The biology of the deep ocean

The Biology of the Deep Ocean Peter Herring

O X FO R D U N IV E R S IT Y PRESS

The Biology of the Deep Ocean

Biology of Habitats Series editors: M . l Crawley, C. Little, T.R.E. Southwood, and S. Ulfstrand T h e intention is to publish attractive texts giving an integrated overview o f the design, physiology, ecology, an d behaviour o f the organism s in given habitats. E ach book will provide inform ation abou t the h ab itat an d the types o f organism s present, on practical aspects o f w orking w ithin the habitats an d the sorts o f studies w hich arc possible, a n d include a discussion o f biodiversity an d conserva­ tion needs. T h e series is intended for naturalists, students studying biological or environm ental sciences, those beginning in d ep en d en t research, an d biologists em barking on research in a new habitat.

T h e B iology o f R ock y S h ores Colin Little and JA . Kitching

T h e B iology o f P o la r H a b ita ts G.E. Fogg

T h e B iology o f P on d s an d L ak es Christa' Bronmark and Lars-Anders Hasson

T h e B io lo gy o f S tre a m s an d R iv ers Paul S. Giller and Bjorn Malmqvist

T h e B io lo gy o f M an g ro v es Peter J. Hogarth

T h e B iology o f Soft S h o res an d E s tu a rie s Colin Little

T h e B io lo gy o f th e D eep O ce a n Peter Herring

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OXFORD U N IV E R S IT Y PR ESS

Great Clarendon Street, Oxford 0X2 6DP Oxford University Press is a departm ent of the University of Oxford. It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide in Oxford New York Auckland Bangkok Buenos Aires Cape Town Chennai Dar es Salaam Delhi Hong Kong Istanbul Karachi IColkata Kuala Lumpur Madrid Melbourne Mexico City Mumbai Nairobi Sao Paulo Shanghai Singapore Taipei Tokyo Toronto w ith an associated company in Berlin Oxford is a registered trade mark of Oxford University Press in the UK and in certain other countries Published in the United States by Oxford University Press Inc., New York © Oxford University Press, 2002 The moral rights of the author have been asserted Database right Oxford University Press (maker) First published 2002 Reprinted 2002 All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, without the prior permission in writing of Oxford University Press, or as expressly perm itted by law, or under terms agreed with the appropriate reprographics rights organization. Enquiries concerning reproduction outside the scope of the above should be sent to the Rights Department, Oxford University Press, at the address above You must not circulate this book in any other binding or cover and you m ust impose this same condition on any acquirer A catalogue record for this book is available from the British Library Library of Congress Cataloging in Publication Data (D ata available) ISBN 0 19 854956 3 (Hbk) ISBN 0 19 854955 5 (Pbk)

Preface

I find the inhabitants o f the deep ocean to be a co n stan t source o f surprise an d delight. Every tim e we think we und erstan d the ecosystem an d the organism s they m anage to p roduce a new rab b it out o f the oceanic hat, so th a t we are required to readjust our previous perspective (picoplankton, iron lim itation, hydrotherm al vent com m unities, m icroscale vortex perception, red biolum inescence, phytodetritus, A rchaebacteria, gelatinous zooplankton, to nam e a few o f the rabbits). I find that audiences at every level are equally enthused ab o u t the novelty an d potential of deep ocean biology a n d it is my hope that this book will help to inform those who already have some inform ation b u t are looking for m ore. It is driven by personal enthusiasm a n d therefore inevitably som ew hat u neq u al in its em phasis on p articu ­ lar topics. Its organization is based on an ann u al series o f lectures given to C am bridge third year students. A n o th er au th o r w ould probably have h ad a differ­ ent view o f the sam e landscape. A lthough I have lim ited the n u m b er o f references in the text (because this was never intended to be an exhaustive survey) I hope the interested read er will be able to pursue a particu lar topic through the ones I have cited. T his has m ean t th at some colleagues will recognize their contributions b u t w ithout direct accreditation. To them I apologize. For those w ho m ay be unfam il­ iar w ith som e o f the organism s present in the deep ocean I have add ed a eucaryote bestiary in the form o f the A ppendix, em phasizing the attributes an d deep ocean contributions o f particu lar taxa. O ccanographv an d its associated technology has dism antled the b arriers betw een the classical disciplines o f science. T h e biology, geology, physics an d chem istry of the deep ocean are inseparably entw ined on all scales from the global to the indi­ vidual, a com m onality w hich is reflected in the present em phasis on biogeochcm istry. T h e organism s an d events in the depths o f the ocean can n o t be divorced from the processes an d conditions nearer the surface, an d I m ake no clear distinction betw een deep ocean biology7an d biological oceanography. O rganism s in teract with each other an d w ith their environm ent, in the ocean as on the land. T h e different scales an d details o f the interactions require different techniques for th eir elucida­ tion. T h e skills of, for exam ple, the ecosystem modeller, the fluid dvnam icist, the visual physiologist an d the m olecular biologist are all essential to in terp ret the in ter­ actions that drive the deep ocean system. M y own interest in, an d know ledge of, the deep ocean is a consequence o f the stim ­ ulus an d enthusiasm o f the m any colleagues w ho have fed an d n u rtu red m y initial curiosity. I have been fortunate in the scientific com radeship an d collaboration w hich has m ade seagoing the m ost rew arding aspect o f my w orking life an d in the

THE BIOLOGY OF THE DEEP OCEAN

opportunities for new observations an d u n d erstan d in g th a t research cruises in all the worlds oceans have provided. T h e periodic accessibility o f live (or at least fresh!) deep-sea anim als has been the spur to m uch o f m y w ork an d it has b een a p articu ­ lar delight to see a n d experience the new opportunities th a t have becom e available through the use o f R.OVs an d m an n ed submersibles. A fter studying the m idw ater fauna for m any years using nets not greatly different from those em ployed by the Challenger expedition m y first experience o f exploring the anim als’ ow n environ­ m ent in the Jo h n so n Sealink was truly inspirational. M ay all deep o cean biologists be similarly inspired by exposure to the realities o f the h ab itat a n d its com m unities. M any friends an d colleagues have been involved in this book, n o t only through their science b u t also through their kindness in com m enting on some or all o f it in earlier drafts. T h e ir com m ents were invariably helpful an d agreeably robust, an d have greatly im proved the final text. I owe a p articu lar d eb t in this respcct to T om A nderson, M a rtin Angel, R ichard Barnes, D avid Billett, Jo h n Blaxter, Q u en tin Bone, G eoff Boxshall, Sir Eric D enton, R on D ouglas, G w yn Griffiths, Patrick H olligan, Ia n Jo in t, M ichael L and, Justin M arshall, Nigel M errett, Ju lian Partridge, Philip Rainbow , Paul Tyler, an d Edith W idder. If I have n o t always fol­ lowed their advice to the letter I hope they will forgive me. Above all others I m ust acknow ledge the help an d continual en couragem ent an d coercion o f my series editor Colin Little, w ho carefully read all the first drafts o f chapters as they em erged erratically into the light an d cheerfully accepted all my cxcuses for dilatoriness. M y thanks are due, too, to C ath y K ennedy an d Ian S herm an at O xford U niversity Press for th eir patience an d for the occasional prodding th a t has finally brought this project to fruition. M ike C onquer, K ate Davis, an d R oger Hollies helped greatly in the p rep aratio n o f figures. B rian Bett, D avid Billett, G eoff Boxshall, H a rry Bryden, M artin Collins, D aniel D esbruyeres, Jo h n G ould, Steve H addock, Francois Lallier, R ichard L am pitt, Justin M arshall, M onty Priede, Paul Tyler, an d C raig Young kindly provided a nu m b er o f them . Everyone involved in deep-sea biology owes a great d eb t to the w ork an d writings o f the late N.B. ‘Freddy’ M arshall. I have n ot only enjoyed his w riting b u t also h ad the pleasure o f his friendship on land a n d com pany at sea. A fter his death it was a great privilege to be able to read an unpublished biographical essay w hich he was preparing. I am m ost grateful to M rs O lg a M arshall an d Freddy’s obituarists for m aking it available to me. I have n o t specifically cited it in this book b ut I know that I have been influenced by it. T h e re are so m any exciting discoveries in deep ocean biology th a t the problem s for an au th o r are how to keep u p and w hat to leave out. T h e pace o f research is accelerating an d has caught the public im agination, greatly aided by some excel­ lent scientific jou rn alism an d by the stunning im ages o f the deep sea an d its inhabitants now available bo th from television broadcasts an d from a w ide range o f websites. T h e old attitude o f 'o u t o f sight, o u t o f m in d ’ has been swept away on this tide o f new inform ation. T h e biology o f the deep ocean concerns us all an d 1 hope th a t this book wrill offer each read er som e new’ fact or insight to spark their interest an d to heighten their aw areness o f its significance — an d its magic.

Contents

C hapter 1

C hapter 2

T h e d eep -sea dim ension

1 2 2 7 15 25

Living, grow ing, an d daylight

27 27 31 37 41 48

T h e fuel source: prim ary production T h e seasonal cycle M easurem ents o f prim ary production G razing an d secondary production Conclusion

C hapter 3

Life a t the b o tto m T h e benthic environm ent Sam pling the benthos Food resources H ydrotherm al vents an d cold seeps T h e h adal zone Spatial heterogeneity Conclusion

C hapter 4

P a tte rn s an d ch an ges G lobal views an d p atterns H orizontal distributions Vertical distributions C onclusion

C hapter 5

1

T h e scale o f the task T h e vertical dim ension D ifferences betw een m arine an d terrestrial ecosystems M easurem ents and m ethods Biological sam pling C onclusion

O n b eing efficient Energy m anagem ent M axim izing energy input— how to eat a lot M axim izing assim ilation efficiency M inim izing energy o utput— how to keep up in the w'ater

50 50 52 60 63 69 70 71 72 72 73 86 96 98 98 98 102 103

THE BIOLOGY OF THE DEEP OCEAN

viii

C hapter 6

M etabolism , energy, an d pressure C onclusion

117 122

Feeling an d h earin g

123 123 124 126 136 138 142 145 147

Sensing vibrations V ibrations in w ater T h e hydrodynam ic recep to r system o f fishes S ound production by fishes Invertebrate hydrodynam ic receptors Sounds o f m arine m am m als E lcctroreception an d m agnetic cues C onclusion

C hapter 7

C h em ical m e ssa g e s T aste or smell? C hem ical cues an d receptors C onclusion

C hapter 8

Seeing in the d a rk Light in the ocean Eyes an d their design conflicts Fish " Invertebrates C onclusion

C hapter 9

C am ou flage, colour, and lights C am ouflage an d colour Lights in a dark environm ent: biolum inescence C onclusion

C hapter 10 Size, sex, and seasonality Life histories Fecundity an d egg size Body size Sex Juvenile characters (progenesis) Seasonality C onclusion

C hapter 11 A w onderful v a rie ty o f life: b iodiversity o f th e d eep -sea fau n a O rigins an d habitats W h at is biodiversity? C onclusion

148 148 149 160 161 161 164 164 174 186 188 188 197 216 217

217 224 227 231 234 234 237

239 239 240 253

CONTENTS

ix

References A ppendix

255

T he m a rin e phyla In troduction ‘K in g d o m ’ Protista: som e im po rtan t heterotrophs K ingdom A nim alia

Index

274 274 274 276 295

1

The deep-sea dimension

The scale of the task Look out across the ocean on a calm day, from the shore o r from the deck o f a ship. T h e vista is d aunting in its scale yet innocuous in its features. B ut b eneath this tranquil skin lies a teem ing horde o f organism s, from the tiniest viruses to the m ightiest whales, all o f w hich arc continually influenced by the physical features o f the seaw ater w ithin w hich thev m ove— an d by w hich they are moved. Evolution occurs apace: ‘Even the m ost peaceful place is full o f strife, w ith any weakness o f its inhabitants at once exploited’ (Jones 1999). T h is is the open-ocean ecosystem; it encom passes the w hole ocean an d excludes only the coastal seas w here w ater depths are less th a n 200 m. We struggle to describe an d to in terp ret the com plexity o f its interactions an d relationships, yet we m ust succeed: the im m ense but ill-understood effects o f the ocean upon o u r clim ate an d u p o n our future will in tu rn determ ine the evolution o f ou r planet. T h e whole open ocean an d its populations com prise a single ecosystcm; a p e rtu r­ bation in any one region may, in tim e, affect locations far rem oved from the orig­ inal site. Nevertheless, the scale o f this ecosystem is so d au n tin g that, in o rd er to describe, analyse, an d ultim ately predict the interrelations w ithin it, a pragm atic approach has to be taken, w hich recognizes particu lar subsets o f the w hole system. Each o f these can then be exam ined separately Useful subsets include recognizable assemblages o f organism s (i.e. species), w hich are associated with p articu lar com binations o f the physical an d chem ical features o f the environ­ m ent. T h e seas cover 71% o f the E a rth ’s surface: 65% is open ocean. T h e im m ense horizontal extent o f this are a suggests th a t biogeographic divisions m ight com prise one such group o f subsets, separating, for exam ple, the highlatitude faunas (Arctic an d A ntarctic) from the low'-latitude E quatorial ones. T hese distinctions are certainly real, an d useful, as we shall see later (C hapter 2). T h e vertical extent o f the open oceans, however, suggests another, unique, group o f ecological subsets, based on depth o f occurrence. T h e oceans have a m axim um vertical extent o f alm ost 11 km. 88% o f the oceans are d eep er th an 1 km an d 76% have depths o f betw een 3 an d 6 km. T h e average deip\h o f the oceans is som e 3.8 km. T his huge th ird dim ension im m ediately sets the oceans ap a rt from the prim arily tw o-dim ensional terrestrial ecosystcm. T h e re is no terrestrial equivalent to the colossal volum e o f the pelagic oceans, inhabited by countless organism s m ost o f w hich pass their entire lives suspended in its midst. I f we assum e th at the average

THE BIOLOGY OF THE DEEP OCEAN

dep th o f the continental life zone is 0.05 km (the height o f a very tall tree) then 99.5% o f the volum e occupied by life on E a rth is co ntained in the oceans.

The vertical dimension T h e unique vertical dim ension has led to the conceptual division o f the oceanic environm ent into three m ain realm s or zones, nam ely the epipelagic, (from the surface to 200 m), the m esopelagic (from 200 to 1000 m) an d the bathypelagic (from 1000 to 6000 m) (Fig. 1.1). T h e boundaries betw een these realm s correlate approxim ately w ith different ccological levels o f light intensity in clear oceanic water. T h e epipelagic realm m arks the limits o f the photic zone, w here daylight is adequate for photosynthesis. In the m esopelagic realm light from the surface (though very dim) m ay still be visible in the clearest o f oceanic water. T h e b athy­ pelagic realm is beyond the reach o f daylight. T h e 6000 m lower lim it o f the bathypelagic realm includes the vast extent o f the abyssal plains b u t excludes the deep trenches, w hich constitute the hadal realm an d extend from 6000 m to the greatest depths. T h e ir contribution to the open-ocean ecosystem is relatively small because they m ake up less th a n 2% o f the seafloor area. For descriptive purposes I shall apply the te rm ‘deep-sea’ loosely, a n d use it for all habitats below the epipelagic zone. T h e biological populations o f these w atery realm s arc divided conveniently into the plankton (plants o r anim als w hich drift in m idw ater, or are unable to swim against a current) an d the nekton (larger m id­ w ater anim als, such as fish, squid, an d shrim p, w hich can swim quite strongly). B eneath them all live the benthos (anim als w hich dwell on o r in the seafloor). But first we m ust be awrare o f how' the oceanic ecosystem differs from the one w ith w hich we are m ost familiar.

Differences between marine and terrestrial ecosystems We are com ponents o f the terrestrial ecosystem an d so we are inclined to assume its structure is the n o rm an d can be used to in terp ret the oceans. We have already seen th a t the scale o f the oceanic ecosystem m akes this a dangerously self-centred assum ption. T h e oceans are different. T h e first need is to adjust o u r m indset from an aerial to an aquatic one. T h e physics o f w ater determ ines m uch o f the uniqueness o f the oceanic ecosystem (D enny 1990) an d it is im p o rtan t th a t we recognize the consequences. I ’he differ­ ence in density is perhaps the m ost striking feature. A t sea level w ater has a density830 tim es th a t o f air; its density varies by only ab o u t 0.8% over the physiological range o f tem peratures an d is equally insensitive to pressure (increasing by only 0.5% for ever)' kilom etre o f depth).

DVM

BIOMASS

LIGHT

TEMPERATURE O’

5'

10-

15-

2 0 -С

ABYSSAL PLAIN

1.1

Some descriptive features of the oceanic environment. Meso- and bathypelagic inhabitants are represented by a lanternfish and an anglerfish, respectively. Also indicated are the extent of diel vertical migration (DVM; Chapter 4), the relative biomass of zoopiankton, the light regime, and the temperature profile of a warm ocean. (Illustration by N.B. Marshall and Lesley Marshall reprinted by permission of the publisher from Marshall 1971. C opyright © by the President and Fellows of Harvard College.)

THE BIOLOGY OF THE DEEP OCEAN

T h e high, relatively invariant density com bines w ith the circulatory m otion to provide the ocean w aters w ith m om entum . M o m en tu m , com bined w ith the car­ rying capacity o f w ater (w hether for salt, heat, or carb o n dioxide), gives the envi­ ro n m en t its defining characteristics an d sets the basic rules for successful survival w ithin it. In contrast, the density o f air is strongly d ep en d en t on b o th tem p era­ ture an d pressure; at one atm osphere the density o f air decreases by 13% over the range 0-4 0 °C an d the density (and pressure) at 5850 m is h alf th at at sea level. T h e w eight o f an organism depends on the difference in density betw een it an d the surrounding fluid; m ost biological m aterials have densities o f 1050- 1200 kg m j in air an d therefore effective densities o f 25-1 7 5 kg m in seaw ater o f density 1025 kg m T h e ir weights in air are thus betw een 50 an d 7 tim es th a t in sea­ water. G ravity places m ajor constraints on terrestrial life, requiring structural investm ent th a t is quite unnecessary in the sea (cf, a tree an d a kelp frond). T h e gravitational costs o f locom otion o n lan d arc potentially higher because b oth walking an d craw ling involve expenditure o f energy against gravity, a cost that does not exist for a neutrally buoyant anim al in the sea. Flying is even m ore costly. However, for a m arine organism the energy gained on the swings o f n eu tral buoy­ ancy m ay be lost on the roundabouts o f drag. T h e density o f the m edium directly affects the pressure drag, the force exerted on a stationary body by a moving fluid; an object o f a given size will experience a pressure d rag in seaw ater 830 times th at in air. D ynam ic lift is similarly affected, so a fin in seaw ater provides 830 times the lift it w ould in air. Life for an aerial organism is a largely con cern ed w ith the strug­ gle against gravity; staying aloft is generally a bigger problem th a n w ind speed. For an oceanic anim al the situation is reversed; n eutral buoyancy can be achieved in a variety o f ways (C hapter 5) but sw im m ing is energetically costly an d for all b u t the largest species the currents an d m otions o f the ocean arc well-nigh irresistible. Seaw ater has a viscosity at 20°C some 60 tim es th at o f air, an d the effects o f tem ­ peratu re on viscosity are reversed in the two m edia. O v er the range 0—30°C the viscosity o f air increases by 9% w hereas th at o f w ater decreases by 45% . T h e fric­ tional (viscous) drag experienced by a deep-sea fish (or one in cold po lar waters) is considerably g reater th an th a t facing a sim ilar fish in w arm surface water. A bird, on the other han d , w ould find flying h ard e r w ork in the tropics. A planktonic organism trying to rem ain in near-surface w aters against gravity faces a h ard er tim e in the tropics th an in the polar regions. M any species o f tropical plankton have an increase in the nu m b er or size o f surface projections th at help to offset the effects o f the reduced viscosity o f the w ater by increasing the d rag and red u c­ ing the rate o f sinking. S eaw ater affects the passage o f both sound waves an d electrom agnetic waves m uch m ore th an air. T h e bulk m odulus o f a m edium is the reciprocal o f its com pressibility and it determ ines the speed o f sound. S o und travels 4.3 times faster in w ater th an in air (1500 an d 350 m s 1 respectively). T h e wavelength at a given frequency is directly p roportio n al to speed so the w avelength in w ater will also be 4.3 times th a t in air. H igher acoustic frequencies will there-

THE DEEP-SEA DIMENSION

5

fore be needed in w ater th an in air for the echolocation o f objects o f sim ilar sizes. T h e attenuation o f sound in w ater is m uch lower th an th at in air so the range over w hich echolocation or sound com m unication can be used is sub­ stantially g reater (C hapter 6). T h e attenuation o f light, on the o th e r h an d , is m uch higher in w ater th an in air. O n a clear night the lights on aircraft, ships, an d beacons are visible over tens o f kilom etres; in the ocean the brightest o f underw ater lights are invisible at a range o f little over 100 m. T his has the overw helm ing effect o f consigning the w hole deep-ocean environm ent to total darkness, an d has stim ulated the evolution o f the bew ildering arrays o f living lights outlined in C h a p te r 9. T h e ocean’s density has the m ost direct an d im m ediate effect on the activities of its inhabitants. Its heat capacity on the other han d , com bined w ith the density, is probably the greatest m o dulator o f the ecosystem as a whole. W ater has a heat capacity alm ost 4000 tim es th a t o f air. T h e surface tem p eratu re o f the sea changes only very slowly in response to changes in air tem perature; the deep sea is at such a great range from these surface effects, a n d its heat capacity is so large, that any deep tem perature changes are largely im perceptible except on geologi­ cal time-scales. T em perature changes on lan d fluctuate (with o th er w eather) on a m uch shorter tim e-scale o f days or even hours an d only at the seasonal level do they begin to interact w ith the generation times o f organism s. T h e shorter-term fluctuations arc effectively decoupled from the ecology. In terrestrial ecosystems ‘w eather’ can therefore be regarded as high-frequency noise an d ‘clim ate’ change is the level at w hich physical an d ecological coupling occurs, on tim e-scales o f centuries o r greater (Steele 1991, 1995). Yet the physical processes in the ocean an d the atm osphere have the sam e basic fluid dynam ics; it is the differences in their tim e an d space scales that set the m arine an d terrestrial ecosystems apart. A cyclonic atm ospheric system o f ab o u t 1000 km in d iam eter lasts for ab o u t a week; the equivalent oceanic eddy has a diam eter o f ab o u t 200 km a n d persists for m onths or years. In the oceans the coupling o f the physical processes w ith the ecology is m uch closer; the organism s are m uch m ore closely linked to the oceanic ‘w eath er’ o f fronts, eddies, an d gyres, and the ‘clim ate’ o f deep circulation p attern s (Fig. 1.2). T h e p rim ary producers o f the ocean (phytoplankton) are very small a n d respond to b rief local m ixing an d turbulence. H erbivores are larger th an the phytoplank­ ton, a n d invertebrates an d vertebrates arc on an increasing scale o f size a n d life­ time. T h ere are few vertebrate (or other) large herbivores. O n lan d the prim ary producers are the largest an d the longest-lived organism s (perhaps 90% o f plant biom ass occurs in trees) and are largely independen t o f local weather. V ertebrate herbivores arc com m on (and include the largest species), yet they an d inverte­ brates are frequently sm aller th an the plants they cat. T h e dom inance o f large p rim ary producers on land is show n by a com parison o f the m ean body mass at m aturity o f organism s in the two environm ents: the m ean mass o f lan d organism s is lO'-TO8 times that o f oceanic ones. L arge body size (for plants an d animals) could be considered a terrestrial adaptation to com bat short-term environm ental variability (C ohen 1994).

THE BIOLOGY OF THE DEEP OCEAN

Fig. 1.2

Logarithmic space- and time-scales fo r (a) atmospheric processes and terrestrial populations and (b) ocean circulation processes and biological size groups in pelagic ecosystems. The figures demonstrate the temporal separation between atmospheric and ecological processes on land and the close correlation in the ocean. (Adapted from Steele 1991.)

T h ere are 3—5 orders o f m agnitude m ore biom ass p er u n it volum e or p e r unit are a on land th an in the sea. M uch o f the biom ass on land is structural m aterial supporting plants (e.g. wood); anim al biom ass is only aro u n d 0.01% o f the total. In the sea it is 10%, 1000 tim es greater. T h e net prim ary productivity o f the land is ab o u t 56 X 1012 kg С p er year (56 G t; T abic 2.1). T h a t o f the oceans is similar b u t w hen the two arc com pared p e r u nit volum e the lan d value is alm ost 200 tim es higher th a n th a t o f the oceans, em phasizing the nutritionally dilute nature o f m uch o f the oceanic environm ent. Far fewer specics have been described from the oceans, perhaps in p a rt a result o f the absence o f large p rim ary producers, cach o f w hich on land supports a whole com m unity o f specics. B enthic m arine com m unities ap p e ar to be m ore diverse th a n pelagic ones, probably because the

THE DEEP-SEA DIMENSION

7

spatial patchiness o f this environm ent lasts m uch longer th an its equivalent in m idw ater (C hapter 11). Analysis o f a n u m b e r o f different food webs has shown th a t despite the fewer m arine species, the trophic interactions in the sea ap p e ar to be m ore com plex th an on land, an d pelagic webs have the longest food-chain lengths (C ohen 1994) though the reasons are n o t yet clear. A n o th er unexpected result o f the analysis is th a t in m arine food webs the average relative biom ass o f anim al predators, an d o f anim al prey, is larger th a n in terrestrial food webs. A gain no satisfactory explanation has yet been proposed.

Measurements and methods W h at do we know7 ab o u t the physics, chem istry an d biology o f the deep oceans, an d how7do w7e m easure the different features? W h at m easurem ents m atter? O u r know ledge o f the oceanic ecosystem is entirely d ep en d en t u p o n o u r skills o f observation, sampling, a n d m easurem ent. O u r interpretations o f the dynam ics of the system will be profoundly biased by the lim itations o f o u r d ata set. ‘Classical’ interpretations an d assum ptions have been regularly o v erturned by im provem ents in sam pling techniques; in the early nineteenth century, for exam ple, the oceans were considered bare o f p lan t life an d the deep sea devoid o f anim al life. We believe that today’s paradigm s are m ore robust— b ut this is no g u arantee th a t they will fare any b etter u n d er the scrutiny o f future generations. T h e study o f the physicochem ical patterns, boundaries, an d characteristics o f the aquatic features o f the E arth (the hydrosphere) constitutes the science o f hydro­ graphy (cf. geography). T h e coastal seas an d open oceans dom inate the hydro­ sphere; indeed, to an alien visitor, this w ould be a w orld com posed largely o f water. O cean o g rap h ers m easure features o f the w ater colum n ranging from those (such as pressure) that are universally consistent, predictable, an d unaffected by the biology, to those (such as nutrients an d oxygen) th at are patchy an d greatly m odified by the organism s. A n o th er w ay o f looking at the w ater is to consider its com ponents (e.g. salts, heat, etc.) an d reflect on how7they affect its o th er p ara m e­ ters (e.g. density, light attenuation). Pressure is a continuous variable in th a t it is largely unaffected by other factors an d is linearly correlated w ith dep th throughout the entire w ater colum n. Its m easurem ent is relatively simple an d it is often used as a surrogate for d ep th because pressure increases by approxim ately 102 kPa (~1 b a r o r 1 atm osphere) for every 10 m o f w'ater depth. N o other p ara m ete r has this continuously linear relation w ith depth th ro u g h o u t the w'ater colum n. D ensity is the nearest equivalent, for gravity determ ines th a t this will increase w ith depth, th o u g h the resulting gradients will not be the sam e in different parts o f the ocean. T h e density o f seaw ater is affected by pressure— but n ot very greatly. Seaw^ater at 5°C has a density at the surface o f 1028 kg m _i; this increases at 4000 m to only 1049 kg m 3. T h e old tales o f ships an d th eir contents sinking until they reached a layer so dense that they w ould han g there suspended for eternity

THE BIOLOGY OF THE DEEP OCEAN

were only myths. It is possible to design instrum ents th a t will sink to a p artic­ ular density horizon, an d whose drift (described as Lagrangian) th en indicates the cu rren t at that depth, but skill an d great precision are req u ired to do so. T h e local density gradients are by no m eans inviolate; they are likely to be dis­ tu rb ed by any neighbouring w'ater m ovem ent. Light intensity is one o f the very few features th a t vary continuously w ith depth; the relationship is exponential, not linear, an d the absolute level is greatly affected by the concentration an d size o f light-scattering particles in the water, as well as by the d a y /n ig h t cycle. D ifferent colours (wavelengths) are differently affected by bo th scattering an d absorption w ithin the w ater itself (C hapter 8). D aylight is an ecological factor only in the epi- an d m esopelagic realm s: indeed in tu rb id w aters its influence m ay be restricted to little m ore th an the top 10 m. T h e two physical param eters that together have the m ost profound effects on the oceans are the tem perature an d salinity o f the water. Both have a direct effect on w ater density an d their com bined effects determ in e m uch o f the ocean structure, through the consequences o f this link. Salinity is a m easure o f the total salt content, not ju st th a t o f sodium chloride, although these arc the ions th at occur at highest concentrations (Table 5.1). Salinity is m ost conveniently m easured as electrical conductivity. A t a given tem perature, the higher the salinity the greater is the density o f water. Sim ilarly at a given salinity, the lower the tem p eratu re the higher is the density o f water. A particu lar mass o f w ater will have a characteris­ tic com bination o f tem perature (T ) an d salinity (S ), w hich in tu rn will determ ine its density an d hence its position in the layers o f decreasing densities stacked one above the oth er w hich m ake up the entire w ater colum n. T h e characteristic 7 7 ,S profile provides a recognizable signature for w ater o f a p articu lar origin, allowing its fate a n d m ovem ents in the ocean to be followed over long periods o f time. T h u s high-salinity w arm w ater from the M ed iterran ean Sea spills over the sill into the A tlantic O cean at the Straits o f G ibraltar and, despite its higher tem perature, is denser (by virtue o f its salinity) th an the surface A tlantic O ce an water. It th e re­ fore sinks until it reaches an equilibrium density an d fans o ut at th a t depth (600-1000 m) I’o r several thousand kilom etres into the A tlantic, being readily recognizable as far n o rth as the British Isles a n d west to the A zores as a thick anom alous layer o f deep w ater w hich is w arm e r an d saltier th an the layers b oth above an d below it (Fig. 1.3). As the M ed iterran ean W'ater flowrs ro u n d the obstruction o f the southw est co rn er o f the Ib erian peninsula (Cape St Vincent), it throw s off num erous eddies (known as M eddics) w hich are exam ples o f sim ilar processes occurring throughout the oceans (C hapter 4). M eddies are up to 100 km in diam eter an d their effects extend dow n to 2000 m. T h ey travel westwards, last up to 5 years, an d som e even reach the C arib b ean , although m ost collide fatally w ith seam ounts along their w ay (R ichardson et al. 2000). O n a larger scalc, density differences com bined w ith the effects o f the E a rth ’s rotation drive the great ocean currents a n d circulation patterns. C old surface w ater from the N orw egian Sea, for exam ple, sinks into the deep A tlantic an d flows ro u n d into the In d ian an d Pacific O ceans, finally retu rn in g to its surface

THE DEEP-SEA DIM ENSION

9

1.3

(a) Warm salty Mediterranean water, produced by surface evaporation and heating, flows into the Atlantic over the Gibraltar sill and is replaced by a less saline surface flow, (b) The outflow can be followed in its deep spread across the Atlantic by the salinity contours (isohalines) at a depth of 1000 m. (After Pinet 1996, from Wust 1961 copyright © by the American Geophysical Union.) (a)

"Tongue" of Mediterranean water

Evaporation and heating

origin after a m illennium o f travel (Fig. 1.4) (G ordon 1986). T his circulatory system is som etim es know n as the G lobal Conveyor. T h e range o f tem peratures an d salinities encountered in the oceans is not large. T em peratures range from some 35°C to -2 °C and salinities from 34 to 38%o (parts p er thousand). T h ere is

THE BIOLOGY OF THE DEEP OCEAN

10

therefore a relative constancy o f tem peratu re an d salinity on a coarse scale. M ost organism s, as they move through the water, will experience only grad u al changes in these an d in m ost other physical param eters. S h arp er boundaries (known as clines) m ay occur u n d er specific conditions w here lim ited m ixing allows the for­ m ation o f steeper chem ical or physical gradients (e.g. o f density at the pvcnocline, o f tem perature at the thcrm ocline, or o f oxygen at the oxycline). T h e only real physical boundaries occur at the sea surface an d the seafloor. D ensity differences betw een adjacent layers o f w ater greatly affect the degree o f mixing. T h e greater the density difference betw een contiguous layers, the g reater is the energy in p u t (e.g. as w ind at the surface) that is required to m ix them , an d hence the g reater is their stability.

The effects of organisms T em perature an d salinity are alm ost entirely unaffected by the activities of organism s in the water. T his is certainly not the case for m any o th er com po­ nents o f seawater, particularly nutrients, oxygen, a n d carb o n dioxide. Dissolved nutrients (particularly nitrate, phosphate, an d silicate) are taken up by phyto­ plankton an d inco rp o rated during photosynthesis into new tissue w here they are locked in an d m ade unavailable to oth er organism s (apart from predators). O nly

Fig. 1.4

The Global Thermohaline Conveyor Belt drives the ocean circulatory system. Surface water cools and sinks in the Norwegian Sea, flowing south and ultimately rising again from the southern hemisphere where it freshens and warms during its centuries-long cir­ culation round the world's oceans. (Courtesy W. X Gould.)

THE DEEP-SEA DIM ENSION

11

d uring the processes o f excretion, or death an d decay; are these nutrients released back into the seaw ater (in the process know n as rem ineralization). U sually this occurs as corpses (or faecal pellets) sink into d eep er w ater as p art o f the export flux from the euphotic zone. D eep w ater therefore contains higher levels o f these dissolved nutrients. T h ey may; however, disappear alm ost entirely from surface layers (above the therm ocline) w hen active photosynthesis is taking place an d they are locked into the phytoplankton, unless they are continuously replenished from deep er w ater by m ixing processes. O xygen is described as a ‘conservative’ elem ent, for it enters the oceans only from the atm osphere by direct solution in the surface w aters or from its p ro duction an d release by phytoplankton d uring photosynthesis— a process w hich also takes place only in the surface layers. All oxygen in the deep sea thus derives from the surface, usually carried dow n in the cold, dense currents produced by the extrem e cooling o f A rctic an d A ntarctic surface waters. In these cold w aters oxygen (and oth er gases) is also m ore soluble th an elsewhere. Nevertheless, all organism s in the sea, at all depths, need oxygen for respiration an d they gradually use up w hat has been b rought dow n from the surface. T h e residual oxygen concentrations in the w ater m ark the difference betw een the original levels a n d the uptake, an d give an indi­ cation o f the level o f biological activity (both o f m icrobes an d o f larger o rg an ­ isms) in particu lar regions o f the ocean. C a rb o n dioxide, too, enters the sea by solution from the atm osphere (as b icar­ bonate), b u t organism s at all depths also produce it d u rin g the process o f aerobic respiration. A m ajor ‘sink’ for carbon dioxide is its in co rp o ratio n (as carbonate) into the calcareous skeletons an d shells o f b o th plants an d anim als. W h en the organism s die the calcium carbonate often ends u p as vast seafloor deposits (e.g. foram iniferal ooze, ptero p o d ooze, coccolithophore plates, coral sand, bones, an d shells), w'hich geological processes m ay eventually convert into chalk or lim estone. T h e budget o f carbon dioxide in the oceans is a com plex one an d its uptake from, an d discharge into, the atm osphere is affected by the acidity, or p H . T h e proccss has a high scientific profile, because the oceans m ay have the potential for lim it­ ing the dam age d one by the artificially increased levels o f carb o n dioxide in our industrial atm osphere. I f m uch o f the excess can be absorbed by the oceans an d locked into new tissue by increased near-surface photosynthesis (and this m aterial is then exported from the surface into the sedim ents to form insoluble deposits on the seafloor), then the increases in atm ospheric carb o n dioxide an d the antici­ p ated clim ate changes (global w arm ing) m ay not be so severe. T h e oceans contain all the naturally occurring elem ents (as well as, increasingly, m any m a n-m ade isotopes, com pounds, an d materials). M an y o f the so-called ‘tra c e ’ elem ents (those present in very low concentrations) m ay also be im p o rtan t requirem ents for one or m ore species an d lim it their distributions or num bers. C opper, iron, strontium , v anadium , sulphur, an d boron, for exam ple, are all neces­ sary for som e organism s. Particular organic com pounds m ay also be essential. O rganism s com pete b oth for the critical inorganic elem ents an d for organic co m ­ pounds such as vitam ins w hen the levels o f these substances becom e limiting.

THE BIOLOG Y OF THE DEEP OCEAN

Remote sensing O u r ability to determ ine the concentrations o f the elem ents an d o f com pounds th a t are apparently nccessary for different spccies has im proved greatly in recent years. T h e laborious m ethods o f w et chem istry necessary for the quantitative analyses o f trace elem ents, an d the ultra-clean conditions req u ired to avoid co n ­ tam ination an d spurious data, arc being com bined an d autom ated. O n e o f the m ajor advances has been the developm ent o f rem ote sensors capable o f contin­ uous readings o f tem perature, conductivity, pressure, light, oxygen, nutrients, fluorescence, an d m any oth er param eters. By inco rp o ratin g such sensors into a towed vehicle, continuous profiles o f these features can now be o b tain ed in real tim e over large areas o f the oceans, opening the w ay for large-scale m apping and the d eterm ination o f global budgets. T h e advent o f the various sensors criss-crossing the occans m ounted on ships, on tow ed vehicles, on teth ered b u t m obile rem otely operated vehicles (ROVs), on free-ranging autonom ous u n d er­ w ater vehicles (AUVs), on fish, birds, or m am m als (M cCaffertv et al. 1999). an d coordinated into networks o f sub-sea observatories (O ceanus 2000), gives great hope for larger-scale analyses o f the oceans’ properties an d populations. T h e data from sensors on tow ed or autonom ous vehicles arc now supplem ented by the inform ation from sim ilar systems m ounted on anch o red or drifting buoys, providing long-term m onitoring at p articu lar locations an d in p articu lar w ater masses, respectively. R em ote sensing o f prim arily physicochem ical param eters has extended to satel­ lites, some o f w hich arc now dedicated to m arine observations. T h e ir d ata have dem onstrated the ubiquity o f eddies an d whorls (Richards an d G ould 1996) at all scales from the ‘m esoscale’ (100s o f km diam eter, Fig. 1.5) to the K olm ogorov scale (mm or less, C h a p te r 6), each scale having different im pacts on the o rg an ­ isms. Biological conclusions can be draw n from some o f these d ata, particularly those involving the distribution o f surface reflectance characteristics at different wavelengths. Such spectral d ata can then be converted to phytoplankton concen­ trations an d correlated w ith sca-surfacc tem peratures. T h e huge areas covered by satellite observations provide a com prehensive inventory o f ocean surface c h a r­ acteristics (Fig. 2.1). These characteristics are convertible, with varying degrees of difficulty and accuracy, into global carbon budgets an d their associated seasonal an d geographical fluctuations. It has been less easy to develop biological sensors capable o f quantitatively converting the three-dim ensional populations in the occans to electronic signals, but considerable progress is now' being m ade in the use o f au to m ated optical m ethods o f particle (and plankton) counting, p u m p sampling, flow cytomctry, holography, and, particularly, acoustic m easurem ents of anim al populations (Foote 2000; Foote and S tanton 2000).

Acoustic methods Acoustic techniques have been perfected by the fishing industry for their p artic­ ular target species but are now being aim ed at a m uch w ider range o f anim al

THE DEEP-SEA DIMENSION

13

1.5

The ubiquitous complexity of eddies and whorls in the surface ocean are made visible in this 1991 satellite image by the high surface reflectance caused by a bloom o f the coccolithophore Emiliana huxleyi between Iceland (top) and the Faeroe Islands (upper right). (Photo: P. Holligan.)

sizes (i.e. sm aller species, an d all kinds o f anim als, from jellies to krill) (Holliday et al. 1990). T h ere are still problem s because the reflected acoustic signal is not necessarily related to the size o f the organism b ut to b oth its ‘acoustic im ped­ ance' and its orientation in the beam o f sound. Nevertheless, the techniques allow rem ote observations o f populations in the sea on the sam e tim e an d space scales as the physical m easurem ents (Foote an d S tanton 2000). It is the only practicable m eans o f assessing, for exam ple, the S ou th ern O cean biom ass of krill, the pivotal species for so m uch o f the open-ocean ecosystem in th at p a r­ ticular region. T h e krill are now subject to substantial com m ercial fishing effort an d accurate quantitative assessment o f their populations is essential for effec­ tive m anagem ent o f both that fishery and others (such as those for icefish an d squid) w hich m ay ultim ately d epend on the krill stocks. In general, an anim al will only reflect sound o f wavelengths shorter th an itself. Sound travels at some 1500 m s 1 in seawater, so a sound o f frequency 150 kH z has a wavelength o f 10 m m . Low er frequencies will reflect a signal off larger anim als (e.g. com m ercial fishes) but for m easurem ents o f zooplankton p o p u la­ tions, frequencies higher than 100 kH z are essential. H igh frequencies are, unfor­ tunately. m uch m ore rapidly attenuated bv seaw ater th an low frequencies, so their

THE BIOLOGY OF THE DEEP OCEAN

effective range is m uch less. Acoustic m ethods have to balance the pow er ou tp u t required for a particu lar frequency against the m inim um range req u ired to reach the species o f interest. M idw ater organism s o f small size (< 1 0 mm) an d living at depths o f a few h u n d red m etres can n o t easily be detected by high-frequency pulses from surface ships. T h e solution is to m o u n t the acoustic system on a tow ed vehicle an d send it to the d ep th o f the anim als, w here the signal range o f the system will n ot be so limiting. Z ooplankton populations are rarely do m in ated by a single species, so the reflected acoustic signal needs to be in terp reted in the context o f a range of species an d sizes, each w ith its ow n acoustic characteristics. T his can be done by using a range o f frequencies sim ultaneously (Pieper et al. 1990), b ut the m ethods need ‘ground tru th in g ’ to identify the species likely to be contributing to the signal at any given locality. N et hauls arc still the m ost effective way o f achieving this, though sim ultaneous optical a n d acoustic im aging o f zooplankton is also p racti­ cable (Benfield et al. 1998; Jaffe el al. 1998). T rials o f an acoustic source m o u n ted on a n et have recently show n good correlations betw een the two sam pling m ethods, but the slow' speed o f a net precludes this being used d u rin g large-scale surveys (G reene et al. 1998). C ertainly acoustic m ethods are now capable b o th o f discrim inating betw een taxa o f sim ilar size an d o f identifying the m ain contributors to the observed backscatter. T h ey are also the only effective present m eans o f d eterm in in g the threedim ensional structure o f zooplankton patches. T h e strength o f a reflected acoustic pulse is a function o f the acoustic im pedance o f the anim al relative to seaw ater an d the area presented to the beam . Acoustic im pedance is the p ro d u ct o f the density o f the tissue an d the speed o f sound. A gelatinous anim al has sim ilar im pedance to seaw ater an d gives a relatively p o o r signal. Very high reflective signals are given by gas-filled spaces; small anim als w'ith gas bladders (e.g. som e siphonophores and m any fish) give m uch stronger signals th an larger ones w ithout them . T h e early recognition o f the im portance o f the use o f acoustics in biological oceanography resulted from the use o f relatively low -frequency echosounders (10-40 kHz) for continuous m easurem ents o f the w'ater d ep th an d for studies o f the surface features o f the seafloor. U nexpected layers o f sound scattering were encountered in m idw ater, at depths o f several h u n d red metres. Even m ore unex­ pected at th a t tim e was the fact that these layers ap p eared to move n earer the surface at dusk an d descend again at daw n, often separating into several discrete layers (Fig. 1.6). We now know th a t these ‘deep scattering layers’ (DSLs) are p o p ­ ulations o f anim als undertaking a regular m igration to an d from the surface (C hapter 4). Strong sound scatterers do n ot have to be very ab u n d a n t to give a strong D SL , so initial attem pts to identify the scatterers by fishing in an d o ut of the D SLs w ere not very conclusive. B etter d ep th control o f m o d e rn n et samplers, com bined w ith direct observations from submcrsibles, have show n th a t D SLs m ay be caused in different regions an d seasons by anim als such as fish, shrim p, an d siphonophores.

THE DEEP-SEA DIM ENSION

15

Fig. 1.6

Echosounder records made at a frequency of 36 kHz in the northeast Atlantic show multiple layers of backscattering. Some of the layers move up from about 400 m just before sunset (above), reaching the surface waters about an hour later. In the morning (below) they move down again just before sunrise. These layers are probably pro­ duced by mesopelagic fish or shrimp undertaking a typical diel vertical migration (Chapter 4).

0 g JZ

Q.

Ф a 700

0 g n Q. Ф О

700

t

SUNRISE

Biological sampling All estim ates o f biological populations, distributions, an d productivity in the open-ocean ecosystem d epend on the validity o f the sam pling techniques (Angel 1977). T h e organism s range in size from viruses to whales. We can neither h arp o o n a virus no r filter a whale; no one sam pling m eth o d can be effective across the w hole size spectrum an d different techniques are used to sam ple different size ranges w ithin it (Table 1.1) (Clarke 1977; O m o ri an d Ikeda 1992; H arris et al. 2000). In addition, the techniques for sam pling the pelagic populations in the open ocean and the benthic ones on the seafloor are very different, although the questions that the samples are intended to answ er are often similar. Benthic sam pling m ethods are sum m arized in C h a p te r 3.

Small organisms At the smallest size ranges o f interest are organism s such as viruses an d bacteria (< 1 (im). T hese can be collected in seaw ater samples that are then concen trated bv centrifugation or by suction filtration through filters with very fine pores. Bacteria and viruses can then be stained, identified, an d cou n ted directly on the

THE BIOLOGY OF THE DEEP OCEAN

16

Table 1.1

Size ranges o f different categories of plankton

Pico

Nano

Micro

Meso

Macro

Mega

0.2-2.0 ц т

2.0-20 ц т

20-200 ц.т

0.2-20 mm

2-20 cm

20-200 cm

Plankton is functionally divisible into zooplankton (the animal heterotrophs) and phytoplankton (the photosynthesizing autotrophs). Some species have intermediate styles of nutrition. Bacterioplankton is a term sometimes used fo r pelagic heterotrophic bacteria; they are usually included in picoplankton. Nekton comprises the larger animals (e.g. crustaceans, squid, fish, etc.) that can swim against a current.

filters, using electron m icroscope techniques. T his is a very laborious procedure an d every m anipulation o f the sam ple reduces the accuracy o f the result. T h e procedure has been greatly im proved by the use o f bacteria-specific fluorescent stains, w hich allow the organism s to be cou n ted (m uch m ore rapidly) u n d er a light m icroscope. Som e differentiation betw een different groups o f b acteria can be achieved w ith these m ethods, b u t for com plete identification it is usually necessary to culture the organism s. T his is a very inefficient process, because only a very small p roportion (< 5 % ) o f the bacteria recognizable in seaw ater can be grow n in culture. A recent approach has been to extract bacterial ribonucleic acid (RNA) from seaw ater samples an d then to exam ine the genetic diversity in this m aterial, rath e r th a n looking directly at the organism s. T his m eth o d shows th a t there is a great range o f genetic diversity in the bacterioplankton, verv m uch m ore th a n th a t present in know n spccies o f m arine b acteria (G iovannoni an d G ary 1993). T h e corollary is th a t there are m any m ore species o f b acteria out there th an arc at present recognized. T h e sam e variety is to be found am ong the sm aller eukaryotes (Lopez-G arcia et al. 2001; M oon-van der Staay et al. 2001).

M ost early studies o f m arine bacteria assum ed th a t they were free-living in seawater. It is clear from m ore recent wrork th a t m any (probably a m ajority) are in practice associated w ith one o r other type o f particle, ranging from m arine snow to the surfaces an d gut flora o f larger anim als. T his greatly com pounds the problem o f achieving accurate values o f abundance. T h e small pore size o f the filters limits the collection o f samples by filtration to relatively small volum es o f wrater; organism s m ay also adhere to the walls o f containers during collection an d preparation. In addition, the m echanical processes o f filtration easily7 disrupt the m ore delicate specics o f m icroorganism s, ren d erin g them unrecognizable. T h e problem s o f sam pling at the smallest size range o f organism s are gradually being overcome. D evelopm ents in flow cytom etry allow the characterization an d counting o f particu lar kinds o f m icroorganism on a continuous basis. T h e effort is being fuelled by the increasing evidence o f their im portance in the energy budgets o f the oceans (C hapter 2). Som e ab u n d a n t anim als (e.g. larvaceans) rely on m icroorganism s for their m ain energy source. T h e ir success at cap tu rin g this size range o f particles is m uch envied by m any m arine microbiologists.

