals with an ecotone. The work suffers because it relied too heavily upon assumptions and was not sufficiently comprehensive.

B. TROPHIC DYNAMIC

ANALYSIS OF (‘OLD FIELD” COMMUNITIES

The second group of papers to be discussed center on the “old field” habitat. Studies have been made under the very different climatic conditions of southern Michigan and Georgia. Golley and Gentry (1964) studied the bioenergetics of the southern harvester ant, Pogonomyrmex badius in South Carolina. They located ant hills in the “old field” study area, labeled individuals radioactively with P32 to estimate the numbers of animals in each hill by mark -release - and recapture methods. Ant hills were excavated to ascertain the numbers of all stages present, and respiration measurements were made on the various stages. Counts indicated that there were 0.0027 hillslm2 and that each hill contained from 4 000 to 6 000 individuals. From data on numbers present and respiration studies, it was calculated that 14.2-47.7 kcal/m2/yearwere lost by the population in respiration. Using the numbers of young found in the hills, plus supplementary data, Golley and Gentry estimated that the ants produced 0.09 kcal/ma in new individuals each year. The authors did not make an estimate of calories lost to the population through death. The total estimates for P . badius were: net productivity 0.09 kcal/m2/year;gross productivity 14.29 to 47.79 kcal/mZ/year. Golley and Gentry reported that the ant was primarily a gramnivore and that the field produced 22 kcal/m2/ year in seeds. The ant, then, consumed the equivalent of 64 to 213% of the seed crop each year. Since the field also supported other gramnivores (mice and sparrows), the authors concluded that other foods must have been used by the ants in addition to seed. The authors noted that the ant consumed more energy than either the sparrow (4kcal/ma/150 days) or the mouse (7-17 kcal/mQ/year)populations associated with it in the “old fields”.

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Because of the division of labor within the colony, the marking technique was not successful for estimating the total number of individuals in the hill. Data for net production were also difficult to evaluate, because the authors took the top birth production figures rather than averages; yet they had no estimate for deaths of adults or young during their life span. Net production, in this case, requires estimates for both parameters because most of the individuals lived more than one year. The important point is, however, that maintenance metabolism required 99.6% of the total assimilated energy. No estimate of ingestion was attempted and, therefore, we have no information on the total number of calories consumed annually by the population. The data presented by Golley and Gentry indicated that, in the “old field”, the harvester ant was an important herbivore converting most of its assimilated energy into maintenance and very littlo energy into net production. Odum et al. (1962) worked in the abandoned fields (“old fields”) associated with the Savannah River Plant of the U.S.A. Atomic Energy Commission, Georgia. The authors concentrated on two grasshopper species (Melanoplus femur-rubrum, and M . biliteratus), the tree cricket (Oeconthusnigricornis), a mouse (Peromyscw polionotus), and a sparrow (Passerculus sandwichensis). The mice were live-trapped, the sparrows captured with mist nets, and the Orthoptera were captured with sweep nets and in cages after the procedures originated by Smalley. Caloric equivalents were obtained by Parr bomb cdorimetery . Metabolism was measured both in terms of caged animals sad by respirometry. The field energy was assumed to be twice maintenance energy (an assumption questioned by McNab, 1963). The authors estimated that gross production of the sparrow was 3.6 kcal/m2/year. However, since Southern Georgia is the wintering range for these birds, there was virtually no net production (0.04 kcal/m2/year).Gross production for the mouse was 6.7 kcal/m2/year, with average net production at only 0.12 kcal/m2/year. Gross production for the Orthoptera was 25-6 kcal/ mZ/year and net production was 4 - 0 kcal/m’a/year.Once the authors had determined the total amount of each food consumed, they could find out how much of the standing crop of peen plants the herbivores utilized. The gramnivorous birds and mice used from 10% to 50% of the seeds consumed, whereas the herbivorous Orthoptera utilized only 2% to 7% of the plant foliage. Golley and Gentry estimated that the ant, P. badius, consumed the equivalent of 64% to 213% of the seed crop on these same fields. Thus it would appear that from 74% to 263% of the seed crop produced on each m2 was used by these three species during the year. This can only imply that ei1;her the seed crop was underestimated or the animal utilization overestimated, or both. Analysis of droppings of vesper and field oparrows in Michigan showed

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that during the spring and early summer before a seed crop was produced, these animals were carnivores. Even during the fall, the birds continued to include insects in their diet along with seeds (personal communication, F. C. Evans). McNab (1963) believed that the food utilization data on the mouse (Odum et al., 1962) were too high. Golley and Gentry (1964) recognized the fact that P. badius must have been using foods other than seeds. Thus, these calculations on seed utilization demonstrate that studies on energetics require careful observations on feeding habits, as well as careful measurements of metabolic and reproductive processes. It is of interest to coppare data from Wiegert’s very careful study (1964) on the spittle bug Philaenus spumarius of “old fields” with the data previously discussed from the salt marsh and the southern “old field”. Wiegert also used the aforementioned sweep net and cage method to measure the spittle bug population. He reported the confidence limits for his samples. Respiration rates were measured on all stages of the animals; the caloric values of these rates were determined; also feeding habits and migratory patterns were studied. A great deal of Wiegert’s study was devoted to the feeding efficiency of the various stages of the spittle bug. He found that the immature individuals were 30% to 58% efficient (average 36%) in assimilating nutriment from the plant sap, while the adults were 71%-80y0 efficient (average 76%) on the same material. However, when it came to listing the productivity for the “old field”, Wiegert ran into difficulty. A population must be able t o produce a minimum number of new individuals, if it is to maintain itself from year to year. The Philaenus population could not do this on the “old field”. Wiegert calculated the intrinsic rate of natural increase of this population on the “old field” to be -5.8 to -6.0. The continued presence of the spittle bug population on the “old field” was supported by immigration of new individuals from surrounding alfalfa fields. Thus, the net production of P. spumarius ranged from 0.048 to 0.096 kcal/m2/ year and the gross productivity ranged from 0.582 to 1.167 kcal/m2/ year. Immigration contributed from 0.516 to 1.138 additional kcal annually to each square meter of the “old field” in the form of immigrants which later failed to survive. I n contrast, a sma€l alfalfa field produced (net) 15.125 kcal/m2of animals. Gross productivity amounted to 38.565 kcal/m2/year. When the alfalfa in this field was cut, and the quantity of primary producers drastically reduced, thereafter the spittle bug adults moved out of these fields into other areas which could support them. Thus, although the “old field” was able to provide sustenance for a certain number of adults, there was not energy sufficient to maintain the population on a permanent basis. Ninety to ninety-five per cent of the adult animals dying on the “old field” were immigrants. Wiegert