THE DEEP-SEA DIM ENSION

17

Medium-sized organisms O rganism s larger th a n about 20 (J,m are routinely sam pled w ith nets. D ifferent m ethods are preferred for the m ore dclicate species at th e low er en d o f the size spectrum (e.g. flagellates an d ciliates); in order to quantify these organism s w ater samples are centrifuged o r carefully filtered a n d m icroscope p reparations o f live or stained organism s in the concentrated sam ple are subjected to im age analysis. N ets are used for a size range extending over alm ost 5 orders o f m agnitude (from 20 J i m phytoplankton cells to 2 m tuna) an d provide a m eans o f concentrating the organism s from the seaw ater in w hich they live (O m ori an d Ikeda 1992; Sam eoto et al. 2000). T h e net is tow ed (or pursed) through the w ater an d it is assum ed th at the w ater flows smooth!)- an d freely through the meshes an d th a t everything larger th a n the m esh size is retained. T h e design o f a net is critical to its effective use: the area o f the holes in the m esh m ust be sufficient for all the w ater entering the m o u th (at the in ten d ed tow ing speed) to flow sm oothly out through the m esh o f the net. A ny reduction in the fil­ tration area below the required m inim um will cause w ater to back up in the net an d will result in a pressure wave in front o f the m o u th , keeping m any organism s out. f o r each net there is therefore a com prom ise betw een m o u th area, length, m esh size (= area o f filtration), an d tow speed. T h e com prom ise is d eterm ined prim arily by the size range o f the organism s that the net is designed to sample (O m ori an d Ikeda 1992). In the three-dim ensional environm ent o f the oceans it is essential to determ ine the depth at w hich particu lar organism s live. T h e d ep th range over w hich a net fishes is therefore a very im p o rtan t piece o f inform ation. T h e simplest m eans of achieving this is to lower a net w ith a w eight on the en d to a know n d epth (which can be determ in ed approximately- by the length o f line paid out) a n d th en to haul it back vertically to the surface. All the organism s in it will have been living betw een its m axim um depth an d the surface, an d th eir concentrations in the fil­ tered colum n o f w-ater can be calculated. By increasing the d epth o f successivc hauls, an d subtracting from the deep ones those anim als already caught in the shallow er ones, a crude picture o f the depth o f occurrence o f different species can be built up. For m any years this was the only m eth o d available. Vertically hauled nets have a disadvantage in that the bridles attach in g the tow ing line to the net m outh, an d the line itself, plough through the w ater im m ediately in front o f the net, an d produce a pressure wave ah ead o f it, frightening away m any anim als that are active swimmers. O n e solution to this problem has been to m ount nets in rigid fram es (usually in pairs) on either side o f the tow ing line, rath e r like a p air o f Bongo drum s (not surprisingly these are know n as Bongo nets), so th a t there is nothing directly in front o f the m outh. A n o th er solution is to use a free-rise net; this has no attached line an d has buoyancy spheres ro u n d the m outh b u t is w eighted w ith ballast so that it sinks slowly w hen p u t in the water. A t a particu lar dep th the ballast is released (either by an acoustic signal from the ship, o r a tim ing device) an d the net then rises slowly to the surface u n d er its own

THE BIOLOGY OF THE DEEP OCEAN

buoyancy, fishing all the way. Such nets can potentially be m ade very large (> 1 0 m diam eter) if assem bled in the water, b u t have proved difficult to deploy. T h e re are obvious disadvantages in only being able to fish a n et from a fixed dep th back to the surface; a m uch b etter indication o f w here anim als live can only be achieved by opening an d closing the nets at know n depths. For vertical nets this was (and often still is) done by sliding a heavy w eight (or ‘m essenger’) dow n the wire to activate a closing m echanism w hich throttles the n et at a specific d epth or (for sm aller nets) closes the m outh by m eans o f a spring-loaded butterfly valve. T h e resulting sam ple has a wrcll-defined vertical d ep th range. T h e volum e of w ater filtered by a vertical net is d eterm in ed by the vertical range over w hich it fishes. It is therefore not possible for a vertical net to filter a large volum e o f w’ater over a lim ited dep th range (unless o f course it were to have an unm anageably vast m outh area). N ets tow ed obliquely or (better) horizontally get over this difficulty. O n e ingenious system used in the past h u n g several nets at different points (i.e. depths) along a traw l wire an d closed them w ith a m essenger system th a t throttled each net as the m essenger hit, at the sam e tim e releasing an o th er m essenger to continue dow n the wire an d activate the next net. T h e system used conical nets an d still h ad the problem o f bridles (and the m ain traw l wire) in front o f the m outh, b u t Bongo nets can be used in a sim ilar way. M o d e rn net systems use rem ote signals to trigger events such as opening an d closing (Clarke 1977). T hese signals m ay be either acoustic pulses or, if the nets are tow ed on an electrically conducting or fibre optic cable, electrical or optical signals sent directly dow n the cable. A single n et tow at a given d ep th requires th at the net be first low ered to the correct depth, th en opened, fished, an d closed again, an d finally recovered by hauling back to the surface. M u ch tim e can be saved, particularly in dcep-w-ater sampling, if several nets can be fished in sequence after low ering an d before hauling back to the surface. M ultiple net systems have therefore been developed, w ith up to 20 separate nets, fished one after the other (Sam eoto el al. 2000). In the M O C N E S S gear (M ultiple O p en in g an d Closing N et E nvironm ental Sam pling System) the nets arc m o u n ted in a fixed fram e an d o pened in sequence by the release o f spring- or elastic-loaded arm s. T hese m ultiple nets can be any one o f a variety o f sizes an d meshes, depending on the target organism s, an d can carry a variety o f environm ental sensors, including the bioacoustic systems noted above (Wiebe et al. 1985). A nother m ultiple system is b ased on the T ucker trawl. T h e original traw l was a single net w ith a rectangular m outh, designed to fish at an angle o f 45°. T h e R ectangular M idw ater Traw l system developed from it has an 8 m 2 n et w ith 4.5 m m m esh an d m oun ted above it is a 1 m 2 n et w ith 0.33 m m m esh. T h is system is designed to catch a w ider (and overlapping) size range o f organism s th an either net w ould do by itself. Because the nets open an d close sim ultaneously the catches are directly com parable. A m odification o f the system has three such pairs o f nets, w hich are fished in sequence, saving the low ering an d recovery time. T hese nets m ay be operated cither acoustically or by direct elec­ trical signals dow n the wire.

THE DEEP-SEA DIM ENSION

19

M ultiple nets can be used to exam ine either the horizontal distributions o f o rg an ­ isms (several nets are fished one after an o th er at the sam e depth) or their vertical stratification (the nets are fished in contiguous vertical strata). Smaller-scale dis­ tributions can be exam ined w ith the L onghurst—H ard y P lankton R ecorder (LH PR), a m odification o f the C ontinuous P lankton R ecorder th a t was designed for routine tow ing by m erch an t ships. In this system the catch reaches the tail o f the net, w here it is strained through a section o f a gauze m esh w ound on a reel. A t p red eterm in ed intervals the reel winds on, advancing the filtering region. T h e previous, used, section w ith its captu red plankton is sandw iched w ith an o th er roll o f gauze an d the two are w ound onto a storage drum , w ith the plankton trap p ed betw een them . T h e resulting long strip o f plankton sandw ich com prises a series of, say, 5-m inute samples w hich, once analysed, can be ‘re a d ’ ra th e r like a series o f film frames. T h e L H P R acts like a single net w ith very m any sequential o pening an d closing codends (the bucket in w hich the catch collects). M ultiple codend buckets have been designed for use on larger trawls, but all such tail-closing devices have the problem th a t plankton m ay n o t w ash rapidly dow n the net an d some will ‘h an g u p ’ on the m esh on the way. T his m eans that anim als caught in the n et in one tim e perio d m ay take different tim es to reach the codend, b lurring the spatial dis­ tinction betw een adjacent samples. T his can only be overcom e by having the opening a n d closing taking place at the m outh o f the net rath e r th an at the codend. T his is now the m e th o d o f choice for larger nets. H ang-ups are only one problem to be faced in the accurate quantitative use o f net samples. A n o th er is th a t o f m esh clogging. I f spiny o r gelatinous anim als are caught they m ay well stick to the m esh o f the net, blocking some o f the filtration area, so th a t the area is finally reduced below the m inim um value for sm ooth fil­ tration. T h e w’ater backs up as a forw ard pressure wave, w hich greatly reduces the sam pling efficiency (rather like trying to catch a fish in an aq u ariu m w ith a ja r already full o f water). Even w ithout a pressure wave ah ead o f it, a net will be clearly visible in well-lit w ater an d will further signal its presence to the anim als in front by its noise, turbulence, and, in the dark, even by the lum inescence it may cause. M any' anim als are undoubtedly' able to avoid such nets. T h e responses of fish to bottom trawls, for exam ple, have been w ell-docum ented: several specics swim for long periods o f tim e ju st ah ead o f the net, finally falling back into it only w'hen they' becom e exhausted. W hen the catches o f a p articu lar species are con­ sistently low er by day th a n they are by night the cause is probably visual avoid­ ance, b u t it can easily be confused w ith the effects o f diel vertical m igration (C hapter 4). T h e m ore active a specics, the m ore likely it is to be able to avoid a net, an d larger individuals will find it easier to do so th an small ones. T his m ay well result in an ap p a ren t bias tow ards sm aller specim ens in a sam pled p o p u la­ tion. In contrast, som e active anim als th a t w ould norm ally avoid a net (e.g. squid) m ay go into it specifically to feed on those specim ens already there. T h e presence in the catch o f fish w ith squid beak bite-m arks, despite the absence o f squid, gives aw ay w hat has happened. Som etim es the p e rp e tra to r is slow in escaping after its m eal an d is also caught.

THE BIOLOGY OF THE DEEP OCEAN

A ttem pts to reduce the problem o f avoidance have focused either on such attrib ­ utes as n et colour and visibility or on designing faster nets. T h e larger nets are usually tow ed at speeds less th a n 2 m s 1 an d one w ay o f increasing the p racti­ cable tow ing speed is to have a m uch sm aller m o u th area opening into a m uch larger filtration cham ber b ehind it. H igh-speed (4-5 m s 1) p lankton samplers, for exam ple, used in fisheries surveys for fish larvae, have a large net enclosed in a rigid torpedo-like fram e w ith a small circular m o u th opening in the centre of the nose cone, i.e. a very high ratio o f m esh area to m o u th area. T h e fast flow through the m o u th is rapidly decelerated by the conical expansion o f the space b ehind it so th a t flow through the m esh is relatively slow' an d the catch rem ains undam aged. O n e pro g ram m e attem pting to sam ple those m esopelagic anim als th at are not caught by sm aller research trawls used a very large com m ercial fishing traw l (an Engels trawl) fished on twin wires in the South A tlantic. T his net caught b oth m ore an d larger specim ens o f the know n m esopelagic fau n a b ut n o t a different fauna. It could not be closed, a n d its huge area m ean t that the increased d rag p re ­ vented it from being used at bathypelagic depths because there was n o t enough wire on the winches! T h e experim ent was n ot continued. C om parisons betw een the benthopelagic fish populations o f one area sam pled w ith different gears, based on catches m ade by the sam e Engels traw l an d two o th er (smaller) b o tto m trawls, show ed m arked differences in the sizes an d abundances o f p articular specics w hen calculated from the different nets (H aedrich an d M errett 1997). Biologists generally prefer to m ake consistent use o f a single gear an d to regard their d ata from different depths, areas, or seasons as relative com parisons rath er th an absolute truths. I f samples are to be taken from abyssal depths (either in m id ­ w ater or on the bottom ) even small trawls present difficulties. For a small semi­ balloon o tter traw l tow ed on a single wire at 2 -3 knots (1-1.5 m s ') it m ay be necessary to pay out some 15 000 m o f wire to reach the abyssal plain (at 5000 m), by w hich tim e the traw l will be some 13 km b eh in d the ship. W ith this m uch wire out the drag on the wire will be m uch greater th an th at o f the n et on the end o f it! L arger nets, like the Engels trawl, are therefore im practicable for deep deploym ent, as noted above. T h e one certainty is th a t all p opulation estimates, by w hatever gear, an d o f w hatever species, will be underestim ates. O ptical techniques are now becom ing routinely av ailable to survey the plankton in real tim e from platform s travelling at up to 5 m s 1(Foote 2000). In the optical particle counter (OPC) the organism s flow th ro u g h a narrow slit, in terru p tin g a light b eam as they pass. T h e ir n um ber an d equivalent spherical d iam eter are then continuously recorded. Particle sizes o f up to a few m illim etres can be m onitored, b u t activc an d larger organism s will n o t be counted. L aser-scanning systems are being developed to increase the effective ap ertu re size an d to m o n ito r larger effec­ tive ‘slices’ o f the water, thereby including a larger size range o f organism s. Im aging systems, including holographic ones, allow identification o f p lankton types at fine spatial resolution an d are dem onstrating how b o th phytoplankton an d zooplankton are often aggregated in very thin layers o f w ater stratified by

THE DEEP-SEA DIMENSION

21

virtue o f their density differences an d ju st centim etres to a few m etres thick. T h e value o f these kinds o f techniques is th a t they are effectively rem ote an d nonintrusive an d the organism ’s behaviour can be m o n ito red w ithout necessarily altering it. T hese m ethods are getting to grips w ith the huge sam pling problem o f d eter­ m ining the three-dim ensional distribution o f species in the o cean so th a t the sep­ aration betw een individuals can be m ore accurately assessed th an nets presently allow. O n e o cean ographer suggested that the ideal system w ould be an endothcrm ic nuclear device that w ould instantly freeze a cubic kilom etre o f w ater; it could then be tow ed to a lab oratory for gradual thaw ing an d the spatial coordi­ nates o f all o f its inhabitants determ ined! A n interesting recent ap p ro ach has been to push a m esh slowly through the w ater on the front o f a subm ersible an d record the lum inous flashes o f plankton species as they are encountered. T his establishes the spatial arran g em en t o f those species w ith distinctive flashes th at occur w ithin the passage volum e o f the m esh (W iddcr an d Jo h n sen 2000). It is, o f course, lim ited to particu lar lum inous species— an d assumes th a t they all flash on contact w ith the m esh an d m ake no attem p t to avoid it. N ets present a particu lar problem w hen sam pling delicatc organism s (e.g. manygelatinous species). A nim als such as siphonophores an d ctenophores are very easily dam aged or destroy-ed by the m echanical abrasion o f the n et an d m ay either break into fragm ents small enough to go th ro u g h the m esh o r simply dis­ integrate into an unrecognizable jelly-. W orking w ith n et-caught specim ens is akin to trying to reconstruct a snowball after it has hit a wall. Recognition o f the im portance o f such anim als in the econom y o f the oceans has h ad to w ait for b etter m ethods o f observation an d sampling, particularly open occan (or ‘blue w ater’) scicntific S cuba diving a n d the use o f m a n n ed subm ersibles an d ROVs w ith video cam eras (Fig. 1.7). S iphonophores an d m edusae are know n to consum e large num bers o f fish larvae, w ith daily consum ptions o f up to 60 an d 90% , respectively, o f the available larvae. T h e ir p red ato ry im portance em p h a­ sizes the void in our ecological know ledge w hich results from o u r inability to d eterm ine their populations accurately. T h e lum inescence technique noted above is applicable to som e o f these animals. N et catches seriously underestim ate the num bers o f the m ore delicate specics an d are rightly criticized for potentially capturing only the slow, the stupid, the greedy; an d the indestructible. Nevertheless, they arc still the best general tools available for sam pling m ost oceanic organism s. I f they are to be used for accu­ rate quantitative w ork then it is very im p o rtan t th a t the flow through the net is known; m ost nets now incorporate a flow7 m eter in the system. K now ledge o f the distance travelled by the tow ing vessel is not enough for calculation o f the volum e filtered, even w ith tod ay ’s G lobal Positioning System (GPS) precision, because the currents at the dep th o f the net m ay be quite different in b oth direc­ tion an d speed to those experienced at the surface. A lmost any sensor can p o te n ­ tially- be add ed to a net to transm it inform ation back to the operator. It is perfectly practicable to fish not ju st at a specific d epth but, w ith the appropriate

THE BIOLOGY OF THE DEEP OCEAN

Fig. 1.7

Siphonophores, such as (a) Bargmannia elongata, are very delicate and impossible to capture intact with a net. This specimen was captured by a manned submersible, the Johnson Sealink, which also (b) videorecorded the extraordinary fishing posture of this specimen (3-4 m long) of an undescribed siphonophore. The ecological importance of these animals would never have been appreciated without the sampling and observations achieved by using submersibles and remotely operated vehicles (ROVs). (Images: S. Haddock and Harbor Branch Oceanographic Institution.)

sensors, along a tem perature interface, at a defined light intensity, o r w ithin the particle plum e o f a deep-sea hydrotherm al vent. Acoustic an d direct telem eter­ ing o f real-tim e inform ation not only ab o u t environm ental variables but also about features o f net perform ance, such as m outh height an d w idth, depth, aspect, height off the bottom , flow, etc., have been p ioneered by b oth the co m ­ m ercial fishing industry an d biological oceanographers. T h e first set o f users are seeking to m axim ize the effectiveness o f the net in catching the target species, the second are also trying to im prove o u r quantitative und erstan d in g o f the three-dim ensional distribution o f open-ocean anim als in tim e an d space. O ne feature o f using nets as quantitative sam plers, to estim ate the abundances o f the organism s they catch on the basis o f a ran d o m distribution, is th at the nets sam ple such a small fraction o f the environm ent th at any anim al o f which we have but a single specim en should in reality be very num erous. T h u s if ju st one specim en o f an anim al is taken durin g the course of, say, 100 trawls using a net with a m outh area o f 8 m 2, each tow ed for 2 h at 1 m s 1, we w ould regard it as very rare. Yet its abundance w ould be 1 p er 5.8 X 101’ m !, that is individ­ uals w ould be about 200 m ap a rt if evenly spaced. W ere it to be globally (and random ly) distributed at all depths we should expect there to be ab o u t 2.5 X 10" individuals worldwide. O f course the anim al w ould not be distributed like that, but w hatever p attern we assum ed would still imply a lot o f individuals (if it has anv avoidance ability it will be even m ore abundant). A nything we catch frequently should be massively abundant. Scaling up like this has huge pitfalls (see C h a p te r 11) but does em phasize w hat a pitifully small fraction o f the oceanic environm ent we have actuallv sam pled an d how w ary we should be in our interpretations o f those samples. We m ust appreciate that ‘ra re ’ in oceanic term s simply m eans ‘rarely caught'.

THE DEEP-SEA DIMENSION

23

Large animals N ets arc alm ost useless for the quantitative capture o f very large anim als. Even the im m ensely long drift nets now em ployed by fisherm en in m any areas o f the w orld can n o t tell us w hat the population densities are, although they m ay enm esh a wide variety o f anim als. Q uantitative nets designed to catch sm aller anim als cannot be scaled u p effectively. Very large nets can n o t be o pened an d closed, and rapidly becom e impossibly difficult to handle. T h e users o f large com m ercial nets, in m idw ater an d on the bottom , are inevitably m ore con cern ed ab o u t m axim iz­ ing the capture efficiency than the)' are ab o u t d eterm in in g the population densities. A m ore successful approach for the capture o f large anim als is to target individu­ als rath e r th an populations, particularly by luring th em w ith bait, ju st as a sport fisherm an does. L ong lines o f baited hooks either suspended in the u p p er few tens o f m etres or laid on the bottom are very successful in the capture o f fast-moving fish such as sharks an d tuna, as well as m any squid, while longlines h u n g several h u n d red m etres deep take the black M ad eiran scabbard fish Aphanopus carbo. Longlines are rath e r indiscrim inate in w hat they catch a n d the near-surface ones, for exam ple, cause the d eath o f foraging seabirds such as albatrosses, as well the fish for w hich they are set. B aited traps placed on the bottom are successful research tools for sam pling b o th fish a n d crustaceans a n d provide the basis for several successful crustacean fisheries in depths o f several h u n d red metres. Large squid are particularly active anim als, an d consequently very difficult to catch, indeed impossible for m any nets. A n alternative ap p ro ach has been to exam ine the stom ach contents o f m ore efficient catching systems such as tuna, seabirds, seals, dolphins, an d toothed whales, particularly the sperm whale. T h e h o rn y m aterial o f w hich squid beaks arc m ade is alm ost indigestible an d the beaks accum ulate in the stom achs o f these anim als an d can be collected an d identified. C om parisons o f these beaks w ith those from sm aller specim ens o f the sam e specics (caught in nets) indicate th a t sperm whales in p articu lar are taking very m uch larger squid th a n oceanographers have ever caught. A very large anim al that has no need ever to com e to the surface could easily rem ain unknow n in the deep oceans— an d it need n o t even be ‘ra re ’ in term s o f num bers. G ian t squid are know n largely from dead specim ens th a t have floated to the surface an d been w ashed ashore (by virtue o f their buoyancy systems, C h a p te r 5), as well as from sperm w hale stom ach contents. I f these anim als h ad sunk instead o f floated we m ight still regard the occasional sailors’ rep o rt o f sighting giant squid as ab o u t as credible as the sighting o f a m erm aid (Fig. 1.8). M uch o f o u r inform ation on the activities and num bers o f the larger m arine m am m als cam e originally from the activities o f their hunters. T h e present tech­ niques rely m uch m ore on the recognition an d following, o r periodic observation, o f specific individuals an d social groups, using criteria such as fin o r head markings. W ork on the larger fishes has m ade m uch use o f tag an d recapture techniques for establishing individual behaviour patterns. R ecent technological advances have

THE BIOLOGY OF THE DEEP OCEAN

Fig. 1.8

Research trawls hardly ever capture giant squid. We have no effective means of sampling their abundance or of assessing their ecology except through their remains in sperm whale stomachs and the occasional strandings of dead specimens, like this 4.66-m Architeuthis washed ashore north of Aberdeen. (Photo: M. C ollins/I. G. Priede.)

m ade it possible to extend this to bait tagging, so th at the initial capture o f the anim al is not always nccessary. It simply has to be induced to swallow the tag with the bait. M iniaturized recording and transm itting devices are now available which can be attached to large crustaceans, fishes, turtles, sea birds, an d m am m als to record a variety o f physiological functions an d environm ental p aram eters (M cCaffertv et al. 1999), or even to video their n o rm al activities. T h e d ata can be dow nloaded to a satellite either w hen the anim al com es to the surface or w hen the tag is autom atically released to float up by itself. By this m eans, individual fishes, penguins, seals, and whales can be tracked for hundreds o f miles while providing a com plete record o f the depths an d durations o f their dives (Fig. 1.9). T h e d ream o f

THE DEEP-SEA DIM ENSION

25

Fig. 1.9

Animals can be used as vehicles for sensors. Data recorded by an instrument package on a southern elephant seal highlight (a) the depth and timing of each dive (time markers 15 mins) and (b) the mean water temperature during the dives, and show (c, a) how much of the for­ aging time is spent in the discontinuity between the cold water at 100-300 m and warmer deeper water. (From Hooker etal. 2000, with permission from the Challenger Society.)

(b)

T°C

(c) 0

% o f dives 4

8

12

16

П Л ’

islls s i

"r— * i —

J

rr“

m any deep-sea biologists is to have sim ilar inform ation available for m any o f the sm aller meso- an d bathypelagic fishes an d invertebrates. We will th en be able to integrate the behavioural characteristics o f individuals w ith the distributional data on populations th a t have been gained using nets a n d o th er tools.

Conclusion T h e oceans are very large an d very deep, an d life occurs everywhere. T h e verti­ cal dim ension provides a convenient w ay o f describing some o f the different

THE BIOLOGY OF THE DEEP OCEAN

environm ents an d their inhabitants as epi-, meso-, or bathypelagic, w ith their benthic parallels. It is necessarily an artificial distinction in so far as there are no sharp boundaries betw een these categories. T h e absence o f physical boundaries sets the oceans ap a rt and, in theory, should simplify the task o f thorough sam ­ pling. In practice, the scale o f the sam pling problem defeats all b u t the m ost p e r­ sistent o f attem pts to quantify the physics, chem istry an d biology, all o f w'hich are continually reshuffled at all scales by the circulation patterns. T his reshuffling is the oceanic equivalent o f terrestrial ‘w eath er’ an d the oceanic ecosystem is far m ore closely coupled to this ‘w eather’ th an is the terrestrial one to its atm ospheric equivalent; the physics an d biology o f the oceans react on sim ilar time-scales. T h e properties o f seaw ater define an d determ in e b oth the characteristics o f the indi­ vidual organism s th a t live w ithin it and the forcing functions o f the ecological processes by w hich they live an d die. R em ote sam pling tools are extending bo th the scale an d the resolution o f physi­ cal m easurem ents; biological sam pling is w orking to achieve a real-tim e equiva­ lence. T h e different sizes o f organism s require different sam pling m ethods. M any o f the present-day solutions have involved technological developm ents o f ancient systems (e.g. nets), b u t the new est techniques arc attem pting to be less intrusive a n d to identify m ore o f the n o rm al distributions an d interactions o f the individ­ ual organism s. Q uantitative sam pling has to be allied to observational recording o f the lifestyles o f the deep-sea fauna (Kunzig 2000). It is also a sobering thought th a t the relatively recent extension o f quantitative sam pling an d experim ent to the m icrobial size range has opened a P an d o ra’s box o f unexpected diversity' processes, an d productivity (C hapter 2).

2

Living, growing, and daylight

The fuel source: primary production Life on earth derives its existence, survival, an d success from p rim ary production, nam ely the biological synthesis o f com plex organic m olecules using inorganic sources o f carbon an d an external source o f energy. T h e open-ocean ecosystcm is sim ilar to the terrestrial one, b o th in this fundam ental principle an d in the b io ­ chem ical pathw ays involved, b u t the players an d the controlling processes are very different. T h e deep-sea fauna are dep en d en t upon them . T h e external energy source is usually light, an d the process is called photosyn­ thesis (organisms w hich m ake their own food using photosynthesis are know n as photoautotrophs). In certain situations non-photosynthetic m icroorganism s utilize the energy stored in chem ical bonds, typically those in hydrogen sulphide or m ethane, instead o f light. T his process is know n as chemosynthesis. All life in the oceans is dep en d en t u p o n these two processes. T h e vast m ajority o f deep-sea organism s obtain their energy second-, third- o r « th-hand from the near-surface photosynthetic phytoplankton (Fig. 2.1). A know iedge o f the controlling processes involved in oceanic p rim ary production and its export into deep er w ater sets the scene for u n d erstanding the ecology o f the deep er com m unities. T h e variability in p rim ary production at the surface is transm itted first to the meso- a n d bathvpelagic anim als below; an d finally to the benthos on the seafloor. Nevertheless, a small (but spectacular) m inority o f deep-sea anim als is d ep en d en t instead on chem osynthelic bacteria at hydrotherm al vents, cold seeps, an d other sites on the seafloor w here sulphide o r m ethane levels are high (below, and C h a p te r 3).

Chemosynthesis M ost b acteria are heterotrophs, that is they obtain their carbon in the form o f dis­ solved o r particulate organic carbon derived from o th er organism s. B acteria that obtain their carbon from inorganic sources, an d their energy from the oxidation o f inorganic substrates containing elem ents such as sulphur, iron, or nitrogen, arc knowrn as chem oautotrophs (by analogy with photosvnthetic photoautotrophs). In all cases the energy is obtained by the oxidation o f the red u ced substrates, and the oxygen source is usually free oxy gen in the water. T h e b acteria flourish at the

Fig. 2.1

Distribution o f primary production in the world ocean. The pattern closely matches that of the surface currents (cf. Fig. 4.1) and probably determines the similar patterns of zooplankton and benthic biomass. (Redrawn and adapted from Couper 1989.)

LIVING, GROWING, AND DAYLIGHT

29

interface betw een w^ater containing the reduced substrate an d oxygenated water, an d arc som etim es so ab u n d a n t th a t they form dense bacterial mats. T h e sub­ strate is usually reduccd sulphur, in the form o f hydrogen sulphide; chem osynthetic bacteria are therefore com m only found in hot sulphur springs on lan d and at the surface o f anoxic sedim ents in estuarinc an d o th er shallow -w ater environ­ m ents. In the deep sea their m ain role is th a t o f p rim ary producers o f new organic m aterial at hydrotherm al vents an d cold (brine) seeps (C hapter 3).

Photosynthesis Photosynthesis com prises three separate processes. In the first an d light-dependent step photons arc absorbed by pigm ents (particularly chlorophylls) a n d their energy is transferred to high-energy molecules such as adenosine triphosphate (ATP) an d X A D P H . T h e sccond step is light-independent an d involves the fixation o f carbon dioxide (CO,,). T h e third step is the process o f respiration, in w hich chemical energy is released by oxidation to fuel the synthesis o f the carbohydrates, fats, p ro ­ teins, an d the pleth o ra o f other organic molecules req u ired for life. T h u s carbon dioxide from the atm osphere dissolves in seaw ater (as bicarbonate) an d is fixed by the phytoplankton to form organic carbon, w ith the release o f oxygen. N ew carbon dioxide is retu rn ed to the seaw ater in the process o f respiration. T h e rad ian t energy' of' the sun is attenuated by? transm ission through seawater; photosynthesis is therefore lim ited to the u p p er well-lit layers o f the ocean, specif­ ically the cuphotic zone, w ithin the epipelagic realm . P rim ary pro d u ctio n (with the exception o f chemosynthesis) can n o t occur w ithin the deep occan environ­ m ent. T his is a very different situation from the terrestrial environm ent, w here p rim ary production takes place alm ost ev eryw here. All deep-sea anim als, indeed m ost m arine anim als, live som e considerable distance from the thin skin o f p lan t life n ear the surface o f the occan, w hereas m ost terrestrial anim als live very elose to (often in o r on) an active source o f p rim ary production. O n lan d the b arren desert an d polar regions arc the exceptions, w here active p rim ary producers m ay be hundreds o f kilom etres away. In the ocean the oligotrophic oceanic gyrres are som etim es described as oceanic deserts (because the standing stock or biom ass in the u p p er w aters is very low) b u t this is really a m isnom er because the gyres have a large p erm a n en t population o f very active p rim ary producers, albeit largely m icrobial ones (see below). T h e basic survival o f every organism depends on achieving a n et energy gain in the balance betw een nutritional profit an d respiratory loss. A continued n et loss m eans starvation. I f the organism is successful in achieving a n et gain, energy can be used for grow th an d reproduction (as well as for avoiding predators) (Fig. 10.1). Photosynthetic organism s are no different, except th a t th eir energy input d epends on their light environm ent. T h e respiration o f a single phytoplankton cell consum es energy, bo th in the light an d in the dark. If the cell is in well-lit w aters its daytim e photosynthetic energy gain will m ore th an offset the day an d night respiratory costs. I f it sinks deeper in the w ater the light will becom e

THE BIOLOGY OF THE DEEP OCEAN

dim m er an d the cell’s energy input will decrease rapidly, b ut its respiratory costs will not dim inish so quickly. At a particu lar depth, the com pensation d ep th , the light intensity is such that the rate o f energy in p u t (photosynthetic p rim ary p ro ­ duction) will be m atched by the respiratory output, an d there will be no n et gain or loss (Fig. 2.2). Below the com pensation d epth the cell can survive for a while, depending on its reserves, but unless it retu rn s to better-illum inated levels (or becom es d o rm an t by shutting dow n its m etabolism ) it will eventually exhaust its resources an d die. T h e light at different depths differs in m ore th an ju st intensity; the spcctral characteristics also change. R ed light is m ore rapidly absorbed th an blue so a Fig. 2.2

The relationships between the compensation depth, the critical depth, and the depth of mixing. At the compensation depth (Dc) the average light intensity is such that a cell's photo­ synthesis (Pc) is equal to its respiration (Rc). As phytoplankton cells in the water column are mixed above and below the compensation depth they experience an average light inten­ sity. When mixing extends to the critical depth (D ), that average light intensity is the same as at the compensation depth; photosynthesis throughout the water column (Pw) matches respiration throughout the water column (RJ). Photosynthesis is represented by the area bounded by the points A, C, and E. Respiration is represented by the area bounded by A, В, C, and D. At the critical depth these tw o areas are equal. If the mixing depth (Dm, to the thermocline) is below the critical depth (as in this figure) then water-column photosynthe­ sis is less than water-column respiration (Pw < RJ) and there is no net production. (From Lalli and Parsons 1993, reprinted by permission of Butterworth Heinemann.)

LIVING, GROWING, AN D DAYLIGHT

31

shallow phytoplankton cell will be exposed to a higher ratio o f red to blue light th an a deeper one. I f a species uses red light (which chlorophyll absorbs effi­ ciently) m ore effectively th a n blue then it will have a shallow er com pensation d ep th th an a species th a t can also use blue light efficiently. D ifferences o f this type are d eterm ined partly by the presence o r absence o f accessory pigm ents, such as carotenoids, w hich absorb blue -green light an d transfer the energy to chlorophyll. N ea r the surface the light levels m ay be so high as to saturate or even inhibit the photosynthetic system an d thus reduce the level o f p rim ary production. T h ere is now evidence th a t the increasing exposure to ultraviolet light, w hich has resulted from decreases in the ozone layer, can also inhibit the photosynthesis o f some near-surface phytoplankton. T h e consequence o f all these variables is that different species o f phytoplankton are adap ted to different levels o f light intensity an d to different spectral ch arac­ teristics, an d it is possible to consider the phytoplankton in term s o f ‘light’ an d ‘shade’ species. Light is, o f course, only one o f the factors th a t can lim it p rim ary production. T em p erature extrem es a n d /o r inadequate levels o f nutrients or tracc elem ents may7 all be lim iting for the grow th o f phytoplankton populations, even before the grazing activities o f the zooplankton im pinge on them . T h e com plex­ ity o f the seasonal succession o f species is a produ ct o f the m ultiple interactions betw een the phytoplankton, the environm ental conditions th at control their grow th an d reproduction, an d the m ortality caused by grazing. T h e succession has im p o rtan t effects on the quantity a n d quality o f the export flux o f carbon from the surface to the deep-sea fauna below7

The seasonal cycle T h e surface phytoplankton populations, an d their p ro d u ctio n an d relation to w’ater tem peratures, are now accessible on a global scale via specialist satellites (Fig, 2.1 a n d C h a p te r 4). Seasonal changes on a large scale close to the surface can therefore be directly m onitored; nevertheless, the vertical processes that drive these changes still have to be inferred. Populations o f p rim ary producers, an d their dynam ics, determ ine the ecology o f the ocean, not the individuals. T h e com pensation dep th for a single cell is thus a somew'hat theoretical concept o f little direct consequence to the population as a w-hole. T h ere will, however, be a dep th at w’hich the total integrated p rim ary p ro duction o f the phytoplankton in the overlying w ater colum n is exactly m atched by their total respiratory loss. T his d ep th is know n as the critical d epth (Fig. 2.2) an d m arks the dep th above w hich the phytoplankton com m unity7 is in energetic equilib­ rium . I f the m ixed d ep th exceeds the critical depth (as in Fig. 2.2) the average light intensity to w hich the phytoplankton in the w ater colum n are exposed will be too low to prevent respiratory losses exceeding photosynthctic gains. C hanges in the critical dep th relative to the dep th o f the m ixed layer m ay therefore have profound consequences for the prim ary p ro duction budget.

THE BIOLOGY OF THE DEEP OCEAN

32

Temperate waters Consider, for exam ple, the annual changes occurring in tem perate occans (Fig. 2.3). In the w inter the surface w ater is cool, th ro u g h lack o f solar heating, an d w inter storm s cause vigorous m ixing o f the w ater colum n. W inter m ixing can extend dow n to 600 -700 m in the north east A tlantic. A t the same tim e the w inter cooling o f the surfacc w ater increases its density enough for it to sink, thus producing considerable convective mixing. D aytim e light intensities are low an d day length is short, so the critical d ep th is m uch shallower th a n the m ixing depth. T h e phvtoplankton populations are now being m ixed well below the critical dep th an d the overall respiration costs greatly exceed the p h o to ­ synthetic input. T h e result is a net loss o f energy to the system, w hich clearly cannot be sustained indefinitely. However, the sam e m ixing process sim ultane­ ously replenishes the surfacc nutrients by bringing up nitrate, silicate, an d ph o s­ p hate from the deeper m ixed layer. As w inter progresses into spring and sum m er the light increases in b o th intensity an d duration. T his drives the critical dep th deep er by increasing the photosvnthetic input above it. A t the sam e tim e the storm s abate an d b o th w ind an d convective m ixing dim inish. T h e p hytoplankton populations are no longer m ixed to below the

Fig. 2.3

Schematic representation of an annual phytoplankton cycle in temperate latitudes. The stratification of the water in summer is broken down by winter mixing. (From Smayda 1972)

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LIVING, GROWING, AN D DAYLIGHT

33

critical depth. T h e presence o f light, nutrients, and lim ited m ixing produces a sub­ stantial net photosynthetic gain recognizable as a rap id grow th in the populations. T h e increased sunlight w arm s the surface layer, whose density decreases; m uch m ore energy is now required to m ix it into the denser w ater below. T h e w ater colum n stratifies into a w arm m ixed surface layer above the colder d eep er water. A ‘spring bloom ’ o f phytoplankton, usually com posed m ainly o f diatom s (Figs 2.4, 2.5), is often the result (Holligan 1987). T hese bloom s m ay im pinge directly on the deep-sea fauna an d profoundly affect their behaviour (C hapter 10). T h e bloom rapidly uses the available nutrients; because the surface m ixed layer is now less dense (and subject to low er w ind stress) its nutrients are no longer replen­ ished by turbulent m ixing w ith the nutrient-rich deeper water. M ost o f the origin­ ally available nutrients are locked into the phytoplankton cells. T h ese cells sink out o f the surface layer or are consum ed by the herbivorous zooplankton. T h e explosive population grow th can no longer be sustained an d only those species th a t can cope w ith the low -nutrient situation continue to grow. T h ese are typically the very small picoplankton and m obile larger phytoplankton such as the coccolithophores an d dinoflagellates (Figs 2.4, 2.5), whose sw im m ing abilities m ake it easier for them to benefit from m icroscale patchiness o f such nutrients as do exist (largely regenerated by zooplankton excretion). T h e seasonal an d regional distri­ bution o f dinoflagellates has im portant consequcnces for the photoecology o f the m idw ater fauna, by virtue o f the intense biolum inescence w hich m any dinofla­ gellates can produce (C hapter 9). T h e seasonal therm ocline m arks a sharp b o u n d ary betw een the w arm surface w ater and the deeper, colder layers; the stability o f the surface m ixed layer results in non-m otile cells sinking tow ards the therm ocline. N utrient-stressed cells ten d to Fig. 2.4

A sample of phytoplankton composed mainly of diatoms and dinoflagellates.

THE BIOLOGY OF THE DEEP OCEAN

Fig. 2.5

Scanning electron micrographs o f the dinoflagellates (a) Ceratocorys gourreti, (b) Ceratium horridum, and (c) Gonyaulax polygramma, the diatoms (d) Thalassiosira sp. and (e) Chaetoceros sp., and (f) the coccolithophore Emiliana huxleyi. (From Delgado and Fortuno 1991, with permission from Scientia Marina.)

bccom e less buoyant, thereby accelerating the sinking process. Phytoplankton are nutrient-lim ited in the u p p er region o f the m ixed layer, while at its low er levels they are light-lim ited. D ifferent species succeed in the two conditions an d the deeper ‘shade’ populations often constitute a deep chlorophyll m axim um , aided by some diffuse m ixing o f nutrients from the layers below. Phytoplankton bloom s can therefore be p ro d u ced (1) by increased light levels, w hich drive the critical depth dow nw ards, o r (2) by increased stability o f the surface layers, w hich brings the m ixed layer above the critical depth. U sually b oth factors are involved an d their synergy results in the rap id explosion of phytoplankton populations in the spring an d early summer. A bloom indicates a rate o f cell production th a t exceeds the losses from sinking an d grazing; only a very small excess rate is needed to produce a bloom . T h e sinking flux is the am o u n t o f p rim ary production (much o f it already eaten at least once, a n d in the form o f faecal pellets) that reaches d eep er water. It reaches 30% o f the total in coastal w aters but only some 5% in oligotrophic regions, w here the m icrobial loop (sec below) drives intense recycling o f carbon an d nutrients. O n a global scale only some 10% o f the p rim ary p ro duction is exported out o f the euphotic zone in the open ocean, an d ju st 1% reaches the seafloor. In early au tu m n increased w ind m ixing forces the m ixed layer deeper, bringing nutrients to the surface. Light levels are still relatively high, an d the critical dep th large, so the phytoplankton m ay produce a m in o r secondary ‘b loom ’, aided by a sum m er decline in the nu m b er o f zooplankton grazers, following a reduction in the nu m b er o f the larger species o f phytoplankton from spring to summer.

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Oligotrophic waters (tropical and subtropical) O th e r species o f phvtoplankton grow m uch b etter in w arm , stable, n u trient-poor (oligotrophic) waters, such as arc found in m any tropical occans a n d w hich develop to a lesser extent in tem perate regions durin g the summ er. D inoflagellates can swim (which helps to co u n ter the risks o f sinking o ut o f the surface waters) and so can the microflagellates. D inoflagellates have cellulose cell walls while the coccolithophores have tiny calcareous plates over th eir surfacc (Fig. 2.5). M any dinoflagellates are at least partly hetcrotrophic, th at is they do n ot d ep en d entirely on photosynthesis for their energy input b u t can also take organic particles an d som etim es even live organism s. Indeed, the diatom s are the only group o f p hyto­ plankton that has no hetcrotrophic specics at all. In the nutrient-lim ited environm ent o f oligotrophic w aters the very small p hyto­ plankton (picophytoplankton, < 2 Jim) dom inate (Fogg 1986; C hisholm 1992; R aven 1998). T h e diffusion bo u n d ary layer o f cells less th an 50 Jim in diam eter is equal to their radius, so the bo u n d ary laver o f picoplankton is m uch th in n er th an th a t o f larger cells, providing an advantage in the absorption o f nutrients from w aters w here nutrien t levels are very low an d w here diffusion rates w ould lim it the grow th o f larger species. А 5 -ц .т cell becom es diffusion-lim ited at n u tri­ ent concentrations o f about 100 nM , w hereas for a 0.35-jim cell the lim iting level is reduced to 5 nM . T h e smallest picoplankton (spherical d iam eter < 1 Jim) include bo th prokaryotes (e.g. Prochlorococcus an d Synechococcus) an d eukaryotes (e.g. Nannochloris an d Ostereococcus). C yanobacteria (e.g. Synechococcus) are particularly successful in the w arm low -nutrient waters; one genus, Trichodesmium, is even able to fix atm ospheric nitrogen, thus com pensating for lim iting levels o f soluble nitrate. T h e very small size o f m ost cyanobacteria enables them to rem ain in sus­ pension for very long periods w ithout significant sinking losses to deep er water. A 20-jim phytoplankton cell (e.g. a diatom ) sinks at ab o u t 1 m d a y 4 , b u t a 1-jJ.m cyanobacterial cell o f sim ilar density will sink at only 2.5 m m day"' (in p racticc it will sink even slower, because it does riot have a silica cell wall an d will probably have a lower density th an the diatom). T h e production o f large diatom s is alm ost entirely d ep en d en t on rem ineralized nitrate from deep w'ater. T his is described as ‘new ’ production, because it relies on an input o f new nitrogen into the system. Phytoplankton th at can utilize am m onia as a nitrogen source have an advantage in oligotrophic w aters because they can continue prim ary production using the am m onia excreted by the zooplankton. T h e ir grow th is described as ‘regenerated’ production. Picoplankton com m unities, in particular, utilize regenerated nutrients ra th e r th an ‘new ’ nitrogen an d ten d therefore to dom inate oligotrophic w'aters, M any o f the smallest species of picoplankton were oncc thought to behave like heterotrophic bacteria, taking dis­ solved organic carb o n from their surroundings. It is now1recognized th at very m any arc autotrophic, actively photosynthetic, organism s (the picophytoplankton) an d m ake a substantial contribution to the p rim ary p roduction budget o f the oceans. T hey are also very abundant: there m ay be 10a> individuals w orldwide o f the com ­ m onest species o f Synechococcus (Raven 1998). T his is betw een 10 an d 100 times

THE BIOLOGY OF THE DEEP OCEAN

36

m ore th a n the total nu m b er o f phytoplankton cells o f «//species larger th an 2 jim! For com parison, the total n u m b er o f m idw ater m icrobes is calculated at 3.1 X 1028 B acteria an d 1.3 X 1028 A rchaea, w ith the latter form ing 20% o f all picoplankton (K arn er et al. 2001), an d there are some Ю10 copcpods (M auchline 1998). T h e photosynthctic significance o f the picoplankton was first recognized in the 1980s (Joint 1986), even though one o f the d o m in an t organism s in some regions, Prochlorococcus, was only described in 1988 (Chisholm 1992). O n e estim ate sug­ gested th a t o f organism s below 200 |im in size the picoplankton (< 2 (im) m ade up 50% o f the photosynthctic biomass, w ith n an oplankton (2-20 (im) m aking up 38% a n d m icroplankton (20-200 Jim) 12% (Longhurst 1985). T h e smallest autotrophs (e.g. Prochlorococcus, at about 0.6 |im ) are particularly im p o rtan t in oligotrophic waters, contributing up to 75% o f the prim ary p roduction o f the < 5 -]im phvtoplankton in the tropical N o rth A tlantic. A n o th er set o f data indi­ cated that picoplankton contribute 45% o f the photosynthctic biom ass in olig­ otrophic w aters an d 60% o f the chlorophyll a (Laws et al. 1984), while a th ird estim ated that cells less th an 1 ц т were responsible for 60% o f the total p ro d u c­ tion in the oligotrophic open ocean (Platt el al. 1983; Li an d P latt 1987). Even in tem perate w aters their contribution is very substantial. T h e Celtic Sea has an ann u al production o f ab o u t 100 g С m 2 p e r year, o f w hich organism s less th a n 1 [im in diam eter contribute 23% (Joint et al. 1986). R ecent d ata confirm these indications an d suggest th a t the picophytoplankton com prise some 24% o f the global phytoplankton biom ass an d are responsible for some 39% o f the global p rim ary productivity (Agawin et al. 2000). M any o f these organism s are so small th a t they can n o t be eaten by the m acro- an d m esozooplankton (copepods, etc.), whose feeding ap paratus has evolved to sieve or filter large cells, such as diatoms, from the water. A large anim al w ould require a very fine m esh to sieve a m eal of nano- an d picoplankton an d at this scale the viscosity o f w ater w ould present a m ajor difficulty (see below). Larvaceans (see A ppendix and below) are specialist feeders on picoplankton an d their disposable houses represent an extraordinarily elegant solution to the problem o f filtering very small particlcs. T h e large-scale subtropical oceanic gyres arc usually reg ard ed as stable, ch arac­ teristically oligotrophic, ecosystems. R ecent studies o f the N o rth Pacific gyre however, suggest a m ajor change in ecosystem structure in response to the 1991 -1992 El N ino event. Increased surface tem p eratu re led to decreased upperocean mixing. T h e resulting drop in ‘new ’ nitrogen encouraged an increase in the abundance o f cyanobacteria, w ith consequent changes in total production, in export production, an d in trophic pathway's (K arl 1999).

Upwelling waters T h e degree o f turbulent m ixing in the surface w aters affects the relative success of different kinds o f phytoplankton. D iatom s have dense silica cell walls, ten d to be quite large, m ay form long chains, a n d sink relatively quickly. T h ey are particularly

LIVING, GROWING, AN D DAYLIGHT

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successful in eutrophic conditions in w hich quite vigorous surface m ixing is com ­ b ined w ith high nutrien t levels. T h e turbulence keeps them in suspension an d the high nutrien t levels m ean th a t their uptake is n o t lim ited by their low ratio of surface area to volume. T h ev are therefore the m ain com p o n en t o f the spring bloom in cool tem perate w aters an d the m ain contributors to the very high p ro ­ ductivity in low cr-latitude upw elling regions, such as the C alifornia C u rren t area, coasts o f Peru and West Africa, an d the A rabian Sea (Fig. 2.1). H ere the seasonal winds tend to drive surface w ater offshore an d this w ater is replaced by w ater (with high nutrien t levels) slowly upw elling from typically 100 to 200 m. T h e continuous in put o f nutrients into the euphotic zone stim ulates intense p roduction d om inated by diatom s. T h e efTects cascade dow n through the w ater colum n to reach the deep-sea populations, bo th those in m idw ater an d those on the bottom . As the upw elled w ater flow's offshore so the cycle o f its productivity (and the species succession) changes gradually from the eutrophic spring bloom conditions typical o f tem perate regions to the picoplankton-dom inated oligotrophic condi­ tions o f the surrounding area. The upw elling in these situations an d the subse­ q u en t burst o f production are very vulnerable to relatively m in o r local climate changes. I f the surface w ater becom es ju st a degree o r two w arm er it can act like a low-density lid on the colder, deeper water, and thus prevent the n o rm al cycle o f upw elling into the euphotic zone. T his is how El N ino affects the Peruvian upw elling (as well as the n o rth Pacific gyre noted above). T h e re is evidence that the C alifornia C u rren t upw elling has declined over the past 40 years; an 80% reduction in zooplankton has been associated w ith a grad u al rise in surface tem ­ perature. T his change m ay reflect a long-term n atu ral oscillation, b u t could also be a response to anthropogenic clim ate changes.

Measurements of primary production A chieving accurate m easurem ents o f p rim ary pro duction is no easy task. T h e m ost widely used m eth o d involves m easuring the uptake by the phvtoplankton o f 1'C tracers, added in the form o f i4C b icarbonate to incubation bottles placed in the dark an d the light. Z ooplankton are first rem oved from the samples to reduce grazing effects. T h e difference in HC uptake betw een the light a n d dark samples gives a m easure o f prim ary production. T h e experim ental procedures involve fil­ tering the phytoplankton from the sam ple but som e o f the picoplankton will be lost unless a filter w'ith pores less th an 2 jj.m is used. D elicate phytoplankton species m ay be broken in the filtration process an d their cell contents lost. B acteria attached to the sides o f the sam ple bottle m ay confuse the results by taking up the tracer differentially in the light an d dark, an d m inute am ounts o f toxic trace m etals may7 leach from the bottles themselves. In the early estim ates of p rim ary production the larger phytoplankton w ere assum ed to be the only ones involved. Recognition o f the role o f autotrophic picoplankton, w ith ap propriate adjustm ents to the experim ental procedures, has led to h igher calculated values, particularly in oligotrophic areas.

THE BIOLOGY OF THE DEEP OCEAN

A nother approach is to m easure the oxygen evolved in photosynthesis, either by direct titration o r by the use o f 1!iO as a tracer, an d to use Liltraclean containers (K err 1986). D irect m easurem ents o f the accum ulation o f photosynthetic oxygen in surface w ater masses or the consum ption o f oxygen in deep w ater (as a m easure o f the prim ary productivity sinking o ut o f the surface layers) provide estim ates on a very m uch larger scale. Both m ethods yield results w hich challenge the conventional incubation m ethods because they give considerably higher values o f prim ary production; one estim ate p u t the am o u n t o f carbon sinking out o f the oligotrophic subtropical A tlantic at 55 g С m 2 p er year, an d this was net production because it did n o t include the p roduction recycled n ea r the surface w ithout sinking. Typical levels o f production in tem perate an d subpolar w aters are 70-120 g G m 2 p er year, in the S outhern O cean (Antarctic) 100 g G m 2 p er year, in the tropical oceans 18—50 g С m 2 p e r year, an d in the high A rctic less th a n 1 g С m 2 p e r year. C oastal production is higher th an th a t o f the open ocean an d m ay reach daily rates in excess o f 3 g G m 2 (com pared w ith open ocean values o f 0.3-0.8 g G m 2), T hese levels are not, o f course, sustained for very long, although a total value o f 389 g С m 2 p er year has been calculated for Long Island Sound. For com parison, the m axim um rates for terrestrial grassland an d rain forests are 2400 an d 3900 g С m 2 p e r year, respectively (Table 2.1). D espite the low er average production rates o f the open ocean, its vast area provides 80% o f the total m arine prim ary production o f ab o u t 50 X 10 13 g G p e r year, an d thus about 40% o f the global total (M artin et al. 1987). Less th a n 1% o f this p rim ary production reaches the seafloor as export flux.

Table 2.1 Some differences between terrestrial and marine pelagic ecosystems (after Parsons 1991, with additions (*) from Falkowski eta/. 1998 and Cohen 1994) Terrestrial

Marine pelagic <10 50-300 g С y e a r 1

P/B

>50 Grass -2400 g С y e a r 1 Rain forest -3900 g С y e a r 1 56.4* Gt С 830* Gt С (-500 Gt is photosynthetically active) 0.07

Animals Growth efficiency (К ) Ecotrophic efficiency (Ee) Ecological efficiency (E = Ee x К ) Fecundity of large predators Number o f species Cannibalism among stocks

-2 -4 % -5-2 0% -1% Low -1 0 6 Rare

-30-40% >80% 5-20% High -1 0 4 Frequent

Plants Carbon to nitrogen ratio Maximum primary production r r r 2 Net primary production (P) Biomass (B)

-5 0 * Gt С 1* G tC

50

LIVING, GROWING, AN D DAYLIGHT

39

Limitations to primary production T h e productivity o f phytoplankton populations is physically lim ited by seasonal changes in light an d tem perature, particularly at high latitudes. However, the two m ain factors th a t lim it productivity in otherw ise ad equate grow th conditions arc the grazing pressure exerted by herbivorous zooplankton (Banse 1995) and the supply o f nutrients. C ontrol by grazing pressure is described as ‘top dow n’ an d control by nutrien t supply as ‘bo tto m u p ’. Both have consequences for the structuring o f the ecosystem (Verity a n d Sm ctacek 1996) Size m atters: diatom s are large cells an d can only be eaten bv large grazers (e.g. copepods). L arge zooplankton can n o t eat very small phytoplankton, so they will n ot flourish until the diatom s appear. T h e grow th rates o f large zooplankton are relatively slow an d it m ay take several weeks for the grazing populations to increase to the po in t w here they control the diatom productivity; T his frequently gives the diatom s tim e to generate a ‘bloom ’ before the larger zooplankton catch up. Both will app ear in (asynchronous) cycles. Size m atters: sm aller zooplankton (microzooplankton) can n o t cat large diatom s b u t they do cat the nano- an d picophytoplankton. T h e ir grow th rates are high so they can control the populations o f small phytoplankton w ithout any significant tim e-lag, an d ‘bloom s’ o f small phytoplankton can never occur. T h e two p o p u la­ tions arc very tightly coupled. T h e generation tim e o f the pico- an d nan o p h y to ­ plankton is so short th a t although the grazing pressure is intense, a n d the standing stock therefore relatively small, the turnover rate (or production) is nevertheless very high. N u trien t lim itation usually occurs w hen all th e available nitrate in the m ixed layer above the seasonal therm ocline has been taken up by the phytoplankton. M uch o f the nitrogen will then sink out o f the m ixed layer as p a rt o f the export flux to deeper water, locked either in intact phytoplankton cells o r in zooplankton tissues. Large cells such as diatom s, w ith a low ratio o f surface area to volum e, will be the first to suffer nitrogen lim itation, becom e less buoyant, a n d rapidly sink o ut o f the m ixed layer. In stable, w arm , w aters the sm aller p hytoplankton will dom inate and will continue to grow' at m uch lower nitrate concentrations th an larger species. O th e r form s o f nitrogen m ay also be available. A few cyanobacteria can fix atm ospheric nitrogen, an d m any o f the sm aller phytoplankton can use instead the nitrogen excreted by zooplankton an d other heterotrophs in the form of am m o n ia to fuel regenerated production. T h e ratio o f new p ro duction to total p roduction is know n as the f ratio; it varies from 0.8 in regions o f active upw elling to 0.0 1 -0 .0 5 in tropical oligotrophic waters. In these oligotrophic regions recycling is very efficient an d losses through sinking are very low. N itrogen is not the only lim iting nutrien t but it is usually the m ost im portant. Silicate can also be occasionally lim iting for diatom s, w hich require it for their silica cell walls. T hese dense cells, w ith their silica content, are destined to sink quite rapidly out o f the surface w aters, taking the silicate w ith them . W indblow n dust m ay provide sufficient silica replenishm ent.

THE BIOLOGY OF THE DEEP OCEAN

In m ost circum stances in the oceans, the presence o f high levels o f nutrients in the surface layers, com bined w ith adequate light, should result in high phyto­ plankton num bers, m anifest as high levels o f chlorophyll a. It is therefore a curious anom aly to find that in the sub-Arctic, in the equatorial Pacific, an d in the S outhern oceans there are high n u trie n t/lo w chlorophyll (HNLG) regions. At first, intense grazing by the zooplankton was th ought to be the cause, keeping the phytoplankton at perm an en tly low densities. However, this assum ption could not be fully substantiated by m easurem ent o f the populations an d processes involved, although it was established that the phytoplankton o f these regions was dom i­ n ated by very small species. A n alternative hypothesis suggested th a t although conventional n u trien t levels were high, concentrations o f iron m ight still be limiting. Iron (like silicate) enters the open oceans prim arily in the form o f w ind-blow n dust, an d the anom alous regions are a long w ay from any such source o f iron. T h e two hypotheses are not m utually exclusive but the debate quickly polarized into the ‘grazing’ an d ‘iron’ camps. T h e problem s o f accurately m easuring very low levels o f iron w ithout contam ination from the experim ental containers an d reagents m ade it difficult to distinguish betw een the two causes. It is now believed th a t the existing small-ccllcd phytoplankton com m unities in these areas seem to be ad ap ted to the conditions o f low iron an d th at their p o p ­ ulations are tightly controlled by m icrozooplankton grazers. U ltraclean experi­ m ents have show n that iron addition to surface w aters in the H N L C regions can indeed stim ulate phytoplankton grow th, an d in p articu lar the large b ut norm ally rare diatom s. T hese organism s arc not grazed efficiently by the existing m icro­ zooplankton and thus proliferate rapidly after the enrichm ent. T hese conclusions have been reinforced by an in situ experim ent in the Pacific in w hich iron sulphate was p u m p ed from a research ship into a 72-km 2 area o f occan. T his resulted in (1) an order o f m agnitude local increase in phytoplankton biomass (a bloom), particularly' o f the larger diatom s, (2) a resulting decrease in nitrate levels by a h a lf (taken up by these cells), an d (3) a reduction in C 0 2 partial pressure (because m ore C 0 2 was taken up in the increased photosynthesis) (Frost 1996; Cullen 1997). T h e n a largcr-scale experim ent in the S o u th ern O cean (8.7 tonnes o f iron sulphate w ere released into a patch 8 km in diam eter) resulted in a tripling in the phytoplankton chlorophyll in the patch over a 2-wcck period. Satellite observations followed the p atch over the following m o n th an d show ed how stir­ ring an d diffusion stretched it into a near-surface ribbon o f high chlorophyll extending for 150 km X 4 km an d accum ulating an estim ated 600-3000 tonnes o f algal carbon. Iron clearly can be lim iting for p articu lar species in p articu lar conditions: nan o m o lar concentrations can change w hole ecosystems (A braham et al. 2000; Boyd et al. 2000: sum m arized by C hisholm 2000). T h e im portance o f these results in biogcochem ical term s is the dem onstration th a t iron addition to H N L C regions could potentially affect climate. T h e draw ­ dow n o f C 0 2 from the atm osphere is increased through en h an ced carb o n fixa­ tion by photoautotrophs, som e o f w hich is subsequently exported to deep w ater

LIVING, GROWING, AND DAYLIGHT

41

in the form o f particulate carbon. In fact, an increase in th e export flux (follow­ ing iron enrichm ent) has n o t yet been observed b u t the experim ents to date were p robably n o t m onitored for long enough to dem onstrate this. T h e results o f the various experim ents have been extrapolated to suggest th at seeding the occans w ith iron could reduce global w arm ing, an d provide a w ay o f recycling old cars! T h e num erous feedback processes involved (Brigg 2000) m ake it a very simplistic view. T h e question ‘W h at limits phytoplankton productio n ?’ clearly has m any different answers. It prom pts the qualified responses ‘W hich kind o f phytoplankton? W here in the global occans? A nd at w hich season?’ T h e answ er is never simply ‘top dow n’ o r ‘bottom u p ’ b u t a variable com bination o f the two. T h e com plexities o f the relationships betw een the physical an d biological envi­ ronm ent o f the oceans, an d the quantitative identification o f the controlling organism s an d processes, are increasingly susceptible to analysis by m odellers o f the oceans biogeochemistry. T his analysis enables the observed changes to be m uch m ore effectively interp reted and for the relations betw een clim ate, p h o to ­ synthesis, an d export flux to be realistically p redicted in a range o f different future scenarios. T h e pow er o f m odelling is revolutionizing o u r u n d erstan d in g o f the global ocean ecosystem. A t present it is largely confined to increasingly detailed stud)7 o f the u p p er few' h u n d red m etres, w here the m ajo r processes are m ost active, b u t it is extending increasingly into the deep ocean.

Grazing and secondary production S econdary production describes the conversion o f the (mainly) photosynthctic p rim ary production into heterotrophic (anim al an d bacterial) biomass. It is the integrated result o f a m aze o f trophic relationships, form ally identified as the food w’cb, an d is com plicated by the fact that m any anim als have a varied diet, con­ sum ing bo th phytoplankton an d oth er prey o f ap p ro p riate particle sizes. T h e quantitative transfer o f biom ass from prim ary to secondary p ro d u ctio n is d eter­ m ined by the energy transfer efficiency o f the p articu lar phytoplankton—zoo­ plankton interaction. T h e grazers generally consum e a very high pro p o rtio n (> 8 0 % ) o f the available prim ary production; this is know n as the ecotrophic. efficiency (Tabic 2.1). O f the 36 G t С prim ary pro d u ctio n in the open ocean (out o f a global figure o f 50 ( it C) only 0.86 G t С (2.4%) is exported to 1000 m , an d less th an 1 % reaches the seafloor, although the p ro p o rtio n transferred through this ‘biological p u m p ’ differs m arkedly in different regions (Doney 1997; L am pitt an d A ntia 1997). T h e size o f the food particles is all-im portant in the grazing rela­ tionships. A budgetary m odel based on d ata from two contrasting regions (a p ro ­ ductive tem perate fjord at D abob Bay, W ashington, an d an oligotrophic Pacific gyre) show ed th at in D ab o b Bay m acroplanktonic herbivores were responsible for 67% o f the daily grazing rate while phytoplankton grow th rates varied seasonally betw een 0.05 an d 0,9 p er day. In the Pacific gyres the equivalent grow th rates were a steady 0.2 per day an d here m icrozooplanktonic herbivores w ere respon­ sible for som e 95% o f the daily grazing (W elschmever an d L orenzcn 1985).

THE BIOLOGY OF THE DEEP OCEAN

In general, the larger the particle the m ore efficient it is as a food source for a given predator. L arge phytoplankton are m ost efficiently consum ed by large herbivores (as in D ab o b Bay) w hereas the sm aller phytoplankton from the Pacific gyres arc consum ed prim arily by the sm aller m icrozooplankton (to w hom the particles are relatively large). E xperim ents show th a t large copepods grow faster w hen fed large phytoplankton th an w hen offered a sim ilar biom ass o f sm aller species. T h e m echanism s by w hich p articu lar zooplankton filter or capture the p rim ary producers arc largely unalterable (e.g. setae on m outhparts, ciliary bands, etc.) an d are only effective over a lim ited size range of food. T h e sam e lim itations apply to subsequent trophic levels: larval salm on can grow' on a diet o f the large copcpod Calamus phimchrus b u t n ot on the sm aller species Pseuclocalanus minutus, even w hen the latter is present at a higher biom ass concentration. As an anim al grows, its optim um food particle size also increases and its ccological nichc w'ill change as it diverts its efforts tow ards prey o f larger particle size. T h e ecological efficiency o f the transfer o f energy betw een p rim ary an d sec­ o ndary production is a function o f the pro p o rtio n o f the p rim ary production consum ed (as food ingested, the ecotrophic efficiency) an d the energy transfer coefficient betw een the two trophic levels (food absorbed X grow th rate) (Table 2.1). Ecological efficiency tends to be inversely correlated w ith the level o f p rim ary production; it m ay be as lowr as 5% in actively upw elling areas w here the phytoplankton grow th rates arc very high b u t n ot all o f it is grazed (i.e. low' ecotrophic efficiency), but in open-ocean oligotrophic areas it is n earer 15-20% (Table 2.1). In the open occan the ecological efficiency is therefore three times th a t o f upwelling areas. T h e efficiency w ith w hich p rim ary p roduction is con­ verted to high-level p red a to r biom ass (tertiary production, e.g. fish) depends very m uch on the nu m b er o f interm ediate stages (trophic levels) in the transfer process. T h e production (P) at a given trophic level is related to the biom ass (B) o f prim ary production by the form ula: P = B E 11 w'here E is the ecological efficiency and n is the n u m b er o f intervening trophic levels. T h e ecological efficiency is a function o f food ingested, food absorbed, an d grow th rate. A bsorption levels are related to the pro p o rtio n o f organic m atter in the diet; detritus feeders, not surprisingly have the lowest absorption levels an d carnivores have the highest. Low' absorption levels are linked to high (> 5 0 % ) net grow th efficiencies, w'hich therefore tend to be high in dctritivores an d herbivores (i.e. at the low er trophic levels). S hort food chains leading from p rim ary p ro d u c­ tion thus have high transfer coefficients, partly because at these trophic levels less energy has to be spent finding the usually m ore a b u n d a n t food. T h e oligotrophic open ocean is often described as a nutritionally dilute environm ent an d low' tran s­ fer coefficients reflect this condition. In oceanic gyres food webs m ay span five trophic levels from the prim ary producers to the fish, w ith a transfer coefficient from each o f only ab o u t 10°/!), th at is an overall transfer o f only 0.001% to fish

LIVING, GROWING, AN D DAYLIGHT

43

biomass. A t the o th e r extrem e are upwelling areas such as the coast o f Peru, w here adult anchovies feed directly on phytoplankton. T h e equivalent o f only 1.5 trophic levels is involved, w ith a transfer coefficient o f 20% at each level, provid­ ing an overall transfer o f 8% o f the prim ary production to fish biomass. Coastal an d upw elling regions, in general, have relatively fewer trophic levels betw een p rim ary production an d fish production th an do the open oceans; this is one of the reasons why they dom inate the contribution to w orld fish production, despite the m uch larger area o f the op en ocean.

The microbial loop in the system H eterotrophic bacteria are present everywhere in the ocean at a level o f ab o u t 10*’ m l 1. T h ey play a crucial role in one trophic pathway, the m icrobial loop (Azam et al. 1983; Fcnchel 1988; Lenz 1992). M any anim als release significant am ounts o f organic m aterial into the water, some o f it in the form o f m ucus an d some as dissolved organic molecules, either through ‘sloppy’ feeding or by direct excretion. Phytoplankton cells contribute m uch o f this m aterial themselves, leaking an d excreting dissolved organic carbon (D O C ) in considerable quantities. T h e value o f this m aterial to the cell is n o t fully understood b ut it m ay aid in the sequester­ ing o f trace elem ents or provide a chem ical b arrier to protect the ccll’s ‘spacc’. H eterotrophic bacteria thrive on this D O C an d it provides an im p o rtan t substrate for their populations, w hich interact w ith bo th the D O C an d particulate m a ter­ ials in com plex ways (Azam 1998). T h e bactcria are too small to be eaten by m csozooplankton (0.2—2 mm), w hich sieve larger cells an d particles from the water. Instead they are grazed by m icroflagellates an d the flagellates are eaten in tu rn by oceanic ciliates. T hus, m uch o f the photosynthetic energy long assum ed to flow along the p ath o f the classical food w eb (i.e. from large phytoplankton (diatom) to m acrozooplankton grazer (c.opepod)) is in fact siphoned off throug h the m icrobial loop (Fig. 2.6; Table 2.2). T h e im portance o f the loop should n ot be underestim ated: calcula­ tions o f the flow through this pathw ay suggest th at up to 60% o f th e ocean’s p rim ary production is consum ed by bactcria. Energetic losses in the loop are high an d it is unlikely th at very m uch o f the original p rim ary p roduction th a t is taken ro u n d this loop gets back to the m acrozooplankton. W h a t the loop does achieve, however, is a rap id recycling (rem ineralization) o f m uch o f the n u trien t load th a t is locked in the tissues o f these organism s, thereby m aintaining p rim ary production. T h e biom ass o f the m icrobial loop organism s is low b ut their m etabolism is high, in contrast to the classical food web, w hich is the other w ay round. T h e m icrobial loop operates throughout the w orld’s oceans b u t is o f p articu lar significance in w arm oligotrophic waters, w hich can n o t su p p o rt a substantial clas­ sical food web. It m ay also have an im p o rtan t role in rem ineralizing iron in ironlim ited areas. D espite the small size o f m ost o f the organism s involved in the m icrobial loop, som e o f the energy cycled through it is retu rn ed to the larger

THE BIOLOGY OF THE DEEP OCEAN

44

Fig. 2.6

Simplified food web structure showing the classical food chain and the microbial loop. The dissolved organic carbon (DOC), which provides the basis for the microbial loop, is produced by all organisms but particularly by the phytoplankton. It is cycled through bac­ teria, heterotrophic nanoflagellates (HNF), and ciliates. The microbial food web includes both the microbial loop and the photosynthetic picoplankton and nanoplankton less than 5 pm. (From I Lenz 1992, 2000.)

Classical food chain

Table 2.2 A comparison between cold- and warm-water ecosystems and microbial and classical food webs (from Lenz 1992) Regime Temperature Light

W ater column

Nutrients

Production

Food w eb

High

New

Classical

Low

Regenerated

Microbial

structure Seasonally

Seasonally

limited

mixed

Warm

Unlimited

Stratified

Biomass

Metabolism

Control

Occurrence

Evolutionary age

Microbial food w eb

Low

High

Grazers

Everywhere

Old

Classical

High

Nutrients

Cold-water

Younger

'B ottom up'

systems

Cold-water

Cold

ecosystems W arm-water ecosystems

Properties

food web

'Тор down' Low

LIVING, GROWING, AN D DAYLIGHT

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zooplankton (mesozooplankton) th a t prey on interm ediate-sized organism s such as the larger ciliates (references in M iller 1993). T his p red atio n has little effect on the low er trophic levels; increasing the num bers o f m esozooplankton does reduce the levels o f m icrozooplankton b u t only slightly increases the grow th rates o f phy­ toplankton an d small heterotrophs (Calbet a n d L an d ry 1999). A t a lower size range there is m uch tighter pred ato ry coupling, th at is betw een the nanozoop lankton (2-20 ц т ) an d the num bers o f bacteria a n d o th er picoplankton. T h e control o f oligotrophic p rim ary production, in particular, is therefore m uch m ore susceptible to changes in the populations o f m icro- an d nanozooplankton th an to changes in the larger m esozooplankton. T h e smaller-size categories will to a considerable extent d eterm in e the com m u ­ nity structure an d function in these environm ents, an d control their contribution to regional productivity (Fenchcl 1988). T h e ratio o f hetcrotrophic to autotrophic biom ass ranges from n ear unity in coastal waters, w here nutrients, not grazers, lim it production, to 2:1 in the open ocean w here p red ato ry control is very tight (Gasol et al. 1997). T h e m ain pathw ays for carbon fluxes in the ocean arc through the classical grazing food chain, the m icrobial loop, sinking, carb o n storage, an d carbon fixation. O ceanic bacteria have a m ajor influence on all o f these (Azam 1998).

Ocean viruses M arine viruses occur at a size scalc below the bacterioplankton. T h e ir co ntribu­ tion to the oceanic ecosystcm is only now being recognized an d is still u n d er debate. A ccurate assessment o f viral num bers is technically very difficult b ut some recent w ork on enclosed volum es (80-litre ‘m esocosm s’) o f coastal seaw ater gave bacterial densities o f (2-6) X 109 p e r litre an d (1.5—2) X 101{) viral particles per litre. T h e au th o rs’ conclusion from analysis o f the bacterial grow th rate was that viruses an d protists (flagellates an d ciliatcs) contributed equally to bacterial m o r­ tality (F uhrm an an d N oble 1995). B acterial viruses, or bacteriophages, coexist w ith specific host b acterial cells an d w'hen they infect the bactcria] cell they induce lysis, resulting in the dispersion of huge num bers o f m ature viral particles. In a no rm al environm ent, w here the num bers o f host bacteria an d o f viruses are relatively stable, the viruses are described as ‘te m p erate’. Occasionally, perhaps in conditions o f phvtoplankton blooms, there m ay be sufficient num bers o f host cells for rare ‘v iru len t’ m utants to cause the bacterial populations to crash. I f the hosts are autotrophic cy anobac­ teria this could have a m ajor effect on local p rim ary productivity b ut this rem ains a theoretical scenario in the absencc o f any certain dem onstration o f its o ccur­ rence. O n e o f the m ain effects o f viruses u n d er n o rm al circum stances m ay be the rem ineralization th a t results from the lysis o f bacterial cells. V iral infections o f larger anim als are probably ju st as prevalent in the ocean (including the deep ocean) as they arc on land, b u t our knowledge o f th em is still ru d im en tary an d we have no w-av o f assessing their im pact.

THE BIOLOG Y OF THE DEEP OCEAN

All these constraints an d m odifiers on the p rim ary p roduction ultim ately affect the deep-sea fauna below, through the quantity an d quality o f m aterial exported from the euphotic zone an d finally deposited on the seafloor. D u rin g its long jo u rn e y this m aterial determ ines the sustainable levels o f pelagic biom ass an d energy consum ption dow n through the oceanic w ater colum n. T h e residue arriving on the bottom controls the level o f the bcnthic populations.

Particle feeders and marine snow A t high latitudes herbivores dom inate the zooplankton (copepods in the Arctic; copepods an d euphausiids in the S outhern O cean), m aking u p some 80% o f the total. A t low'cr latitudes the proportion o f herbivores drops to 3 0 -4 0 % , again reflecting the sm aller sizes o f p rim ary producers at these latitudes an d the in ter­ m ediary role o f the organism s involved in the m icrobial loop. A sim ilar reduction in herbivores occurs in the vertical dim ension. In the top 200 m o f the N o rth Pacific filter feeders m ake up m ore th a n 98% o f the total mass o f copepods. Below 1000 m the proportion falls to less th an 10%, w ith p red ato ry species an d m ixed feeders dom inating. T h e debris o f m ucus-feeding webs, gelatinous m aterial from oth er anim als, an d detrital particles form ‘m arine snow7’ (Alldredge an d Silver 1988; L am p itt 1996). T his contributes a m ajor food source for m any o f the sm aller anim als living w ithin the photic zone an d for those well below it: it has been estim ated th a t for every 1 g o f organism in the sea there are 10 g o f particles (and 100 g o f dissolved organic m atter). M arine snow does not, o f course, fall at the rate o f real snow'. Its sinking rate is m ore akin to th at o f dust particles in the atm osphere an d it is to be found in quantity at all depths (Fig. 2.7). Filter feeders such as salps rem ove this particulate m aterial indiscrim inately over a size range o f less th a n 1 jam to m ore th an 1 m m , while m any o f the sm aller zooplankton species (e.g. copepods an d ostracods) probably browse on the particles o f m arine snow' (Fig. 2.7) an d their associated bacterial flora (whose abundan ce m ay be en h an ced by 3—4 orders o f m agnitude over th a t in the surrounding water). T h e result is th at the biom ass density o f small invertebrates associated w ith m arine snow' particles m ay be very m uch greater th a n in the water, m aking the snow an attractive nutritional target. T h e sm aller organism s associated w ith m arine snow dom inate the rem ineraliza­ tion processes; this is the converse o f the situation in open w^ater. T h e m ost effi­ cient filter feeders on very small particles are the larvaceans. T h e filtration ap paratus inside their elaborate house has a m esh o f only ab o u t 0.2 X 1.0 J im an d can readily trap b actcria an d the sm aller picoplankton, as L o h m an n recog­ nized at the tu rn o f the last century. W hen the system clogs, the house (from a few cm to 2 m diam eter) is ab a n d o n ed and a new one secreted. T his m ay occur 5—15 times a day an d the discarded houses provide a significant p ro p o rtio n o f m arine snow particles in some regions. T h e faecal pellets or strings produced by the grazers are some o f the m ost im por­ ta n t o f the m an)' inanim ate nutritious particles in the water. A lthough they contain

LIVING, GROWING, AN D DAYLIGHT

47

Fig. 2.7

An in situ photograph of a marine snow aggregate, derived from a discarded larvacean house, with associated copepods of the genus Oncaea (1.5 mm) grazing on the snow. (Photo: ]. King, University of California.)

‘f

a relatively high p roportion o f refractory m aterial they also contain m uch u n d i­ gested or only partly digested m aterial, particularly in conditions o f high phyto­ plankton abundances w hen the grazers fail to assimilate m uch o f w hat they ingest. In some areas and seasons undigested phytoplankton m ay be a m ajor com ponent o f m arine snow aggregates (C hapter 10). Faecal pellets sedim ent at different rates (Fig. 2.8) an d provide an im p o rtan t food source for m any detritivorous species o f zooplankton. T h e m ultiple recycling o f the m aterial accelerates the rem ineraliza­ tion o f the contained nutrients an d contributes directly to regenerated p rim ary production. Detritivores, as a specialized trophic group, com prise only 1-5% o f plankton biomass. D etritus an d m arine snow also feature in the diet o f m any less specialized omnivores, including several m esopelagic shrim p. Surveys o f a n u m b er o f pelagic ecosystems indicate that herbivores com prise on average 46% o f the com m unity while p redators an d om nivores each contribute 27% .

Viscous effects of sticky water T h e historic im pression that particle size is the critical elem ent for m ost oceanic herbivores has been based on the concept o f a m echanical filtering system b ut it is now know n from high-speed cinem atography studies th at even classical grazers, such as copepods, exercise a considerable degree o f individual particle selection. C alanoid copepods are the m ost ab u n d an t m ulticellular anim als in the sea. T h ey m ake up m ore th an 70% o f all net-collected zooplankton an d constitute the single m ost im portant group o f grazers (M auchline 1998). O n e secret o f their success m ay be th at they operate at the interface betw een the viscous w orld o f the phytoplankton (Reynolds num ber, Re, < 1 ) an d the inertial w orld o f predators such as arrow w orm s (Re 1-2000). C o pepod feeding currents operate at Re 10 1—10 2 an d provide a lam in ar flow conveyor belt o f viscous w ater w ithin w hich food particles can be recognized

THE BIOLOGY OF THE DEEP OCEAN

48

Fig. 2.8

Sediment traps, set at various depths in the water column, collect the downward (export) flux in the form of sinking particles. The trap funnels sedimenting particles into sample jars mounted beneath in a rotating carousel. The preset rotation rate allows consecutive jars to collect the integrated flux over periods of hours or weeks. O nce the trap is recovered, the sequence of samples (which may extend over a year or more) provides information on the quantity, quality, and timing of marine snow 'falls'. (Photo: R. S. Lampitt.)

Я Н » К Г ’- ’-

an d then intercepted (Strickler 1985). T h e flow is fast enough to en train even sw im m ing protists such as flagellates an d ciliates. T h e particle selection m ay be chem o- or m echanosensory, or a com bination o f the two (C hapters 6 an d 7), an d it em phasizes the flexibility an d focus o f the feeding process. T h e w ork has also dem onstrated the need to recognize the constraints im posed by low Reynolds num bers on the feeding m echanism s o f m any o th er small zooplank­ ton. W ater behaves like a very syrupy fluid for organism s the size o f p hyto­ plankton an d m icrozooplankton. Scaling up the sensory an d hydrodynam ic problem s facing a copepod, for exam ple, puts them into perspective. T h ey are akin to those o f a diver, im m ersed in the dark in syrup, w ho is trying to use a knife an d fork to get a m eal out o f suspended rice grains! Viscous forces d o m i­ nate, an d inertial forces are insignificant.

Conclusion T h e oceanic ecosystem is driven by light, ju st as is the terrestrial one. T h e effects o f transm ission through seaw ater on the intensity an d spectral co n ten t o f sunlight w ithin the u pper layers determ ine m any o f the characteristics o f the p rim ary p ro ­ ducers, ju st as in terrestrial systems. Light is one critical factor for photosynthesis; an o th er is the level o f key nutrients. T h e interactions betw een these two com po­ nents, com bined w ith the physiological specializations o f different species o f phy­ toplankton, define the seasonal changes an d d ep th distributions o f the production processes, w hich have knock-on consequences for the deep-sea fauna. T h e

LIVING, GROWING, AND DAYLIGHT

49

p rim ary producers on land fix 56.4 X 10b g С p er y ear (56 Gt); the total biomass, o r standing stock (almost literally!), is 830 X 10lr’ g C , giving a turnover o f 7% (Table 2.1). In the occans the corresponding values are 50 X 10|J an d 1 X 10b g G p er year, respectively, giving a turnover o f alm ost 5000% ! T his p h en o m en al dif­ ference highlights not only the very rap id turnover in the occans b u t also the dif­ ferent qualities o f the resulting standing stock as food m aterial an d the consequent high ecological efficiency o f the oceanic ecosystcm (Table 2.1). This efficiency has to be particularly refined by the deep-sea fauna, alm ost all o f w hich arc far rem oved from the source o f p rim a ry production. Very small photosyn­ thetic cells play a m ajo r role in m any regions, particularly oligotrophic waters, an d their m inute size restricts the species o f zooplankton grazers th at can utilize them to those w'hose feeding m echanism s are efficient at low Reynolds num ber. H eterotrophic bacteria siphon off some o f the prim ary p ro duction through the m icrobial loop an d the w hole com m unity can be critically lim ited by trace ele­ m ents (and probably trace organics). S econdary (and tertiary) p ro duction is ch an ­ nelled very differently in oligotrophic an d eutrophic w aters, an d has different efficiencies. A lm ost all organism s, at all depths, are d ep e n d en t on the processes in the euphotic zone. T h e populations o f anim als in the bathypelagic zone an d on the deep-sea floor are at the end o f the photosynthctic line; th eir num bers an d ecolo­ gies arc d eterm ined by the levels o f carbon exported from the surface an d its sub­ sequent fate en route to the bottom . T h e populations furthest rem oved are those on the seafloor.

3

Life at the bottom

The benthic environment T h e organism s furthest aw ay from the surface productivity are, o f course, those at the bottom o f the ocean. T h e title o f this ch ap ter recognizes th at this special fauna includes those that live on, in, an d ju st above the seafloor. T h e first two categories com prise the benthos (cf. plankton an d nekton), an d respectively describe w hat are technically know n as the epifauna an d the infauna. T h e third category relates to the benthopelagic fauna, those pelagic anim als th at live in elose association w ith the seafloor (Fig. 3.1). Ju st as the pelagic realm is sep ara­ ble into depth-related divisions (C hapter 1), so do biologists recognize depthrelated divisions o f the benthic realm . T h e region th a t extends to 0.2 km (the shelf edge) is know n as the sublittoral, the bathyal extends from 0.2 to 3 km, the abyssal from 3 to 6 km, an d the h adal region is th at in the deep trenches ( > 6 km). T h e changing topography o f these regions, from the lan d edge to the greatest depths, is further described in term s o f the shelf break, continental slope, continental rise, abyssal plains (com prising 50% o f the seafloor), an d deep trenches (Fig. 3.1). M ajo r geological features o f the seafloor scenery present in

Fig. 3.1

Diagram to illustrate the main descriptive areas of the seafloor and their relation to the pelagic zones (cf. Fig. 1.1). Arrows indicate the potential directions of movement of organisms and organic material.

LIFE AT THE BOTTOM

51

p articu lar ocean basins include canyons, seam ounts, an d the m id-ocean ridges (Gage a n d Tyler 1991). A t the im m ediate interface betw een the w ater an d the seafloor frictional forces reduce the cu rren t speed to zero. T h e curren t increases gradually w ith distance from the b o tto m until the free-flow velocity is reached. T h e interm ediate region is know n as the ‘benthic b o u n d ary layer’ an d its thickness depends on the cu rren t speed. It is often considered to be the layer w ithin w hich the b o tto m generates turbulent flow, an d m ay extend to 100 m o r so. It has im p o rtan t consequences for the suspension o f particles an d their availability as a food source. Passive suspen­ sion feeding at the interface w ould be futile because the cu rren t speed is zero; activc suspension feeding is possible (by setting up a w ater current) b u t the p um ping effort required to m aintain an adequate flow o f particles increases w ith proxim ity to the bottom . A t the interface w ith soft sedim ents there is no rigid b o u n d ary as there is on a h ard seafloor an d the consistency o f the sedim ents will d eterm ine the rate o f deceleration o f the currents. D eposit feeding is d ep en d en t upon the quality an d quantity o f the particle flux an d is unaffected by the effects o f the bcnthic b o u n d arv layer— unless the currents are so strong as to scour the sedim ents an d cause them to be resuspended. T h e benthic realm in deep w ater was once assum ed to be relatively peaceful and unaffected by strong currents. It is now know n th at deep currents o f cold w ater flowing from high latitudes tow ards the equator m ay generate high-energy eddies w hich can affect the seafloor over w hich they travel. T hese eddies produce ‘benthic storm s’ w ith cu rren t speeds o f m ore th an 40 cm s '. In one carefully studied area (at a dep th o f 4800 m on the continental rise betw een G ape G od an d N ova Scotia— the H igh-E nergy B enthic B oundary Layer E xperim ent (HEBBLE) site) there m ay be 8—10 such ‘storm s’ p er vear, each lasting 2 20 days (Hollister an d Nowell 1991). T h e curren t scours the sedim ents an d creates a very high sedi­ m ent load in the overlying w ater (described as a thick ncpheloid layer). T h e sedi­ m ent settles out at a m ean rate o f ab o u t 1.4 cm p e r m onth. O th e r ncpheloid layers are som etim es form ed by the im pact o f in tern al waves on the continental slope and they m ay tran sp o rt sediment: out into the open ocean. T h in n e r ncpheloid layers are often present close to the bottom . Such layers greatly affect the benthic com m unities, either by7providing new food supplies or by sm othering the sessile fauna. A t a m uch less extrem e level, the zonation observed in several deep bcnthic com ­ m unities is probably causcd by local variations in the cu rren t regim es in their areas. T h e zonation reflects the consequent differences in sedim ent loading an d the specific requirem ents o f particu lar faunal groups, whose distribution may7also be d eterm ined by the characteristics o f different w'ater masses. Very soft sedim ents m ay behave like high-density fluids an d be unstable. O n the continental slope any sudden m echanical failure (triggered p erh ap s by7 a seismic shudder) can send millions o f tons o f a sedim en t-w ater slurry hurtling dow n the slope in an u nderw ater avalanchc o f unim aginable proportions. T h e sedim ent slurry (or mudslide) m ay travel hundreds o f kilom etres, b earin g all before it,

THE BIOLOGY OF THE DEEP OCEAN

before settling out. Such catastrophic events are u n co m m o n b u t their effects on the benthic fauna m ay persist for decades (C h ap ter 11). T hese mudslides are know n as turbidity currents an d their settled sedim ents are recognizable geologi­ cally as turbidites.

Sampling the benthos Sam pling this environm ent is not easy. C orers, dredges, an d grabs were originally designed for sam pling the geology o f the seabed b u t have been m odified to capture the biology too. Nets, traw led along the seafloor o r m o u n ted on a sled fram e, catch com m ercial species o f fish, shrim p, an d shellfish in shallow w aters an d som e o f the sam e traw ls have been pressed into use for deep-sea sam pling (Gage an d Tyler 1991). Extensive technological developm ent o f the n et sensors an d controls ensures th a t sled nets, in particular, o pen an d close at the start an d end o f each tow, during w hich they take as quantitative a sam ple o f the benthic population as possible. P lankton nets can be m o u n ted on top o f the sled for sam ­ pling the plankton ju st above the bottom . T hese types o f net are very effective on the sedim ent-covered abyssal plains an d gently sloping continental rise b ut are inappropriate for deploym ent over very rocky terrain (such as the m id-ocean ridges), w here they w ould be neither quantitative n o r likely to survive the condi­ tions for long. Canyons an d their walls present an alm ost intractable sam pling challenge. Consequently, there has been increasing use o f p h o tographic an d video-sam pling systems m ounted either on platform s tow ed ju st above the seafloor, or on rem otely operated vehicles (ROVs) an d m an n ed submersibles. T h e great technological advances in seafloor exploration, often driven by the needs o f oil com panies, have yielded a huge am o u n t o f visual d ata a n d allowed large-scale seafloor-im aging surveys to be used to study the b cn th ic fauna (Fig. 3.2). Even surveys carried out for other purposes (e.g. those on the sunken Titanic an d Derbyshire) yield valuable descriptive d ata on the biology o f the region (e.g. V inogradov 2000). D irect observations from subm ersibles am plify the recorded data. ROVs an d subm ersibles can ascend slowly up the steepest o f canyon sides, achieving a com prehensive survey o f the often very rich b u t poorly know n fauna clinging to the near-vertical walls. All these m ethods presuppose first th at the anim als are on the surface (i.e. epibenthic), second th at they are large enough to be recognized from the im ages (i.e. p a rt o f the m egafauna, > 2 .5 m m in size, see below), an d third th a t the)' are w ell-enough know n to be identifiable w ithout the actual specimen! Som e species have even been (optimistically) described from p hotographs alone. Som etim es the anim als can be recognized from their characteristic m ounds, burrow s, or tracks (known as ie b e n sp u re n ’) (Fig. 3.3). T h e relatively low cu rren t speeds in m ost abyssal areas allow these tracks an d trails to persist for periods o f weeks, m onths, or even years, so that the surface presents a kind o f biological palim psest, slowly overw ritten but w ith the recent messages quite legible

LIFE AT THE BOTTOM

53

3.2

Survey pictures northwest of the Shetland Islands taken from a camera towed 3 m above the bottom at depths of about 1000 m show tracks, trails, mounds, and various animals on the sediment surface, including (arrows) an octopod (left) and brittle-stars (right). (Photos: B. Bett.)

ШЯШШШШШЩШЛ, ШШЯШЯЯШШШШШШ

(H eczen an d H ollister 1971). T h e ir persistence depends on the general level of benthic activity in any given region, an d they are likely to persist longest ben eath the oligotrophic oceanic gyres. M any ROVs an d alm ost all subm ersibles are able to capture specific anim als for m ore detailed exam ination or experim ental study, but it is still very difficult to obtain quantitative samples th a t are truly represen­ tative o f populations from sites such as canyon walls, hydrotherm al vents, or rocky outcrops. Visual counts provide b etter representations o f the w hole p o p u ­ lations th an do the exploratory scoops or suction sam ples th a t are the only ones easily attainable w ith these vehicles. Im aging techniques are o f little help w ith m ost o f the infauna. M ost m em bers of this fauna are cither too small a n d /o r too well buried to be visible, although burrow s or m ounds can occasionally be used as estim ates o f abundance. Specialized corers are now routinely em ployed to obtain either one large or several smaller, sim ultaneous, samples o f the sedim ents an d their inhabitants (Fig. 3.4), w ith m inim al disturbance o f the extrem e surface layer (this weakly com ­ pacted region is easily blown aw ay by the ‘bow w ave’ o f geological corers). T h e cores can then be cut into dep th layers an d the anim als w ashed from the sedi­ m ents an d sieved through a series o f increasingly finer meshes. T hose anim als retained on a 0.5 m m m esh are know n as the m acrofauna (m acrobenthos), an d those subsequently retained on m esh o f about 0.05 m m as the m eiofauna. T h e m egafauna (> 2 .5 mm) dom inate the catches o f trawls, sleds, an d dredges b u t are rarely encountered in core samples. T h e sedim ents will contain both dead shells an d live specim ens o f m any very small anim als, particularly foram iniferans, an d specific stains can be used to dis­ tinguish these different com ponents in the preserved samples. T h e infauna is subject to m arked changes in the sedim ent environm ent, the m ost notable being the reduction in oxygen concentrations to zero w ithin 5 -2 0 cm o f the sedim ent surface. T h e vertical zonation o f the infauna reflects the nutritional gradient, with the greatest num bers in the u p p er few millimetres. Burrow ing anim als affect the

THE BIOLOGY OF THE DEEP OCEAN

54

Fig. 3.3

Different species leave different tracks or 'lebenspuren'. Both images are from 4000 m on the Cape Verde abyssal plain, (a) is the forward view from the epibenthic sled and shows mounds with apical holes and radiating patterns. The second image (b) is from a survey camera 3 m above the seafloor (cf. Fig. 3.2) and gives an overhead view of a line o f similar mounds leading to 1m diam. star-shaped patterns. They are the feeding patterns o f a large echiuran worm and the mounds mark its previous positions, showing how it moved on as each site was worked out. (Photos: B. Bett.)

■

zonation by altering the characteristics o f the sedim ent surrounding the burrows. T h ey an d oth er causes o f biotu rb atio n continuously m odify the sedi­ m ent structure, m aking it a dynam ic ra th e r th an a static environm ent.

LIFE AT THE BOTTOM

55

3.4

A sediment core from 2000 m in the Porcupine Seabight, collected with a multicorer device in a tube of 56 mm diameter. An undisturbed fluffy layer of phytodetritus is visible on the surface. (Photo: D. S. M. Billett.)

I-, macro-, and meiofauna T h e benthic fauna is usually subdivided into size-based categories. L arger anim als, w hich can be seen in p hotographs an d caught in trawls, com prise the m egafauna. T h e m egafauna includes both m obile (‘e rra n t’) an d sessile com po­ nents. T h e form er includes m any echinoderm s, molluscs (including octopods), sea spiders (pycnogonids), true crabs, h erm it crabs, shrimps, squat lobsters, an d the b enthic fishes. Som e o f the last three groups spend a considerable tim e in burrows. H olothurians are particularly com m on in the deep sea, som etim es o ccurring in aggregations or ‘h erds’ (Fig. 3.5), an d a few o f their species have w orldwide distributions. Brittle-stars m ay also be hugely ab u n d a n t in certain localities. B enthic fishes are typically sedentary, spending m uch o f their tim e resting on the bottom as ‘sit an d w ait’ predators, an d have little need for the buoy­ ancy adaptations o f their benthopclagic neighbours (C hapter 5). T h ey include the skates, rays, an d scorpion fishes, and, in the deep sea, the eelpouts (Zoarcidae) an d sea-snails (Liparidae). B etter know n are the trip o d fishes (Bathypterois), w hich have an extrem e developm ent o f the fin rays, on w hich the fish perches, holding the head an d body well above the bottom an d facing into the current. T h e sup­ p o rting undercarriage o f fin rays is m uch shorter in their relatives Ipnops, Bathymicrops, an d Chlorophthalmus. Scavenging hagfishes are benthic to the degree that they live in burrows. T h e sessile m egafauna includes xcnophyophores, sponges, anem ones, gorgonians, pennatulids, corals, crinoids, barnacles, brachiopods, mussels, an d ascidians. X enophyophores are large, single-celled, deposit feeders an d arc som etim es very

THE BIOLOGY OF THE DEEP OCEAN

56

Fig. 3.5

An aggregation of the 3-4-cm deep-sea hoiothurian Kolga hyalina at 2000 m in the Porcupine Seabight. Such aggregations may be reproductive or represent accumulation at a particularly rich feeding site. (Photo: D. S. M. Billett.)

a b u n d a n t (Fig. 3.6), b u t m ost o f the sessile m egafauna are suspension feeders. M any o f the latter are attached by long stalks w hich raise th em up out o f the frictional zone an d into the current, w here they adjust their orientation to m ax ­ imize their opportunities for particle capture (Fig. 3.7). T h ey arc m ore ab u n d an t w here bottom currents are strong enough to cause some resuspension o f the sed­ im ents. D ense sedim ent particles soon settle o ut b ut the lighter organic com po­ nents an d finer particlcs persist in suspension (as nepheloid layers) an d provide feeding opportunities for those anim als raised a little above the bottom . Some typical suspension feeders (e.g. ascidians) have responded to the lim itations o f the available food by becom e secondarily p red ato ry (C hapter 5). A few o f the m egafauna are infaunal, living buried in the sedim ents (e.g. ech iu ran w orm s and the hoiothurian Molpadid). T h e m egafaunal biom ass declines m arkedly w ith dep th (Fig 3.8) an d is correlated w ith surface p ro duction (T hurston et al. 1998). T h e m acrofauna com prises those sm aller anim als retained on a sieve o f 0.5m m m esh, although the te rm is used loosely an d depends m uch on the m esh size chosen for the researcher’s p articular application. T h e m acrofauna is d o m ­ inated by polychaete w orm s an d peracarid crustaceans (isopods, am phipods, tanaidaceans, an d cum aceans; see A ppendix), b ut molluscs an d the w orm -like phyla (e.g. sipunculids, priapulids, echiurans, pogonophores, etc.; see A ppendix) arc also im portant. M ost m acrofauna are n o t suspension feeders b ut rath er sedim ent feeders, scavengers, or carnivores. P articular species are usually co n ­ fined to a single oceanic basin, an d abyssal species generally have a w ider dis­ tribution th an slope species. A m ong the molluscs the few suspension feeders tend to have large (metabolically inert) shells b ut reduced soft parts, an d in

LIFE AT THE BOTTOM

57

Fig. 3.6

Xenophyophores photographed from the epibenthic sled at 4000 m on the Cape Verde abyssal plain. These very large (50 mm diameter) but fragile foraminiferans are often missed in net samples because they are so easily destroyed. Photographs show them to be very abundant and ecologically important. (Photo: D. S. M. Billett.)

Fig. 3.7

Four frames of a time-lapse camera series at 4000 m on the Porcupine abyssal plain. The suspension-feeding anemone Sicyonis tuberculata (28 cm diameter) adjusts its ori­ entation to face into the changing direction o f the near-bottom current. Tidal effects on current are often visible in the changing behaviour o f deep-sea populations. (Photo: R. Lampitt.)