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was able to calculate the ecological efficiency (gross efficiency of yield/ ingestion) by assuming “instantaneous predahion”. The figures he obtained ranged from 0.8~0-17-4%. Wiegert’s paper is significant, not only because it is an example of careful analysis, but because it dealt with a species in the two extremes of its total habitat range. The gross and net productivities in the alfalfa field exceeded most other productivities for arthropods reported in the literature (save that of P.badius,Golley and Gentry, 1964). Yet, in the “old field” the spittle bugs could not survive. Wiegert’s study pointed again to the inadequacy of the Lindeman model in a situation of imbalance. Another study made on this “old field” of the E. S. George Reserve was concerned with the soil arthropods (Engelmann, 1961). The study used the author’s results and data collected previously by Hairston and Byers (1954). The mite population was estimated from monthly soil samples processed in Tullgren funnels. Indivilduals of each species were weighed on a quartz helix balance, and the numbers and weight data were used to estimate biomass. Data on respiration rates measured with a, simple constant pressure respirometer were used in conjunction with biomass information to calculate total maintenance metabolism. Radiotracer experiments gave figures on ingestion. Soil organisms were cultured in the laboratory and studied to gain information on life span, ingestion and egestion, and birth rate. Infor mation from cultures and field data provided a basis for making assumptions on survival. From these data a complete energy balance sheet was constructed for the Oribatei. The study approached the problem of energetics at two levels: fist at a lower level, or taxon, concentrating upon the Oribatei; on a second level all of the soil arthropods were included. The analysis of data on oribatids resulted in estimates as follows: a standing crop of 0.27 kcal on an average square meter of “old field”; ingested 10.248 kcal; assimilated 2.058 kcal; respired 1.965 kcal, and lost through mortality 0.43 kcal each year. These data and preserved materials of Hairston and Byers (1954) were used to estimate the ecological efficiency of the carnivores with respect to the herbivores. Knowledge of respiration estimates and assimilation efficiency for both herbivores and carnivores made possible calculations of efficiency values. The most reasonable ecological efficiencies ranged from 8% to 30% with 16.90/,, the most probable value. The production on this field was very low when compared with the area sampled by Berthet, for example. Nematodes andnrotiferswere scarce in the poor, well-drained field soil. The combined respiration of these organisms yielded about 0.36 kcal/m2/year.

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This study had two positive aspects from the standpoint of energetics. First, the work represented an attempt to analyze total flow of energy through the soil. Second, all of the data in the oribatid balance sheet were a product of separate observations; none of the figures were derived from equations. The study had several inadequacies which could affect the significance of the results. Taxonomic identification was the greatest deficiency. Secondly, there was a problem of questionable efficiency of the Tullgren extractor, particularly when used on dry summer samples. Finally, temperatures of microhabitats were not known. I am now acquiring additional new information which may increase the figures for net and gross productivity of the Oribatei. Let us move to another study of an “old field” habitat. The subject of a paper by Golley (1960) was the food chain involving the bluegrassvole-least weasel. Golley obtained data on abundance, age structure, respiration, assimilation, and egestion rates of the vole Microtus. The least weasel (Muste&) data were largely based upon assumptions, the majority of them reasonable! Good information was obtained on the food of the mouse which was Kentucky bluegrass ( P o a pratensis). Golley calculated that a standing crop of 0.021-0.553 kcal of mouse on 1 m2 would release 17 kcal in respiration and produce 0.517 kcal in young each year. As was the case in Wiegert’s study, it was difficult to balance the ledger because of caloric transport. The mice were able to maintain themselves in the area, although Golley found evidence of both immigration and emigration. An estimated 1-35 kcal/m2/year of mice moved into the area, a quantity almost twice that accounted for by net production. Thus, on the portion of the “old field” studied, the number of deaths was higher than the number of individuals produced on that area. The gross productivity of the Microtus population was 17.517 kcal/m2/year. Mustejh, the least weasel, had a net productivity of 0.013 kcal/m2/year and a gross. productivity of 5.564 kcal/m2/year. Nicrotus used 1.6% of the total net production of the Kentucky bluegrass, while Muste& consumed 31% of the net production of the Microtus population. Though not calculated by Golley, ecological efficiencies for the weasel and mouse would be 2.3%. This percentage represented only a portion of predation, as the weasel was not the only predator on the mouse population. Most of Golley’s figures seemed to be reasonable. An analysis of the food chain is a very fruitful approach to the energetics problem. He did, however, get an unexpectedly high estimate for the assimilation rate of Microtus (90%). Most other herbivores assimilate from 65% to 76% of their food (Brody [1945, p. 801,McNab [1963], Pearson [1960]). If the rate ci