THE BIOLOGY OF THE DEEP OCEAN

Fig. 3.8

Profile showing how the biomass o f megabenthos (expressed as lo g10 grams ash-free dry w t [AFDW] rrr2) decreases with depth in the Porcupine Seabight off southwest Ireland. (From Lampitt et al. 1986, with permission from Springer-Verlag.) LogI0gAFDw/m2

the protobranchs the gut increases in length in deep er specics. Both characters arc responses to the difficulties o f acquiring an d absorbing enough nourish­ m ent. B eneath oligotrophic surface w aters the individual m acrofauna ten d to be smaller, probably as a response to food lim itation. Isopods have a g reater diversity o f species u n d er these oligotrophic conditions b u t cum aceans, in contrast, are m ore sparse. T h e m eiofauna is com posed o f those anim als w hich pass through the m acrofaunal screen an d arc retained on the finest meshes, dow n to ab o u t 50 |im . In m ost habitats foram iniferans com prise the m ost individuals b ut nem atode w orm s the m ost species -and m ake up m ost o f the biomass. Foram iniferans include b oth suspension an d deposit feeders, while nem atodes are m ainly m icrobial grazers. N em atodes have a higher diversity in abyssal sedim ents th an in bathyal ones and, excluding the non-agglutinatcd foram iniferans, m ake up 85—9 5 fH> o f the m etazoan biom ass o f the abyssal m eiofauna. O th e r significant com ponents o f the m eiofauna include harpacticoid copepods, ostracods, kinorhynchs, tardigrades, an d loriciferans (Appendix).

LIFE AT THE BOTTOM

59

The benthopelagic fauna T h e benthopelagic fauna is m ade up m ainly o f fishes, but also includes the cirrate octopods, usually observed sw im m ing a few m etres above the bottom . Some sw im m ing holothurians should perhaps also be included, although m ost (but not all) o f them settle on the seabed to feed. T h e re arc also specialist benthic siphonophores th a t an ch o r themselves by their tentacles, for all the w orld like m iniature hot-air balloons. T h e num erous sm aller invertebrates th at live in the w ater ju st above the b ottom are m ore difficult to recognize. As M arshall (1979) p u t it ‘U ntil suitable nets are designed, the small m em bers o f this fau n a m ust be sought alm ost entirely inside the kinds th a t are large enough to ap p e ar in bottom photography.’ Special b ottom traw'ls a n d sleds are now beginning to sam ple some o f these anim als outside their predators. Benthopelagic fishes are the best-know n com pon en t o f the fauna. T h ey are the deep-sea equivalent o f the dem ersal fishes, or g ro u n d fish, recognized elsewhere by fisheries biologists. T h e rattails (m acrourids) are probably the d o m in an t single group but slickheads (alepocephalids), squaloid sharks, spiny-eels (notacanths), halosaurs, deep-sea cods (morids), brotulids, an d synaphobranchid cels arc all im p o rtan t contributors to the fauna. It should n ot be assum ed th at all these anim als arc perm an en tly w edded to the bottom ; individuals arc n ot infrequently found hundreds o f m etres above the bottom an d clearly m any m ake extensive excursions into m idw ater. N evertheless, their prim e h ab itat is the bathypelagic-benthic interface a n d it is for this environm ent that they are adapted. T h ey are very unlike their neighbours im m ediately overhead, the truly m idw ater bathypelagic species. T h ey are robust m uscular fishes (with sufficiently palatable flesh to support an exploratory rattail fishery on the continental slope). T h ey usually have a swim bladder, the length o f whose capillary rete reflects the depth at w hich the species live (C hapter 5), an d have calcified scales an d well-ossified skeletons. T hey are active sw im m ers an d m any have an elongate body form w ith a long, tapering tail an d dorsal fin. T h e slow u nd u lato ry tail sw im m ing seen in m any video sequences seems to be a very econom ical w ay o f moving over the sed­ im ents an d m ay also reducc the hydroacoustic noise (C hapter 6). T h e benthopelagic fauna have the best o f both worlds. T h ey can feed directly on the benthos or utilize the bathy- an d m esopelagic anim als above them . T h e benthopelagic an d m esopelagic fauna m eet on the continental slope an d rise. Analysis o f stom ach contents shows th a t m any bcnthopelagic fishes on the slope m ake the m ost o f this situation by taking mesopielagic prey. T his strategy is particularly profitable because on the slope some meso- an d bathypelagic anim als m ay accu­ m ulate close to the bottom (e.g. lantcrnfishes an d m idw ater shrimp). A lepocephalid fishes cat m edusae an d oth er gelatinous anim als while spiny-eels take sessile hydrozoans, bryozoans, an d anem ones, as well as pelagic prey. O n e group o f rattails (the bathygadines) take m obile prey above the bottom ; their jaws are term inal, their gillrakers close-knit, and their fin arran g em en t tends to keep the h ead up. M ost m em bers o f the o th e r group (the m acrourincs) have ventral protrusible jaw s an d a reinforced snout, an d the fin p attern keeps the head down.

THE BIOLOG Y OF THE DEEP OCEAN

T hese anim als take epifaunal prey as they move over the b o tto m an d probably also root in the sedim ents for food such as polychaetes an d echinoderm s. T h e biom ass o f benthopelagic fishes is o f the o rd er o f a few gram s p er square m etre o f seafloor; that o f the bathypelagic fishes above th em is at best only a few m il­ ligram s p er cubic m etre o f water. E xploitation o f the benthopelagic interface yields high dividends for those species th at have m ade the physiological invest­ m ent required to live there.

Food resources W ith the exception o f the hydrotherm al vents (see below), the food resources available to the seafloor fau n a derive alm ost entirely from photosynthesis n ea r the surface. T h e surface m aterial sinks, in part, as a fine detrital drizzle b u t in tem ­ perate regions som e o f it m ay sedim ent directly as a seasonal deposition o f largely unaltered phytodctritus (C hapter 10). Large food-falls, too, are im p o rtan t to the seafloor economy. T h e largest arc the carcasses o f whales, seals, dolphins, an d large fishes, b u t there is also significant dro p -o u t from dense near-surface sw arm s o f gelatinous anim als such as Pyrosomas or salps. Pyrosoma colonies, for example, reach near-surface densities o f m ore th a n 40 individuals p er cubic m etre. D ead, but largely intact, colonies have been seen on the seafloor at ab o u t 5000 m. Sinking Sargassum w eed, seagrasscs, an d even terrestrial p lan t debris (e.g. logs an d branches) can all be im portant. C am eras can be m o u n ted above artificial b ait cans (or even large carcasses, such as those o f dolphins) and the w'holc assembly then deployed on the seafloor to see w hich o f the fauna are attracted an d how long the bait lasts. T h e rap id ap p e ar­ ance o f scavenging hagfishes, rattails, squaloid sharks, sy naphobranchid eels, squat lobsters, an d shrim ps such as Plesiopenaeus testifies to the im portance and accessibility o f large food-falls in fulfilling the nutritional needs o f m any specics, particularly the benthopelagic fauna (Fig. 7.1). However, the scavengers par excel­ lence are lysianassid am phipods, typified by Eurylhenes, w hich rapidly reduce the largest carcass to skin an d bone a n d arc clearly ad ap ted to take very large meals on the rare occasions w hen they becom e available (C hapter 5). Feeding at a foodfall has risks. L arger species attracted to the fall m ay also feed on th eir smaller com petitors. It is perhaps for this reason th at the soft-cuticled brooding females of Eurythenes arc found not on the bottom , like the hard-cuticled juveniles, b ut 1000 m or m ore above the bottom , in the relative safety o f the im poverished bathvpclagic fauna. After all, one good m eal (75% o f body weight, C h a p te r 5) will sustain a m ature female for well over a year. V ariations in the supply o f carbon to the seafloor m ay explain the differences in the m egafaunal anim als attracted to bait in different areas an d depths (cf. Fig. 8.8). Two abyssal sites in the eastern N o rth A tlantic (one tem perate, one tropical) have been studied recently, using baited cam eras. R attails d om inated the arrivals at the tem perate site, w hereas the shrim p Plesiopenaeus took over at the tropical site.

LIFE AT THE BOTTOM

61

Sm aller particles in the form o f faecal pellets, m arine snow, an d crustacean m oults are im portant contributors to the dow nw ard flux. Faecal pellets sink at rates o f up to 1000 m p er day, fast enough for m any to reach the seafloor w ithout being intercepted an d recycled en route. T h e fate, quantity, an d tim ing o f sinking m aterial can now be estim ated by capturing it in sedim ent traps m o u n ted at dif­ ferent heights above the seafloor (Fig. 2.7). T h e resulting sedim ent accum ulation rates reach 20 cm per 1000 years on the continental slope (about 0.5 jxm p er day), reducing to 0.1—0.2 cm p er 1000 years in the red clay regions o f the abyssal plains. All the benthic fauna are dep en d en t on this m eagre supply an d the sedi­ m ents are continuously rew orked by one species after an o th er to extract the last vestiges o f nourishm ent from it. A hoiothurian m ay ingest 100 g o f sedim ent a day (Fig. 3.9), an d an echinoid will then ingest the h o lo th u rian ’s faecal cast in an hour. T h e am o u n t o f sedim ent available is increased by the burrow ing activities o f the m acrofauna, w hich mix it to depths o f several centim etres. In conditions w here deposit feeders are num erous, the entire u p p er layer o f the sedim ents m ay be rew orked every few m onths (and lebenspuren becom e equiva­ lently ephem eral). T h e nutritional content o f the sedim ent is partly derived from the bacterial flora w ithin it an d for m any anim als the selection o f sedim ent p a rti­ cles is a m atter o f care an d sensory skill. H olothurians are particularly com petent particle pickers, using their oral papillae to select their meals. T h e basis o f selec­ tion is not know n but it is likely to be chemoscnsory. Som e anim als m ay also be able to use dissolved organic m atter. Betw een 50 an d 85% o f the organic carbon is rem ineralized (returned into solution) in the first year after it reaches the seafloor; the rem ainder has a residence tim e o f 15-150 years (cf. 0 .3 -3 years

3.9

Time-lapse images (separated by 30 min) of the 15 cm hoiothurian Benthogone rosea ploughing through the sediment at 2008 m in the Porcupine Seabight and leaving a coil of faeces along its track. (Photos: R. Lampitt.)

THE BIOLOGY OF THE DEEP OCEAN

residence tim e in the w ater column). T h e shallow er sedim ents are com posed largely o f carbonate-containing oozes, b ut low7 tem p eratu re an d high pressure increases the solubility o f calcium carbonate. Consequently, in the A tlantic the carbonate dissolves below7about 5000 m (in the Pacific below ab o u t 3500 m) an d carbonate oozes are replaced by siliceous oozes. T h e low rate o f bacterial action on the deep-sea floor was starkly dem onstrated in 1968 w7hen the subm ersible Alvin sank in 1540 m o f water, taking w ith it a packed lunch-box containing an apple an d a bologna sandwich. W h en the vehiclc was recovered 10 m onths later the sandw ich was hardly affected by bacterial decay, yet a sim ilar one in a refrigerator at the sam e tem p eratu re w'ould have rotted in a few7weeks. It is strange to think th at h ad the sandw ich n o t been in the box, som ething w ould undoubtedly have eaten it— an d thereby delayed the sub­ sequent burst o f scientific interest in deep-sea m icrobiology th at was stim ulated by the apparently im m ortal sandwich. T h e increased pressure o f deep w ater has a synergistic effect w ith the low tem ­ p eratu re to reduce the m etabolic rate o f bacterial action to a fraction o f that at the surface (C hapter 5). Sedim ent com m unity respiration m easurem ents show7 an equivalent decline w ith depth, but this ap p a ren t direct relationship is com ­ plicated by a parallel general decrease in the nutritional value o f the sediment. Yet grow th rates can be very high (C hapter 10) an d some b acteria are barophilic, grow ing faster at high pressures th an at lower ones; consequently, the grow th an d respiration rates o f deep-sea organism s m easured at surface pres­ sures m ay give a very m isleading picture o f the rates in situ. M an y o f the bcnthic organism s seem to have a strategy o f reducing their routine m etabolism betw een m eals b u t rapidly enhancing it w hen food finally becom es available. N o t sur­ prisingly, scavengers increase in nu m b er w ith d ep th b u t specialist carnivores decline. T h e seafloor o f the continental slope is m uch closer to the pro d u ctio n at the surface th an are the abyssal plains. Particles falling from the surface w aters on to the slope are m uch less likely to be extensively rew orked before they reach the bo tto m an d there will also be particulate in p u t from the land. T h e shal­ low er sedim ents are therefore likely to be m uch richer in nutrim ent. T his is reflected by the relative abundance o f b o th species an d individuals in these environm ents. M ost o f the larger benthopelagic an d benthic species live betw een 200 and 1000 m —y e t this m akes up only 4.3% o f the o cean ’s area. T h e continental slope an d rise together com prise only some 10% o f the ocean floor, but support m ore th an 75% o f the benthic biomass. R attail fishes typify this shallow dom inance. T h ere arc som e 40 species in the W estern N o rth A tlantic; 24 o f these have centres o f ab u n d an ce betw een 200 an d 1000 m, 11 betw een 1000 and 2000 m, an d only five are m ost ab u n d a n t below7 2000 m (M arshall 1979). Surface-derived food resources arc the only ones available to m ost o f the benthos but a few-7have access to, and have evolved around, resources o f benthic origin.

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63

Hydrothermal vents and cold seeps In the 1960s an d early 1970s m easurem ents o f tem p eratu re an d salinity close to the deep-sea floor show ed occasional anom alies o f higher tem p eratu re (and som etim es higher salinity). T hese anom alies occurred at locations associated with rift zones an d seafloor spreading. It was assum ed th at h ot fluids, som etim es in the form o f very saline brines, w ere escaping through vents in the seafloor. T his was visually confirm ed by the first subm ersible visit to such a site in 1974. A lthough o f considerable interest to geologists an d geochem ists, these results seem ed of little relevance to biologists— until, that is, rem ote cam eras p h o to g rap h ed assem ­ blages o f unusually large clam shells in one such region n ear the G alapagos Islands. In 1977, w hen the geologists h ad the first o p p ortunity to visit the site w ith a m anned subm ersible, they were com pletely un p rep ared for w hat they found— a biological com m unity o f extraordinary luxuriance an d beauty, do m in ated by giant clam s an d huge tubew orm s, an d alm ost entirely com posed o f anim als new to sciencc (Fig. 3.10). T h e discovery o f the extraordinary com m unities present at m any hydrotherm al vents (extended, later, to cold seeps) has been the m ost excit­ ing biological advance in the deep sea in the past 50 years (Tunnicliffe 1991; Childress an d Fisher 1992; Tunnicliffe et al. 1998; V an D over 1995, 2000). It h ad been a longstanding assum ption, alm ost a dogm a, th at all biological life in the deep sea was ultim ately fuelled by the photosynthesis th a t occurred in the photic zone. T hese discoveries changed all that. Life at h ydrotherm al vents depends not on photosynthesis b u t instead on the activities o f chem osynthetic b ac­ teria, w hich use the oxygen in seaw ater to oxidize reduced inorganic com pounds

Fig. 3.10 A cluster of the hydrothermal vent vestimentiferan Riftia pachyptila from a hydrothermal site on the east Pacific Rise. The dark trophosome is scarlet in life and the white tubes are about 20 mm in diameter. (Photo: HOPE/IFREMER.)

THE BIOLOGY OF THE DEEP OCEAN

(usually sulphides) o r m ethane. T h e energy th a t results from this reaction is then used to synthesize com plex organic molecules using dissolved carbon dioxide (in the form o f b icarbonate ions) as the source o f carbon. T h e process is directly an al­ ogous to photosynthesis, in w hich the energy source is light from the sun. T h e chem osvnthetic bacteria provide the nutritional resources for a w hole host o f specialized anim als w'hose existence was unim agined until those iconoclastic dives. Seaw ater percolates deep beneath the ocean into the e a rth ’s crust, w here it is heated by geotherm al processes an d m uch o f its contained sulphate (Table 5.1) is reduced to sulphide. It is then vented at the spreading centres along the oceanic ridges an d elsewhere. T h e high tem peratu re a n d pressure o f the w ater causes m any o f the m inerals along its way to dissolve. As a result it contains a h e a \y b urden o f solutes (particularly h c a \y metals) w hen it finally em erges through the seafloor, at tem peratures often m ore th an 350°C. As the vent fluid mixes w ith the cold deep w ater ju st above the bottom , the rap id drop in tem p eratu re im m edi­ ately causes m uch o f the m ineral conten t to precipitate o ut o f solution. T h e superheated w ater thus gushes forth from the narro w pipew ork o f the crustal plum bing, spewing out from narrow' ‘chim ncys’ on the seafloor, a n d producing billowing clouds o f dark o r light particulate m aterial as it drops m uch o f its inor­ ganic load. T hese clouds are the black or w hite ‘sm okers’ that form such an awesome spectacle for the intrepid observer. T h ey form a buoyant ‘p lu m e’ w hich ascends an d mixes w ith the am bient seaw ater until it achieves n eu tral density, spreading out at a density interface a few h u n d red m etres above the bottom . Very vigorous eruptions can shoot a ‘m egaplum e’ considerably higher into the w ater colum n. T h e precipitated m aterial also builds up ro u n d the edges o f the chim ­ neys, w hich can grow into fragile, hollow, colum ns o f sulphide reaching to 45 m in height (Fig. 3.11). Even taller chim neys (60 m) m ade o f carb o n ate an d silica have been rep o rted recently from a new site in the m id-A tlantic. T h e h o t w ater m ay also escape by m eans o f a cooler diffuse flow over a m uch w ider area. H ere the vent effluent is visible in the lights o f the exploring subm ersible n o t as a gushing ‘sm oker’ but as a shim m ering region w here the hot flow' mixes w ith the icy bottom water. T h e challenge for the chem osynthetic organism s is to m ake the m ost o f the steep gradients betw een the h o t sulphide-rich w-'ater an d the surrounding oxygenated w’ater. T h e interface provides an ideal environm ent for the m icroorganism s, p ro ­ viding they can avoid the very highest tem peratures. T h e b acteria often form dense m ats several m illim etres thick. T hese provide ‘grazing’ for some organism s, b u t m any o f the larger invertebrates h arb o u r their own chem osynthetic bacteria as endo- or exo-symbionts. At least 10 phyla includc species th at h arb o u r chem oautotrophic symbionts. T hese bacteria provide the m ain source o f n o u r­ ishm ent for m any o f the specialist fauna at h ydrotherm al vents; some o f their hosts (particularly annelid w orm s and vestimentiferans) lack any gut o f their own, an d d ep en d wholly on the endosym bionts for their energy. Molluscs, flatworm s, pogonophorcs, an d vestim entiferans have only intracellular symbionts. Species in oth er phyla (protists, sponges, annelids, arthropods, echinoderm s, nem atodes, an d priapulids) m ay have either extracellular or intracellular sym bionts (Fisher 1996).

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Fig. 3.11 The fauna of the hydrothermal vents on the mid-Atlantic ridge is dominated by shrimp. Rimicaris exoculata (100 mm) swarms over the sulphide chimneys at the 2300 m Rainbow hydrothermal site. (Photo: IFREMER/PICO cruise/MAST3 AMORES).

M ulticellular anim als w ith sym bionts work the interface betw een oxygenated an d sulphide-rich w aters by orientating themselves across it, by w ater pum ping, or by active m ovem ent betw een the two environm ents. T h e spatial distribution o f dif­ ferent trophic guilds o f the vent fauna m ay well be d eterm in ed by the chem ical speciation o f sulphur an d the local (and tem poral) availability o f free sulphide to sym bionts (Childress and Fisher 1992; V an D over 2000; L uther et al. 2001). In some anim als (such as clams an d seep vestimentiferans) sulphide an d oxygen are taken up through different parts o f the body an d delivered separately to the bacteria. In others (such as hydrotherm al vestim entiferans an d mussels), b o th are absorbed across the respiratory surfaces. Sulphide is highly toxic to m ost anim als; mussels first convert it to thiosulphate before transporting it to the symbionts. M any other species transport it linked to a specific binding protein (Childress and Fisher 1992). Indeed, the symbioses m ay well have evolved originally as a m eans o f detoxifying sulphide in the host tissues. Sulphur is deposited w ithin the b ac­ teria w here it m ay accum ulate to m ake up m ore th an 10% o f the dry w eight of the host tissue. Technically an d historically, the vent com m unities are still d ep en d ­ ent on light energy from the sun, because the oxygen in the seaw ater is ultim ately the product o f photosynthesis (C hapter 2). Practically an d immediately, they are nevertheless independent. I f the sun were to be extinguished tom orrow they could continue to flourish for m illennia (Tunnicliffe 1992), at least until the decline in global tem peratures induced m ajor changes in deep currents— or until the photosynthetic oxygen ra n out. T h e m ost vulnerable species w ould be those w ith planktotrophic larvae o r w ith a dietary need for p articu lar com pounds o f photosynthctic origin.

THE BIOLOGY OF THE DEEP OCEAN

In the Pacific O ccan the hydrotherm al vent fauna is d om inated by bivalve m ol­ luscs an d vestim entiferan w orm s, both fuelled by endosym bionts. T h e largest of the w orm s (Rifllia) live in thickets o f tubes (Fig. 3.10), each tube up to 25 m m in diam eter an d a m etre or m ore in length. A scarlet crow n o f gills extends out o f the tube. T h e ir appearance so im pressed the first observers th at one densely p o p ­ ulated area was nam ed the Rose G ard en an d an o th er the G ard en o f Eden! A ssociated w ith the w orm thickets are m any small limpets, snails, oth er worm s, crabs, squat lobsters, and zoarcid fishes, alm ost all o f th em unique to the vents. T h e thickets an d the populations are very dynam ic, w ith great changes visible in apparently established com m unities revisited after a period o f only 2—3 years. V ent com m unities on the A tlantic m id-ocean ridge w ere discovered in the early 1980s an d found to have a rath e r different fauna, usually dom inated by decapod shrim ps (family Bresiliidae), w ith mussels an d clam s sim ilar to those in the Pacific (Van D over 1995). T h e vent com m unities o f b o th occans h arb o u r num erous polychaetc w orm s. T h e bresiliid shrim p sw arm in countless millions on an d aro u n d the chim neys at m any A tlantic vent sites, b u t the reasons for their do m i­ nance, an d for the alm ost com plete absence o f vestim entiferans, are n ot u n d er­ stood (Fig. 3.11). Sim ilar shrim ps have recently been found to be ab u n d an t at southern Indian O cean vent sites. T h e A tlantic mussels have endosym bionts w ithin the gills an d the shrim p m aintain ‘gard en s’ o f exosym bionts on their gills an d exoskeleton. H ydro th erm al vents occur at sites from shallow' w ater to the deep sea. T h e ir initial novelty provided a w hole new' fauna th a t needed to be described an d allowed the taxonom ists to indulge their whimsies in n am in g the anim als after features o f the geology (e.g. snail Ventsia an d p o g o n o p h o ran w orm s Riftia an d Ridgeia), p articular vent fields (e.g. am p h ip o d Luckia striki), or the subm ersibles th at w ere used to explore an d sam ple the environm ent (e.g. polychaete w orm Alvinella, crab Cyanagrea, snail Shinkailepas, nam ed after the subm ersibles Alvin, Cyana, an d Shinkai). T h e first sites discovered w ere few' an d far betw een, an d were know n to be ephem eral, w ith lifetimes o f only a few decades. Indeed, one site at 9°N on the E ast Pacific Rise w'as first visited in 1989 an d revisited in 1991, only for the stunned observers to discover th a t the com m unity h ad been largely destroyed, w ith freshly dead anim als scattered aroun d , some o f th em even partially inciner­ ated, an d new' volcanic rock widely visible. T h e dives h ad missed a new' eruption by just a m atter o f days an d h ad witnessed the (tem porary) destruction o f a vent com munity. Even at th a t early stage the new h ot vents w ere blow ing o ut bacterial aggregates in a snow'-like blizzard (Lutz an d H ay m o n 1994; K unzig 2000; Van D over 2000). D ead sites, m arked by num bers o f em pty mussel shells b ut no rem aining hydrotherm al activity, are frequent. T his has led to considerable debate as to how the unique fauna m anages to m aintain its existence an d disperse effectively enough to reach new sites. It is now clear th at h ydrotherm al sites are m uch com ­ m oner th an initially thought, with, for exam ple, one every few tens o f kilom etres over m uch o f the m id-A tlantic ridge. N ew sites arc being found alm ost w herever

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the seafloor geology is appropriate an d the technology is available to investigate it. T h e perceived difficulties o f recruitm ent a n d colonization dim inish w ith the recognition o f m ore sites b u t the rates a n d processes involved are still little u n d e r­ stood. Certainly, recolonization o f a new site can occur very rapidly, an d it has been possible to follow the process in repeated visits to the new site on the East Pacific Rise noted above (Lutz a n d H ay m o n 1994; Shank et al. 1998). C lum ps of large tubew orm s (Tevnia) w ere present only a year later, spaw ning vestimcntiferans (Riftia) over a m etre long w'ere found after 21 m onths, an d mussels by late 1995. G enetic analyses o f shrim p populations at different sites on the m id-A tlantic ridge show th a t there is clearly considerable gene flow betw een th em (i.e. individuals transferring betw een the sites as adults or larvae). Sim ilar results have been o btained w ith a variety o f species at the G alapagos an d East Pacific Rise loca­ tions. M ixing am ong populations seems to be a general p h en o m en o n w ithin and betw een vent sectors on the sam e ridge an d m ust be achieved by w idespread dis­ tribution o f the larvae o f hydrotherm al vent species in the overlying w ater colum ns (Tyler an d Young 1999). It is easy to recognize the potential for larval dispersal, w ith the individuals perh ap s entrained in large eddies o f the vent plum e, b u t m uch h ard er to identify the m eans w hereby the larvae alight at an appropriate site. It is ironic th a t although the first dem onstration o f sulphur-oxidizing endosym ­ bionts was in the deep-sea vent fauna in 1980, the b actcria have subsequently been found in anim als from m any shallow -w ater habitats w ith sim ilar chem ical characteristics (e.g. sew’age outfalls, pulp-m ill effluents, an d o th er anoxic muds). N ot all endosym bionts use reduced sulphur com pounds; some use reduced carbon com pounds, particularly m ethane (such b acteria are know n as m ethanotrophs). T hese m icroorganism s are particularly prevalent at subm arine seeps (‘cold seeps’, in contrast to the hot hydrotherm al sites) w here w ater or brine co n ­ taining hydrocarbons (and often sulphides) trickles o ut from geological strata (usually limestone) exposed ben eath the sea (Olu and Sibuet 1998). T h e sym­ bionts are present in molluscs, pogonophores, an d sponges. G as (methane) exchange betw een the seaw ater an d the sym bionts is facilitated by their location in the extensive gill epithelium of, for exam ple, their bivalve hosts. T h e fluid th at em erges from cold brine seeps has a m uch greater density th a n the surrounding w ater; this can result in the bizarre sight o f a reflective lake or p o n d deep in the ocean, w here the brine collects in a depression on the seafloor an d is so dense th at it does not m ix readily w ith the w'ater above it. C hem osynthetic species flourish at its edges. M ethane occurs as a gas or, u n d er pressure, as a solid ice (m ethane hydrate). In shallow' water, m ethane readily em erges from the seafloor as stream s o f gas bubbles (these are easily visible on echosounder records, w hich can be used to search for such sites). O n the deep ocean floor the high pressures encourage the form ation o f m ethane icc an d there are large deposits o f this m aterial in certain regions. Small changes in w ater tem perature could lead to a phase change an d

THE BIOLOGY OF THE DEEP OCEAN

gasification o f the deposits. A t one site in the G u lf o f M exico there is even a p a r­ ticular polychaete w orm (known colloquially as the ‘ice w o rm ’) th at lives in depressions on the blocks o f m ethane ice. The w idespread occurrence of m ethane (and other hydrocarbons) offers extensive opportunities b oth to m ethanotrophic bacteria an d to those anim als th a t can em ploy the b acteria as symbionts, although thiotrophic bacteria are at least as com m on at cold seeps as m ethanotrophs. Som e species o f mussel an d snail hedge their bets by h arb o u rin g both kinds o f symbionts. A wide range o f biological an d geological situations provides local reducing envi­ ronm ents in the deep sea w ithin w hich thiotrophic a n d /o r m ethanotrophic b ac­ tcria flourish, often in corporated in symbiotic associations in com m unities that are allied taxonom icallv to those at hydrotherm al vents (‘C ognate sites’; Van D over 2000). A nim als w ith chem osynthetic endosym bionts have, for example, been found on an d aro u n d w hale carcasses on the deep-sea floor (Smith et al. 1998). T h e decaying oily tissues provide reducing, sulphur-rich, conditions w hich are ideal for the sym bionts an d w hich m ay persist for m any m onths or years. At the tim e o f w riting some 16 species associated with w hale carcasses are also found at vents o r seeps. W hale carcasses (of which, at any one time, there are m any thousand scattered on the seabed) m ay thus provide additional seafloor ‘stepping stones’ for the dispersal o f species from one h ydrotherm al vent or cold seep to another. W hales are o f relatively recent origin, yet there arc m uch older fossil vent com m unities. T h e carcasses o f other large m arin e vertebrates (including ichthyosaurs) m ay have served the sam e purpose in the M esozoic as those of wrhales do now--. L arvae in the w ater colum n settle at ap p ro p riate sites, w hether hydrotherm al vents, cold seeps, or w hale carcasses. Any sim ilar ‘red u cin g ’ site will do equally well for some species. Large vestim entiferans (Lametlibrachia) an d mussels related to those at w hale carcasscs an d seeps were found in the hold o f a ship th at sank off N W Spain in 1979 (D ando et a l 1992). T h e hold contained sunflower seeds an d bags o f beans w hich decayed to generate the ap p ro p riate reducing environm ent for the vestim entiferans to grow-' at rates o f ab o u t 100 m m p er year. It is a com ­ plete m ystery w here the larvae originated because these w orm s are otherw ise know n only at hydrotherm al an d eold-seep sites in the Pacific, b ut their arrival in the hold show ed th at there m ust be oth er (still unknown) colonies in the Atlantic. T h e hydrotherm al vents have been described as oases in the deep sea, in refer­ ence to the dram atic increase in local production relative to the surrounding abyssal seafloor (one o f the vestim entiferans has even been given the generic nam e Oasisia). Biomass values m ay reach 10 -50 kg m 2 a n d the physiological rates o f the organism s are often little different from those o f shallow -w atcr species. Fossil sulphide chim neys a n d shell assemblages attest to the long evolutionary history o f these com m unities. D ram atic though they arc, it is im p o rtan t to rem em b er th a t they are o f very lim ited area. T h e ir local contribution to deep-sea production m ay be very high, b u t their global contribution is estim ated at only ab o u t 0.03% o f global oceanic p rim a ry production, o r 3% o f the total carbon

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flux to the deep-sea floor (Van D over 2000). T h e ir spatial isolation has analogies w ith th a t o f the deepest (hadal) regions o f the ocean.

The hadal zone T h e seafloor trenches plu m m et from 6000 m to alm ost 11 000 m an d provide the deepest ocean environm ents (Fig. 3.1). T h ere are 37 trenches (28 in the Pacific) an d a few are m ore th a n 2000 km long. Nevertheless, w-ith an area o f 4.5 X 10<} km 2 they com prise only ju st over 1 % o f the seafloor area. T his h ad al (or ultraabyssal) region provides a unique h abitat w here organism s are exposed to the greatest hydrostatic pressures. T h e faunas arc subject to seismic activity an d sed­ im ent slum ps because m ost trenches lie in the earth q u ak e zones w here the seafloor plates are subducted beneath the continents. D espite the in h eren t fasci­ nation o f exploring the life in these rem ote an d isolated regions, the small extent o f the zone and its g reat distance from the surface has m ean t th a t there have been few biological investigations o f the fauna an d alm ost all relate to the b enthos (just 80 b ottom traw l an d grab samples w ere know’n to W olff in 1970). T h e pio n eer­ ing Galathea an d Vitiaz expeditions were the sources o f these samples. T h ey were able to drop grabs an d send bottom trawls alm ost vertically to the seafloor, letting the traw l drag across the bo tto m as the ship drifted. M ore recent studies have also used pop-up baited traps set at h ad al depths. T h e re is also a lim ited, but rapidly enlarging, archive o f p hotographs an d videoim ages o f the h ad al seafloor. T h e bathvscaphc Trieste is the only m an n ed vchiclc ever to have reach ed the greatest depths. T h e few observations m ade on th a t unique occasion in 1960 (see p. 163) w ere also o f the seafloor (Piccard an d D ietz 1961). By contrast, there has been little study o f the pelagic fauna o f the h ad al zone. N o m idw ater traw ling pro g ram m e w ith closing nets has yet been undertaken, and the use o f open nets m akes it impossible to distinguish the anim als caught below 6000 m from those taken betw een 6000 m an d the surface. T h e absence o f midwrater traw'l d ata is hardly surprising, because to fish a large m idw ater trawl at 9000 m w ould require a m inim um o f 15 km o f traw l wire, a n d 20 km w ould give m ore certainty o f reaching the req u ired depth (C hapter 1). N o present research ship has this capability N ew technology in the form o f ROVs has already h a d an im pact; the Ja p an ese R O V Kaiko can reach full ocean d ep th an d has been instrum ental in the discover)7 o f a hyd ro th erm al vent an d its asso­ ciated chem osynthetic com m unity at 7326 m in the J a p a n T ren ch (Fujikura et al. 1999). Fladal sam pling is technically very dem anding, achieves few samples p er day o f shiptim e, an d has little perceived econom ic value. It is thus prohibitively expensive for m ost institutions and nations. T h ere is an in term ediate benthic zone o f ab o u t 6—7 km w here the h ad al an d deep abyssal fauna overlap b u t the faunal com position does n ot change m arkedly either dow n the 6—11 km dep th range or from one trench to an o th er (Wolff 1970; Belyaev 1972, 1989; V inogradova 1997). T h e true hadal fauna has no d ecapod crustaceans

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70

and very few bryozoans, cum aceans, fishes, coelenterates (apart from actinians and scyphozoans), or echinoderm s other th an holothurians. H olothurians are by far the m ost ab u n d a n t o f the m egafauna an d polychaete w orm s dom inate the m acrofauna. T h ere are also relatively higher proportions o f species o f bivalves, echiurans, an d am phipods th a n at abyssal depths (3000-6000 m). T h e samples o f h adal fauna that have been collected so far show a high degree o f endem ism . T h e distribution o f individual species is often lim ited either to a single trench o r to the trenches w ithin a single oceanic basin (Vinogradova 1997). D ata published in 1989 by Belyaev show'ed that o f m ore th an 600 species collected at h adal depths, 56% wrere endem ic to hadal regions (the rem aining 44% w ere also know n from abyssal samples). Remarkably, 47% w ere know n only from a single trench an d only 3% from two or m ore widely separated trenches (Vinogradova 1997). However, the sam ple num bers an d locations arc relatively few an d m ore extensive sam pling is likely to decrease the perceived degree o f endem ism . V inogradova (1997) notes that this will certainly apply to the notional hadopelagic fauna as it becom es b etter know n and concludes th at ‘the reality o f a separate pelagic fauna in the hadal region should be reconsidered’. P opulations o f the scavenging am phipod Hirondella gigas from different trenches show sufficient m orphological differences to identify their origins with consider­ able confidence (France 1993). By contrast, Pacific populations o f the related abyssal am phipod Eurythenes gryllus show little genetic divergence at sites w ithin the sam e depth zone in an oceanic basin, but m arked divergence, to the level of cryptic taxa, in different dep th zones (France an d K ocher 1996). T h e conclusion is th a t gene flow' betw een adjacent trench populations w ithin a basin is very lim ited (similar to the lim ited flow betw een hydrotherm al vent populations on different ridges). D espite the differences in the traw ling eq u ip m en t used by different expeditions there is a consistent— an d staggering— num erical dom inance o f holothurians below' 8000 m: holothurians com prised up to 98% in n u m b er o f individuals an d m ore than 99% in w et w eight o f some Vitiaz samples from the K u ril-K a m ch a tk a T rench (Belyaev 1989, cited in W olff 1970). T h e hadal fauna in general shows no particu lar m orphological features although increased gigantism seems to be a feature o f hadal isopods an d some other crustaceans (Wolff 1970). A bsence or reduction o f eyes an d pigm ent is com m on b ut these are also features o f m any shallower benthic anim als (C hapter 9). Biochem ical adaptations to the very high pressures are undoubtedly present in all the endem ic hadal organism s but have been recognized so far only in a barophilic bacterium (Fang et al. 2000).

Spatial heterogeneity T h e illusion o f the uniform ity an d tranquillity o f the deep-sea floor has been shattered by its recent exploration. Vents a n d seeps provide dram atically different

LIFE AT THE BOTTOM

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local environm ents contrasting hugely w ith the adjacent seafloor. Physical factors everywhere p roducc g reat variations in sedim ent size, stability, an d com position; anim als superim pose a three-dim ensional com plexity by virtue o f their burrow ­ ing, pum ping, sweeping, feeding, an d excretory activities. T h e w idespread spatial heterogeneity generated by these factors is p erp etu ated by the general absence o f destructively strong currents. T h e environm ent is far m ore diverse th a n the pelagic one; the heterogeneity exists at scales relevant to every kind o f organism , is recognizable everywhere, an d is responsible for the unexpectedly high diversity o f the fauna (see C h a p te r 11).

Conclusion T h e benthic a n d benthopelagic environm ents are very different habitats w hen com pared w ith the w ater colum n above. T h ey are prim arily tw o-dim ensional an d their inhabitants d epend for their nutrition mostly on the largesse o f the m id ­ w ater fauna that intercepts the production exported from the surface. Nevertheless, the seasonal characteristics o f the surfacc w aters still determ in e the lifestyle an d com position o f the benthic populations deep below. T h e accum ula­ tion o f all kinds o f trophic end-products o f the surface photosynthesis provides rich pickings for those organism s capable o f extracting n ourishm ent from the sed­ im ents, o r ad ep t at com peting w ith oth er scavengers for larger particles. T h e envi­ ro n m en t is both dynam ic an d heterogeneous, the scale ranging from the fresh lava an d m ountainously rocky topography o f the m id-ocean ridges to the deep sedi­ m ent layers o f the abyssal basins an d the steep canyons o f the continental slope. M any o f these areas are difficult to sam ple at all, others are difficult to do so q u a n ­ titatively, yet core samples provide inform ation on the spatial structure o f the fauna on a scale still unavailable to the m idw ater biologist. S uspended particles provide nutritional opportunities for grow th and, in the form o f turbidity currents, for local death. O n the slopes the fau n a overlaps the meso- an d bathypelagic populations an d their daily m igrations, providing further scope for trophic enterprise by the benthopelagic fauna. T h e benthic an d benthopelagic m cgafauna are generally larger th a n their pelagic co u n ter­ parts, indicating th a t w ith m etabolic p rudence the resources available are suffi­ cient for substantial individual growth. T h e teem ing, bactcria-fed populations at the hydrotherm al vents an d cold seeps reinforcc the m essage th at life on the deep-sea floor can have an energy an d an activity th at seems to be largely denied to the bathypelagic populations ju st above.

Patterns and changes

al views and patterns I f we consider (rightly) that the global oceans are vast, mobile, an d dynam ic living spaces, interconnected across the surface o f the E arth, it is tem pting to assume (wrongly) th a t their inhabitants are uniform ly distributed th ro u g h o u t the oceans’ volume. T h e tem ptation is there because m ost o f the organism s are small an d can n o t be seen from the surface. T h e A tlantic O cean has a replacem ent tim e o f ab o u t 250 years, h a lf th a t o f the Pacific; if the oceans’ w aters are continually mixing, surely the organism s m ust be equally well mixed? Yet experience tells us that m a n ta rays are not seen in the N o rth Sea, n o r A ntarctic krill in the M editerranean. Similarly, in the vertical dim ension, we know th a t ad u lt angler­ fish are not caught n ear the surface, nor, if we w ere in a deep submersible, w’ould we expect to see a haddock swim by at 6000 m. O rganism s arc not evenly distributed, either horizontally or vertically. T h e obvious physical an d biological gradients betw een the o cean ’s surface an d its depths m ake it fairly easy to accept that species m ight, in general, be lim ited to p articular dep th horizons. T h e horizontal gradients arc m uch less obvious, an d the horizontal space available is so m uch g reater (thousands o f kilometres, com ­ p are d w ith ju st eleven vertically) th a t it is m uch less ap p aren t why spccies m ight be lim ited in their horizontal distribution. R ecent developm ents in rem ote sensing using satellites, however, have revolution­ ized our perspectives. Two satellites in particular, first the C oastal Z one C olour S canner (CZCS), now defunct, an d recently the Sea-viewing W ide Field-of-vicw Sensor (SeaWiFS) have allowed us to look globally at the oceans rath e r th a n ju st locally. T h e satellite m easures the surface reflectance o f the ocean w ithin selected bandw idths o f the visible spectrum , providing a continuous global view of changes in the near-surface scattering an d chlorophyll concentrations. From the data we can discrim inate betw een different do m in an t groups o f phytoplankton an d even betw een ‘new ’ o r ‘regenerated ’ production (C hapter 2). T h u s the region-specific seasonal changes in ecological processes, as expressed in the changes in phvtoplankton populations (convertible w ith caution into prim ary production), can now be m onitored over the whole ocean. I f the assum ption is m ade th a t secondary and te rtia n ' pro duction o f zooplankton an d nekton throughout the w ater colum n is dep en d en t on these surface p h en o m en a, th en it m av be possible to construct a global biogeograph)' w ithin w hich ‘d om ains’ (or

PATTERNS AND CHANGES

73

‘biom es’) an d ‘provinces’ can be recognized, analogous to those identified in te r­ restrial ecosystems (e.g. savannah, forest, grassland, a n d desert). Such a tem plate has been suggested by L onghurst (1998) w ho identifies four global biom es (the Polar, Coastal, W esterly W'inds, an d T rad e Wrind biomes) divis­ ible in the various oceans into a total o f som e 52 biogeographic provinces (Fig. 4,1). H e regards these as denoting ‘the 1” an d 2° hierarchical areas o f the u p p er ocean for w hich definable an d observable boundaries are suggested an d w ithin w'hich . . . unique ecological characteristics m ay be p red icted ’. In essence, the m ajor p attern s are defined by physical processes th at d eterm in e the spatial an d seasonal p atterns o f p rim ary production. T h e close global m atch betw een the ocean circulation p atterns a n d the levels o f p rim ary production, o f zooplankton biomass, an d o f benthic biom ass em phasize the close global coupling betw een the physics an d the biology (Fig. 2.1).

Horizontal distributions If we w’ish to establish how an d why organism s are distributed th ro u g h o u t the oceans, the first problem we have to solve is how to go ab o u t it w ith the sam pling tools we have at our disposal (C hapter 1). T his is fundam entally a problem of scale in tim e an d spacc (H aury et al. 1978). A n u m b er o f samples taken over a large area will provide inform ation about the biogeography o f oceanic organism s,

Fig. 4.1

The map shows the main oceanic current patterns and the biogeographical domains and provinces, which correspond to particular climatic and near-surface oceanographic condi­ tions. Polar, Trade Wind, and Westerly provinces are indicated by P, T, and W, respectively. The North Pacific Polar Front Convergence and the Southern Subtropical Convergence are shown dark, and the Antarctic Convergence as a line o f small circles. The biological consequences of the differences cascade down to the deep midwater populations and to the benthos, although with increasing depth horizontal transport processes rapidly blur the boundaries. (From Cox and M oore 2000, after Longhurst 1995.)

THE BIOLOGY OF THE DEEP OCEAN

while the sam e n u m b e r o f sam ples taken over a very m uch sm aller area m ight tell us ab o u t patchiness. T h e satellite d ata do provide b o th — b ut can n o t tell us ab o u t species, n o r about distributions extending from below the surface into the deep sea. Indeed, as a consequence o f this lim itation L onghurst (1998) considered th at ‘It is difficult to sec how progress in und erstan d in g these [benthic an d bathy­ pelagic] ecosystems can accelerate in the foreseeable fu tu re’. Patchiness in the pelagic oceanic environm ent is conceptually different from that on land, an d from th a t on the sea bottom . Patchiness on the seafloor is a p roduct o f persistent local spatial heterogeneity, w hich is lacking in the pelagic environ­ m ent. A lthough there is spatial heterogeneity it is n o t locally persistent. As one pelagic biologist has pointed out: ‘In substrate-dependent systems patchiness usually m eans the absence o f organism s w hereas in the pelagic systems patchiness m eans the presence o f organism s’ a n d ‘A lmost n o thing o f significance th a t g en­ erates patchiness in substrate-oriented systems is im p o rtan t in the pelagic realm ’ (H am ner 1988). All organism s are small in com parison w ith the extent o f the oceans, so the scale o f biogcographic sam pling is not affected by the size o f the organism (although, o f course, the sam pler is; C h a p te r 1). T h e scalc o f patchiness, however, is directly related to the size o f the organism (H aurv et al. 1978). D ifferent sam pling scales are required to identify patchiness in, for exam ple, phytoplankton, euphausiids, an d fish, but patchiness in euphausiids an d fish larvae o f sim ilar sizes can be exam ined using the sam e sam pling scales.

Large-scale distributions (biogeography) T h e first attem pt to exam ine the occurrence o f oceanic anim als in all the w orld’s oceans w7as that o f the Challenger expedition in 1872. T h e first task o f the biolo­ gists after the vessel’s retu rn in 1876 was to describe the m any new species of anim als that h a d been collected. T h e grad u al outlining o f p attern s o f distribution was to take very m uch longer and require m any m ore expeditions an d sam pling program m es. Since th a t tim e a g reat m any samples have been taken in the various oceans, often w ith different objectives, an d we have gradually accum ulated sufficient d ata points to interp ret the general distribution p attern s o f particular, frequently caught, organism s. T hese biological p attern s can then be linked w ith the physical occanographic m easurem ents, w hich arc usually m ade in o rd er to identify the wrater masses and the circulation p atterns o f a region. It m ay th en be possible to sec w hether there arc any clear correlations th at can help to explain why a specics has only a lim ited biogcographic distribution (Angel 1994), D escription o f the p attern is the first step. T h e longer-term aim is to recognize how it is m aintained an d wc really do n o t yet u n d erstan d this. It seems to involve the large-scale climatic an d oceanographic processes, recognizable by SeaW iFS. T hese processes result in the generation o f w ater masses an d circulation pattern s

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75

w hich persist on geological time-scales, an d w hich in teract w ith the m echanism s o f speciation (M cG ow an 1974). In consequence, the study o f oceanic biogeographv has forged strong ties betw een biologists an d physicists in their com m on search for an u n d erstanding o f the dynam ics o f the oceans an d th eir inhabitants.

Physical factors N o m atter how detailed the satellite im ages o f the surface, the distribution of anim als ben eath the surface can only be established by sampling. Nevertheless, it has been clear from the earliest days that anim al distributions an d ocean physics arc intim ately related. O n e exam ple o f physics-related biogeography, identified long before satellite surface d ata becam e available, is the distribution in the Indian O cean o f 17 species o f euphausiid shrim ps o f the genus Euphausia. O c e a n ­ ographic expeditions have collected enough samples over the years for the latitu­ dinal distributions to be reasonably well defined. T h e re is a steady succession of species to be found as w’e progress northw ards from the A ntarctic shelf edge to the equator an d beyond (Fig. 4.2). A t first sight there is no obvious reason for the clear limits to m any species’ range, b u t w hen the m ajo r o ceanographic features, or convergences, are superim posed on the distribution p attern it is im m ediately ap p a ren t that they act as unseen boundaries. T h ese convergences m ark the b oundaries betw een m ajor oceanic w ater masses, w here one w ater mass m ay sink

Fig. 4.2

The latitudinal distributions of species of Euphausia in the southern hemisphere show marked discontinuities which are closely correlated with major oceanographic features such as the shelf edge, Antarctic Convergence (AC), Subtropical Convergence (STC), and Tropical Convergence (TC). The width o f the blocks indicates the relative proportion of that species taken at each latitude. (From Baker 1965, with permission from Cambridge University Press.) RARAGIBBA TENERA Q oДЮ МЕОЕАЕ BREVIS MUTiCA

THE BIOLOGY OF THE DEEP OCEAN

beneath an o th er (as at the A ntarctic convergence) an d w here the m in o r physical gradients w ithin the adjacent w ater masses steepen suddenly at the interface betw een the two. T h ey are sem i-perm anent features o f the ocean circulation system, although their positions an d intensities changc w ith b oth tim e an d season. Interactions betw een w ater masses often result in intense local mixing, replenish­ ing surface nutrients an d producing an increase in local p rim ary p ro duction an d the subsequent populations o f zooplankton. Convergences arc very large-scale exam ples o f ocean ‘fronts’. Fronts occur at all tim e- an d spacc-scales w here two w'ater masses o f significantly different ch arac­ teristics m eet. O ften they are visible not only from the satellite b ut also to the sea­ farer as differences in w ater colour, surface roughness, o r accum ulations of flotsam along the intervening boundary. T h e ir effects often extend well out o f sight into the deep occan. In the oceanic sp ace-tim e continuum o f processes they are places w here physical an d biological processes tend to coincide an d their study helps us to interp ret the p atterns o f plankton distribution (Sournia 1994). Fronts m ark the boundaries betw een different regions, b ut they are leaky and elastic boundaries. The}7can be linear at the edge o f a large cu rren t or circular at the p eriphery o f an eddy. T h e physical changes across them m ay n o t be very great, w ith the result that the physical changes th a t occur over a few tens of m etres in the vertical dim ension (e.g. across a pycnocline) m ay only be m atched by moving hundreds o f kilom etres horizontally. T h e satellite ‘sees’ fronts as surface p h en o m en a but the recognizable m eanders, eddies, filaments, an d squirts not only take place in three dim ensions but can also originate at any d ep th w here currents interact. Som etim es a single oceanic feature m ay be so overw helm ing th a t it alone d eter­ m ines the geographic distribution o f man}7species, b oth in m idw ater an d on the bottom . A case in p o in t is the existence o f parts o f the ocean w here the level o f oxygen in the w ater below the surfacc m ixed layer drops to a vanishingly low con­ centration. T his m ay h ap p en because the w ater al th a t site is replenished only very slowly or is effectively stagnant (as in the C ariaco T rench in the C aribbean). It m ay also h ap p en even w hen there is a steady circulation o f the water, if the rate o f consum ption o f the oxygen exceeds the rate o f in p u t from the incom ing currents. T h e two m ain areas w here this occurs arc the N o rth ern In d ian O ccan an d the central eastern tropical Pacific (ETP). Both are regions o f upw elling an d intense surfacc production; n o t all o f this production is consum ed by the zooplankton an d as the residue sinks, along w ith the zooplankton’s faecal pellets, it is oxidized during the desccnt, resulting in the rem oval o f alm ost all o f the oxygen in the 1000 m o r so below the m ixed layer. T hese areas are very challenging for m ost midw ater anim als, w hich cannot tolerate the hypoxic conditions in the layer. M ost species present elsewhere in the respective oceans are therefore excluded from the low-oxygen water. Nevertheless, there are a few7specics in m ost taxonom ic groups that have adap ted to cope w ith these conditions an d their distributions often directly reflect the p atterns o f the oxygen m inim um layers. In the E T P p articu lar cuphausiid shrim ps an d scopelarchid fishes arc endem ic to the oxygen m inim um

PATTERNS AN D CHANGES

77

layer, as show n in Fig. 4.3. Euphausia distinguenda is endem ic to the E T P an d ab u n ­ d an t in the oxygen m inim um region. E. eximia has a sim ilar range b u t is m ost a b u n d a n t at the edges o f the oxygen m inim um . In the In d ian O cean som e myctophid fishes arc similarly characteristic o f the low-oxygen region (e.g. Diaphus arabicus, Benthosema pterotum) and can clearly cope with it (Fig. 4.4). T h e codiet fish Bregmaceros nectabanus occurs in the A tlantic, Pacific, an d In d ian O ceans, b u t in each case is largely restricted to regions w here there are intense oxygen m inim um layers, including all three noted above.

Faunal provinces O xygen m inim a provide extrem e exam ples o f single oceanographic features th at d eterm ine the distribution p atterns o f some specics. M ost d eterm in in g features are m ore subtle integrals o f several characteristics o f the w ater mass. R ecognition o f these com es only gradually, w ith the steady accum ulation o f relevant d ata (including satellite imagery) an d their correlation w ith species distributions. A single research cruise w7ill not suffice to describe, an d th en disentangle, the distri­ bution p atterns o f the Pacific O cean. A cruisc targeted at a specific region, however, using the accum ulated know ledge from m any previous cruises as its foundation, can contribute very significantly to the in terp retatio n o f the patterns. Ju st such a program m e in the Pacific, undertak en by M cG ow an (1974) an d his colleagues at the Scripps Institution o f O ceanograp h y in C alifornia, has led to a m uch clearer view o f how oceanic ecosystems are structured an d m aintained.

Fig. 4.3

The ranges of the euphausiid shrimps Euphausia eximia and E. distinguenda in the eastern tropical Pacific are closely linked to the subsurface low-oxygen zone. The former is most abundant at the margins o f the zone and the latter in the centre of the zone. (From Brinton 1980, reprinted with permission from Elsevier Science.)

140°

100°

60°

140°

100°

60°

THE BIOLOGY OF THE DEEP OCEAN

Fig. 4.4

The vertical profile of oxygen in the northwest Indian Ocean shows a pronounced minimum between 200 and 1200 m. The superimposed day and night depth distributions o f the lanternfish Hygophum proximum show that it spends the day in the low-oxygen water and at night undertakes a diel vertical migration into oxygenated water.

100

No. o f H. proxim um !\(f m 3 80 60 40 20 0

20

T h e first step was the establishm ent o f the distribution ranges o f species from a n u m b er o f different groups o f organism s, w hich required the involvem ent in the pro g ram m e o f specialists in the taxonom y o f these groups. M ost species for w hich sufficient inform ation was available h ad ranges restricted to p articu lar areas o f the Pacific, an d m ost ranges fitted w ithin a few basic patterns. T hese w ere found to apply to anim als as diverse in structure a n d h ab it as foram iniferans, chaetognaths, euphausiids, ptcropods, copepods, an d fish. T h e p attern s were clarified by defining a ‘100% core zone’ for each pattern ; this defined the area w here the indi­ vidual ranges o f all species showing th a t p attern overlapped. T h e resultant m ap (Fig. 4.5) shows eight m ain ‘core zones’, w ith a general sym­ m etry betw een the n o rth an d south Pacific. T h ese are referred to as biotic provinces, an d com prise the Subarctic a n d Subantarctic, the N o rth an d South T ransition, the N o rth an d South C entral, the E quatorial, an d the E astern T ropical Pacific zones (the latter w ith its d o m in an t oxygen m inim um layer). T h ere is an additional (not shown, but broader) p attern o f organism s, nam ely the W arm W ater ‘C osm opolites’, w hich overlaps the E quatorial an d C en tral zones but

PATTERNS AN D CHANGES

79

4.5

The patterns of the core biotic provinces of the oceanic Pacific, derived from the biolog­ ical distributions and the hydrography. Each stippled area indicates the main population centre of a particular recognizable community (note the northern and southern central gyre communities, and the one associated with the eastern tropical Pacific low-oxygen region; Fig. 4.3). (From McGowan 1974.)

i60"w extends considerably further west. T hese species should p erhaps be considered as opportunists. T h e biotic provinces are not exclusive groups o f species: the pairs o f n orth an d south C en tral zones, north and south T ransition zones, an d the Subarctic an d Subantarctic zones all have species in com m on b u t the populations are separated by a central gap in their distributions. T his type o f non-continuous specics distribution is know n as ‘am phitropical’. T h ere is a strong basis for considering these faunal provinces as ecosystems, in the sense that they are real com m unities evolved (and evolving) in response to com m on physical features o f the environm ent. T h e fact th at m any o f the provinces arc scm i-enclosed, in that they coincide w ith recognized recirculating w ater masses (e.g. the N o rth an d South C entral zones are close to the centres o f large anticyclonic gyres), gives them som e degree o f isolation an d provides the opportunity for adaptation, species succession, an d the developm ent o f som e­ thing akin to the terrestrial concept o f ‘clim ax’ com m unities.

THE BIOLOGY OF THE DEEP OCEAN

T h e persistence o f this circulatory isolation is geological in its time-scale, because the circulation p atterns o f the Pacific are tied to the size an d shape o f its basin, the direction o f rotation o f the E arth, the w ind systems (driven by the geologically cooler poles), an d the w ater densities, determ in ed by the p attern o f rainfall an d evaporation at the surface. T h e provinces arc ancient features an d their very scale provides a buffer against short-term fluctuations. T h e ir cycles o f abu n d an ce are tuned to clim ate, not to w eather, an d the horizontal gradients w ithin them arc gentle an d contain no m ajor fronts. T h ey are n o t ju st surface phen o m en a; their influence extends into the deep sea. A detailed analysis o f the N o rth ern C entral zone provides an exam ple o f the sub­ tlety an d com plexity o f the environm ental differences w hich the organism s of p articular ecosystems experience. T his zone differs from the adjacent zones in its low n utrient concentrations, its low standing crop o f phytoplankton an d zoo­ plankton, its high average surface tem peratu re an d salinity, an d in the seasonal changes in all these factors. M aps o f these features an d o f the anim al distributions show the close similarities. A lthough I have described these ecosystems as separate entities, p artly m ain ­ tained by the structure o f the ocean circulation, there is also a very substan­ tial tran sp o rt (advection) into and out o f them , so their populations are continually exposed to im m igration an d em igration, the latter including some o f the p rim ary production that is generated w ithin each ecosystem. T his con­ tinual flux betw een ecosystems (and across the intervening regions betw een them) is the level to w hich the oceans an d their inhabitants arc m ixed throughout, b u t the tim e-scale is long an d the degree to w hich it occurs is lim ited an d variable. T h e Pacific O cean has been the subject o f p articu lar scrutiny b u t the sam e type o f p atterns probably occur elsewhere. T h e distribution o f lanternfishes (M vctophidae) in the A tlantic has led Backus a n d colleagues at the W oods H ole O ceanographic Institution to recognize seven faunal regions an d 19 faunal provinces, although the environm ental differences betw een them are less well researched th an those in the Pacific (Backus et al. 1977). T h e technique o f p rin ­ cipal com ponent analvsis similarly sorts the decapod shrim ps o f the eastern N o rth A tlantic into 14 faunal groups whose three-dim ensional distribution is largely explicable in term s o f the classical N o rth A tlantic circulation p attern s (Fasham an d Foxton 1979). D ata from the Indian O ccan arc still too sparse to draw convincing conclusions ab o u t the scale an d distribution o f oceanic provinces there. T h e A ntarctic O ccan has a m ajo r feature, the circum polar current, flowing ro u n d A ntarctica. T his provides a continual polar-scalc m ixing o f the ocean an d contributes significantly to the region’s m uch m ore uniform oceanic biogeography. T h e general conclusions concerning the distribution o f organism s th at can be draw n from the satellite data and from deep-sea sam pling arc sim ilar in principle. Biological distributions arc often lim ited and, for v ery small organism s, usually determ ined by the physics; anim als in the depths arc inevitably affected by the

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photosynthetic processes occurring above them . T h e differences in the described p atterns are largely m atters o f sam pling adequacy an d detailed interpretation.

Active transport T h e scale o f p attern is continuous: below the scale o f the persistent oceanic provinces arc large-scale w ater m ovem ents that tran sp o rt organism s from one p a rt o f the ocean to an o th er over periods o f weeks to years. M in o r changes in the curren t p attern o f the G u lf Stream result in the unexpected ap p earan cc o f w arm er-w ater species in the English C hannel, giving rise to the concept o f ‘indi­ cator species’ from w hich to identify a particu lar w ater mass. M ost ocean o g ra­ phers now prefer to regard these specics as indicators o f p articu lar ocean processes ra th e r th an ju st o f w ater masses, looking to a m ore dynam ic in te rp re­ tation. C on cern is now being raised that the persistent th erm o h alin e circulation o f the N o rth A tlantic is vulnerable to the clim atic consequences o f global w arm ing. Its potential reversal would have m ajor (but uncertain) consequences for the faunal patterns. Satellite imagery, particularly sea-surface tem peratu re m easurem ent, has p ro ­ vided a vivid indication o f the scalc o f these advective transports o f w ater an d organism s (Richards an d G ould 1996). W arm -w ater currents such as the G ulf S tream an d K uroshio ap p e ar as m eandering stream s w hen viewed at this range. T h e ir short-term fluctuations can be m onitored continuously in a m a n n er that was never possible using ju st ships as the observing platform s. Nevertheless, ship­ b o ard m easurem ents provided the first intim ation o f one o f the m ost rem arkable p h en o m en a associated w ith the m ajor curren t stream s, nam ely the probability that they will behave ju st like a large river on a flat plain an d form m eanders. In the occans these m eanders readily pinch off from the m ain stream , enclosing a large slug o f w ater from one or other side w ithin a ring o f the original cu rren t (like ox-bow' lakes on land). These rings w ere first studied in the A tlantic, as ‘slingshots’ throw n off by the G u lf S tream (Richardson 1983). T h e m ajor curren t system o f the G u lf S tream separates the high productivity an d cold w ater on the eastern U S continental slope from the w arm b ut low productivity w ater o f the Sargasso Sea. W h en a m ean d er pushes o ut to the west o f the m ain stream it will enclose a core o f w arm Sargasso Sea water, while it will have a core o f cold shelf w ater if it pushes o ut to the east. If the m ean d er then breaks aw ay from the m ain curren t as a ring, the core w ater goes with it. Both ‘w arm -co re’ rings (heading tow ards the shelf edge) an d ‘cold-core’ rings (heading into the Atlantic) arc form ed frequently, b ut the latter persist for longer as the)’ track across the w estern A tlantic. T hey are advcctivc m ovem ents o f very large volum es o f water: 5—10 cold-corc rings form every year, com prising cylinders of w ater some 150 -300 km in d iam eter and at least 2 .5 -3 km deep. T h e ir m o m en tu m carries them eastw ards, rotating anticlockwisc; some move south an d re-m erge w ith the G u lf Stream , others persist for 1 3 years, identifiable from their surface tem perature signature (Fig 4.6).

THE BIOLOGY OF THE DEEP OCEAN

Fig. 4.6

Schematic diagram showing (above) the formation of a ring enclosing a cold core of slope water and (below) the distribution, rotation, and direction o f travel of warm-core and cold-core Gulf Stream rings. (From Richardson 1976, 1983, with permission from Springer-Verlag and Oceanus.)

T h e original populations in the cold-core w ater arc tran sp o rted w ith it into an alien tem perature an d productivity environm ent from w hich they are initially insulated by the thick (up to 100 km) sheath o f G u lf S tream w ater ro u n d the core. T h e pres­ ence o f shelf species in the m id-A tlantic can n o t therefore really be reg ard ed as an extension o f their n atural range but rath e r as an artificial tran sp lan t from the n o rm al one. T h e lifetime o f the cold-core rings may, however, be long enough for one o r m ore generations o f a p articular species to take place w ithin the core o f the ring before it degenerates (The R ing G roup 1981; W iebc 1982). By following the biological changcs w ithin a single ring it is possible to see the grad u al physiological declinc o f some slope-w ater species an d their disappearance as they starve to death, w hile w arm -w ater species gradually invade the core (Wiebe an d Boyd 1978). Should the presence o f reproducing individuals be regarded as indicative o f their

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n atu ral range? O r are they really the oceanic equivalent o f the d oom ed em igrants on an A m azonian reed island swept out into the Atlantic? Both views are valid; som e organism s will survive the move, others will perish. G u lf S tream rings provide a large-scale exam ple o f a p h en o m en o n th a t occurs at all scales. Sim ilar rings have now been identified in association w ith m any other currents and less clearly defined m esoscale eddies (hundreds o f kilom etres in diam eter) arc w idespread in the w orld oceans (e.g. M eddies, C h a p te r 1). Satellite im agery provides a dram atic picture o f the im m ensely com plex eddies, swirls, an d filam ents o f w ater that m ake up the surface layers o f an o ccan w hich looks deceptively uniform from the deck o f a ship (Fig. 1.5). W ater m ovem ents o f these kinds result in patchy distributions o f organism s, an d on this patchiness is superim posed the local patchiness th a t results from the activities o f the organism s themselves.

Small-scale distributions (patchiness) Patchiness o f organism s in the ocean m ay be causcd by: (1) (2) (3) (4) (5)

physicochem ical gradients (e.g. o f tem peratu re or nutrients); mass w ater tran sp o rt (as noted above); reproductive and social p atterns (e.g. sw arm ing an d schooling behaviour); interspecific com petitive o r predatory7interactions (e.g. grazing); substrate heterogeneity (especially applicable to the seafloor).

D ifferent sam pling m ethods arc required for different patch sizes an d different organism s. T h e sm aller the scale o f the patch, the finer the sam pling resolution needs to be (Platt a n d D en m an 1980). Large nets an d discrete w ater samples are inappropriate tools for small patches of, respectively, zooplankton o r phvtoplankton. C ontinuous sam pling m ethods are the only ones th a t can give th e necessary spatial fine detail. L arge phytoplankton patches can be seen from satellites an d sm aller ones delineated by continuous m easurem ents o f fluorescence; zooplank­ ton patches can be m onitored by their high-frequcncy acoustic backscatter. ‘Particles’, w hether zooplankton or phytoplankton, can be counted and sorted into size spectra by continuous flow cytom etry an d optical plankton counters, while larger zooplankton can be sam pled at intervals o f only a few tens o f m etres w ith the L o n g h u rst-H a rd y P lankton R ecorder (C hapter 1), Patchiness on the seafloor can be identified an d analysed using ph o to g rap h ic surveys o r core samples, depending on the size o f organism involved (C h ap ter 3). Patches o f small organism s are form ed continuously in m idw ater by fronts, eddies, internal waves, and w'ind, and continuously dispersed by the process of diffusion. T h e potential speed o f this dispersion is indicated by an experim ent in which a 200-kg sam ple o f a fluorescent dye was p u t into the sea an d its spread m onitored. After only 21 days it covered 3000 k n r\ In the facc o f this passive dis­ persion a small p atch will n o t rem ain intact for long. A p atch o f phytoplankton needs to be 10-100 km in diam eter for it to persist for long in the face o f passive

THE BIOLOGY OF THE DEEP OCEAN

dispersion. In areas w here the grow th rate is low (e.g. the Sargasso Sea) large patches m ay never be generated. L arger organism s are less subject to passive dis­ persion. It has been possible, for exam ple, to track the progress o f patches of copepods in the N o rth Sea for over two m onths. T h e tools o f m olecular biology are now available to study dispersal in zooplankton an d give us inform ation ab o u t the historical m ixing processes betw een populations. Linking the m olecular level to the global, ‘Q uantification o f dispersal m ay allow assessment an d prediction of spatial p atterns o f biological productivity in m arine ecosystem s’ (Bucklin 1995). G razing is a m ajor cause o f patchiness. O v er the L ong Island shelf it has been cal­ culated th a t approxim ately 50% o f the annual particulate p rim ary production is consum ed by grazing zooplankton. M u ch o f the spring bloom is n o t grazed because the zooplankton populations lag behind the phvtoplankton production, b ut the autum n one is overgrazed because the position is reversed (Dagg an d T u rn e r 1982). N u trien t levels m ay lim it phytoplankton grow th (C hapter 2) an d the local regenera­ tion o f nitrogen by the excretory activities o f zooplankton m ay stim ulate local (i.e. patchy) bursts o f growth. T h e consequenccs o f the patchy distribution o f food, w hether phytoplankton o r zooplankton, can be profound. C opepods such as Acartia an d Centropages need a constant high level o f food availability. T h ey will n ot succeed unless they encounter large patches o f phytoplankton. Pseudocalanus an d Calanus on the other h an d can cope w ith m ore discontinuous feeding an d therefore arc less susceptible to the vagaries o f phytoplankton patchiness. D agg (1977) has p ointed out that zooplankton and phytoplankton arc patchy on alm ost any tem poral o r spatial scale considered. We m ust try to sec variability from the point o f view o f the individual anim al w ithin the zooplankton, because the an im al’s perception o f a heterogeneous distribution o f food is likely to be quite different from that o f o u r (much larger) instrum ents. A nim als such as the chaetognath Sagitta can eat enough food in a few m inutes to suffice for 24 hours. Patchy food will be non-patchy in term s o f the ch aeto g n ath ’s m etabolism , so long as it encounters a p atch once a day. In other w ords the food is perceived in a m ore uniform wav th an it actually occurs in the environm ent. Patchincss to a scaveng­ ing rattail is very different to th a t experienced by a suspension-feeding stalked crinoid. Z ooplankton w ith a rapid breeding cycle will, in general, be favoured by conditions in w hich patchcs persist for a m o n th or m ore, long enough for them to com plete their full cycle. Slower breeders will be favoured w here patchcs are m ore short-lived and food concentrations generally lower. D espite the accepted im por­ tance o f such biological interactions in the generation an d m ain ten an ce o f p atch ­ incss, a detailed study o f the phytoplankton an d zooplankton patchiness in the N o rth Sea an d British C olum bia coast concluded th at ‘A t least in these systems the intensity, m orphology, an d scale dcpendcnce o f the plankton spatial p attern are stronglv regulated by, an d spatially correlated w ith, physical oceanographic processes (turbulent advection, upwelling, convcrgencc an d vertical m ixing)’ (Mackas et al. 1985). A classic exam ple o f the significance o f patchincss in the success o r failure o f a p o p ­ ulation is that described by Lasker (1975). Larvae o f the N o rth ern Anchovy,

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Engraulis mordax, need a m inim um concentration o f food particles w ithin 2.5 days o f hatching to feed successfully. Lasker tested lab o rato ry -reared larvae in the n atu ral conditions off the coast o f C alifornia a n d found th at feeding in the surface w ater was m inim al but th a t a deeper patch o f phytoplankton allowed extensive feeding. In M arch an d A pril 1974 a dense layer o f phytoplankton some 100 km long was present w hich supported successful feeding by the larvae. A storm later m ixed the top 20 m o f the w ater colum n, dispersed the phytoplankton p atch, and effectively destroyed the larval feeding grounds, ensuring that any anchovy larvae in the area simply did n o t survive. In general, a stable ocean is best for larval sur­ vival in the апсЬолу, a n d there is a linear relationship betw een daily larval survival an d the num bers o f calm periods p er m onth. Benthic storm s can have sim ilar cat­ astrophic effects on the inhabitants o f scoured sedim ents (C hapter 3). X ot all storm s are bad. T h e A tlantic m en h ad en spawns offshore b ut m etam o r­ phoses in estuaries; winds cause upwelling at the w estern edge o f the G u lf Stream an d the result is high nutrien t an d phytoplankton levels. Spaw ning in this w ater is m axim al d uring storm s w hich drive the w ater tow ards the shore. T h e larvae are retained an d feed w ithin the w ater mass as it moves shorew ard, allowing them to enter the estuaries a m onth or two later. Even small-scale turbulence can be advantageous; at low prey densities it increases the en co u n ter rate betw een fish larvae an d their prey. O n the oth er hand, not all patches are good. M ortality rates o f young fish by predation can be correlated w ith patchincss. T h e ir own p re d a ­ tors have greatest im pact on a dense patch o f larvae, an d to reduce pred atio n losses there has to be a com prom ise betw een high densities o f food organism s an d low- densities o f w ell-dispersed larvae. T h a t grazing causes patchiness seems intuitively obvious, b u t it is n o t so easy to find direct evidence for it in the open occan. C ircum stantial evidence com es from the fact th a t detailed surveys o f zooplankton an d phytoplankton have found a negative correlation betw een the two at all spatial scales, an d th a t the spatial vari­ ance o f am m o n ia (indicative o f zooplankton excretion) is correlated w ith the spatial variance o f chlorophyll. It is still w ell-nigh impossible in the o pen o cean to distinguish patchiness o f a p articular food organism induced by a p articular species o f grazer, but one study in a large enclosure o r ‘m esocosm ’ showed how the cuphausiid Thysanoessa raschii was rapidly attracted to an introduced p atch o f algae, its abundan ce in the patch increasing by an o rd er o f m agnitude in h alf an h o u r (Price 1989). It is im p o rtan t to rem em ber th a t the integrated cues o u r instru­ m ents use (e.g. chlorophyll fluorescence) are a very coarse representation o f the value o f the food available to the zooplankton. P articular specics o f zooplankton only thrive on p articu lar spccics or sizes o f phvtoplankton, an d other spccics m ay even be toxic (C h ap ter 7). In one experim ent the copepod Acartia was fed different specics o f phytoplankton a n d only reproduced well on the larger species, so in this case phytoplankton ccll size seems to be im portant (Verity an d S m ayda 1989). In a different set o f experim ents on Calanus pacifkus five species o f phytoplankton p roduced good grow th an d five others were no b etter th an filtered seawater. N o correlation could be found w ith cell size,

THE BIOLOGY OF THE DEEP OCEAN

carbon content, shape, or texture an d the authors concluded th at m ore subtle nutritional deficiencies were responsible for the species w hich yielded m inim al grow th (H untley et a l 1987). Survey d ata can easily m ask local patchiness by co n ­ sidering only the average level o f phytoplankton. O n e detailed com parison betw een the feeding requirem ents o f the copepod C. pacificus an d environm ental levels o f phytoplankton dem onstrated an average value ad equate to support the species, but a finer scale analysis revealed th at at 25 out o f the 61 sites th at were sam pled the phytoplankton levels were inadequate to m atch the co p ep o d ’s respi­ ratory losses (M ullin an d Brooks 1976). T h e spatial scale o f sam pling (and analy­ sis) is all-im portant. T h e authors o f this w ork concluded: ‘T h e ecological consequences will d epend on the rapidity with w hich turbulence, im balance of prim ary production an d grazing, an d vertical m ovem ents o f plants an d anim als rearran g e the spatial pattern o f m alnutrition an d surfeit.’ Som e grazers can cope w ith very large differences in food availability. T h e arctic an d subarctic copepod Neocalanus plumchms is found in the B ering Sea w here it has access to chlorophyll levels as high as 10 m g m :i on w hich it achieves an ingestion rate o f some 14-135 ng chlorophyll h '. In contrast, those individuals in the high arctic Pacific experience chlorophyll levels only 10% o f those in the B ering Sea a n d their ingestion rates reach only 0.3—2 ng h '. T h e result is th a t n o t only is the copcpodite V body size o f the Bering Sea specim ens twice that o f those in the Pacific b u t they also reach this develop­ m ent stage in h alf the tim e (46 days against 91 days). T h e flexible physiology o f the species, however, does allow the Pacific specim ens to survive, despite the near-starvation conditions (Dagg 1991).

Vertical distributions I have considered biogeograph}' an d patchiness as if they were largely twodim ensional p henom ena. T his is convenient b ut illusory. In the real w orld o f the oceans (and the sediments) all distributions have a th ird dim ension, the vertical one. Becausc the scales (distances) on which organism s arc distributed are so com pressed in the vertical dim ension it is often h ard e r to recognize an d q u a n ­ tify vertical patchiness (or layering) th an horizontal patchiness. In any event, the two are inseparable; integrating instrum ents such as fluorescence sensors show great variability in the vertical distribution o f chlorophyll (and therefore phvtoplankton) an d acoustic backscatter m easurem ents d em onstrate the vertical patchiness o f a w ide range o f anim als, from plankton to fish. R a p id changes in small-scale three-dim ensional distributions occur as a consequence o f anim al behaviour. T h e u n derw ater observations o f diving biologists have show n how p articu lar species o f zooplankton can aggregate into dense sw arm s o f varying shape u n d er the influence o f social, reproductive, or defensive behaviours (O m ori and H a m n e r 1982; H a m n e r 1988). T hese aggregations can certainly som etim es spread out horizontally at a physical interface, such as the th e rm o ­ cline, but the m ore activc the organism the less constrained will the aggregations

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be by such local gradients. C opepods, mysids, krill, decap o d shrimps, polychacte w orm s, fish, an d squid all form such sw arm s (in w hich they are u n oriented rel­ ative to each other) o r schools (in w hich the orientation is m ore defined). T hese aggregations can vary m arkedly in ab u ndance over very short vertical an d h o ri­ zontal distances, providing extrem e patchincss in three dim ensions. ‘H erd s’ of holothurians (Fig. 3.5) provide a benthic counterp art. N ew optical an d acoustic techniques, whose discrim ination is vastly superior to the older m ethods, are opening the eyes o f biological oceanographers to the extrem ely fine layering o f m any species o f zooplankton. N et sam pling m ay indicate an average density of, say, 1 copepod m 3 b u t fincr-scale observations m ay show th at the net data m ask the fact th a t the m axim um population density is really up to 6 orders o f m ag ­ n itude higher but is distributed in layers less th a n 1 m thick. T h e layers m ay also contain higher concentrations o f phytoplankton a n d /o r m arine snow. U n d er the conditions in the layers, the scope for interactions betw een individuals becom es com pletely different. ‘Biom ass’ is a convenient integral for com paring biological distributions on the large scale an d is particularly useful w hen considering the vertical com ponent. It is m ost com m only (and easily) m easured from n et samples as displacem ent volum e p e r u nit volum e o f water. In general, the pelagic an d planktonic biom ass declines logarithm ically from a m axim um value n ear the surfacc to a m inim um close to the seafloor (Fig. 4.7). T his generalization holds for alm ost all the w'orld’s oceans a n d is a consequence o f the lim itation o f p rim ary p ro ­ duction (i.e. the basic source o f food for everything else) to those surface w aters w ith adequate light intensities. T h e 10% that is exported to deep er w ater has to fuel the entire m eso- an d bathypelagic populations, as well as m ost o f the benthos. T h e further from this prim e source o f en erg y the low er the biomass. T his is often referred to as an ‘inverted pyram id’ o f biomass. I f this general p icture is separated into its com ponent parts (i.e. into different groups o f animals) the vertical distributions are m ore varied. T aken even further, to the species level, we find it is m ade up o f a mosaic o f vertical p attern s an d ab u n ­ dances (e.g. a lot o f m ackerel in the u p p er layers an d far fewer anglerfishes in d eep water). T his vertical distribution is n o t an im m utable one; m ajo r changes occur w ithin it, on a w hole range o f different time-scales. Vertical advective changes, however, induced by the vertical transport o f w ater masses, are rare w hen com pared w ith horizontal advection. T his is because the density structure o f the oceans provides the w ater colum n w ith vertical stability, w ith the result that a great deal m ore physical energy is required to initiate vertical changes in the w’ater structure th an horizontal ones. Generally, such vertical tran sp o rt as does occur is m ost obvious in coastal upwelling, wiren seasonal winds bring w ater from depths o f 100 m or so up to the surface. Nevertheless, there are locations w here the com bination o f topography, seasonal winds, an d wreak density' strat­ ification induce currents that bring deep-w ater anim als to the surface (e.g. in the S trait o f M essina). T h e re arc also dow nw ard transports, such as at the S trait o f G ibraltar, w here dense saline w ater from the M ed iterran ean flows

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88

Fig. 4.7

Regression lines for the changes in biomass with depth at eight positions in the eastern North Atlantic Vertical. Biomass of plankton (В, C, F, G, 0.33 mm mesh net) and nekton (A, D, E, H, 4.5 mm mesh net) was measured as wet displacement volume per 1000 m5 of water. (From Angel and Baker 1982.)

over the sill into the A tlantic carrying its associated fau n a w ith it an d spread­ ing out at an equilibrium dep th o f 600-1 0 0 0 m (Fig. 1.3). Vertical advection is m ost ap p a ren t in the w inter w ind-m ixing o f the u p p er few h u n d red m etres of the w ater colum n in tem perate a n d subpolar latitudes, b ut this is a general m ixing rath e r th an a one-w ay transport. U p w ard tran sp o rt off the b o tto m in deep w ater can result from the effects o f h ydrotherm al vents (C hapter 3). H o t, buoyant fluids from the vents entrain b o tto m w ater in a vertical plum e that m ay rise for several h u n d red m etres before it is sufficiently m ixed to reach neutral buoyancy. Like smoke from a chimney, b o tto m currents m ay cause the plum e to throw off eddies which in tu rn m ay entrain larvae a n d disperse them well beyond the im m ediate vent site. Active m igrations arc a m uch m ore frequent cause o f m ajo r changes in the verti­ cal distribution p atterns o f m any different species. T h e time-scales on w hich these occur fall into two m ain categories, ontogenetic an d diel.

PATTERNS AND CHANGES

89

Ontogenetic vertical migration T h e ab u n d a n t food supply n ea rer the surface an d the small particle size available there m ake it an ideal feeding ground for the larvae o f m any meso- a n d bathy­ pelagic species. T h e larvae o f deep-w ater squid, fish, an d shrim ps can be found close to the surfacc an d as they grow they tend to live deep er an d d eep er in the w ater colum n, sinking either gradually over their w hole developm ent p erio d or m ore suddenly at a p articular stage o f m etam orphosis. T h e sam e applies to oth er groups in w hich the adults m ay n o t live so deep (e.g. ostracods, chaetognaths, euphausiids, etc.). T his has the add ed benefit th a t the adults a n d larvae are spa­ tially separated. T h ey do not com pete for the sam e resources, n o r are the adults likely to en counter their own larvae d uring their search for prey. T h e spatial sep­ aration betw een larvae, juveniles, an d adults m ay apply n o t only n ea r the surface b u t also in deep water, w here vertical separation on the basis o f size m ay occur at depths o f several kilometres. Seasonal changes in vertical distribution are often synchronized w ith ontoge­ netic changes an d constitute an environm entally linked form o f the latter. T hey are usually recognizable as a response to extrem e seasonal variability in the food supply (prim ary productivity) at the surface an d are therefore m ost fre­ quently encountered at high latitudes. In the north east A tlantic the copepod Calanus finmarchicus, for exam ple, overw inters as the p re-adult copepodite V stage at ab o u t 1000 m , living on its fat reserves. In the spring it m oults to the adult form an d rises into the surface w aters as the spring bloom gets u n d er way. Neocalanus plumchms behaves similarly in the n o rth Pacific, except th a t its w inter dep th is only some 100-250 m an d the behaviour p a tte rn varies co n ­ siderably betw een populations in different areas. A very intense seasonal vari­ ability in food supply is also a feature o f upw elling areas, an d the copepods Calanus pacificus a n d Calanoid.es carinatus rem ain at d ep th in the intervals betw een the upw elling periods in the eastern Pacific, eastern A tlantic, a n d n o rth ­ w estern In d ian O ceans. T h e deep-w ater d o rm a n t phase o f m any o f these m igrations is often regarded as equivalent to diapause in insects, w hen the m etabolic rate is m uch reduced (e.g. M iller an d C lem ons 1988), Regardless o f w hether there is an internally-m ediated physiological diapause, the desccnt into deeper, colder, w ater itself reduces the m etabolic dem ands o f body m ain te­ nance. D uring the A ntarctic w inter some copepods have a real dorm ancy, while oth er anim als (e.g. euphausiids an d hyperiid am phipods) simply reduce their m etabolic rates an d live largely on their reserves, w ithout any associated seasonal m igration. T h e synchrony o f seasonal vertical m igration w ith local changes in advective tran sp o rt o f w'ater m ay result in the retention o f a species in a lim ited area. T h e best exam ples o f this occur in the A ntarctic; several species o f copepod (Rhincalanus nasutus, Calanoides acutus) an d euphausiid (Euphausia superba) concen­ trate at 25 0 -5 0 0 m d uring the winter, in w ater th a t is tran sp o rted southw ards. T h ey rise to the surfacc d uring the spring an d summ er, are carried northw ards to the A ntarctic convergence an d descend again to 250 m in the autum n.

THE BIOLOGY OF THE DEEP OCEAN

Diel vertical migration It has long been know n th a t anim als that are n o t at the surface during the day can often be found there at night. T his is the result o f diel vertical m igration (DVM), w hich occurs in all planktonic an d pelagic groups o f anim als, although its expres­ sion has alm ost as m any form s as there arc m igrating species. A second d em o n ­ stration o f D V M cam e w ith the w'artime advent o f acoustics to m ap the occan floor (and to search for subm arines). O n e or m ore deep scattering layers (DSLs) w ere detected in m idw atcr, and, m ore rem arkably still, they rose to the surface at dusk (at rates o f up to 300 m h ') and descended again aro u n d daw'n (Fig. 1.6). We now’ recognize th a t these D SLs consist o f populations o f fish, shrim p, o r even siphonophores undertaking D V M , although it has never been easy to say precisely w hich species is responsible for a p articular scattering layer. R ecognizing th at it happens is one thing; showing w hat behaviour p attern s an d controlling factors are involved an d achieving accurate m easurem ents o f the rate an d range o f D V M in different species is quite another. H aving achieved at least some o f this in fo rm a­ tion the phen o m en o n still has to be explained.

Sampling strategies Sam pling, as usual, provides the first hurdle. I f a population o f m arine anim als is thought to be present at the same, unchanging, dep th by day an d by night th en a series o f net tows can be used to slice up the w'ater colum n into a series o f co n ­ tiguous horizontal layers o f defined depth. T his will define the vertical extent of the population. However, if the population changes its dep th on a diel basis the problem becom cs m uch m ore com plicated. It will ap p e ar in different dep th bands at different times. T h e absence o f a spccies from one sam ple at a p articu lar d epth does n o t m ean it is never there; its presence does n ot m ean it is always there. Two strategies have been em ployed to try to resolve these difficulties. T h e first assumes th at there is a defined day dep th range an d a (different) defined night d ep th range, w ith a short period o f m igration betw een them . T his p attern can be adequately described bv slicing up the w ater colum n in the sam e way, b ut doing it twice —once by day an d once by night— an d n ot sam pling at all during the p re ­ sum ed tim e o f m igration (this is often arbitrarily attem p ted by having a protocol o f not sam pling for one h o u r either side o f daw n an d dusk). T his is the way m ost DVM s have been, an d still arc, determ ined. Its advantage is th at it gives infor­ m ation on the population distribution by day an d by night; its disadvantage is that it gives no inform ation on tim ing (because this has been assum ed in the sam pling protocol to be com pleted d uring daw n an d dusk). T h e second appro ach is to fish a series o f nets at one o r m ore fixed depths, as continuously as possible. T hese nets will intercept the m igration an d give inform ation on its timing, b u t they do n ot define the full dep th range o f either the population or the D VM . Both sam ­ pling techniques are lim ited by the fact th at n et hauls take tim e; m ultiple net systems (C hapter 1) reduce this problem , b ut resolution in b oth tim e an d space

PATTERNS AND CHANGES

91

rem ains necessarily lim ited. Figure 4.8 shows a typical result o f the two strategies on a single species, the m esopelagic shrim p Systellaspis debilis. T h e results o f these two sam pling strategies can be sum m arized by saying that m ost species o f epi- an d m esopelagic plankton an d nekton show a D V M in trop­ ical and tem perate latitudes b u t th a t it is reduced or absent in p o lar regions. Bathypelagic species only rarely have a D V M . T h ere are differences in the scale an d tim ing o f D V M s betw een seasons, betw een species (Fig. 4.9), betw een differ­ en t populations, a n d betw een the sexes an d stages o f the sam e specics, while some specics reverse the usual direction o f m igration. In the last case the spccics o r p o p ­ ulations m igrate dow nw ards at night an d upw'ards by day, b ut the n o rm al basic p a tte rn involves an upw ard m ovem ent at dusk, some dispersion aro u n d m idnight (‘m idnight sinking’), an d a descent aro u n d daw n. Fast-m oving nekton species tend to m igrate as rath e r discrete populations, while the slower zooplankton p o p u la­ tions tend to ‘sm ear’ m ore (i.e. there is considerable variation in the rate o f m ig ra­ tion, w ith m any individuals lagging behind the leaders). T h e vertical distances travelled are generally o f the order o f 1O' to 5 X 104 body lengths, th a t is from 50 to 250 m for a large copepod an d aro u n d 500 to 700 m for a small lanternfish (myctophid) or large dccapod shrim p. All these generalizations con cern p o p u la­ tions an d averages; it has n o t yet been possible to m o n ito r the diel m ovem ents o f an individual copepod, m yctophid, o r shrim p, although this w ould be the basis of the ideal d ata set. At the m o m en t we can n o t even be sure th a t a p articu lar indi­ vidual m igrates upw ards every night. T h e scalc o f this pheno m en o n is rem arkable: in the Pacific some 43% o f the indi­ viduals an d 47% o f the biom ass m igrate from below 400 m bv day to above it at night (M aynard etal. 1975). Some, adm ittedly speculative, calculations (Longhurst 1976) suggest th a t there m ay be a vertical translocation o f 25 tons km-2 day 1from 250 m to the surface, alm ost 10<Jtons day 1over the w hole w orld oceans. T his stag­ gering (and rhythm ic) biological flux has extensive consequences for the rate of tran sp o rt o f carbon from the surface to the seafloor.

Causes and consequences W hy do they do it? A nd w hat controls the p attern o f the m igrations? T h e inverted pyram id o f biom ass provides a clue to the answ er to the first question an d the link w ith dusk an d daw n a clue to the second. U pw ard m igration takes an anim al into an environm ent w ith a higher biomass, th at is w ith m ore concentrated food supplies (Fig. 4.7). T his is the m ain benefit o f DV M . If herbivorous copepods, for exam ple, m igrate upw ards to feed on the surface phytoplankton their populations will be com pressed in the u p p er layers an d their p redators will benefit if they follow th em up. T h e result is th at the biom ass m axim um n ear the surface becom es even g reater at night. B ut why go to the effort o f m igration? W hy n o t stay in the upper layers all the time? T h e answ er seems to be the need to escape from visual predators. T h e surface w aters are


100 m

Depth (m)

250 m

дЫ

450 m

Д.1..1П0.

T im e (h)

aXk 600 m

.n n n 9

N os o f anim als

Fig. 4.8

13

17

Д.Д.Ц.11 g.Q .ru..n. • 21

1

5

9

13

17

21

1

5

9

T im e (h)

The pattern of diel vertical migration of the shrimp Systellaspis debilis (a) sampled off the Canary Islands with net tows at different depths and (b) sampled further north (44°N 13°W) using repeated tows at four depths (shaded area is night­ time). The first method simply describes the depth distribution. The second also gives information on the timing of the migration and rate of ascent and descent, resulting in the average population profile shown in (c). (Reprinted from Foxton 1970, with permission from Cambridge University Press, and from Roe 1984a, with permission from Elsevier Science.)

PATTERNS AND CHANGES

93

Fig. 4.9

At 28°N 14°W the different species of the copepod genus Pleuromamma are vertically segregated by day (stippled) but their diel migrations result in greater overlap at night (black). A question mark indicates probable occurrence but no sample taken; the total numbers of each species taken by day and by night are given below the plots. (From Roe 1972, with permission from Cam bridge University Press.)

о 200

5

400

«Г G w)0 800

1000 P. xiphias

2289

4440

P. a b d o tn im iis

P. robuslu

6032 14%

P. borealis

368

P. p iseki

344 132 H 496

P. gracilis

3416 17(4 3000 3248

well-lit by day an d visual hunters arc on the look-out for p rey b u t by night they are less effective an d the risks o f being eaten are m uch lower. T hose anim als that do stay n ear the surfacc by day have elaborate cam ouflage to reduce the risks o f detection (see C h a p te r 9). T h e bo tto m line is w h eth er the energy cost o f m ig ra­ tion is offset by the com bination o f increased food availability an d decreased predation pressure. T h e calculation is further com plicated by the fact th at in general a daytim e dcscent takes an anim al into colder water. T his will reduce the m ctabolic rate, an d slow dow n developm ent, but it m ay increase the p ro p o rtio n o f food energy converted into grow th because respiratory dem ands will be decreased. Indeed this was once considered the m ain cncrgctic benefit o f D VM , with the corollary that D V M should be o f m ost benefit in a stable w'ater colum n w ith high tem perature gradients. T h e energetic costs o f m igration seems to be lowr, if the value o f 0.3% o f basal m etabolic rate th a t has been calculated for a copepod is m ore generally applicable. C alculations o f the dem ographic value o f D V M to p articu lar species o f copepod have tried to take all these factors into consideration. In a study o f Calanus pacificus (Frost 1988) adult females show ed seasonal an d in teran n u al variability in their D V M , w hich was u nrelated to food availability, grow th rate, o r th erm al stratifica­ tion. T h e study concluded th a t there was no evidence for the postulated m ctabolic benefits an d th a t the p atterns w’crc consistent w ith the dem ographic benefits of p red a to r avoidance (Bollens an d Frost 1989). W ork on the copepod Emytemora (Vuorinen 1987) sim ilarly concluded th a t D V M (to deeper, colder water) was advantageous w'hen daily m ortality n ea r the surface exceeded 7.5% . A third study (Bollens an d Frost 1991) looked at Euchaeta an d found th at females carrying eggs h ad a w eaker D V M th a n those w ithout eggs. T h e Pacific h errin g preferentially preyed on the m ore visible egg-bearing females an d it was beneficial for these females to stay at dep th if th a t achieved a reduction in m ortality o f 26% . T his was enough to offset the costs o f slow-cr egg developm ent.

THE BIOLOGY OF THE DEEP OCEAN

O h m a n (1990) looked at different populations o f Pseudocalanus th a t h ad very vari­ able p atterns o f D V M . A n orm al D V M occurred at shallow sites w here inverte­ b rate non-visual p redators w ere low an d fish visual predators dom inated. No D V M occurred w hen p red a to r populations w ere very low. A reverse m igration took place at deep sites w here invertebrate p redators (larger copepods, chaetognaths, etc.) w ere particularly abundant. T h e latter arc largely non-visual p red a­ tors; daylight has little effect on their success rate an d th eir D V M s left Pseudocalanus particularly vulnerable at night, resulting in the developm ent o f a reverse m igration. T h e p atterns o f m igration h ad no correlation w ith food distri­ butions or tem perature structure, and reduction in m ortality o f 12% p e r day was sufficient to gain a benefit from D V M . T h e Pseudocalanus populations arc very flexible in their D V M responses to p articu lar selection pressures. T h e first clear picture o f the response o f D V M pattern s to different p red ato r pressures cam e from studies o f freshw ater copepods in lakes w ith know n histories o f fish stocking. T h e range o f D V M was p ro portional to the historic tim e over w hich the copepods h ad been exposed to fish predators. M ore recent studies have tried to establish experim entally w hich particu lar cues the prey populations are responding to in their change in D V M behaviour (as in Pseudocalanus, above). T h e m arine copepod Acartia hudsonica responds in mesocosm s to active free-sw im m ing stickleback p redators by initiating D V M b ut does n o t do so if the sticklebacks are caged. It also responds to stickleback mimics during the day b ut n ot at night. T h e response seems to be visually or m echanically initiated, an d n o t to some chem ical exudate from the predator. O n the oth er han d , work w ith freshw ater zooplankton indicates that chem ical cucs from predators will initiate DV M . D ifferent species respond to different cues. It is not yet clear w'hether the behavioural changes are phenotypic or genotypic in origin. Individuals do change their D V M behaviour, suggesting a phenotypic plasticity, but there is also evidence for genetically based differences in the D V M o f Daphnia clones w ithin a single population. A nother freshw ater study (Neill 1992) found that copepods have b o th dcvelopm entallyfixed an d p redator-induced m igrations at different stages o f their life history. H e concluded th a t at each stage an d size the genes coding for differences in the p h e­ notypic expression o f D V M were selected by local pred atio n pressure. G iven the identified variety' o f D V M in the open occan, no single explanation seems likely to satisfy all cases! T h e control o f the tim ing o f D V M is a different problem . Light seems to be the do m in an t factor. T h e vertical distribution o f anim als in the w'ater is very sensitive to changes in overhead light. A recent study' in N orw ay show ed th a t the optical properties o f the w ater greatly affect anim al vertical distributions. Fish an d euphausiids w ere ab o u t 100 m shallower in a region o f high phytoplankton (and therefore m ore opaque water) one side o f a front th an in the clcarcr w ater on the other side (K aartvedt et al. 1996). Scattering lay'crs move upw ards in response to clouds covering the sun, an d to eclipses, an d dow nw ards to artificial lights. A nu m b er o f observations have dem onstrated th a t the m ovem ents o f these layers are closely correlated w ith the daw n an d dusk changes in the light levels. T his led

PATTERNS AN D CHANGES

95

to the concept that anim als rem ain at a preferred light intensity an d follow this level (or isolume) up an d dow n at daw n an d dusk. T his is feasible for a few active species but the observed m igration rates o f m ost planktonic anim als are too slow to keep up w ith an (instrum ent-m easured) isolume at these times o f rap id change (120 m h '), although some copepods can ap p ro ach this rate (Roe 1984£). In ad d i­ tion, a species’ population m ay be spread over a vertical range encom passing up to three orders o f m agnitude difference in light intensity. M igrators m ay respond instead to the rate o f change o f light intensity, beginning their D V M w hen this reaches a particu lar level. A n internal rhythm , perh ap s continually reset by changes in light intensity, could also be involved b u t there is no experim ental evi­ dence yet. Alternatively, a rhythm m ight simply prevent an anim al responding inappropriately to transient stimuli such as fleeting clouds. In situ observations o f m igrating zooplankton, coupled w ith m easurem ents o f environm ental light levels at depth, show that the diel m igrations o f different species are staggered an d that daytim e dep th distributions do n o t necessarily d eterm ine the order o f m igration; th a t is different species m ay have different thresholds for the sam e cue for m igration (Frank an d W idder 1997). C orrelations o f D V M s w ith instrum ent-m easured isolumes are inevitably flawed because the instrum ent has a different spectral an d adaptive response to the eye o f the organism . M ore refined assessm ent on the basis o f the m igra­ to r’s visual sensitivities shows th a t the observed sw im m ing speeds o f some shrim p (6 -11 cm s ') are adequate to m aintain the anim als w ithin physiologi­ cally appropriate isolumes (W idder an d Frank 2001). If visual p red atio n is the driving force then sm aller species will be less conspicuous at any given light intensity an d should be able to move up earlier (and descend later) th an larger species. T h e re is som e recent evidence to support this prediction (De R obertis et al. 2000). T h e absence o f D V M in m ost species w hich live below 1000 m is correlated w ith the absence at these depths o f any detectable light cues from the surface, yet there rem ain a few ap p a ren t cases o f D V M from below 1000 m (e.g. the m yctophid Ceratoscofielus warmingi). Perhaps a rhythm reset by m o o n ­ light m ight be involved. T h e lu n ar cycle certainly affects the am plitude o f the m igrations o f species o f the m yctophid Hygophum (Linkowski 1996). A bsent or w eak D V M in high latitudes (where there is little th erm al stratification) has been argued as support for the m etabolic advantage hypothesis b u t is explained equally' well by the m ore constant light environm ent th ro u g h o u t m uch o f the year. T h e flexibility a n d subtleties o f different D V M s indicate th a t rigid adherence to light as the controlling factor is probably' a simplistic view. It is very likely th a t the D V M s o f individuals arc fine-tuned through such factors as hunger, satiation, an d contact w ith phytoplankton or zooplankton aggregations, an d are constrained by such physical boundaries as steep gradients o f tem perature, salinity o r oxygen. T h e consequences o f D V M are m ore com plex th a n simply the avoidance o f p redators a n d the search for food. A short vertical displacem ent will expose an organism to a m uch w ider range o f environm ental conditions th an a lengthy'

THE BIOLOGY OF THE DEEP OCEAN

horizontal displacem ent. T h e differential cu rren t shear at different depths also results in a vertical m igrant being transp o rted horizontally for considerable dis­ tances an d never retu rn in g to the sam e packet o f water. Populations spread ver­ tically will be dispersed m ore rapidly th an those tightly bunched. T his dispersion has potential reproductive benefits in the encounter o f m ates, an d genetic b en e­ fits in a m ore extensive gene flow w ithin the population. I f D V M s are o f greater am plitude in areas o f low' food (because the w ater is clearer), an d this certainly seems to apply to DSLs, lateral tran sp o rt will be greater and anim als will th e re­ fore ten d to accum ulatc u n d er the m ore productive areas w here their D V M s arc reduced. I f anim als undertaking D V M feed at the surface (as m any dem onstrably do; M errett an d R oe 1974), an d then carry the food in their guts dow n to clay depths w'here they void their faecal pellets, they will greatly increase the export flux of carbon from the surfacc to the seafloor. T his is because their sw im m ing rate, an d the sinking rate o f their faecal pellets, will be generally faster th an the descent rate o f the surface particles and will reduce the bacterial an d o th er rew orking o f the m aterial en route. T h e flux o f organic m aterial, b oth dow nw ards an d upw ards, is affected by the range o f ontogenetic, seasonal, an d diel m igrations w hich m ay overlap spatially to such an extent th a t they provide a ladder o f m igrations linking the organism s on the seafloor w ith those at the surface.

Conclusion O rganism s have a non -ran d o m distribution at all scales o f space an d time. T h e sm aller the organism the m ore its distribution is d eterm in ed by the physical m otions o f the w ater w ithin w'hich it lives, b u t no organism is so large th a t its dis­ tribution is wholly unaffected by advectivc forces. T h e scales o f advcction range from m ajor currents and their spun-off rings, th ro u g h mesoscale eddies, dow n to local turbulence an d diffusive processes. H orizontal distributions can be in ter­ preted in the context o f these factors, an d o f geological changcs in the ocean basins, to explain the observed patterns. T hese p attern s range in scale from biogeography to patchiness, and their accurate delineation is often lim ited by the available sam pling m ethods. P atterns an d changes in vertical distributions are m ore often biologically d eter­ m ined th a n are horizontal ones, but at the finer scale all are at the m ercy of oceanographic m ixing processes. T hese processes range from w ind m ixing at the surfacc, through internal waves at density interfaces, dow n to benthic storm s and tidal oscillations on the seafloor. O ntogenetic, seasonal, an d d iu rn al vertical m igrations have m ajor consequences for the biological fluxes betw een the surface and the sediments, as well as for the horizontal distributions o f the organism s involved. T h e three-dim ensional p atterns in the distributions o f different oceanic anim als are not rigidly fixed but are very dynam ic; they are closely interlinked by the feeding requirem ents o f the different species involved.

PATTERNS AN D CHANGES

97

A t present o u r know ledge o f biological m ovem ents is m ainly at the level of integrated populations. A lthough som e o f the larger vertebrates can now be m onitored individually, we still have little inkling o f the reasons why m ost deep-sea anim als are w here they are, o r w h at triggers individuals to change their distributions.

5

On being efficient

Energy management In open w ater food is often reliably available in p articu lar regions or seasons (e.g. in m any coastal regions a n d /o r springtim e). In these circum stances anim als are neither constrained to get the last calorie o u t o f their diet n o r is energy conser­ vation a high priority. O n e frequent result is fast-swimming, solidly m uscular anim als w ith skeletons to m atch. A nother is ‘messy’ feeding, in w hich carnivores scatter scraps o f prey and herbivores eat m ore th an they can process, allowing a considerable portion o f the ingested phytoplankton to pass through the gut u n a b ­ sorbed. In contrast, the food levels (‘biom ass’ o r organic carbon) in the deeper layers o f the ocean are greatly reduced (C hapter 4) an d the energetic constraints on the meso- an d bathypelagic anim als th a t inhabit this world are very m uch m ore severe. T h e key to survival is energy m anagem ent. T his is a threefold task. T h e first o f these is to m axim ize the energy input, th at is finding a n d eating w'hatever food there m ay be; the second is to be as efficient as possible in its subsequent digestion, absorption, an d m etabolic conversion; an d the th ird is to lim it the expenditure o f that h ard -ea rn e d energy to the essential m inim um .

Maximizing energy input— how to eat a lot In the epipelagic near-surface layers there are m any large fast carnivores (e.g. sharks, tuna, squid, whales, an d dolphin) as well as an im m ense variety o f planktonic filter feeders, all ultim ately dep en d en t u p o n the p rim ary p ro duction in the w ell-illum inated (euphotic) zone. Filter feeders thrive because there are so m any very small organism s, from b actcria to large diatom s an d from microflagellates to larval crustaceans. Even fishes can becom e successful filter feeders in these cir­ cum stances. A lthough the vast m ajority o f m arine fishes are carnivores, in n ear­ surface regions o f high productivity (such as upwelling areas) the concentrations o f larger phytoplankton are sufficient to su p p o rt huge populations o f filterfeeding sardines and anchovies. T hese small fishes use th eir gill filam ents to strain out the large diatom s th a t dom inate the phytoplankton populations o f such areas. T h ey provide the basis for huge com m ercial fisheries as well as a food resource for large num bers o f local carnivores, particularly seabirds. A t a m uch larger scale,

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the baleen whales an d w hale sharks are also efficient filter feeders in the p ro d u c­ tive coastal o r polar w aters, although their filtered ‘particles’ com prise small anim als such as copepods an d the som ew hat larger euphausiid shrim ps (krill), rath e r th an phytoplankton. Filtering seaw ater for its particulate nutritional co ntent can be an energetically dem anding m eth o d o f feeding, particularly w hen the cu rren t o f w ater to be fil­ tered has to be generated by the organism itself, as is the case for all planktonic anim als an d for activc suspension feeders in the benthos. Particulate organic carbon levels o f at least 25 jig С 1 1 are required to provide a filter-feeding plank­ tonic organism w ith a net energy gain. T his value is easily exceeded in m ost coastal w aters b u t in the deep sea the levels o f organic carb o n range from next to n othing to aro u n d 70 (j.g С 1 *. Even though ‘m ean ’ levels m ay m ask m uch higher local concentrations at density interfaces, it is still the case th a t m any deep-sea anim als are exposed to conditions in w hich a n o rm al filter feeder w ould starve. T h ere are, therefore, fewer successful filter feeders in deep w ater an d some o f those that are there have larger filtering systems to cope w ith the paucity o f p a r­ ticles (e.g. the giant appcndicularian Ba.thochord.eus). A n o th er solution for such anim als is to forage in particu lar layers o f w ater w here the particles m ay be m ore concentrated, for exam ple at density interfaces (C hapter 1). M any o f the groups o f bcnthic anim als th at typify the filter-feeding lifestyle in shallow w ater have deep-sea representatives th a t have becom e predatory. T h ere are, for exam ple, p redatory deep-sea bivalve molluscs, tunicates, an d sponges. T h e ir filtering systems, w hich reach such a high degree o f developm ent in shallow -w ater species, are greatly reduced. A lternative m ethods o f active o r passive prey capture have been evolved, including trap p in g an d seizing prey (tunicates), entangling prey (sponges), an d sticky tentacles (bivalves). In essence, these anim als have greatly increased the particle size to w hich they are adap ted an d have thereby m oved from m icrophagous suspension feeding to m acrophagy (Gage an d Tyler 1991). In the deep er w aters o f the oceans there is a m uch g reater tendency for anim als to aw ait the arrival o f food particles or prey rath e r th a n to search th em out actively (thus m inim izing energy expenditure— see below). T his has resulted in a m ore stealthy style o f feeding, w ith the consequent em phasis on lures a n d /o r the evolution o f elongated appendages th a t increase the active volum e o f w ater co n ­ trolled or m onitored by the anim al (C hapters 6 an d 10). A consequence o f the lim ited availability o f fo o d /p re y is th a t m any anim als have developed ways of coping w ith m uch larger food particles, relative to their own body size, th a n the equivalent shallow er species. A m ong the fishes there is a tendency for the teeth an d jaw s (i.e. the prey capture apparatus) to becom e appreciably enlarged, result­ ing in m any o f them being given com m on nam es w hich refer to these features (e.g. ‘fang to o th ’ Anoplogaster; ‘dragonfish’ stomiids; ‘loose ja w s’ malacosteids). N ot only are the teeth hugely enlarged a n d /o r the jaw s elongated b u t the gape m ay also be greatly increased by m aking the ja w articulations so flexible so th a t they can effectively be dislocated. Very large or long teeth provide alm ost no scope for cutting the prey into pieces o f convenient size for swallowing; the fish m ust gulp

THE BIOLOGY OF THE DEEP OCEAN

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the prey dow n whole, the teeth m ay fold backw ards an d in m any eases swallow­ ing is assisted by the presence o f pharyng eal teeth w hich grasp a n d m assage the prey dow n the throat. T h e m ethod is very m uch akin to th a t em ployed by m any snakes (and perh ap s used by som e dinosaurs), w hich rely on a sim ilar ability to dislocate the jaws. T his parallel is recognized in the use o f the nam e ‘viperfish’ for Chaidiodus (Fig. 5.1). In situations w here food m ay be very scarce, an d little effort is expended in actively hunting for it, it seems an appro p riate strategy to m axim ize the size o f food that can be taken. It could be fatal to have to miss a m eal because it is too large. H aving swallowed the prey the p red a to r still has to accom m odate it. In order to be able to ingest very large meals m any fishes have evolved extraordi­ narily extensible stom achs, so m uch so th a t some (e.g. anglerfishes an d chiasm odontids) are quite capable o f containing prey larger th a n themselves. A gain the parallel w ith some snakes is very close (Fig. 5.2). Fish are n o t alone in this ability; m any comb-jellies are equally able to engulf prey (usually other jellies) larger than themselves. It has been widely suggested that deep-sea anim als can n o t afford to be too selective in their diet, w ith the result th at they should take a wide variety o f sizes an d types o f prey an d that this trait should be m ore ap p a ren t in the bathypelagic species than the m esopelagic ones, reflecting the relative availability

Fig. 5.1

The head flexes and the jaws of the viperfish Chauliodus open widely during the capture and swallowing of large prey, which may have been attracted by a luminous lure on the elongated dorsal fin ray. (From Tchernavin 1953.)

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5.2

The very elastic stomach o f a 90 mm Chiasmodon can accommodate prey larger than itself.

o f food in these two realms. Som e evidence to support this idea com es from an analysis o f the m outh size relative to body size in the lanternfishes (M yctophidae) an d the bigscales (M elam phaeidae) (Ebeling an d C ailliet 1974). T h e deepest-living species o f bo th families are equipped to eat the broadest array o f food sizes. Besides having large jaw s they also have w ell-developed pharyngeal baskets w hich allow them to take sm aller prey as well. T h e m uch larger jaw s in deeper species are related partly to the fact th a t the body size of d eeper species tends to be greater an d jaw length scales w ith body length. T h e d eeper m elam phaeids also have a disproportionate enlargem ent o f the m outh. A nother exam ple is the deep-living gonostom atid fish Gonostoma bathyphilum, w hich has longer an d m ore loosely attached jaw s th an its shallower relative G. atlanticum. T heoretical analyses tend to support these conclusions. It has been argued th at w here food is scarce, anim als need to spend m ore tim e foraging (i.e. searching for food), an d th a t the longer the tim e required for foraging the larger the prey th at should be taken. T h e energy cost o f the increased foraging tim e m ay be offset by p utting less energy into grow th, resulting in an overall decrease in the body size (C hapter 10). Som e recom pense can be gained by increasing the relative size of the m outh. A larger m outh should enable a w ider range o f food to be han d led with a m inim al add ed energy expense. Female anglerfishes provide classic exam ples o f this lurk-and-lure m ode o f life. T h e globular shape o f m ost species shows im m ediately th at they are n ot ad ap ted for sustained rap id swimming, their teeth an d gape are huge co m p ared to the body size, an d they can cope w ith very large prey through the possession o f an elastic stom ach. Instead o f searching for prey, a lum inous lure attracts it to them . Analysis o f the stom ach contents o f anglerfishes suggests th at they take b o th large an d small prey as available.

THE BIOLOGY OF THE DEEP OCEAN

T h e concept of' deep-w ater fishes being generalists in th eir diet an d taking any­ thing they can has support from work on the hatchetfish Slemoptyx w hich con­ cluded th a t ‘prey selection appears regulated . . . by the nearest available prey th at this species can perceive, capture an d swallow’ (Hopkins an d B aird 1973). T h e sam e is p robably true for m ost lanternfish, although some species m ay focus on particu lar prey types (Sutton et al. 1998). O n the o th er h an d , a n u m b er o f m idwrater dragonfishes ap p e ar to be rem arkably specific in their diets, different species preferentially taking copepods, squid, decap o d shrim p, or o th er fishes (Sutton and H opkins 1996). C learly there is no h a rd an d fast rule applicable th ro u g h o u t the m idw ater fauna. Invertebrates are m ore constrained in the size o f food particles they can ingest because they have not developed m outhp arts capable o f dealing w ith very large lumps. Even large shrim p are obliged to take their food in small pieces an d only the cephalopods are capable o f taking quite large chunks o f food at a time. T h ere is little inform ation on the am ount o f food th a t can be taken at one tim e by inver­ tebrates b u t there are som e crustaceans th at are know n to be able to distend themselves m ightily w hen opportunity arises an d thus take m eals th at are a sub­ stantial p roportion o f their total weight. T his is the case, for exam ple, in J\rebaliopsis, some ostracods, the m isophrioid copcpods, an d in the scavenging am phipods Pamlicella an d Eurythenes. T h e m eals taken by adults o f these am phipods can excccd 70% o f their body w eight and they, like the copepods, are able to expand their volum es rapidly by m eans o f clastic intersegm ental regions (H argrave et al. 1994). E ach grow th increm ent (instar) in the juveniles probably represents one m eal. A nu m b er o f terrestrial arth ro p o d parasites (e.g. ticks an d rcduviid bugs) use the sam e solution to overcome the potential lim itations o f a rigid exoskeleton while engorging a single large meal. A t the low tem peratures an d m etabolic rates characteristic o f deep-sea anim als a large m eal m ay suffice for m ore th an a year.

Maximizing assimilation efficiency Ingesting the m eal is only the first step in energy efficiency; the organic m aterial m ust then be absorbed before it can becom e available. E stim ating the assim ilation efficiency o f oceanic anim als is not easy b u t some progress can be m ade by m eas­ uring the relative am ounts o f food and o f faeces a n d d eterm in in g their relative biochem ical (and hence calorific) values. M easurem ents o f this sort on m idw ater fishes have show n th at am bush predators, wrhich are interm itten t feeders, have rel­ atively high efficiencies (about 40%) com pared w ith values o f 30% in regular feeders (e.g. m igratory lanternfish (mvctophids)). Assim ilation efficiencies are gen­ erally higher in species w ith longer intestines th a n in those w ith shorter ones, and this m ay also reflect the type o f food (Robison an d Bailey 1982). Fish feeding m ainly on gelatinous zooplankton (some m elam phaeids) have considerably longer intestines to assimilate the very lim ited am o u n t o f n u trien t m aterial from am ong the w atery m atrix.

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C om parisons o f the gut lengths o f fishes from different depths lead to the co n ­ clusion that deeper species have g reater assim ilation efficiencies, reflecting their m ore lim ited opportunity for feeding. T h e sam e relationship is found in ecologi­ cally equivalent species from low productivity areas such as the n o rth Pacific gyre an d the m uch m ore productive coastal zones: the form er have the higher assimi­ lation efficiencies. D espite the increased effort at assimilation, fishes from these oligotrophic w aters also contain less fat and m ore w ater th a n th eir relatives in m ore eutrophic w'aters; they seem chronically undernourished.

Minimizing energy output— how to keep up in the water A ju m b o je t has to m aintain sufficient forw ard speed to generate the aerodynam ic lift th a t keeps the plane up in the air. It cannot hover or fly backw ards. A planktonic or pelagic organism has ju st the sam e problem . I f it stops sw im m ing (or dies) it will sink into the abyss, ju st as certainly as the aircraft will fall if the engines fail. T h e sinking velocity (I7) o f a spherical particle in lam in ar flow is defined by Stokes’ law, from w hich is derived the relationship: f/oc { Pi -

w here p x an d /?2 are the densities o f the: particle an d o f the fluid, respectively r is the radius o f the particle, an d (I is the dynam ic viscosity o f the fluid. T h e aircraft will fall very fast because the density difference betw een it an d the air is very great an d the dynam ic viscosity o f air is very low'. T h e m arine organism sinks m ore slowly because the density difference betw een it an d the w ater is m uch sm aller an d the dynam ic viscosity o f w ater is higher. But it will still sink, an d p re ­ cious energy will have to be expended in the sw im m ing th a t is necessary to m ain ­ tain position against the force o f gravity. Large anim als will sink m uch m ore rapidly th an small ones (the r'2 te rm in the relationship above) even though the generation o f turbulence by the larger size m ay reduce the sinking rate som ew hat below the theoretical m axim um . I f energy in the form o f available food is plentiful, an d n o t difficult to acquire, then sw im m ing m ay be the best solution, an d num erous anim als, from pteropods to fish, spend m uch o f their tim e a n d effort in sw im m ing to stay up, i.e. g en erat­ ing hydrodynam ic lift. A fast sw im m er such as a m ackerel o r tu n a generates dynam ic lift by the continuous flow o f w ater over its p ectoral fins (Alexander 1990). Like the ju m b o jet, it can n o t stop o r go backw ards w ithout sinking. T h e fins do not need to be proportionally as large as the wings o f a plane, o r o f a bird, because the density difference betw een the fish an d the w'ater is relatively small. O nly if the fish chooses to take to the air do the lift-generating fins have to becom e very large— as has h ap p en ed w ith flying fish. T h e hydrodynam ic m ethod o f obtaining lift has two costs, an indirect one in the form o f d rag from the fins, w hich increases the energy requirem ent for a given forw ard speed, an d a direct

THE BIOLOG Y OF THE DEEP OCEAN

one in the need to m aintain a continuous forw ard m otion to generate enough lift to prevent sinking. Ju st as in the case o f the ju m b o jet, the speed through the w ater m ust excced a critical value before hydrodynam ic lift becom es an efficient m eans o f staying up in the w ater colum n. T h e critical speed is achieved by a n u m b e r o f very fast scom broid fishes, for exam ple, w hich have dispensed w ith the swimbladder an d have densities o f ab o u t 1080-1090 kg m 3 (Alexander 1990). Large, fast-sw im m ing pred ato ry fishes m aintain a very high m etabolic rate in « 'a rm surfacc w aters b u t few have expanded their ranges into colder tem perate or d eeper waters, w here m etabolic h eat loss w ould reduce their body tem peratures to those o f the environm ent, an d reduce th eir activities equivalently. T h e few that have expanded their niches (some sharks, tunas, billfishes, an d mackerels) have done so by developing m uscular an d vascular specializations th at m ain tain all or p a rt o f the body significantly above the am bient w ater tem perature. T unas an d sharks retain the internal heat th a t is generated as a by-product o f oxidative m etabolism by having a body w ith a low th erm al conductance an d cou n tercu r­ rent heat-retentive vascular plum bing. Billfishes an d the butterfly m ackerel heat only the brain an d eyes. T h ey pass the blood th ro u g h a special ‘furnace m ad e o f m uscle’, an eye muscle w hich produces heat, n o t force, an d is different in the two types o f fish (Block el al. 1993). T h e heat is retain ed in the b rain by co u n tercu r­ ren t vascular systems, an d this tem peratu re en h an cem en t o f the neurosensorv system allows the fishes to forage effectively in colder waters, including occasional vertical excursions o f a few h u n d red metres. O nly a few m am m als (e.g. sperm whales) whose internal tem peratures are m ain ­ tained by an insulating layer o f very thick blubber, m ake really deep foraging excursions (of 1 km or more). E ctotherm ic anim als th a t live p erm an en tly in the very cold w ater o f the deep-sea environm ent (and p o lar waters) can n o t (as far as we know) take advantage o f adaptations like those in the tu n a an d billfish, an d consequently arc restricted to m ctabolic life at low tem peratures. Even if a very large deep-sea fish (with a suitably low surfacc-to-volum c ratio and ad equate insu­ lation) w ere to attem pt this lifestyle it w ould alm ost ccrtainly be unable to find a sufficient am ount o f food to fuel the furnacc. B ut if it did succeed we w ould p ro b ­ ably never be able to capture it anyw ay . . . T h e sm aller the density difference betw een the organism a n d the seawater, the less will be the cost o f staying up in the w ater colum n. W h en the organism ’s density equals that o f the seaw ater surrounding it, the organism is said to be n eu ­ trally buoyant and the perils o f sinking are elim inated. Seaw ater w ith a salinity o f 35%o (parts p er thousand) and a tem p eratu re o f 20°C has a density o f 1026 kg m ;i. M any essential biological m aterials, for exam ple bone (2040 kg m ;i), chitin, muscle (1050-1060 kg m 3), an d protein (1030 kg m :i), have a g reater density an d will cause an anim al to sink. A few m aterials are less dense (e.g. water, fats and oils, gases) an d will provide static lift. By adjusting the proportions o f different m aterials in its body an organism can reduce the density difference, and in som e cases elim inate it altogether (Fig. 5.3; D en to n an d M arshall 1958; D en to n 1963; Schm idt-N ielsen 1997). T his will either allow m ore

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Fig. 5.3

A buoyancy budget for the mesopelagic fish Gonostoma elongatum and a shallow water wrasse, Ctenolabrus rupestris. The wrasse has a gas-filled swimbladder whose lift (-5.4 g) offsets the negative buoyancy of the skeleton (Sk), cartilage (C), and protein (muscle). Fat and dilute body fluids provide only small contributions to buoyancy. G. elongatum has no swimbladder and achieves near-neutral buoyancy by a great reduction in skeleton and muscle and a much greater reliance on fat and dilute body fluids. (From Denton and Marshall 1958, with permission from Cambridge University Press.)

Gonostoma elongatum

o f its acquired energy to be channelled into grow th an d reproduction, or will reduce the level o f intake required for survival an d hence allow a change in lifestyle a n d /o r colonization o f low food environm ents. Every biological response is a com prom ise am ong conflicting options. T h e degree to w hich different pelagic species have com prom ised in reducing dense tissues an d increasing less dense ones covers the com plete gam ut o f options. R arely is a single option em ployed; usually a suite o f related adaptations is to be found.

Changes in water and ionic content O n e o f the sim plest m eans o f reducing the density o f tissues is to increase their w ater content. D istilled w ater has a density o f 1000 kg m \ w hereas the density' o f seaw ater is ab o u t 1026 kg m 3. A n organism with a m ean density o f 1060 kg m ;i (whose tissue fluids are assum ed to be o f the sam e osm otic strength as sea­ water) w ould need to m ore th a n double its volum e (increasing it by 10 6 0 /1 0 2 6 X 100%, i.e. 103%) to achieve neutral buoy'ancy by' increasing its w ater content. N ote th at the calculation assumes it. is adding salt-free w ater w ith a density7 o f

THE BIOLOG Y OF THE DEEP OCEAN

1000 kg m :i, and gaining 26 m g o f lift from each g ram added, to set against its original w eight in water. As the tissues becom e m ore dilute the salt-free w ater w ould have to be p u m p e d in against an increasing osm otic gradient. O nce neutral buoyancy has finally been achieved, the organism w ould be faced w ith a co n tin ­ uous energy cost in m aintaining the new (and now greatly reduced) osm otic p res­ sure against the higher value o f the surrounding seawater. T h e addition, instead, o f 103% o f isosmotic seaw ater w ould n o t provide any actual lift b u t w ould reduce the overall density to (1060 X 100 + 1026 X 103) /2 0 3 , i.e. 1043 kg m 3. T h e sinking rate w ould therefore be reduced by the reduction in density difference. O n the other h an d , because the ratio o f frictional (drag) surface area to volum e decreases as the anim al gets larger, the increased size will slightly increase the sinking rate. Very m any m arin e anim als have a very high w ater content; the so-called gelatinous zooplankton typify this style o f co n ­ struction. M edusae, siphonophores, ctenophores, larvaceans, salps, an d some polychaetes, pteropods, an d heteropods are all com ponents o f this fauna, whose ecological im portance in the oceanic econom y is becom ing increasingly recog­ nized. Jelly also covers m uch o f the body o f some n o n -m ig ran t deep-sea fishes an d m ay com prise m ore th an a third o f their body weight. In d eed in a large spec­ im en o f Chauliodus the jelly m ay reach 10 m m in thickness over the dorsal an d ventral midline. In Bathylagus the subcutaneous layer is 96% water, is low in ionic content, an d is positively buoyant (Yancey el al. 1989). U nlike sharks, teleost fishes have body fluids th a t are dilute relative to seaw ater (hyposmotic). T hese fluids will provide some lift b u t their contribution varies co n ­ siderably. In the deep er m idw ater fishes the w ater co n ten t o f the body increases m arkedly w ith increasing depth o f occurrence (Childress an d N ygaard 1973). Analyses o f groups o f 3 0 -4 0 species each from California, H aw aii, an d the G u lf o f M exico all yielded a sim ilar conclusion. O n e result o f the higher w ater content is th a t the anim als have a lowrer caloric co n ten t p er unit weight; they will provide less energy for a p red a to r than will a shallower living specics o f equivalent size (Fig. 5.4). O n e benefit o f the hyposm otic body fluids in pelagic fishes lies in the provision o f buoyancy for the eggs. M any species have eggs w ith an im perm eable outer m em ­ bran e and, w hen laid, they' rise to the productive surface w aters w here they' hatch an d the larvae develop. If an increase in w ater content is accom panied by' an adjustm ent o f the ionic com position o f the body fluids then it is possible for an organism to gain sub­ stantial buoyancy' benefits w ithout experiencing severe osmotic problem s. T his is achieved because some ions arc m ore dense th a n others. For exam ple, if all the o th e r ions in seaw ater w ere to be replaced in the tissues by sodium an d chloride the resulting isosmotic fluid w ould give a static relative lift o f ab o u t 3.5 m g m l'1. In practice, m ost gelatinous organism s have m odified th eir bodyfluid com positions, replacing dense ions with less dense ions while retaining the overall osm otic balancc. Ions w ith a high m olecular w eight (e.g. K +, C a 2+, M g2+, S 0 42 ) are replaced by ions w ith low er values (N a+, N H ++, СГ). A

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Fig. 5.4

The energy content o f a number of midwater fishes as a function of their habitat depth (plotted as minimum depth of occurrence). The decline with depth correlates with an increased water content. The higher calorific value of shallower species provides another benefit of night-time vertical migration to near-surface waters, where prey may be ener­ getically more rewarding. (Reprinted from Childress and Nygaard 1973, with permission from Elsevier Science.)

p articular feature o f the gelatinous species is th a t m any o f th em exclude the S O ,2 ion an d replace it w ith C l (Bidigare an d Biggs 1980). Sulphate is by far the m ost dense o f the m ajor ions in seawater, w ith a m olecular w eight o f 96.1, an d is the fourth m ost a b u n d a n t (after C l , N a +, an d M g2+) (Tabic 5.1). Its exclusion dow n to 40% o f the level in seaw ater can provide static lift o f ab o u t 1.5 m g m l'1 (Fig. 5.5). Sim ilar exclusion o f divalent ions probably also provides static lift for som e diatom an d dinoflagellate species. T h e am m onium ion is particularly light (mol. wt 18.0) an d is widely used as a replacem ent, for exam ple, for C a 21' an d M g2+, particularly by some squids. M any families o f squid store large quantities o f N H 4+ in th eir tissues, as N H 4C1. T h e cranchiid squids store it in large volum es o f coclom ic fluid an d the histioteuthid squids (and som e others) in special tissue spaces in the arm s (Table 5.1; Clarke et al. 1979). Because am m o n ia is a p ro d u ct o f protein m etabolism it is readily avail­ able to these anim als, provided they can store it in a non-toxic form . N H 4+ com ­ prises 80% o f the cations in the cranchiid coelomic fluid, giving som e 16 m g m l 1 static lift, that is 65% o f the 26 m g m l 1 th a t distilled w ater w ould provide. Squid arc n o t the only m arine anim als to use am m o n iu m as a buoyancy aid. Som e crustaceans do so as well, particularly species o f the deep-sea shrim p Notostomus (these anim als stand out in a traw l catch bccause they are am ong the very few crustaceans that float). T h ey have carapaces inflated w ith large volumes

THE BIOLOGY OF THE DEEP OCEAN

108

Table 5.1 Ion composition (mmol I-1) o f seawater, Notostom us gibbosus carapace fluid (from Sanders and Childress 1988), Histioteuthis arms (from Clarke et al. 1979) and Helicocranchia (from Denton et al. 1969) Ion

M ol.w t

Seawater

(g mol h1)

(mmol I-1) (g h1)

Na+ 23.0 NH4+ 18.0 K' 39.1 Me3NIT 60.0 M g2+ 24.3 Ca21 40.1 СГ 35.3 96.1 Totals

so42-

Fig. 5.5

470.20 0.00 9.96 0.00 53.57 10.23 548.30 28.25

10.800 0.000 0.389 0.000 1.302 0.410 19.465 2.715 35.081

Notostom us carapace fluid (mmol H) (g H)

Histioteuthis arms (mmol H) (g h1)

62.1 296.0 10.8 127.6 3.5 0.0 511.7 1.2

138 438 18

3.1 7.9 0.7

530

18.7

1.428 5.328 0.422 7.656 0.085 0.000 18.165 0.115 33.199

Helicocranchia (mmol I-’) (g f ) 85 470 3.5

642

1.96 8.46 0.14

22.7

Many gelatinous animals reduce their density by isosmotically replacing much of the sul­ phate in their tissues with chloride ions. The figure shows how the degree of sulphate exclusion differs in different species of cnidarians (Aequorea, Pelagia, Beroe, Cestus), molluscs (Pterotrachea, Cymbulia), and saips (Salpa, Thalia). (Reprinted from Denton 1963, with permission from Elsevier Science.)

o f fluid containing both am m onium and, in even larger quantities, trim ethylam ine, replacing alm ost 90% o f the equivalent N a + in seaw ater (Table 5.1).

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T rim ethylam ine is a heavy ion (mol. w t 60.0) bu t provides significant static lift bccausc it has w hat is calk'd a ‘positive partial m olal volum e’ (Sanders an d C hildress 1988). Solutions o f the ion have a g reater volum e (and therefore lower density) th a n the sum o f the ion volum e a n d the w ater volume. T his co u n terin ­ tuitive effect occurs because the ions disrupt the m olecular structure o f the w ater in their vicinity. T h e am m onium ion has a sim ilar b u t m uch w eaker effect. T h e net result in .Notostomusgibbosus is th a t the carapace fluid provides 17.7 m g ml 1 lift in seawater. In Notostomus the ions are also present in the an im al’s blood, and it is not clear how it m anages to control the potential toxicity o f these com pounds to oth er tissues in the body. U rea, trim ethylam ine oxide, an d betaine are present in the plasm a an d muscle o f the Port Jackson shark, an d other elasm obranchs, an d help to balance the osm otic pressure to th a t o f seawater. All three com pounds have positive partial molal volumes an d therefore also contribute significantly to buoyancy balancc. T rim ethylam ine m ay have an o th er function in some deep-sea anim als. Its levels in species from several phyla are higher in the deeper-living species, including benthic ones for w hom the raised levels could have no buoyancy value. T h ere is some evidence th a t it m ay play a role in stabilizing the structures o f proteins against the deform ing cffects o f high pressure (Gillett et al. 1997; Kelly an d Yancey 1999).

Using fat and oil M odified body fluids provide considerable static lift for a w ide variety o f o rg an ­ isms b u t large fluid volum es are needed for the effect to be significant. A n osmotic balance has also to be m aintained. T h e use o f osmotically inert m aterials w ith densities even lower th an th a t o f pure w ater provides m uch g reater static lift, with fewer m etabolic penalties. Fats an d oils (lipids) are just such m aterials an d are widely accum ulated by m arine anim als. T h ey also have the advantage o f being relatively incom pressible, so their value is unaffected by depth. T h e m ost im p o rtan t types o f lipid th a t are accum ulated in sufficient quantities to have a buoyancy benefit are triglycerides, glycerol ethers, w ax esters, a n d longchain hydrocarbons. T h e ir densities range from ab o u t 920 kg m :i for triglyccrides (e.g. cod liver oil) a n d 850 kg m 3 for w ax esters (in crustaceans, lanternfish, an d the coelacanth) to 780 an d 860 kg m 3 for the hydrocarbons pristane (in some copcpods) an d squalcne (deep-sea sharks), respectively. Because lipids arc utilized for oth er purposes (e.g. as energy stores, as th e rm al insulation, an d as acoustic lenses) it is not possible to dissociate these functions from th a t o f buoyancy. However, because the buoyancy benefit is d eterm ined by the difference in density betw een the lipid an d seawater, given volum es o f w ax esters a n d squalene provide alm ost twice as m uch static lift as the sam e volum e o f triglycerides. I f n eu tral buoyancy is the m ain objective then lighter lipids tend to be preferentially accum ulated; triglycerides have a p rim ary role as an energy reserve.

THE BIOLOGY OF THE DEEP OCEAN

M easurem ents o f the am o u n t o f lipid in the tissues o f different m arine anim als have show n th a t in teleost fishes the levels do n ot vary significantly w ith depth; lipid values ranging from 2.9 to 63.3% o f the ash-free dry w eight have been rep o rted from m idw atcr fishes off California. Because the w ater content o f the fishes increases w ith dep th , lipid as a percentage o f the wet w eight decreases equivalently (Childress an d N ygaard 1973). Sim ilar results were obtained for anim als from the G u lf o f M exico an d from H aw aii. T h e H aw aiian species generally h a d low er lipid levels th an the C alifornian specics. A ntarctic notothenioid fishes, o r icefish, lack a sw im bladder an d they, too, accum ulate lipids to achieve neutral buoyancy. In an analysis o f several kinds o f occanic crustaceans the lipid values range from 3.3 to 66% o f the ash-free dry weight, an d ten d to increase w ith increasing h ab itat d ep th (Childress an d N ygaard 1974). T hose species occurring n ea r the surface have lipid values o f 1—3% o f their w et weight, while in m esopelagic spccics this increases to 6- 2 0 % .

C rustaceans have no gas-filled space (such as a sw im bladder), w hich could provide buoyancy; higher levels o f fat in deep-living species provide an altern a­ tive, reducing the sw im m ing effort needed to m aintain position in the w ater colum n. S qualoid sharks are the anim als th at m ost obviously use lipid as a buoy­ ancy aid. M any o f these (particularly the deep-w ater species, such as Centroscymnus, w hich cruise slowly ju st above the bottom ) have huge livers occu­ pying som e 65% o f the body cavity an d containing very large am ounts o f b oth the hydrocarbon squalene an d glyccrol ethers. T h e livers o f these fish constitute 25% o f their total w eight (our livers are only 5% o f o u r total weight). T hese n ear-bottom sharks have small pectoral fins, in m arked contrast to the m idw ater sharks, w hich have m uch less lipid and com bine large fins (which generate hydrodynam ic lift) w ith low -densitv body fluids. T h e ir cartilaginous skeletons are also m uch less m ineralized th a n those o f bony fish. T h e H olocephali (rabbit­ fishes) have a sim ilar lifestyle to the deep-w ater sharks an d their liver oil is largely squalene. This, com bined w ith a great reduction in skeleton calcification, brings them close to n eutral buoyancy. T h e lungs o f m arine m am m als (and birds) provide buoyancy n ea r the surface b ut ten d to collapse u n d er pressure w hen diving and it is in these circum ­ stances that high lipid levels m ay be o f significance. In m ost cases the prim e role o f the lipids will be th a t o f th erm al insulation but a buoyancy co ntribu­ tion also seems likely, particularly in the sperm w hale whose h ead contains huge am ounts o f w ax esters. T his deep-diving anim al probably uses tem perature-controlled adjustm ents o f the density o f the sperm aceti in its head as a buoyancy aid. A t the surface it cools the lipid by using seaw ater taken in through the nostrils and reducing the blood supply to the sperm aceti; as the sperm aceti cools its volum e decreases an d its density increases giving the whale assistance in the deep dive. At the botto m o f the dive the w hale reopens the blood supply to the sperm aceti a n d the w ax w arm s up, increasing in volum e an d decreasing in density, thus providing additional buoyancy for the retu rn jo u rn e y to the surface (Clarke 1970).

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Using gas Gas-filled spaces provide the m axim um possible static lift for an organism (e.g. the density o f oxygen at 0.2 M P a (2 atm) an d 0°C is only 2.8 kg n r 3), an d gases to fill the spaces are freely available dissolved in the surrounding seawater. B ut gas is very com pressible. T h e lift it provides is d eterm ined by its volum e, an d its volum e varies w ith the pressure, following Boyle’s law. T his is o f little consequence for an o rg an ­ ism that lives continually at or n ear the surfacc an d w hich therefore is n ot exposed to significant pressure changes. In the p articular com m unity o f anim als w hich live at the air—w ater interface (the pleuston), an d w hich (except as larvae) rem ain there throughout their lives, there are several species th at use gas as a m eans o f staying at the interface. For m any o f them the gas is acquired directly from the air. T h e purple snail Janthina encloses a bubble o f air w ith the front o f its foot a n d secretes ro u n d it a covering o f m ucus w hich sets into a h a rd balloon-like capsule. As it grows the anim al adds m ore an d m ore bubble balloons to its collection, m aking a buoyant raft from w hich it hangs, finally laying its eggs on the u ndersurface o f the raft. T h e little n u dibranch Glaucus gulps in bubbles o f air an d transfers th em along the gut to diverticula th a t ru n into its finger-like lateral appendages; it th en floats upside dow n at the a ir-se a interface. L arvae o f the goose b arnaclc Lepasfascicularis will settle on any piece o f flotsam, from a feather to an old lum p o f oil. T h e flotsam w ould soon sink u n d er the w eight o f grow ing barnacles but the anim als secrete a m ucuscovered gas bubble at the base o f the stalk a n d eventually these bubbles take over the role o f flotation, helped by the fact that this species also greatly reduces its calcareous plates (i.e. its high-density tissues). Tw o coelenterates epitom ize the gas-supported fauna at the o cean’s surface, nam ely the cho ndrophore Velella (Sail-by-the-W ind) an d the siphonophore Physalia (Portuguese M an o ’War). Velella has a little oval cartilaginous float con­ taining m any cham bers o f gas, from w hich its sail projects into the air. Physalia has a float (which looks ra th e r like an inflated pink plastic bag) from w hich h an g all the individuals o f the colony including the stinging tentacles, w hich m ay be m any m etres in length. T h e gas in the float o f Physalia is secreted from a specialized tissue (the gas gland) an d is m ainly carbon m onoxide. Glaucus browses on Physalia, and, like som e oth er nudibranchs, is som ehow able to sequester the undischarged stinging ncm atocysts an d store them in its owrn tissues as a defence. M idw ater siphonophores o f the group to w hich Physalia belongs (the physonects) have a very m uch sm aller gas float at the u pper end o f the long stem. T his p ro ­ vides som e buoyancy an d its gas volum e can be regulated by secretion o r by ex tru ­ sion through a pore. A dditional buoyancy is achieved by ion replacem ent in the gelatinous bracts an d sw im m ing bells o f these animals. Anim als living at g reat depth a n d /o r carrying o ut rap id vertical m ovem ents in the w ater colum n face the greatest problem s in using gas as the m ain buoyancy aid. T hose in deep w ater have to overcom e the problem s o f secreting gas (and p re ­ venting diffusion losses) against the very high am bient pressure. T hose m oving vertically have also to adjust continually the quantity' (mass) o f gas in the gas space

THE BIOLOGY OF THE DEEP OCEAN

to achicvc a constant gas volum e in the face o f changes in pressure. In very deep w ater the increased mass o f gas will be at a higher density T h u s at 4000 m the density o f oxygen rises to 4.6 kg m :i, but this will have a negligible effect (<0.2% ) on the lift it provides. T h e m etabolic task o f m aintaining a gas space in the m idw ater environm ent is greatly simplified if the space is m ade incom pressible. T h e gas w ithin the space rem ains at atm ospheric pressure an d constant volum e regardless o f the depth. T h e lift it provides therefore also rem ains constant. T his m eth o d is em ployed by some cephalopods, notably cuttlefish, Nautilus, an d Spirula. T hese anim als sccrctc a rigid cham bered shell, each cham ber o f w hich is filled initially w ith fluid and linked to the previous one by a calcified tube (the siphuncle). T h e epithelial cells o f the siphuncle contain biochem ical pum ps th a t rem ove ions from the fluid; w ater follows the ions by osmosis an d gas at blood partial pressure (~ atm o ­ spheric) diffuses in to take its place. T h e ch am b er is th en sealed an d an o th er one secreted alongside. Cuttlefish have very m any small cham bers th a t m ake up the calcareous cuttlcbonc. All the deeper-living species (down to 400 m) are small an d have narrow ’ cuttlebones w ith very closclv packed septa an d m odified sutures betw een the septa. T h e vertical distribution o f cach species is physically lim ited by a characteristic pressure (or equivalent depth) at w hich the ch am b er strength­ ening will fail an d the gas space will implode. Nautilus species have a very large external shell constructed similarly exccpt th at consecutive cham bers form a spiral, w ith the earliest ones at its centre. T h e siphunclc runs through the m iddle o f them all, m arking the sites o f the epiderm al ion pum ps. A m m onites w ere constructed on a sim ilar p attern an d probably used a sim ilar buoyancy system. Spirula is a small m esopelagic species o f squid, regu­ larly distributed dow n to 6 0 0 -7 0 0 m an d undertak in g substantial vertical m igra­ tions. It too has a spiral, cham bered shell, b u t in this case the shell is internal (Fig. 5.6). In laboratory tests the cham bers rem ain intact at a pressure equivalent to 1000 m depth, finally im ploding at the equivalent o f ab o u t 1200 m. T h e gas-filled sw im bladder o f bony fishes (teleosts) is potentially the m ost flexible o f all buoyancy systems. T h e specific gravity o f seaw ater is 1.026 an d the specific gravity o f a fish w ithout its sw im bladder is ab o u t 1.07. To achieve neutral buoy­ ancy the gas in the sw im bladder o f m arine fishes therefore needs to occupy ab o u t 5% o f the body volum e at any given depth. I f a fish w ith a full sw im bladder were to rem ain at one depth it w ould have no buoyancy problem s, except th at of topping up the gas against natural diffusive leakage. Investing the wall o f the sw im bladder w ith relatively gas-im perm eable m aterial, particularly fat or layers o f guanine crystals, will reduce gas leakage. T h e g reater the d ep th (i.e. pressure), the greater the potential rate o f diffusive loss; deeper-living fishes consequently have thicker layers o f guanine in their sw im bladder walls th an do shallow ones. T h e guanine crystals give the sw im bladder a silvery ap p earan ce (C hapter 9). T h e flexibility o f the sw im bladder wall contrasts w ith the rigid walls o f the gas float in ccphalopods such as Nautilus. T h e sw im bladder is highly com pressible an d this presents different problem s for shallow- an d deep-living fishes. Consider, first,

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Fig. 5.6

The mesopelagic squid Spirula (left) achieves neutral buoyancy by maintaining gas-filled chambers in the internal shell shown in the X-ray (right).

a fish neutrally buoyant at the surface. Pressure at the surface is 1 atm (0.1 MPa); pressure increases approxim ately 0.1 M P a for every 10 m increase in depth. If the fish descends from the surface to 10 m the pressure will double an d this will halve the gas volum e w ithin the swimbladder, according to Boyle’s law (pressure X volum e is a constant; P V = K). In order to m aintain a constant gas volum e (and hencc buoyancy) during the descent to 10 m, the fish m ust secrete an additional mass o f gas, equal to that originally present, at the sam e rate as it is descending. T h e problem for this shallow-living fish is therefore th a t o f rap id secretion o f gas to offset rap id an d proportionally large increases in pressure. T h e sam e additional mass o f gas will be required to m aintain the sw im bladder volum e constant for every additional 10 m the fish descends. T h u s a fish at 400 m descending to 410 m will also experience a pressure increase o f 0.1 M P a (1 atm) b ut because the gas in the sw im bladder started w ith a pressure o f 4.1 M P a (41 atm) the volum e will only decrease by 0 .1 /4 .1 (2.4%) an d the effect on the fish’s buoyancy will be equivalently small. T h ere is less need for rapid adjustm ent o f the gas volume, although to m ain tain neutral buoyancy the mass o f gas th at has to be secreted is the same. T h e additional physiological problem faced by this fish is th a t o f secret­ ing gas into the sw im bladder against a total pressure o f 4.2 M Pa. W h at happens w hen these two fishes swim back up to their initial depths? W h en the one at 10 m reaches 5 m the pressure will be 0.15 M Pa, the gas volum e will have increased by a third an d the lift will have increased similarly. T h e fish will

THE BIOLOGY OF THE DEEP OCEAN

be experiencing a rapidly accelerating lift, w hich could result in an uncontrolled ascent to the surfacc unless the gas volum e (i.e. mass) is continuously red u ced on the way. T h e consequences o f an uncontrolled ascent (‘the b en d s’ in a h u m an diver) can be seen in the appearance o f m any o f the fishes in a com m ercial trawl: they have sw im bladders w hich have expanded so m uch on the w ay to the surface th a t they now p ro tru d e out o f the an im al’s m outh. T h e fish at 410 m has a sim ilar problem , nam ely th a t o f absorbing gas as it ascends to 400 m, b u t the potential volum e (and buoyancy) increase from 410 to 400 m is sufficiently small to be m ore readily offset by sw im m ing a n d /o r slower gas reabsorption. A scent thus poses a greater threat to buoyancy control th an does descent, espe­ cially n ea r the surface. Som e near-surface fish, like the herring, solve the problem by having a d u ct that links the sw im bladder to the gut lum en. A ir can be taken in at the surface to top-up secreted gas an d the sw im bladder volum e can be adjusted, particularly during ascent, by venting cxcess air through the m outh. T his type o f ‘o p en ’ sw im bladder is described as physostom atous. Closed ones, w ith no external duct, are physoclistous. M any fast-sw im m ing surface fish that w ould norm ally change dep th rapidly an d often (e.g. tuna) have dispensed alto­ gether w ith a sw im bladder (and its problems!) an d d ep en d largely on hydrody­ nam ic lift for their buoyancy. M idw ater fishes such as the lanternfishes, w hich undertake extensive diel vertical m igrations, often restrict gas buoyancy to the n o n-m igrant larvae, filling the sw im bladder with fat as they m ature. T hose w ith the greatest vertical m igratory ranges facc the m ost difficulties in controlling their gas volum e; the result is that they have the largest am o u n t o f fat in their swim­ bladders (Bone 1973). T h e relation betw een gas, fat, an d reduced body fluids in providing buoyancy varies greatly betw een species. Species o f the midw-ater fish genus Gonostoma, for exam ple, have m arkedly different d ep th distributions an d differ in their relative use o f fat, dilute body fluids, an d gas (Figs 5.3, 5.7) (D enton an d M arshall 1958). T h e problem s o f secreting gas against very high pressures seem to have resulted in the loss o f the sw im bladder in m any deep-living fishes, b u t it is still retained in som e larger benthopelagic species at great depths (around 5000 m); these fishes rem ain close to the b o tto m an d do n ot have to com pensate for rap id d ep th changes. Fish w ith elosed sw im bladders (physoclists) secrete gas into the sw im bladder across a specialized p ortion o f its wall, know n as the gas gland. H ow do they do this? T h e first clue com es from analysis o f the gas in the swimbladder, w hich contains oxygen, nitrogen, an d carbon dioxide, like the atm osphere (and like the seaw ater w-’hich is in equilibrium w ith it), b u t in different proportions. O xygen is the m ain com po­ nent, m aking up some 63% o f freshly secreted gas in the codfish, for example. G ases dissolved in the arterial blood are in equilibrium w ith the seaw ater bath in g the gills. O xygen therefore com prises abou t 20% o f the gas dissolved in the blood. T his is at a partial pressure (or tension) o f 0.02 M P a (0.2 atm), the sam e as in air. N itrogen has a partial pressure o f 0.08 M P a (0.8 atm) an d C O z less then 0.005 M P a (0.05 atm). O xygen is also b o u n d to the haem oglobin, b ut this oxygen does not contribute to the partial pressure. G as is released from the blood at the

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Fig. 5.7

X-rays o f three species of Gonostoma with different depth distributions. The shallowest one (G. atlanticum, top) has gas in its swimbladder and a strongly ossified skeleton. The middle one (G. elongatum) has a weaker skeleton and no swimbladder (see Fig. 5.3), and the deepest species (G. bathyphilum, bottom) has very little ossification and very watery tissues.

gas gland because the cells o f the gas gland secrcte lactic acid. T his ad d ed solute decreases the solubility o f all the dissolved gases, releasing small am ounts o f all of them from solution into the swimbladder. T h e lactate has an additional, an d m uch greater, effcct on the oxygen that is bo u n d to the haem oglobin in the blood corpuscles. T h e lactic acid reduces the p H o f the blood (increases the acidity). O xygen binds m uch less well to fish haem oglobin at acid p H , even at high pres­ sures o f pure oxygen, i.e. the haem oglobin’s capacity for carrying oxygen is reduced. T his is a general characteristic o f haem oglobins an d is know n as the R oot effect. Crucially, it is very m uch m ore pow erful in fish haem oglobin th an in th a t o f m am m als. O xygen is therefore very rapidly driven off the haem oglobin a n d out o f solution into the swimbladder. T his is know n as the Single C oncen tratin g Effect. T h e gas in the sw im bladder thus becom es considerably enriched w ith oxygen (i.e. at a higher partial pressure com pared w ith th at in the blood; Pelster 1997; S chm idt-N ielsen 1997). T h e venous blood leaving the gas gland is in equilibrium w ith the gas in the swimbladder. A lthough it now contains a sm aller quantity of oxygen th an the arterial blood entering the gland, th at oxygen is nevertheless at a higher partial pressure because m ore o f it is now in solution instead o f being bo u n d to the haem oglobin. In a fish at the surfacc this m echanism by itself will provide a small flux o f all blood gases into the sw im bladder an d a relative enhancem en t o f the oxygen p artial pres­ sure. A t greater depths the gas gland has to secrete gas into a sw im bladder that

THE BIOLOGY OF THE DEEP OCEAN

already contains gas at high pressure, yet the partial pressure o f oxygen in the blood rem ains at ab o u t 0.02 M P a (0.2 atm). Secretion o f gas (particularly oxygen) against the high pressures is achieved by m ultiplying the action o f the single concentrating effect m any times, through an intim ate association o f the arterial an d venous cap ­ illaries o f the gas gland in w hich they are arran g ed as a co u n tercu rren t system. T his system is know n as the rete mirabile. In the co u n tcrcu rren t system lactate in the venous capillaries is able to diffuse gradually across into the arterial capillaries, low­ ering the p H , releasing oxygen, and thus increasing the p artial pressure o f oxygen in the incom ing blood before it even reaches the gas gland. H ere the gas gland cells produce even m ore lactic acid to cnhancc the effect still further. T h e higher partial pressure o f oxygen in the venous capillaries allows this oxygen to diffuse back across the co untercurrent system to the arterial capillaries, even though the absolute am ounts o f oxygen p er u nit volum e o f blood are lower in the venous ca p ­ illaries. As the lactic acid also diffuses across to the arterial capillaries the venous blood p H gradually rises again and oxygen is able to recom bine w ith the h aem o ­ globin. However, this recom bination is a m uch slower process th an the initial R oot effect an d the oxygen is therefore available over a m uch longer rime in the rete for diffusion back to the arterial capillaries. T h e rete thus acts as a trap to retain and augm ent the gases in the sw im bladder (Fig. 5.8).

Fig. 5.8

Diagram showing (a) the blood circulation to the swimbladder of a typical fish. Gas is supplied to the special gas-secreting gland through a set o f closely apposed arterial and venous capillaries (the rete mirabile) and can be reabsorbed through other capillaries spread over the wall of the posterior region of the swimbladder. The latter capillaries are shut off during gas secretion. The rete (b), represented here as a single loop in a fish at 1000 m (100 atm), is a countercurrent multiplier system of thousands of vessels. The gas gland produces lactic acid, causing oxygen in the arterial blood to be released from its binding to haemoglobin and to diffuse into the swimbladder. The oxygen tension in the venous capillary also rises (bound oxygen comprises most o f the oxygen in the incoming arterial blood but does not contribute to the tension). Gas diffuses across from the venous to the arterial capillary during its return along the rete (the numbers indicate the relative oxygen tension in atmospheres) and is thus retained in the loop. The venous blood leaving the rete contains less oxygen per millilitre than the incoming arterial blood but has a higher oxygen tension. (From Schmidt-Nielsen 1995, with permission from Cambridge University Press.) (a)

(b)

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Fig. 5.9

The length of the rete in different deep-sea fishes (mainly benthopelagic species) increases in relation to their mean depth of occurrence. (From Pelster 1997, with permis­ sion from Academic Press.)

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T h e length o f the rete determ ines the overall efficiency o f this system. A n cel has about 1O’ venous a n d arterial capillaries in its 4 m m rete, providing w ithin it an overall length o f some 400 m o f each! For fish w ith sw im bladders there is a close correlation betw een the dep th at w hich a species lives an d the length o f its coun­ tercu rren t system; the longest rete (about 25 mm) are present in abyssal species living at ab o u t 5000 m (Fig. 5.9) (M arshall 1971, 1979). A specialized region o f the sw im bladder wall, called the oval, is present in som e species to accelcrate gas reabsorption w hen specifically required. A t other times a sphincter seals this area off from the rest o f the sw'imbladder to reduce gas leakage. T h e fine control o f gas secretion an d reabsorption has provided a system for the m ain ten an ce of n eutral buoyancy w hich has freed the bony fishes from the structural lim itations o f hydrodynam ic lift. It has given them a freedom o f design n o t available to their cartilaginous relatives.

Metabolism, energy, and pressure Metabolic rates For pelagic anim als one o f the inevitable consequenccs o f reducing the m etabolically active tissues, such as muscle, an d increasing the w'ater co n ten t o f the body in the interests o f buoyancy, is th a t the anim al’s overall m etabolic dem ands are reduced (or the individual can becom e larger at the sam e m etabolic cost, see C h a p te r 10). In cither ease there will be a reduction in the m ctabolic rate p e r unit mass o f tissue. T his is m ost easily quantified by m easuring the respiratory rate (oxygen dem and) o f these anim als. Both fishes an d shrim ps show a well-defined reduction in respiration rate w ith increasing dep th o f occurrence (Fig. 5.10) w hen

THE BIOLOGY OF THE DEEP OCEAN

118

m easured at atm ospheric pressure an d h ab itat tem peratures. C ould this not simply be a consequence o f the low er tem peratures th at they experience with increasing depth? N o, this cannot explain the full degree o f reduction in respira­ tory rates. T h e know n tem perature effects (the rates o f change for a 10°C tem ­ p eratu re change, or Q,I(), w ith a usual value o f aro u n d 2) are n ot large enough in m ost cases to explain the changes w ith depth. T his is particularly ap p aren t in the n atu ral experim ent involving the A ntarctic pelagic fauna; these anim als show a sim ilar reduction in respiratory rate w ith d ep th b ut the w ater colum n is alm ost isotherm al, th at is the tem p eratu re in deep w ater is only a degree or so different from th a t at the surface, so the tem peratu re effect can n o t be the controlling one. T h e conclusion to be draw n is that in these anim als ‘there is an in h eren t red u c­ tion in m etabolic rate with increasing d e p th ’ (Torres et al. 1979). Som e polar shallow -w ater species show evidence o f m etabolic ad ap tatio n to the low environm ental tem peratures (i.e. ‘cold ad a p ta tio n ’), w ith the result th at their m etabolic rates are higher th a n w ould be expected by extrapolation from results obtained on related species living at higher tem peratures. T h e deep-sea fauna m ight be cxpected to show sim ilar m etabolic adap tatio n , o r com pensation for dif­ ferent h ab itat tem peratures. T h e respiratory d ata do suggest some degree o f tem ­ peratu re com pensation by deep A ntarctic fishes. T h e ir respiratory rates arc considerably higher th an are those o f C alifornian fishes extrapolated to A ntarctic tem peratures (Fig. 5.10) (Torres an d Som cro 1988a,b). T h e d ata also show th at tem perature com pensation (i.e. the m ain ten an ce o f sim ilar respiratory rates by the different groups o f fishes at their respective h ab itat tem peratures) is now here

Fig. 5.10 Oxygen consumption plotted against depth of occurrence (a) for California fishes at 10°C and 5°C depending on habitat depth and (b) for Antarctic fishes at 0.5°C. The data show that the reduction in oxygen consumption with depth is not a function of habitat temperature but is an inherent metabolic change. (Reprinted from Torres and Somero 1988a, with permission from Elsevier Science.)

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n ea r com plete. T h e indications o f som e degree o f w hole-anim al cold ad ap tatio n by the A ntarctic species is reinforced by in vitro studies o f the m etabolic activity of isolated b rain a n d gill tissues, w hich show ed a considerable degree o f tem p eratu re com pensation w hen A ntarctic, tem perate, and tropical species were com pared (Somero 1998). Som e other depth-related effect m ust account for the reduction in m etabolic rates in deep-sea anim als. Possible factors m ight be increased pressure, absence o f light, o r changes in oxygen concentrations. T h e respiratory m easurem ents discusscd above w ere m ade at atm ospheric pressure. G ould the increased pressure at d ep th raise the respiratory rates o f deep-sea anim als an d com pensate for the effects o f lower tem peratures? T h e lim ited d ata on respiratory rates m easured on repres­ surized anim als rule out this hypothesis; the stim ulatory effects o f pressure are far too small to produce the observed differences. A few fish have been successfully trapped an d studied in an in situ respirom eter. T h e results confirm th a t the n atu ral m etabolic rates are very low an d certainly' not significantly en h an ced by the higher pressure. O xygen levels in general are high throughout m ost o f the deep sea, except in the few p e rm a n e n t oxygen m inim um zones such as the eastern tropical Pacific and the n o rth ern In d ian O cean. T h e respiratory d ata (Fig. 5.10) include fishes from C alifornia, w hich are exposed to such a zone, an d fishes from the A ntarctic and G u lf o f M exico, w hich are not, yet all three groups show sim ilar decreases in res­ piratory rates w ith depth. A n alternative hypothesis is that anim als at epipelagic an d u p p er mesopelagic depths, exposed to day'light a n d subject to visual predators, p u t a lot o f m etabolic effort into their locom otory systems either to catch prey' o r to avoid predators. A nim als in the lower meso- an d bathypelagic zones are n ot exposed to this visual p redation pressure an d can reducc the m etabolic effort devoted to locom otion. T h e depth-related reduction in respiratory rates w ould therefore reflect the red u c­ tion in sw im m ing effort (Childress et al. 1980; Childress 1995). T his hypothesis is supported by the fact that non-visual predators such as chaetognaths, jellyfish, an d w orm s do n o t show the sam e depth-related decline in respiratory rates as do fish, shrim p, an d cephalopods. Benthic anim als also show’ no decline in respira­ tory rates w ith depth, other th a n those directly attributable to red u ced tem p era­ tures. T h e decline observed in the pelagic realm seems to be closely linked to locom otory ability. Analysis o f enzym e activity, particularly lactate dehydrogenase (LDH), w hich reflects the m uscle’s capability o f supporting A T P generation d uring high-speed anaerobic bursts o f activity, confirm s th a t L D H activity also declines sharply w ith m inim um depth o f occurrence (Somero 1998). O th er enzym e analyses support the interpretation o f a d ep th-related reduction in loco­ m otory ability' in fishes— but n o t in non-visual p redators such as jellyfish and chaetognaths. T h e A T P-generating enzym e systems o f b rain tissue, on the other h an d , show no such depth-related changes (Childress an d Som ero 1979). R eduction o f the locom otory sy'stem seems to be the key to the observed depthrelated changes in w hole-anim al m etabolic rates.

THE BIOLOGY OF THE DEEP OCEAN

H ydro th erm al vent fish, w hich live in a deep, wholly dark, b u t very dynam ic an d densely populated habitat, have locom otory systems a n d m etabolic rates equiva­ lent to those o f shallow -w ater fishes. T h u s w here there is b o th sufficient food to support a high m etabolic rate an d a selective advantage in active locom otion, m etabolic rates can be h ig h —in the deep sea, ju st as elsewhere. A n aquatic anim al w ith a high m ctabolic rate needs a large respiratory area an d a high w ater flow across it. O xygen m ust be taken up efficiently by the blood an d rapidly transported by the circulatory system to the tissues w here it is needed. In deep-sea anim als w ith a reduced m ctabolic rate these requirem ents are relaxed an d concom itant changes have occurred in the blood an d circulatory systems. D eep-sea fishes in general have fewer a n d sm aller gill filam ents th an do related shallow -w ater species o f equivalent size. T h e am o u n t o f haem oglobin in the blood (often recorded as the hacm atocrit, the p ro p o rtio n o f the blood volume occupied by red blood cells) determ ines m uch o f its oxygen-carrying capacity. H aem atocrits o f m esopelagic species w ithout sw im bladders are bctw'een ab o u t 5 an d 10%. T hese fishes are those w ith a high w ater content an d very little red (aerobic) muscle. T h ey also have a relatively small h eart an d large lym phatic system. M esopelagic species w ith a sw im bladder have a higher h aem atocrit (14-35% ), lower w ater content, m ore red muscle, a n d sm aller lym ph ducts. Active surfacc fishes such as flying fish have haem atocrits o f 50% or m ore. D eep benthic specics w ith sw im bladders have haem atocrits sim ilar to those o f their m esopelagic counterparts. T h e fewer but generally larger red blood cells o f deep-sea specics are probably m ore econom ical to produce an d to m ain tain th an sm aller ones o f equivalent haem oglobin content (Blaxter et al. 1971; G ra h am et al. 1985). H e a rt sizes reflect activity profiles. A m ackerel’s h eart is 0,2% o f its body volume, an d that o f a cod 0.13% , but a bottom -living plaice has a h eart only 0.06% o f its body volume. H e a rt w eight is to some extent a function o f blood viscosity, w hich affects the force required to p u m p it ro u n d the body. Viscosity increases as tem ­ p era tu re falls, so deep-sea (and polar) species have a potentially increased blood viscosity. In practice, the blood viscosity o f b o th groups o f fishes is generally low an d less tem peratu re-d ep en d en t th an that o f shallow species. Coryphaenoid.es is a large benthopelagic rattail, but it has a h ea rt o f sim ilar proportions to th a t o f the plaice (G reer-W alker et al. 1985), an d its low rate o f m etabolism is indicated by the fact th a t it has a respiratory rate only 5 % th at o f a cod. T h e hearts o f deepsea fishes arc simply sm aller pum ps b u t they are no less m uscular ones. T h e ir protein concentrations arc unchanged, unlike the sw im m ing muscles w hich have only h alf the protein content o f the sw im m ing muscles o f shallow' specics. Low tem perature affects not only blood viscosity b u t also oxygen solubility in blood plasm a. Fishes, such as the A ntarctic icefishes, living at very low tem p era­ tures an d w ith sluggish lifestyles can get by w ithout any haem oglobin an d rely solely on the increased solubility o f oxygen in their plasm a. N o deep-sea fishes are know n w ith the sam e adap tatio n but the tem peratures at w hich the icefishes live are several degrees low er th an those w hich occur at abyssal depths in other regions.

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D ecapod shrim ps (and m any o th e r invertebrates) have haem ocyanin as the oxygen-binding pigm ent in their blood. T h e haem ocyanins o f b o th vertically m igrating an d non-m ig ran t shrim p have high affinities for oxygen at low tem p er­ atures. N on-m igrants, w hich live in a narrow tem p eratu re range a n d constant low-oxygen tension, have a lower haem ocyanin concentration in th eir blood th an m igrants b u t the haem ocyanin has a high affinity for oxygen an d is tem p eratu re insensitive. M igrants have tem perature-sensitive haem ocyanins whose oxygen affinity declines in w arm e r near-surface wraters— b u t here the oxygen levels are higher (Sanders a n d C hildress 1990). T his is highly adaptive in th at it allows the haem ocyanin to rem ain functional over the w hole o f the wide range o f conditions encountered by the m igrants.

Pressure effects A lthough pressure effects are not the root cause o f the decline in m etabolic rate w ith depth, adaptations to high pressure are essential prerequisites for success in the deep sea (Siebenaller 1987; Sicbenallcr an d Som ero 1989; Som ero 1992; G ibbs 1997). W h en shallow specics are exposed to a cold environm ent (e.g. in the A ntarctic) they com pensate to som e degree by increasing the concentrations o f key enzym es as w'ell as by evolving m ore efficient enzymes. We m ight think that deep-sea anim als w ould do som ething sim ilar to offset the lower tem peratures o f their h abitat but in practice the higher pressures require different adaptations. C old-adapted p o la r species are not autom atically p re-ad ap ted for deep-sea life. Pressure affects any reaction system th a t involves a change in volum e; in practice this includes m ost biochem ical reaction systems. Enzym es control the m etabolism o f every organism . Enzym es are large proteins whose structural conform ations determ ine their substrate (ligand) binding properties; these conform ations alter frequently during the reaction an d affect n o t only the substrate b inding b u t also the binding o f solvent ro u n d the enzyme. Pressure affects the rates an d precise regulation o f enzym e catalysis as well as the enzym e structure itself (Somero 1998). T h e enzym es o f deep-sea anim als generally have a reduced pressure sensitivity w hen com pared w ith equivalent enzym es from shallow er species. T h ey continue to w ork at pressures at w hich the shallow er systems are disrupted. W h en com ­ pare d at atm ospheric pressure, however, they have low er catalytic efficiencies. It appears th at the price o f pressure insensitivity is a reduction in efficiency (loss of com petitive ability) relative to the enzym es o f shallow specics (Somero an d Siebenaller 1979). T h e key feature o f pressure adap tatio n in enzym es is the ability to m aintain effective regulation o f catalysis an d pro tein structure rath e r th a n to m aintain the absolute rate at w hich catalysis occurs. A single pressure-insensitive enzym e is utilized by species whose vertical (depth) range varies d u rin g their life­ tim e (e.g. during ontogenetic m igrations), rath e r th an a series o f isozymes o f dif­ ferent pressure sensitivities expressed at different periods o f the life history (cf. visual pigm ents, C h a p te r 8) (Siebenaller 1987).

THE BIOLOGY OF THE DEEP OCEAN

Enzym es an d oth er proteins are n o t the only biological com ponents affected by pressure. A nother im p o rtan t one is the phospholipid in cell m em branes. A t low tem peratures lipids ten d to be less fluid (just as b u tte r is h ard en ed by cooling it). M aintaining the correct balance o f fluidity in cell m em branes (the optim al liquidcrystalline state) is essential for th e transfer processes across the m em b ran e to co n ­ tinue normally. Increased pressure also m akes m em b ran e lipids less fluid. T h e com bined effect o f high pressure an d low' tem p eratu re on deep-sea cell m em ­ branes is equivalent to p utting them in a deep-frceze at a tem p eratu re o f ab o u t —15°C. Som e m em brane adap tatio n is essential if they are to continue to work effectively T h e fluidity o f the lipids can be increased by changing th eir com posi­ tion, specifically by increasing the conten t o f u n satu rated fatty acids (just as in ‘spreadable’ butters). T his is cxactlv w hat takes place in the cell m em branes of deep-sea species u n d er w hat is described as ‘hom eoviscous’ ad ap tatio n , th at is the adjustm ent o f com position to m aintain a consistent fluidity u n d er different envi­ ronm ental conditions (e.g. D eL ong an d Yayanos 1985; Fang et al. 2000). It is crit­ ical in m aintaining the clectrophysiological com petence o f cell m em branes (Somero 1998).

Conclusion Survival requires a successful energy budget, whose balance is allowed to be over­ draw n only occasionally an d briefly. Food provides the incom e, while respiration an d locom otion are the regular expenses. G row th an d reproduction constitute the m ain investm ents (C hapter 10). Fast-sw im m ing h u n ters are the big spenders, and need to reap appropriately large an d frequent rew'ards. M ost bathypelagic anim als are equivalently frugal spenders, successfully eking o ut a m ore erratic incom c by virtue o f low'er regular expenses. T h ey achievc this by a reduction in active locom otion, correlated w ith a low ered m etabolic rate. A daptations to high pressure are at the cost o f enzym atic efficiency, w hich m ay further reduce m eta­ bolic rates, an d involve com pensatory adjustm ents to m em b ran e fluidity. Buoyancy aids are critical enablcrs o f this low-activity lifestyle b ut cach m ech a­ nism has its own benefits an d consequences. Fluid-based n eu tral buoyancy results in an increase in the bulk o f an organism , w hich increases its d rag an d hence the energy required at a given size to achieve a p articu lar speed through the water. G as m inim izes both this increased bulk an d the drag-associated energy costs, b ut restricts rap id vertical changes. T h e fish sw im bladder represents the greatest evo­ lutionary developm ent o f gas buoyancy; and for its op eratio n depends very m uch on the spccial characteristics o f fish haem oglobin. T h e efficiency o f different buoyancy aids an d the size an d lifestyle o f the o rg an ­ ism are inextricably linked an d m ay differ even in closely related species. T h e eco­ nom ics o f survival in the deep sea have num erous, equally successful, energy m anagem ent solutions.

6

Feeling and hearing

Sensing vibrations A night-tim e w alk in a dark w ood (where our visual sense tem porarily fails) provides a rem in d er o f the inform ation o u r various m echanoreceptors can give us ab o u t the environm ent an d its inhabitants. T h e distant rum ble o f thunder, a breath o f w ind, th e brush o f a m oth, the squeal o f a cap tu red m ouse, the squeak o f a bat, o r the hoot o f an owl, each adds to o u r knowledge o f the sur­ roundings even though bo th ou r perceptions an d o u r interpretations are inevitably lim ited. E ach o f these sensations has its equivalent in the occan, m uch o f w hich is dark som e o f the tim e an d m ost o f w hich is d ark all o f the time. O ceanic anim als need sensory systems (m echanoreceptors) th a t can detect these sounds an d m ovem ents an d unscram ble th eir various messages (Hawkins 1985).

We tend to regard feeling an d hearing (touch a n d sound) as quite separate sensory systems. In tru th th e distinction betw een the stimuli becom es b lu rred at low frequencies, particularly w hen the vibration is tran sm itted th ro u g h the g round as well as the air (e.g. the approach o f a train or the deep rum ble o f an elephant). Fishes em ploy very sim ilar sensory units for the detection o f b oth sound (as pressure waves) an d w ater m otion (as particle velocity, or displacem ent) an d for m ost aquatic anim als the distinction betw een the two is prim arily a m atter o f range. T h e m echanoreceptors o f oceanic anim als detect shear betw een themselves an d either the external seaw ater or the internal fluids, d epending on w here they are sited. T hey are naturally m ost often located on the external surface o f an anim al, as setae, hairs, or bundles o f h air cclls. Alternatively, if the receptors are coupled to structures, such as the otoliths o f fish an d the statoliths o f invertebrates, w hich are m uch denser th an the tissue fluids in w hich they are suspended or supported, they will also detect the shear th at results from the inertial differences during acceleration. A cceleration m ay also be detected by the m otion o f fluid acting directly on the sensory cells, as occurs in ou r own sem icircular canals. T h e acceleration m ay be linear or angular (rotational) as we experience in, respectively7, a lift or a co rn erin g car. T h e ensuing sensations are the ones the designers o f them e-park rides try' to maximize.

THE BIOLOGY OF THE DEEP OCEAN

Vibrations in water T h e ocean is a noisy plaee, although a diver w ould be largely unaw are o f it because his senses are not tuned to the environm ent. O u r ears are specialized to analyse sounds into tones o f different frequencies. Fishes an d m any oth er m arine anim als are m uch m ore concerned w ith m aking rap id responses to b rief noises th an w ith frequency analysis. A quatic anim als experience a variety of hydrodynam ic disturbances in their im m ediate environm ent. Surface waves, rainfall, turbulence, an d anim als feeding, swimming, an d signalling all produce different sounds. Sounds are distortions in the flow o f a fluid (w hether the fluid be air or water) an d are produced w hen an organism , or any p a rt o f it, moves relative to the flow. T hese sounds are o f varying frequency; sw im m ing an d feeding noises range up to 50 H z, vocalization 5 0 -4 0 0 H z, an d echolocation by m arine m am m als up to 150 kH z. M any o f these vibrations are p roduced acci­ dentally b u t others are deliberate, for com m unication purposes, an d have differ­ ent wavelengths (A.) an d frequencies. H ow are they transm itted through the w ater? T h e distortions or sounds spread from the po in t o f origin as waves o f acoustic pressure; as they spread they carry inform ation ab o u t the am plitude, frequency, an d direction o f the cause o f the disturbance. S ound waves travel ab o u t 4.3 times faster in seaw ater th an in air. T h e w avelength o f a given sound frequency is thus 4.3 times longer in seawater, w hich has consequences for both echolocation an d hearing, as we shall see below. A t the sam e tim e the m otion (vibration) o f the sound source produces a to-and-fro m ovem ent o f the fluid p a r­ ticles aro u n d it. A ir is so com pressible that the transm ission o f this effect is neg­ ligible an d we only sense the pressure com p o n en t o f a sound wave. W'ater is m uch less com pressible an d the local flow cffcct is a very im p o rtan t p a rt o f the acoustic field. T heoretical analysis o f the transm ission o f sounds pro d u ced by aquatic anim als usually treats them in term s o f these two com ponents, the far field an d the n ear field, an d a source such as the beating tail o f a fish is usually m odelled as a small vibrating sphere. T h e ability to sense an d interp ret these two kinds o f inform ation is critical to the survival o f deep-sea anim als, while the ability to produce vibrations in a con­ trolled way provides the potential for sound com m unication an d the transm ission o f detailed inform ation from one individual to another, provided o f course th at the sound can be detected (Hawkins an d M yrberg 1983). For com parison, we h ea r over a frequency range o f 30 H z to 20 kH z, w hales an d dolphins 20 H z to 150 kH z, bats 15 to 200 kH z, an d fishes 20 H z to m ore th a n 100 kH z. O u r ears are m ost sensitive to frequencies aro u n d 3 kH z a n d a co d ’s ear to 20 to 300 H z. O u r voice range is from 100 H z to 1 kH z, the sounds o f fishes 50 H z to 5 kH z, o f snapping shrim ps 3 to 5 kH z, o f crickets 2 to 100 kH z, o f b at squeaks 30 kH z (similar to a dolphin), o f vole squeaks 4 to 7 kH z, an d o f an elep h an t rum ble 100 to 400 H z (D usenberry 1992).

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The far field T h e far-held com ponent com prises the acoustic pressure waves th at p ropagate from the sound source at a velocity o f ab o u t 1500 m s 1, w ith little loss of energy. T h e energy in an acoustic wave is divided equally betw een the p o ten ­ tial energy stored in the com pressions an d decom pressions in the m edium an d the kinetic energy7 in the increased velocities o f particles in the m edium . If the wav e is spherical its attenuation rate is proportional to 1/ r w here r is the dis­ tance from the source. T h e acoustic wave can stim ulate receptors by virtue o f the pressure gradients that exist at any instant betw een different phases o f the wave. T h e gradient will be greatest at points h a lf a w avelength ap a rt along the direction in w hich the wave is travelling. However, if the w avelength is very long relative to the length o f a fish (a 300 H z sound has a wavelength o f 5 m) the pressure gradients betw een points on the fish’s body will b e very small. How? then, can an anim al detect a distant sound o r vibration? E ither by being directly sensitive to the acoustic pressure wave or by converting (transducing) the arriving pressure wave into a large enough local particle velocity to be detected (Blaxter 1980). The anim al will then have access to the far-field com ­ p o n en t o f the sound source an d all the benefits o f the m uch greater range o f detection th a t this offers. M ost tissues are close to acoustic transparency w hen co m p ared w ith seaw ater (i.e. have a sim ilar acoustic im pedance) an d the passage o f the pressure wave will produce the sam e particle acceleration in the tissue as it docs in sea­ w ater— an d be largely undetectablc. However, tissues o f very high or very low density (e.g. bo n e o r gas) have m arkedly different acoustic im pedances, and consequently different accelerations to those o f the rest o f the anim al. T h e direct response o f dense otoliths or statoliths to an acoustic wave therefore p ro ­ duces a shear relative to the receptor cells associated w ith th em in the inner ea r (see below'). An anim al containing a gas bubble or gas blad d er can also indirectly sense the farficld acoustic wave because it will induce the bubble to vibrate. W h en the sound frequency is close to the resonant frequency o f the bubble the induced vibration is enhanced 3 -1 0 times. As it vibrates, the bubble re-radiates the acoustic energy an d generates its own ncar-ficld and far-field effects. I f the bubble is close enough to particle displacem ent receptors (or physically coupled to them ) th en the farfield pressure effect o f the original stimulus can again be detected as a near-field particle velocity. T h e bubble’s resonant frequency increases w ith b o th an increase in am bient pressure a n d a decrease in size. Even if the bubble (or sw im bladder) size is actively m ain tain ed (C hapter 5), its resonant frequency will be greatly affected by changes in the anim al’s depth. For exam ple, if a bubble o f diam eter 0.2 m m has a resonant frequency o f 40 kH z at 50 m d ep th this will increase to 90 kH z if the anim al descends to 200 m (typical o f som e diel vertical migrations).

THE BIOLOG Y OF THE DEEP OCEAN

The near field Close to the source the near-field com pon en t becom es im portant. T his is a hydrodynam ic wave th a t does not propagate and w hich can be m odelled on the basis that the m edium is incom pressible. Particle velocities o f the n ear field are g reater th an those o f the far field for positions close to the source b u t their values atten ­ uate m ore rapidly w ith distance: particle velocity falls as 1/ r 2 for a pulsating source an d 1/ r3 for a vibrating source (e.g. a fish’s tail). T h e particle velocities for the near-field an d far-field com ponents o f a p articu lar sound frequency are equal at X /2 n , i.e. at about one-sixth o f the w'avelength. A sound source w ith a fre­ quency o f 100 H z has a w avelength o f 15 m in seaw ater an d therefore a n ear­ field dom inated region o f ab o u t 2.4 m; a source with a frequency o f 1 kH z has a w avelength o f 1.5 m an d a n ea r field o f 0.24 m. T h e stimuli th at the near-field particle velocities provide to the receptors along a fish’s lateral line can be esti­ m ated either by assum ing the fish is stationary, in w-hieh case the stimulus to any receptor is propo rtio n al to the particle velocity in the adjacent m edium , or byassum ing that the fish is rigid along its long axis an d vibrates as a single u n it in the pressure field. In the latter case, if a fish is o riented w ith its h ead pointing tow ards the source, the vibrations o f the fish will be the sam e at all positions, an d equal to th a t in the m edium at some point m idw ay along the body7. Consequently, the vibrations o f the m edium will be greater th an those o f the fish at the head end an d less th an those o f the fish at the tail. T h e receptors on the head an d tail will receive stimuli o f opposite sign an d at the midway- position the stimulus will be zero. T h e m agnitude o f the net stimulus will fall very rapidly7 w ith the distance from the source (as 1 /r 4) an d the p attern o f stimuli will change greatly in response to small changes in the relative position o f the fish an d the sound source. Any anim al w ith sensors th a t are capable o f detecting the near-field stimuli will be able to m onitor the very steep signal g radient th at occurs along the length o f an arrav o f those sensors (D enton an d G ray 1982, 1988; D en to n 1991).

The hydrodynamic receptor system of fishes Fishes an d oth er primarily7aquatic vertebrates (e.g. am phibians) have developed a com plex arran g em en t o f hydrodynam ic receptors com m on to all inertial, lateral line an d h earing systems (M ontgom ery an d P ankhurst 1997). It is based on a single type o f receptor cell, the h air cell, so-called because it bears a n u m b er of hair-like structures on its surface. T h e lateral line system an d the m em branous laby'rinth o f the ea r both have h air cells an d they7develop from neighbouring ecto­ d erm al thickenings in the embry7o. As a result o f th eir com m on origin, an d their structural similarities, the two systems are often referred to as the acoustico-lateralis system, or the octavo-lateralis system (Popper 1996; C oom bs an d M ontgom ery7 1998). T h e latter nam e is used in recognition o f the fact th at the labyrinth’s function is not just acoustic (auditory) b ut is also proprioceptive (posi­ tion sensing) an d th a t it is innervated via the eighth cranial nerve (Table 6.1).

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Neuromast structure and distribution A group o f hair cells a n d their supporting cells form a neurom ast organ (Fig. 6.1). E ach epiderm al h air cell typically has a long stiff cilium (kinocilium), sited asym ­ m etrically on the cell surface, an d a group o f shorter stereociiia (technically stereovilli, because they lack the m icro tubular ultrastructure typical o f cilia). T h e stereociiia tend to increase in length tow ards the kinocilium . T h e kinocilia an d stereociiia o f all the h a ir cells in a neurom ast organ insert into an elliptical gelat­ inous structure, the cupula, w hich is secreted by the supporting cells. A ny m ove­ m en t o f the cupula causes the bundle o f cilia to bend. T h e asym m etry o f the kinocilium provides a directional sensitivity; bending o f the bundle tow ards the kinocilium causes depolarization an d excitation o f the h air cell, b ending in the other direction hyperpolarization an d inhibition (Blaxter 1987). E ach h air cell has a dual innervation com prising b o th afferent sensory an d efferent inhibitory fibres. All the hair cells in a given neurom ast organ in the lateral line are p o la r­ ized along a com m on axis b u t com prise two populations oriented in opposite directions. T h e w hole organ therefore has an axis o f m axim um sensitivity. T h e displacem ent sensitivity o f the h air cells is very acute; estim ates p u t the threshold m ovem ent as low as 0 .1 -0 .5 nm . A lthough they have tim e constants w hich ren d er them potentially capable o f responding to kilohertz frequencies, the m echanical coupling w ith the w ater reduces the natu ral resonance frequency to a few 100 Hz. N curom ast organs in the lateral line systems o f fishes m ay be free-standing on the surfacc o f the skin (as in fish larvae) or enclosed in grooves o r canals. T h ere is great variation in the distribution and p roportio n o f these types in different species, an d in th e detailed structure o f the neurom ast organs themselves (Coom bs et al. 1988; P opper 1996; C oom bs an d M o n tg o m ery 1998). T h e d im en ­ sions o f the neurom ast com ponents, such as cupula size an d stereovillus length, tune the frequency sensitivity o f particu lar organs. Free-standing neurom asts respond to frequencies o f 10-100 H z, those in canals to frequencies o f 5 0 -4 0 0

Fig. 6.1

A single hair cell bears a long kinocilium and numerous short stereociiia and has both efferent (E) and afferent (A) innervation. Hair cells form the sensory basis o f the different neuromast organs of the acousticolateralis system (free neuromasts, lateral line organ, and otolith organ) and the electroreceptive ampullary organ. (From Blaxter 1987, with per­ mission from Cambridge University Press.)

Hair ceil

THE BIOLOGY OF THE DEEP OCEAN

H z, In any one species there are fewer h air cells in a free neurom ast (tens to h u n ­ dreds) th a n in a canal neurom ast (typically several h u n d red to a thousand). C anal neurom asts m ay be very large in some deep-sea species. In the rattail Coryphaenoides rupestris, for exam ple, they are up to 0.5 m m in d iam eter an d contain tens o f thousands o f hair cells. Free neurom asts are present on the head, trunk, an d caudal fins o f m any deep-sea species an d in some bathypclagic fam i­ lies (e.g. anglerfishes, snipe eels, an d gulper eels) they m ay be m o u n ted on long papillae o r stalks. L ateral line canals are typically found on the h ead an d trunk an d usually' open to the exterior through a series o f pores or bran ch in g tubules th at link adjacent n eu ­ rom ast organs. T h e trunk canal (the visible lateral line) usually runs the length of the body on each side an d m ay o r m ay not connect to the h ea d canals (Fig. 6.2). In some specics it is broken into separate in d ep en d en t segments, in others it is m ultiplied so that there are several canals ru n n in g in parallel. C anals m ay be Fig. 6.2

General patterns (a) o f lateral line and head canals and superficial neuromasts in bony fishes. Double solid lines indicate canals, dashed lines the position of canals (or superfi­ cial neuromasts thought to have replaced canals), and connected dots the positions of other superficial neuromasts. IO, infraorbital; SO, supraorbital; ОТ, otic; PO, postotic; PRO, preopercular; MD, mandibular; T, temporal; ST, supratemporal; TR, trunk. The lateral line canals on a mesopelagic Searsia (b) are much narrower than those of the deep-sea halosaur Aldrovandia (c) and the rattail or macrourid Coelorhynchus (d). (From Coom bs et al. 1988, with permission from Springer-Verlag, and illustrations by N.B. Marshall and Lesley Marshall reprinted by permission of the publisher from Marshall 1971. C o pyrig ht© by the President and Fellows of Harvard College.)

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supported by cartilage (in the chim aeras, rabbitfishes, a n d ratfishes) or by bony rings. O n the trunk o f m any fishes the canals ru n th ro u g h a series o f overlapping, shingle-like scales. T h e trunk canal is missing altogether in the clupeid (herringlike) fishes. H ea d canals usually com prise three m ain branches (big. 6.2), one above the eye, one below the eye on the u p p er jaw, an d one run n in g from b eh in d the eye dow n to the low’er ja w (Blaxter 1987; C oom bs et al. 1988). T h e three branches m ay n ot be connected o r even com plete. In som e species a canal across the top o f the head links the canals on each side. In the clupeoid fishes the h ea d canal system is sim ilar b u t the tubules an d pores connecting it to the exterior are hugely elaborated. M any deep-sea fishes have greatly enlarged h ead canals w hich form huge sinuses (tuned to lowrer frequencies); these cover up to h alf the area o f the head in the rattail Coelorhynchusflabellispinis (Fig. 6.2), In a nu m b er o f cases the h ead canals are covered by a thin flexible m em brane an d in the m elam p h aeid Poromitra the m em ­ b ran e is pierced by pores. In the fangtooth Anoplogaster there are no pores an d the underlying canal is divided into com partm ents by bony partitions. T h e cupulae lie in small openings in these partitions (Fig. 6.3). Bathypelagic fishes typically have large cupulae an d neurom asts, stalked free neu ­ rom asts, an d enlarged h ead sinuses, all o f w hich probably increase the sensitivity o f the systems (Figs 6.2, 6.4, 6.5). L arge cupulae, w hich constrict or partially block th e canals, enhance the sensitivity to higher frequencies. Closed canals w ith rigid

6.3

Diagrams illustrating the variety of lateral line systems found in fishes. Also shown for each fish is a cross-section o f the canal at a neuromast, (a) In Fundulus the cupula almost blocks the canal; (b) in the sprat the cupula is narrow; (c) in the ventral canal of the ray a cupula runs the length of the canal, which has rigid walls and a compliant surface; (d) in the deepsea Poromitra the head canal is covered by a thin membrane with holes in it and the cupulae are low; (e) in the deep-sea fang-tooth Anoplogaster the canal is covered by a thin contin­ uous membrane and divided into compartments by partitions. Cupulae lie in openings in the partitions. (From Denton and Gray 1988, with permission from Springer-Verlag.)

thin membrane

Fundulus

d

holes

Poromitra

A

Ь

0 Clupeid (Sprat) Ь A.

" A'

шмтшт e

£ Ray(ventral)

В

Anoplogaster

/

_B'

THE BIOLOGY OF THE DEEP OCEAN

130

covers a n d pores also em phasize the higher frequencies, w hereas o pen canals or grooves provide g reater sensitivity to low frequencies. Flexible m em branes over the canals provide a resonant structure, w hich greatly enhances the response aro u n d the resonant frequency. C alculations suggest th a t Poromitra, for example, m ay be 100 tim es m ore sensitive th an a sprat in the 5 -1 5 FIz range (D enton an d G ray 1988). T h e lateral line system links to the cerebellum . T h e relative enlarge­ m en t o f this region o f the brain in deep-sea fish is an o th er indication o f the im portance o f the lateral line system in the bathypelagic environm ent. H a ir cells have been identified in the cephalochordate Branchiostoma; lam preys an d hagfishes have free neurom asts in lines over their heads an d trunks b ut they do not have canals. E lasm obranchs (sharks, skates, an d rays) have an arran g em en t of lateral line canals on the h ead an d trunk w hich open th ro u g h pores an d w hich are

Fig. 6.4

Neuromasts in deep-sea fishes: (a) the head of Melanonus (with the epidermis removed) shows the long strap-like neuromasts in the wide canals (cf. Fig. 6.2d); (b) superficial neu­ romasts are grouped at the tip of a papilla on the anglerfish Phrynichthys. (Photos: N. 1 Marshall.)

Fig. 6.5

The anglerfish Caulophryne has an extreme development of superficial neuromasts on very long hair-like papillae and elongate fin rays.

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ra th e r sim ilar to those o f bony fishes. Free neurom asts occur in skin pits in rays an d u n d er specially m odified scales o f sharks. M an y elasm obranchs (and some other fishes an d am phibians) have neurom ast organs specially m odified for elec­ troreception (see below).

Mode of action H ow is the lateral line used? T his relatively simple question does n o t have an equally simple answ er because there is still debate over the full capabilities o f the system. From the structural arrangem ents it is clear th a t fluid shear acts on the cupula, ben d in g the bundles o f cilia on the h air cells. Free neurom asts, on the fish’s surface, are likely to be the m ost sensitive structures b u t are vulnerable to the ‘noise’ engendered by a fish’s ow n m ovem ents (in a few species there are even some on the caudal fin). T hese neurom asts do n o t always have a cupula but w'here there is one the axis o f sensitivity o f the h air cells is along its long axis; that is, it is friction-coupled to the w'ater, or velocity-sensitive. T h e h air cells lie w ithin the fluid b o u n d ary layer at the skin surface an d they occupy the region w here the m axim um velocity gradient occurs w hen the w ater moves relative to the fish. Increasing the height o f the cupula o r raising the neurom ast on a papilla (Figs 6.4, 6.5) will increase the sensitivity to low frequencies an d to slow flow-s. It has been dem onstrated recently th a t the free neurom asts are involved in recognizing the direction o f slow currents (rheotaxis) a n d th a t their response threshold is reduced in the presence o f food odours. T his will be o f p articular value to deep-sea scavengers. Conversely, the free ncurom asts could sense the sw im m ing velocity an d act as proprioreccptors, a helpful attribute in the featureless m idw ater environm ent. F u rth er increases in sensitivity can be achieved by having the h air cell axis at right angles to th a t o f the cupula; th a t is, it becom es displacem ent-sensitive— but increasingly susceptible to self-generated noise. T h ere is some evidence th at this is reduced by efferent inhibition o f the hair cells during active swimming. C an al neurom asts are m ore isolated from the effects o f the an im al’s ow n movements. T h e canal neurom ast system, w ith its series o f pores, could potentially m easure pressure gradients betw een adjaccnt pores an d hence the w ater velocities flowingover them . T h e canal system responds to higher frequencies th an do free-standing organs but in m an)' deep-sea fishes the adaptations o f the canal system enhance its response to lower frequencies (M arshall 1996). T h e system does n ot respond to large currents o r w ater m ovem ents th a t displace the w hole fish: it is sensitive only to a very local je t or wave. T h e m ain function o f the lateral line system as a w’holc is p robably the detection o f m ovem ents at close range (within one o r two body lengths), b o th those o f neighbours in schools an d those of potential p red ato rs or prey (Table 6.1). T h e escape responses o f h erring larvae, for exam ple, im prove as the head canals develop. Strong circum stantial evidence for its function in schooling com es from

THE BIOLOGY OF THE DEEP OCEAN

w ork on larval silvcrside, whose schooling abilities develop in parallel w ith the neurom asts. Schooling is a pow erful defence against those visual p redators th at norm ally target single individuals. M aintain in g position w ithin the school is vital and is achieved by a com bination o f hydrodynam ic (acoustic) an d visual cues. Schooling an d non-oriented sw'arming behaviour in deep-w ater species is very difficult to identify, an d w-ould have less value in dim light, b u t has been observed in some u pper ocean lanternfishes. Surface-living fishes use the lateral line to detect waves an d ripples generated by struggling prey at the a ir-w a te r interface. In d eep er species the response is direct. For exam ple, the h ead canal neurom asts in the A ntarctic fish Pagothenia borchgrevinki respond to w aterborne vibrations an d have a m axim al sensitivity at about 40 H z, sim ilar to peaks in the pow er spectra o f the frequencies p ro d u ced by swim­ m ing zooplankton prey. W hen an am phip o d crustacean is teth ered near the fish’s h ead the electrical discharge in the lateral line axons m atchcs its sw im m ing m ove­ m ents (M ontgom ery an d M acD o n ald et al. 1987). T h e half-beak Hyporhamphus ihi is a n octurnal p red a to r o f plankton an d can locate live prey in total darkness. It has lateral line extensions along the characteristically elongated lower jaw and, in com bination w ith its eel-like body an d sw im m ing behaviour, uses this extended lateral line system to find its prey. T h e axis o f m axim um sensitivity o f canal neurom asts is defined by the axis o f the canal. T h e com plex orientation o f canals, particularly on the head, or o f arrays o f free-standing organs (e.g. in anglerfishes) m ay provide one w ay of analysing the direction o f the source o f any hydrodynam ic signal. T h e p attern o f net accelerations on the ncurom asts will change m arkedly w ith the position o r angle o f a fish relative to a vibrating source. D ifferences in signal am plitude along the length o f the trunk lateral line (resulting from the g rad ien t in particle displacem ent) will be sm aller for shorter fishes; if the distance to the vibrating

Table 6.1 Comparison between the fish lateral line and auditory systems (Coombs and Montgomery 1998) Lateral line system Receptor organs

Superficial and canal neuromasts Receptor Dispersed on body distribution surface Innervation 3-5 separate cranial nerves Effective stimulus Differential movement between the fish and the surrounding water Stimulus encoding Pressure gradient patterns 1-2 body lengths Distance range Frequency range <1 Hz to 200 Hz

Auditory system O tolithic ear and air cavity Clustered in cranial cavity Eighth nerve complex

O tolithic ear

Whole-body acceleration

Compression of air cavity

Acceleration

Pressure fluctuations

10 body lengths <1 Hz to 500 Hz

100 body lengths <1 Hz to 180 kHz

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source is large the stimuli reaching the fish will be very w eak (as a result o f 1/ rs attenuation) an d the differences along the short body length very small. T h e longer the lateral line, the g reater the signal differential along it, so there is a potential sensitivity' gain in having an elongate body (as in the half-beak, above). T his m ay be an im portant factor in the evolution o f the elongate bodies o f m any deep-sea fishes (e.g. dragonfishes, halosaurs, m acrourids, gulper eels, snipe cels, etc.). T h e body is deepest at the h ead a n d often laterally flattened (quite unlike the fusiform shape o f epipelagic fishes, whose body' is usually thickest some 40% along its length). Eel-like fishes swim by undulations o f the w hole body or o f the elongate dorsal fin. T h e ir shape probably provides less hy drodynam ic disturbance th an the tail beats o f other fishes; thus there is less likelihood o f leaving detectable hydrodynam ic ‘footprints’ or vortices (or biolum inesccnce). T his is a real threat; blind seals, for exam ple, can use their m echanoreceptors to find an d follow the p ath o f a (tail-swimming) fish up to 5 m inutes after it has passed. T h e acoustic cover o f stationary', neutrally buoyant anim als such as anglerfishes will be broken only by the hydrodynam ic w hisper o f their respiratory m ovem ents. T rip o d fishes, w'hich perch stationary above the bottom on their elongated fin ray's, similarly7 m aintain a silent vigil, w ith their sensitivity heightened by the lack o f background noise.

The inner ear fishes and other anim als have com plex equilibrium receptors th a t use gravity as a reference for determ ining changes in position. T h e vestibular organs an d sem i­ circular canals o f the in n er ear provide fishes w ith a neurom ast-based m eans of sensing acceleration in three orthogonal planes, an d at the sam e tim e offer the scope for far-field sound detection (Blaxter 1980; H aw kins an d M yrberg 1983; Popper 1996). In bony fishes there is fluid continuity' betw een three sem icircular canals, each o f w hich has an expansion or am pulla containing a recep to r (or crista), m ade up o f neurom ast organs oriented in one direction an d whose cilia are inserted into a cupula (Fig. 6.6). In lam preys there are only7two canals an d in the hagfish Myxine only one. Below the sem icircular canals lie the vestibular organs, the sacculus, lagena, an d utriculus, each o f w hich has a sensory region (or macula) located in a different plane. T h e m acula bears array's o f h air cells in dif­ ferent orientations an d an otolith o f crystalline calcium carbonate, separated from the h air cells by a m em brane. T h e sacculus is m uch the largest o f these three organs. E lasm obranchs have a structurally sim ilar arran g em en t, b ut have n u m e r­ ous small crystals (otoconia) instead o f single otoliths. T h e inner ea r o f a fish is structurally isolated from the outside w ater a n d the h air cells are therefore decoupled from external particle displacem ent. T h e m ovem ent o f fluid in the sem icircular canals gives inform ation on an g u lar acceleration while the inertia o f the otolith provides a response to linear acceleration. Because the acoustic properties o f the otolith are so different from those o f seaw ater its relative

THE BIOLOGY OF THE DEEP OCEAN

Fig. 6.6

The organization o f the inner ear of a cod Gadus morhua. The sensory membranes, or maculae, are shown with the polarity o f their hair cells indicated by the arrows. The left ear is shown in (a) lateral view and (b) dorsal view, and a schematic cross-section through the utricuius (c) shows the otolith mounted above the hair cells. (From Hawkins 1985, with permission from the Company of Biologists.)

m ovem ent in an u nderw ater sound field also produces shear forces at the m acula a n d hence the potential for hearing (through particle displacem ent). T his ‘d irect’ hearing is probably available to all non-specialist fishes (Popper 1996), is o f low sensitivity, an d is lim ited to frequencies o f up to a few h u n d red hertz (Table 6.1). G as is m uch less dense th an water; by coupling a gas space to the m aculae (Fig. 6.7), h earing specialists use the pressure wave to greatly en hance the sensitivity a n d frequency range (up to several kHz). T his is achieved in clupeid fishes by two gas-filled otic bullae. A stiff clastic m em b ran e in each bulla separates gas on one side from fluid on the other. T h e fluid connects to the utricuius through a small

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hole in the bulla, located close to the utricular m acula. Pressure-induced vib ra­ tions o f the bulla m em b ran e drive fluid to a n d fro through the hole. S ound pres­ sure changes are converted into particle displacem ents th a t stim ulate the utricular m acula. T h e utricular fluid is separated from th at o f the lateral line canal on the head by a second elastic m em brane, the lateral recess m em brane. T h e gas­ g enerated m ovem ents o f fluid in the otic bulla an d in the utricuius are further transm itted through this m em brane to the lateral line neurom asts. Clupeids m ake extensive vertical m igrations an d the elastic m em branes in the bullae w ould burst if the mass o f gas in the bullae were to rem ain constant as the fish ascends and descends. T h e bulla gas, however, is coupled to th at in the sw im bladder through two rostral (forward) extensions o f the swimbladder, each only 8 J im in diam eter, although 7 -8 m m long in a 300 m m herring. As the fish ascends or descends in the water, gas flows slowly through these extensions to equilibrate the tension of the bulla m em brane (Blaxter 1980). T h e sw im bladder is directly coupled to the ear o f som e shallow an d freshw ater hearing specialists by a series o f small bones, the W eberian ossicles. D irect cou­ pling o f this sort does n o t occur in any deep-sea fishes. I f the sw im bladder o f a hearing specialist is deflated the enh an cem en t o f its hearing is lost. O n the other h an d , the hearing o f a non-specialist can be im proved m erely by inflating a small balloon very close to the head, m im icking the effects o f a coupled swimbladder. We tell the direction o f a sound from the signal delay an d the phase an d intensity differences betw een our two ears (aided in m any m am m als by m ovem ents of the

Fig. 6.7

Modes of stimulation o f the ear of a bony fish. The upper diagram shows direct stimulation of the otolith by particle displacement; the lower shows indirect stimulation, in which the gas-filled swimbladder vibrates in response to the pressure component of the same sound source and re-radiates particle displacement to the ears. (From Popper 1996, copyright Overseas Publishers Association N.V., with permission from Taylor & Francis Ltd.) Direct stimulation of the ear by particle motion set up by the sound source Otolith o rg an s o f th e ear

Indirect stimulation of the ear by re-radiation of the pressure signal by the swim bladder Otolith Sensory epithelium

THE BIOLOGY OF THE DEEP OCEAN

external pinnae). A fish can n o t use these m ethods. T h e increased speed o f sound in w ater m akes the delay too short, the generally small size o f the head relative to the w avelength m akes phase differences indistinguishable, an d the acoustic trans­ parency o f the fish prevents any acoustic shadow ing betw een the labyrinths. A typical vibration receptor organ in a fish has two large groups o f h air cells oppo­ sitely oriented so th a t each group is excited by m ovem ents in opposite directions. W ith this arran g em en t inform ation ab o u t b rief noises can be transm itted to the brain, each pressure peak being represented by the activity o f a large n u m b er o f receptors. T h e polarity is unam biguous because o f the identity o f the group o f receptors excited, and the tim e o f each peak o f com pression or decom pression is represented by the activity o f a large nu m b er o f receptors. T his allows the fish to discrim inate sound direction using the available near-field inform ation from the lateral line (which m ay be long enough to d eterm in e direction by phase differ­ ences) as well as inform ation from the different planes o f the three m aculae in the inner ear. T h e cod, for exam ple, can discrim inate sound sources 20° apart, in b oth the horizontal an d vertical planes. H um an s (in air) an d dolphins (in water) can distinguish sound sources ju st 1° ap a rt (Popper 1996).

Sound production by fishes Fish th a t can h ea r sounds have to do so against the background noise, for exam ple sw im m ing noises (especially schools o f fish), feeding noises (e.g. the rasping o f parrotfish on coral), an d the deliberate noises o f o th er animals. N o t all fishes w ith specialist h earing are sound producers, so perception o f the background acoustic ‘im age’ seems to be a valuable capability in itself. O nly a m inority o f fishes are vocal, that is intentionally producc sounds, b ut the ability is present in m any u n re­ lated groups. Fish sounds range from 50 to 5000 H z w ith m ost betw een 100 an d 800 H z. Som e m ake sounds by grinding teeth or fins together (filcfish Monacanthus an d the H acm ulidae or grunts), others force w ater o u t o f the gills (some gobies an d blennies). Still others use the sw im bladder as a drum . T rigger fishes b eat the sw im bladder w ith a fin, but m any fishes have specialized d ru m m in g muscles wirich insert directly on to the sw im bladder o r on to adjacent ossicles or ligam ents (e.g. the deep-sea m acrourids an d brotulids; gadoids such as cod, haddock, an d saithe; shallow w ater sciaenids, zeids, an d sea-robin (Prionotus)). M any o f these fishes use sounds to signal to the opposite sex an d there is often a m arked sexual dim orphism o f the d rum m in g system. In the deep sea, for exam ple, only males o f the m acrourids, o f one group o f brotulids, an d o f the ophidiid Barathrodemus have dru m m in g muscles (Fig. 6.8). Nevertheless, b o th sexes o f the m acrourids have large saccular otoliths, presum ably for detecting the sounds; species o f m acrourid th a t do not have d ru m m in g muscles have small sacculi (M arshall 1971, 1979). Toadfish m ales ‘call’ to females over long distances a n d there m ay be courtship ‘conversations’ (the goby Bathygobius soporator). T h e dru m m in g calls m ay have a territorial role as well as a sexual one. Sounds m ay also be defensive, as in the burrfish Chilomycterus, sculpins, an d the flying g u rn ard

FEELING AN D HEARING

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Fig. 6.8

Sound-producing drumming muscles (Dm) insert on to the swimbladder (Sb) and body wall in the deep-sea rattail Malacocephalus (left). Those of the brotulid M onom itopus (right) insert on to the swimbladder, the modified ribs, and the otic capsule. The capsule contains a large saccular otolith (So). (From Marshall 1962.) Dm

Dm

Malacocephalus

Monomitopus

(which spreads its spiny gill-covers at the sam e time). It is quite disconcerting to grasp a pony fish (Gazzci) an d have it g ru n t at you (and flash, C h a p te r 8); no d o u b t the effect serves similarly against m ore usual predators. T h e deep-sea fishes capable o f sound production, particularly the benthopelagic m acrourids, brotulids, a n d deep-sea cods, live ju st above the seafloor on the co n ­ tinental slopes (M arshall 1962, 1967a). In general, n eith er the pelagic n o r the abyssal relatives o f these fishes have the sam e capability. In those m acrourids, for exam ple, wrhich live at abyssal depths yet retain a swim bladder, it m ay be th at the decreased elasticity o f the sw im bladder (or the increased gas density at abyssal pressures) m akes it ineffective as a vibrator o r sound radiator. C ertainly the very high pressure w ould greatly increase the resonan t frequency. D ivers b reath in g a h elium /oxygen m ixture at dep th suffer M ickey M ouse-like vocal distortions as a result o f the increased gas density; perh ap s the calls o f these fishes w ould be sim­ ilarly distorted to a high-pitched squeak! In all these sound-producing fishes the sacculus is very large, indicating a high sensitivity to the acoustic pressure weaves. In oth er deep-sea fishes it is relatively small. T h e m ost contentious issue for som e tim e has been w h eth er fishes use the lateral line for hearing. Recordings from the lateral line nerve show th a t some fishes cer­ tainly respond to sound sources w ith frequencies up to ab o u t 200 H z in the near field, th a t is at very close range (~ 1 body length). T h e behavioural value o f these responses m ust be doubtful, however, because the lateral line will alm ost certainly

THE BIOLOGY OF THE DEEP OCEAN

already have detected the hydrodynam ic disturbance o f an anim al so close to it before it produces any sounds. N ear-field sound reception is certainly not the m ain function o f the lateral line system and. w ith one exception, far-field sound reception by the lateral line is not possible. T h e one exception (noted above) is w hen the gas in the otic capsule o f clupeid fishes transduces far-field sound pres­ sure to near-field particle displacem ent w ithin the lateral line canals. T his m ay be the basis for the ultrasound sensitivity (to 180 kHz) o f the A m erican shad w hich helps it to avoid the high-frequency echolocation pulses o f dolphins (just as some m oths can detect the ultrasound o f pred ato ry bats) (M ann el al. 1997).

Invertebrate hydrodynamic receptors Vibration receptors M ost m arine invertebrates probably sense only the near-field effects o f vibrations (Budelm ann 1989). A t the sim plest level these vibrations m ay be used to identify potential prey. A lm ost all invertebrates oth er th an the arthropods em ploy ciliated h air cells, very sim ilar to those in the fish lateral line system, as their m ech an o re­ ceptors. T hese cells have one or m ore kinocilia and, if single, the kinocilium is surrounded by a collar o f sh orter stereovilli. T h e cilia m ay project directly into the fluid or be coupled to it by insertion into a gelatinous cupula (e.g. in salps), w hich effectively amplifies an d integrates the m ovem ent o f a group o f h air cells. T h e cupula easily dissolves in fixatives so there is often d o u b t as to w hether it is norm ally present. M edusae, polyps, an d ctenophores give behavioural responses to low -frequency vibrations an d have h air cells o f this type, w hich are presum ed to be the sensory receptors. In the m edusa Aglantha the h air cells are arran g ed in row's o f different polarities. A rrow w orm s (chaetognaths) respond to a frequency o f 12 o r 30 H z (Spadella) o r 150 H z (Sagitta) by striking at the source, an d m ay prey on p articular species o f copepod by selecting th eir vibration frequencies. A rthropods have innervated setae as their prim e m echanoreceptors. C opepods have particularly long m cchanoreceptor setae on the ends o f their antennae, coupled through a flexible joint to m odified ciliary cells. T hese p articu lar recep­ tors develop early in the larval life, prim arily to initiate escape reactions by rec­ ognizing the hydrodynam ic signals generated by potential p redators (Fields and Yen 1997). T h e second use o f such setae on the antennules (usually m ore proximally sited) is for sensing the approach o f anim ate a n d inanim ate food particles draw n inw ards in the w ater currents generated by the feeding appendages (Koehl an d Stricklcr 1981; Stricldcr 1985). In Euchaeta rimana the m ale does n ot feed and, as it m atures, loses the proxim al prey-sensing setae on the antennule an d acquires chem oreccptors for sensing the female, while still retaining the predator-sensing m echanorcceptive setae at the tip (Fig. 6.9) (Boxshall et al. 1997). R ecent w ork has show n th a t copepods can also use their m echanoreceptors to follow p articu lar trails; the hydrodynam ic ‘footprint’ left by even a small organism persists for m any seconds. C opepods, for exam ple, will recognize an d follow the p ath o f a pipette

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6.9

The predatory copepod Euchaeta rimana has long mechanosensory setae at tw o loca­ tions on the antennule, forming a proximal group and a group at the distal tip. (a) The two groups are located in different components of the flow vortex. The distal ones in the outer sensory vortex (osv) are responsive to the vibrations of a potential predator and initiate an escape jump. The proximal setae, shown in (b) in a scanning electron micrograph, lie within the inner viscous vortex (ivv) and are sensitive to the vibrations of potential prey. The proximal setae are lost in non-feeding adult males. (G. A. Boxshall unpublished, after Strickler 1985.)

tip in the w ater tens o f seconds later (i.e. at ranges o f several cm). T h eir m echanoreceptors respond to vibrations at frequencies o f up to 2 kH z a n d am pli­ tudes as low as 4 nm (Boxshall 1998). T hese new findings o f long-range perception help to reconcile the fact th a t the n earest-neighbour distances in all b u t very dense aggregations (> 1 0 b copepods m 3) ap peared previously to be greater th an the m axim um range at w hich one individual could detect the presence o f an o th er (H aury an d Y am azaki 1995). G hem oreception (C hapter 7) further extends this range. T h e sensory com petence o f these anim als is clearly m uch greater th an we h ad previously recognized. Parasitic copepod larvae respond to very low frequencies (~3 Hz), sim ilar to the sw im m ing frequencies produced by their hosts. M echanoreceptive signals provide close-range inform ation w ithin the sw arm s an d schools o f krill an d o th er anim als, although the sexual gatherings of, for exam ple, sergestid shrim p an d squid m ay initially owe as m uch to scent. C opepods use a com bination o f m echanoreception an d chem oreception (C hapter 7) in their m ating encounters, d u rin g w hich they follow hydrodynam ic an d chem ical trails an d respond to p articu lar hydrodynam ic p atterns (hops) induced in females by the (chemical?) presence o f males (Boxshall 1998; Yen 2000). L arger anim als such as lobsters an d shrim p have high num bers o f m ech an o re­ ceptors, sim ilar to those in copepods, distributed over alm ost every p a rt o f the body. T h e shrim p Crnngon is m axim ally sensitive to a vibration frequency o f 170 H z, w ith a stimulus threshold corresponding to a particle displacem ent o f 700 nm . T h e sensitivities o f other crustaceans (mainly decapods) cover a frequency

THE BIOLOGY OF THE DEEP OCEAN

range o f 0 .5 -3 0 0 H z w ith a m inim um m easured displacem ent threshold o f 200 nm , although behavioural experim ents suggest the existence o f receptors w ith thresholds up to 3 orders o f m agnitude lower (i.e. sim ilar to those in fish). S hrim p such as the sergestids an d m any penaeids are im p o rtan t m em bers o f the m idw ater an d epibenthic com m unities. T h ey have very characteristic antennae, w hich consist o f a short rigid base and a long tapering filam ent, o r flagellum, bearing flexible m echanoreceptive setae on each segm ent (D enton an d G ray 1986). T h e anten n al bases are held some 45° upw ards an d outw ards from the body so that the flexible region trails parallel to, an d some w ay o u t from, the body axis on each side. E ach segm ent bears curved lateral setae w ith accessory hairs that form a tube-like arran g em en t dow n the length o f the flagellum; w ithin this setal tube lie the m echanorcccptive setae (Fig. 6.10). T h e arran g em en t provides a system for the near-field detection o f vibrating sources (just like a fish’s lateral line) while it places the detector physically n ea rer the source an d decouples it from the shrim p’s own body m ovem ents. T h e flagellum is often m uch longer th an the shrim p a n d trails well b eh in d it. Because the near-field effect has such a steep g ra­ dient o f attenuation, differences in signal am plitudes detectable along the length o f the flagellum can indicate the direction o f the source. Sergestids can probably detect the range an d position o f a vibrating object at least 20 cm distant. T h e flagellum also bears num erous chem oreceptors. Relatively little is know n ab o u t the m echanoreceptive structures o f m ost oceanic invertebrates b u t there can be no d oubt th at all anim als are well supplied with these sensory elem ents an d th a t they are likely to b e o f p articular im portance to

Fig. 6.10 Some penaeid shrimp (a) have a rigid proximal portion o f the antenna from which trails a long antennal flagellum, whose function is analogous to the lateral line of fishes. Mechanoreceptor setae are housed within a tube-like array o f curved setae (b, c) and respond to vibrations in the water. (From Denton and Gray 1986, with permission from The Royal Society.)

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the active p redators in their search for, an d identification of, p otential prey. C ephalopods (squid, cuttlefish, an d octopus) are particularly effective p redators an d have the m ost com plex arran g em en t o f ciliated sensory cells o f any inverte­ b rate (B udelm ann 1980, 1996). E ight to ten lines o f ciliated cells ru n from the back o f the h ea d on to the arm s. T h e group o f kinocilia in each cell are aligned parallel to the course o f each line an d the w hole system is closely analogous to the h ead canals o f the fish lateral line. In Sepia hatchlings an d Lolliguncula adults the cells respond w ith a threshold o f ab o u t 200 n m particle displacem ent at 75-1 0 0 H z. V ibration sensitivity has been dem onstrated in a n u m b er o f other cephalopods an d one, the oceanic squid Todarodes, is attracted to a signal fre­ quency' o f 600 H z (a response utilized by Ja p an ese squid fishermen). It seems likely' th a t this ciliated line sensory sy7stcm, only' recently identified, will be o f p a r­ ticular im portance to deep-sea species, in parallel w ith the lateral line develop­ m ent in deep-sea fishes. Predators are not, o f course, the only anim als w ith hair cells. Sim ilar receptors have been recognized in filter feeders such as the tunicate Ciona an d the planktonic larvacean Oikopleura.

Statocysts Statocysts occur in a great many' invertebrates, from ctenophores an d m edusae to squid an d shrim p. M ost seem to be primarily' equilibrium (gravity) receptors b u t some are elaborately m odified to sense acceleration an d perh ap s even sounds. T h e statocysts o f decapod crustaceans take various form s (a simple bowl or a three-dim ensional canal sy'stcm) a n d are sensitive to angular acceleration, as are those o f mysids. T h e m ost elaborate equilibrium recep to r system am ong the invertebrates is th a t o f the cephalopods, whose statocysts consist o f fluid-filled cavities (B udelm ann 1996). W ithin these cavities rows o f h air cells form a ridge or crista w hich w inds ro u n d the cavity so th a t it covers all three orthogonal planes. E ach crista is subdivided into sections, four in squid an d nine in octopods. E ach section has its own cupula into w hich the elongated row's o f h air cell kinocilia are inserted. E ach row' is polarized to respond to m ovem ent only' in one direction, across th e axis o f the crista, an d every crista section has row's o f h air cells p o lar­ ized in opposite directions. F luid m ovem ents resulting from an g u lar or linear acceleration act on the cupulae a n d b en d the kinocilia. T h e organization a n d size o f the statocysts reflect the lifestyle o f their ow'ners. Large statocysts arc m ore sensitive to gravity an d acceleration an d are present in slow-moving species, w hereas small statocysts are less sensitive an d m ore fre­ quently found in fast-m oving species. T h e activities o f the h air cells an d the affer­ ent first-order neurons linked to them are m odulated from the b rain by an efferent innervation, w'hich is largely inhibitory. T h e system has an ex trao rd in ary conver­ gence w ith that o f fishes. In squid additional control o f roll an d pitch betw een the h ead a n d body7 is achieved by7 the activity o f hair cells arran g ed in lines on the dorsal side o f the neck an d polarized to respond in either the longitudinal or transverse body axis.

THE BIOLOG Y OF THE DEEP OCEAN

T h e gravity receptors o f cephalopods, an d the statocysts o f decapods an d mysids, have the potential to respond directly7 to the pressure wave com p o n en t o f v ib ra­ tions in the w ater by virtue o f the coupling o f the recep to r cells to the dense sta­ toliths, Som e experim ental studies have dem onstrated a vibration response in the crayfish statocy7st (at frequencies below 200 Hz) an d the cephalopod statocy7st also responds to vibrational stimuli. Several species o f decapod crustaceans m ake sounds. A m ong these are the crayfish Palinurus w ith a frequency7spectrum extend­ ing to 9 kH z (produced by stridulation w ith the base o f the antenna) a n d species o f snapping shrim p (Alpheidae) w hich produce a loud (20 N m 2 at 1 m) b ro ad ­ b an d noise (with a frequency range o f up to 9 kHz) by snapping the m oveable ‘finger’ o f the claw on to the im m ovable ‘th u m b ’. A rgum ents ab o u t w hether squid or other anim als can ‘h e a r’ d ep en d largely on the definition o f u n derw ater hearing. I f the ability is defined as a direct sensitivity to the far-field pressure wave com ponent o f a vibration (through shear at the sta­ tolith), then these anim als probably can hear. I f h earin g has to involve the tran s­ duction an d am plification o f the pressure wave by a gas bladder, th en they cannot. T his is despite the fact that cuttlefish an d som e o th er cephalopods (e.g. Nautilus an d the oceanic squid Spirula) do contain gas cham bers. T h e ir gas spaces are enclosed in rigid shells that can n o t vibrate an d are used solely for buoy7ancy control (C hapter 5). Som e siphonophores do have flexible gas bladders an d could potentially ‘h e a r’ w ith them , b u t there is no inform ation yet concerning the m echanoreceptors in these anim als, let alone ones linked in any w ay to the gas bladders. Sucker receptors in cephalopods have also been described. A lthough their func­ tion has not been clearly7 identified it is probable th at they are involved in touch discrim ination an d touch learning, skills for w hich the cephalopods are renow ned.

Sounds of marine mammals M arine m am m als contribute considerably to the acoustic b ackground o f the deep ocean. M ost m arine m am m als are noisily7vocal, b ut those th a t spend tim e ashore (e.g. seals an d sealions) ten d to concentrate their sound pro d u ctio n on this phase o f their life. T his is because the requirem ents o f sound p ro d u ctio n in air an d w ater are very different an d they7 have settled for a system th at works best in air (where m ost o f the social period o f their lives is spent) an d w hich involves the larynx a n d vocal chords as in terrestrial m am m als. Nevertheless, som e o f them are know n to have additional repertoires o f u n d erw ater calls. D olphins an d whales (cetaceans) spend their entire lives in the ocean y7ct rem ain highly vocal anim als (Evans 1987). Som e o f their sounds are loud enough to be h ea rd by h um an listeners out o f the water, but this is a chance feature o f a very com plex system exquisitely ad ap ted to their aquatic lifesty'le. T h ey do n o t have vocal chords, though they do, o f course, have lungs a n d a larynx. It is a hum bling fact th a t m ost nineteenth-century7 zoologists dogm atically assum ed th at the lack of vocal chords m ean t th a t cetaceans w ere m ute an d arrogantly discounted the frequent reports to the co ntrary from m ore know ledgeable fisherm en.

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T h e developm ent o f sensitive hydrophones, stim ulated by the m ilitary needs for u n derw ater surveillance, has opened ou r ears to the variety an d com plexity o f cetacean sounds. At the sam e tim e the intelligence o f these anim als has enabled us to ask them questions (albeit very' clumsily, thro u g h train in g program m es w ith captive animals), w hich have show n us some o f the subtleties o f th eir vocal an d auditory skills an d their associated cognitive abilities. It now appears th a t all cetaceans use som e form o f social sound com m unication a n d th at the odontocetes (toothed whales an d dolphins) additionally use sound for echolocation (and possibly for stunning o r disorienting prey) (Au 2000). T h e sounds o f baleen whales (mysticetes) are best know n th ro u g h the publicity given to the eerie ‘songs’ o f the h um pback w'hale (a recording o f w hich was sent w ith the Voyager interplanetary mission) an d the grow ing realization o f their individuality. T hese w hales m ake relatively low -frequency sounds (40 H z to 5 kHz), variously described as ‘m o an s’, ‘groans’, Svails’, ‘scream s’, an d ‘screeches’ (Clark 1990). O nly m ales ‘sing’ an d the singing is lim ited to the breeding grounds. T h e songs are very repetitive, whales from different areas have recognizably dif­ ferent ‘dialects’ an d individuals can be recognized by their unique voices. T h e songs are continually changing an d an entire song is changed after ab o u t 8 years. Songs last for 5 -3 5 m inutes, an d m ay be repeated alm ost w ithout pause for hours at a time. Som e 20 basic ‘syllables’ have been identified; syllables are gro u p ed into repeating sequences called ‘phrases’ an d groups o f sim ilar phrases m ake up a lim ited nu m b er o f basic ‘them es’. R ecent studies o f A ustralian populations have show n th at cultural changes can occur: an east coast population replaced their previous song w ith one le arn t from west coast m igrants. T h e sounds are very loud an d can certainly be h ea rd for tens o f kilometres. U n d er m ost circum stances the sound range w ould be lim ited by reduction o f the intensity through spherical spreading an d by reflection off the surfacc or b o tto m o f the sea. T h e re is one physical situation w here this does not occur, know n as the SO FA R channel (SO und Fixing A nd Ranging). S ound o f a given frequency em itted in this p articular layer will be rcfractcd b o th dow nw ards by the w ater mass above an d upw ards by the w ater mass below, thus confining it w ithin the layer a n d preventing any reflective losses. A n intense sound at this dep th has the potential to travel h u n ­ dreds, p erh ap s thousands, o f kilom etres an d still be loud enough to be heard. It has even been suggested th a t a hum p b ack w hale ‘singing’ into this channel in the n o rth ern hem isphere w ith low -frequency sound (which has the lowest atten u atio n rate) m ight be h ea rd by other hum pbacks in the S o u th ern O cean! It is as if the w'hale is calling dow n a very long tube. H ighly speculative th o u g h this suggestion still is, it docs em phasize the potential for acoustic com m unication open to these anim als. Fin whales have been observed to change direction in response to calls from other individuals several kilom etres distant. T oothed whales (odontocctes), w hich com prise narw hal, dolphins, porpoises, sperm whales, killer whales, pilot an d w hite whales, m ake sounds consisting o f whistle-like squeals an d clicks (with frequencies o f 10—300 kH z an d signal d u ra ­ tions ranging from several m inutes to a few tens o f microseconds). T h e clicks are

THE BIOLOGY OF THE DEEP OCEAN

produced singly or in bursts at repetition rates o f up to 1500 H z an d they have been described as ‘creaks’, ‘barks’, an d ‘snores’. T h e squeals seem to be used for individual com m unication while the clicks are the basis for echolocation. T h eir ability was only discovered in the late 1940s, an d even by 1967 there were only two spccics, the h arb o u r porpoise an d A tlantic bottlenose dolphin, know n to use echolocation. It is now known to be a w idespread ability o f this group of cetaceans (Au 1993). It is used in ju st the sam e w ay as bats use sound, w ith an increasingly rap id production o f clicks as a target or obstacle is approached. Sounds are only reflected efficiently by objects larger th an the w avelength o f the sound; bats an d dolphins echolocate using sim ilar frequency ranges b ut the longer w avelength in w ater m eans th a t dolphins can n o t detect insect-sized objects. T h e intensity o f an echo is inversely proportional to the fourth pow er o f the wave­ length; an echo in air at a given frequency is thus 4.34 (= 342) tim es stronger th an one in water. T h e echo intensity from a spherical object is also directly p ro p o r­ tional to the sixth pow er o f the object’s radius. E cholocating aquatic anim als m ust therefore either h u n t larger prey th a n bats or, in theory, use higher frequencies (but these w'ould have a g reater attenuation). T rained dolphins an d killer whales, w ith their eyes covered by soft suction cups, have show n quite rem arkable skill in discrim inating betw een targets o f very sim ilar size, shape, an d texture. T hese tests only indicate an isolated skill, w hich w ould norm ally be used as p a rt o f a w ider repertoire, m uch o f it learn ed through experience or perhaps through com m unication w ith others o f the sam e species. ‘E m otional state’ (as we u n derstand it) m ay also affect the an im al’s discrim inatory perform ance a n d be reflected in its social com m unication sounds. T h e lack o f vocal chords has posed no hin d ran ce to cetaceans in their sound production, b u t the precise alternative m echanism s are n ot yet clear. T h e larynx contains m em branous cartilages that can probably be m ade to vibrate an d the blowhole lips are som etim es seen vibrating at the sam e tim e as sounds are being produced. D olphins focus the sound by refraction through the fat-filled ‘m elon’ on the front o f the dolphin head, producing a narro w an d intense sound beam . T h e retu rn in g echo is channelled to the acoustically isolated inner car by oilfilled sinuses in the lower jaw (Fig 6.11). It is assum ed th at sim ilar focusing occurs in the sperm w hale, w hich has a huge reservoir o f sperm aceti oil at the front o f the head; this m ay also be used for buoyancy control (sec C h a p te r 5). S tranded whales have been reported to em it very intense sound beam s, pow er­ ful enough to feel like a physical blow. T his has led to speculation th at sperm whales m ay use an intense burst o f sound to stun their prey (largely squid) b ut there is no direct evidence that this can be achieved or is even attem pted. S perm whales are probably the deepest-diving whales a n d m ay be able to com m unicate over long distances. W hen diving they7em it clicks w ith distinctive repetition rates (or codas) m ore o r less continuously, perhaps for echolocation. T h e clicks m ay also have a com m unication role; one -whale will answ er an o th er w ith the same coda an d different populations have different codas. It is also possible th a t males m ay be able to assess each others relative size by the pulse characteristics in the signals.

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Fig. 6.11 The outgoing acoustic signals of dolphins are focused through the fat-filled melon; the incoming echoes are transmitted to the bulla of the ear through a fatty acoustic channel in the lower jaw. (From Evans 1987 © Chryalis Books.)

Electroreception and magnetic cues T h e oceans contain a great m any sources o f electric a n d electrom agnetic fields. As a result o f their breathing an d sw im m ing m ovem ents m ost anim als produce a w eak D C field (in one direction) an d m any also generate an A C field (in altern at­ ing directions). N ot surprisingly, a nu m b er o f fishes have acquired electrorecep­ tors, w hich give them the ability to sense some o f these signals. All elasm obranchs an d som e teleosts have specialized organs capable o f detecting w-eak electric cu r­ rents. T h ey take the form o f either am pullary or tuberous organs, w hich are scat­ tered over the head a n d /o r body an d are clearly derived from neurom asts (Fig. 6,1). Ampullary- organs in elasm obranchs, the ratfish Hydrolagus colliei, an d the m arine catfish Plotosus anguillaris are know n as the am pullae o f Lorenzini, an d are usually arran g ed in clusters on the head, an terio r body, an d pectoral fins. T h e am pullae are lined w ith a sensory epithelium containing h air cell receptors b earing kinocilia an d are connected to the surface by a very long (5 -150 mm) jelly-filled canal. T h e receptors give long-lasting responses to low -frequency stimuli. Ampullary- organs also occur in some teleosts (mostly freshwater, w ith m uch shorter jelly canals) a n d am phibians, and, as in the elasm obranchs, are n o t restricted to species w ith their own electric organs. T uberous organs occur only in certain families o f weakly electric freshw ater fishes; they are ep id erm al capsules w ith a sensory' epithelium b u t arc not connected to the exterior an d arc 3 -4 orders o f m agnitude less sensitive th an am pullary organs. T h e receptors give b rief responses to the continuous, weak, high-frequency signals em itted by the fish an d are used in social com m unication an d objcct location (electrolocation).

THE BIOLOG Y OF THE DEEP OCEAN

E lasm obranchs respond to the w eak electric fields o f prey species an d to the e a rth ’s m agnetic field (K alm ijn 1982). In skates an d rays the am pullae o f L orenzini arc m ainly ventrally distributed, com pensating for the reduced visual input ben eath the flattened body. T his is n ot the case in the m ore conical-shaped sharks. T h e size o f the am pullae in different species o f skates increases with habitat dep th from the surface to 2000 m. Similarly, the deeper-living individuals o f one species (Raja radiata, w hich has a d ep th range o f 50—850 m) have larger am pullae, particularly those ro u n d the m o u th (Raschi a n d A dam s 1988). T h e electroreceptors probably assist in accurately directing the feeding strike. All skates also have electric organs along the tail th at produce w eak interm itten t dis­ charges. T h e discharges can be detected by the fish’s ow n electroreceptors and m ay have a com m unicative role because th eir rate increases w'hen two individu­ als m eet. T h e discharges o f the electric ray Torpedo are m uch stronger (they can produce b rief shocks o f up to 50 am ps o f current) an d are delivered to stun its prey o r as a defencc. They, a n d the stargazer fish Astroscopus y-graecum, produce volleys o f discharges. All these electric organs arc derived from m odified muscle. Sharks an d dogfish will attack buried prey, even w hen deprived o f any visual or chem ical cues to the prey ’s position. Prev species generate w eak electrical fields, w hich the sharks detect. T h e 1-m-long dogfish Mustelus cards will selectively strike a t dipole fields o f up to 8 H z, a n d D C from ranges o f up to 0.5 m, indicating a sensitivity o f ab o u t 10 nV cm 1 (equivalent to the voltage g rad ien t generated by a 1.5-volt b attery w ith its poles 1500 km apart!). T h e blue shark Prionace glauca also selectively attacks electrodes that sim ulate the signals o f prey. T h e feeding o f these fishes tends to be initiated by long-range o d o u r cues, w hich guide the approach, but the final attack is directed by the clectroreceptors. In the absence o f visual cues, deep-sea sharks are likely to be m ore reliant on th eir electroreceptors th an shallow er species. T h e rem arkable sensitivity can only be m ain tain ed by filtering out the electric ‘noise’ generated by the anim als themselves; this appears to be done centrally in the hindbrain. T h e electric field itself gives no inform ation on the direction o f the source; this inform ation only becom es available w hen the shark moves through the field. T h e electric fields produced by ocean currents a n d by elasm obranchs themselves as they move through the e a rth ’s m agnetic field are well w ithin the detection range o f their clectroreceptors. T h e induced voltage gradients d ep en d on the direction the shark is heading an d could potentially be used as an electrom agnetic compass. T h e stingray Urolophus halleri can be train ed to choose betw een m agnetic east an d west in fields o f sim ilar m agnitude to those pro d u ced by oceanic cu r­ rents, so m agnetic orientation in the ocean is quite possible. H am m erh ea d sharks ap p e ar to use m agnetic intensity gradients to retu rn to the sam e area on seam ounts each night. Turtles achieve rem arkable feats o f navigation w hen they retu rn to their nesting beaches from feeding grounds som etim es thousands of kilom etres distant. Satellite tracking has show n th at individuals travel in nearly straight lines d uring these m igrations. H atchling loggerhead turtles can distin­ guish bo th betw een different m agnetic inclination angles an d betw een the m ag­ netic field intensities they w ould encounter during the m igrations. T h ese field

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differences m ight be used to follow m agnetic pathways, as has been suggested for som e m igrating whales an d dolphins, o r even to learn the gradients in these two features a n d develop a m agnetic tw o-coordinate m ap for use in the long-distance adult m igrations (L ohm ann an d L o h m an n 1996). M agnetic m aterial, possibly m agnetite, has been found in the brains o f several whales an d dolphins so it is possible that these anim als, too, can use the e a rth ’s m agnetic field for navigation purposes. A correlation betw een the strandings of cetaceans an d the m agnetic field lines intersecting the coast has also been sug­ gested. Spiny lobsters, too, respond to experim ental changes in the m agnetic field an d m ay use the capability for hom ing or m igrations.

Conclusion M echanoreception in the ocean is m uch m ore th a n a simple contact sensory system. It provides an organism w ith detailed knowledge o f b o th its own position an d velocity in space an d its relation to others, both close by an d at great distance. T h e evolution o f hair cells has resulted in sim ilar structures in m any different groups o f anim als, subserving a quite rem arkable repertoire o f activities. H air cells in the lateral line an d its analogues m onitor the near-field environm ent to d eterm ine in m any cases n o t only the existence o f a vibration b u t also its am pli­ tude a n d direction. In the inner ear, o r its equivalent, bundles o f h air cells act as far-field detectors o f sound pressure a n d /o r as accelerom eters; the two systems are intim ately linked in p articu lar fishes such as the clupeids. A nim als th at produce their own sound signals exploit the discrim inatory capabilities o f h air cell systems to listen to conspecifics, an d others have extended th eir use to the detec­ tion o f electrom agnetic waves for b oth prey detection an d navigation. In general, aquatic anim als are m ost sensitive to near-field (particle displacem ent) acoustic inform ation, in contrast to terrestrial anim als w hich d ep en d largely on far-field (pressure wave) inform ation. H ydrodynam ic signals last m uch longer in w ater th a n they do in air. T h ey can provide detailed inform ation ab o u t the identity an d recent spatial history o f an o th er organism . Wc are ju st beginning to realize how' widely they are exploited by the anim als o f the open ocean; there is every' likelihood th at the deep-sea fauna is far m ore aw are o f their value th an we have yet recognized.

Chemical messages

or smell? T h e oceanic habitat is aw ash w ith organic com pounds released deliberately or accidentally by the organism s th at live w ithin it. Seaw ater n ot only bathes the outer surface o f an organism but in m ost m ulticellular anim als it also travels through it, dow n the gut lum en. Every' living organism is effectively a leaky bag o f organic molecules, w ith survival being d ep en d en t upon achieving the right balance o f m olecular input and output, b oth qualitatively an d quantitatively. Each m olecule cast into the w aters has the potential o f a message in a bottle: it contains or encodes inform ation about the source. It rem ains only potential until the message has been bo th read an d understood (decoded), at w hich p o in t the inform ation becom es useful. C hem orcception is all ab o u t m axim izing the inform ation value o f this m olecular soup. As large anim als in a terrestrial environm ent we are accustom ed to distinguish­ ing clearly betw een taste an d smell. T h e form er is a ‘co n tact’ sensation an d the latter a ‘distance’ one, dep en d en t on the volatility o f od o u r m olecules in the air. T his distinction is m uch less clear in w ater w'here the senses o f taste, touch, an d smell form a b road continuum (Atem a 1980). Som e scientists prefer the concept o f a ‘com m on’ chem ical sense, while recognizing th at there are different reflexes an d learning-associated behaviours generic ally ascribable to ‘taste’ and to ‘sm ell’. Smell is the distance sense, on the basis o f w hich behavioural decisions arc m ade, largely ab o u t m ovem ent to or from the source; taste is the local sense on w hich actions (e.g. feeding) arc taken. T h e difference can be sum m ed up in the aphorism ‘Taste acts, smell thinks’. In the larger, m ore active anim als (e.g. fish, squid, and shrimps) long-range chem ical inform ation is particularly valu­ able because their sw im m ing pow ers give them the potential ability to reach a distant source; consequently, special organ systems for smell (olfaction) can som etim es be recognized. Fish, in particular, have nasal capsules containing sep­ arate olfactory lamellae, whose degree o f elaboration gives an indication o f the relative im portance o f olfaction in the lives o f different species a n d /o r sexes (M arshall 19676, 1979).

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Chemical cues and receptors C hem ical cues can be used for m any different purposes an d affect m any different behaviours (Bakus et al. 1986; R ittschoff an d B onaventura 1986; Z im m er an d B utm an 2000). T h e m ost basic o f these is in feeding, including b o th food o r prey recognition an d p red a to r deterrence. H om ing, settlem ent, an d m ain ten an ce of symbiotic associations provide o th e r crucial roles for chem orcception, while intraspecific chem ically-m ediated behaviours involve social interactions, espe­ cially sexual behaviour. Sexual functions include b o th sexual attraction an d recog­ nition betw een individuals and, w here gam etes arc broadcast into the water, the chem ical recognition o f an egg by the appropriate sperm . C hem icals p roduced specifically for their com m unicative value are know n as allom ones; they arc divis­ ible into kairom oncs, w hich act on other species, an d pherom ones, w hich are for intraspccific signalling (Larsson an d D odson 1993). C hem oreceptors have close affinities w ith m echanoreceptors. M ost identified chem orcceptor cells end in cilia an d the)' m ay occur anyw here on the anim al, often in very large num bers (one estim ate puts the n u m b er o f ch em oreccptor cclls in a m edium -sized lobster at ab o u t 1 million) (Laverack 1988). T h e cilia m ay be little or greatly m odified an d it is quite possible th a t som e recep to r cells m ay have dual roles as chem o- and m echanoreceptors. C rustacean aesthetascs occur on the antennules an d are am ong the m ost characteristic chem oreceptors (Fig. 7.1), being thin-w alled u n ta n n ed cuticular setae ending in a cilium an d having up to several h u n d red associated nerve fibres. O th e r crustacean chem oreceptors m ay have only two o r three nerve fibres. Som e chem oreceptors are sensitive only to one particu lar com pound; others respond to a w ide variety o f substances. T h e olfactory epithelium in the organs o f some anim als (fishes, sea-slugs, etc.) m ay form hugely expanded lam ellae (evocatively described in a deep-sea fish by N. B. M arshall as like ‘a sprig o f broccoli’) and be so placed th a t a cu rren t o f w ater passes alm ost continuously across it.

Feeding T h e only certain evidence for chem oreception is the experim ental dem onstration o f behavioural o r neurophysiological responses to specific stimuli. N o t surpris­ ingly, there is very little such evidence for deep-sea anim als. Nevertheless, th ere is com pelling evidence for food recognition bv m eans o f distance chem oreception at abyssal depths (to 5000 m). T his com cs from the studies w ith b aited tim e-lapse an d video cam cras w hich show a rap id aggregation o f scavenging anim als aro u n d a bait package, ranging from w idely-foraging hagfishes, sy naphobranchid eels, an d m acrourid fishes to crabs, shrim ps, an d am phipods (Fig. 7.2). T h e cam cras show' that these scavengers arrive upcurrent, following the dow nstream odour plum e from the bait.

THE BIOLOGY OF THE DEEP OCEAN

150

Fig. 7.1

Crustacean aesthetascs are pore-bearing setae that function as chemoreceptors. This aesthetasc is from the deep-sea copepod Misophria; note the more typical mechanical setae inserted above and below. (Photo: G. A. Boxshall.)

Fig. 7.2

Many animals use chemoreception to find food-falls in the deep sea. At this site at 900 m off the Falkland Islands squid carcasses tied to the cross-bar have attracted a writhing mass of hagfish. (Photo: I. G. Priede/M. Collins.)

Studies o f captu red am phipods o f the gen era Orchomene an d Paralicella suggest an additional twist to this behaviour. W hen they are exposed to bait o d o u r they show a rapid increase in oxygen consum ption lasting up to 8 hours. T hese anim als arc probably able to w ithstand long periods o f relative starvation by entering a resting

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state o f m etabolic torpor. T h e chem ical cues w afting past th em from a food-fall trigger in them a state o f heightened m etabolic arousal an d allow them to locate the food source rapidly an d m axim ize their energy consum ption (Smith an d Baldw in 1982). Indeed they ap p ear on the bait w ithin 30 to 40 m inutes o f its arrival on the bottom . T h e alerting effect o f the o d o u r is analogous to its effect on the free neurom ast responses o f some fishes (C h ap ter 6). Studies o f several o ther species o f Orckomene have show'n th a t the olfactory receptors or aesthetascs occur prim arily on the antennae, while taste receptors are widely distributed on the m outhparts a n d thoracic lim bs (K aufm ann 1994). Larger anim als such as m acrourid fishes probably u ndertake m ore active forag­ ing. T h ey can be induced to swallow acoustic tags h idden in the b ait an d the m ovem ents o f individuals can subsequently be followed for several days. T h ey do not rem ain in the vicinity o f the bait for long, apparently m oving off to forage further afield as the com petition at the b ait increases from later arrivals, an d the likelihood o f a net energy gain decreases rapidly. C ounts o f the nerve fibres in the olfactory an d optic nerves o f rattails show' that, despite their large eyes, there are 3 -4 tim es as m any olfactory fibres as there are optic ones. T his ratio is sim ilar to th a t in the catfish; clearly, olfactory inform ation plays a key role in the lives o f b o th these bottom -living fishes (H ara 1993, 1994). R ecent studies have dem onstrated th a t copepods can discrim inate very effectively betw een different species o f phytoplankton, an d th a t the discrim ination is partly chem osensory (Koehl an d Strickler 1981; Cowles et al. 1988). In Pleuromamma xiphias the anten n ae have m echanoreceptors only at the distal tips w hereas chem oreceptors an d ‘m ixed m odality’ receptors are m ost ab u n d an t on the prox­ im al third o f the antenna. M ixed m odality receptors arc p resu m ed to com bine b o th m echano- an d chem oreception a n d the w hole suite o f receptors is used to discrim inate betw een oncom ing particles (Lenz et al. 1996). C opepods can enhance the reception o f a chem ical signal by providing a suitable flow' field ro u n d the anten n al receptors. Lobsters sit quietly an d sam ple the w ater w ith flick­ ing m ovem ents o f their antennae, resetting the chem oreceptors on th em by p eri­ odically clearing the w ater (and chem ical stimuli) en train ed ro u n d them . C opepods create flow fields w ith their appendages a n d move as a w hole through the w'ater, so th a t there is a lam in ar flow ‘scanning cu rre n t’ across the array o f chem oscnsors. In an om nivore such as Pleuromamma xiphias a high-shear flow’ field distorts the od o u r structure ro u n d a food particle, so the chcm oreceptors are able to give the copepod advance w arning o f the food’s appro ach (Figs 7.3, 7.4). C arnivorous copepods, such as Euchaeta rimana, have low -shcar feeding currents. T hese currents still tran sp o rt chem ical stimuli but the low shear reduces the scope for rem ote chem oreception (M oore et al. 1999). T his is p robably the trad e-o ff for m inim izing the cu rren t so th a t its hydrodynam ic signal does n o t w arn m echanosensitive prey (Boxshall 1998). T h ere is an interesting parallel betw een the m ixed m odality receptors in copepods an d the presence o f specialized m echanoreceptive neurom asts associated with the olfactory organs o f m any fishes, including the deep-sea Poromitra. M ixcd-funetion

THE BIOLOG Y OF THE DEEP OCEAN

152

Fig. 7.3

Diagram o f the potential changes in odour structure (shaded circles) surrounding an algal cell (black spot) as it is approached by a copepod under (a) no shear and (b) sheared flow conditions. The motion of the copepod (thick arrows) and that o f the water (thin arrows) are indicated. (From M oore et al. 1999 with permission.)

Fig. 7.4

A flow diagram o f a chemosensory model, with a mechanosensory component, illustrates possible feeding responses to different sensory stimuli in a copepod feeding on phyto­ plankton and zooplankton. (M odified from Mauchline 1998, with permission, after Poulet et al. 1986.)

Zooplankton

Phvloplankton

D istu rb an ce/ tu rb u len ce/sh ear

Chemoreceptors

R e cep to r signal

None

Positive

Positive Negative

Passive Passive ingestion ingestion

Rejection / avoidancc

Passive ingestion

Selective capture

Negative

Escape reaction

receptors, o r groups o f receptors com bining b oth m cchanorcceptivc an d chcm oreceptive functions, m ay well be m ore w idespread. O bservations such as those noted above do n o t nents o f the chem ical cocktail from the bait behaviour. Som e experim ents clearly im plicate sergestid shrim p Acetes have been observed to

indicate precisely w hich com po­ o r food are responsible for the am ino acids. Individuals o f the follow' specific chem ical ‘trails’.

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Particles o f food or o f p ap e r soaked in particu lar am ino acids (alanine, m eth io ­ nine, or leucine) w ere m arked w ith dye an d then dro p p ed experim entally in a large aq u ariu m containing the shrim p. D uring ran d o m sw im m ing m ovem ents the shrim p encountered the particle pathw ay (made visible to the observer as a thin th read o f dye) an d im m ediately followed the trail dow nw ards tow ards the source. In this case they were not following a concentration g rad ien t because they only tracked dow nw ards, even if th e particle was experim entally draw n upw ards (H am ner an d H a m n e r 1977). T h e copepod Temora can detect certain am ino acids at concentrations o f 10 '—10 8 м an d is able to recognize the chem ­ ical trail left by a sinking particlc (e.g. o f m arine snow) in just the sam e w ay as Acetes, but does follow the concentration gradient. T h e giant deep-sea mysid Gnathophausia (which can be m ain tain ed in the laboratory for over a year) is also sensitive to particu lar am ino acids at concentrations as low as 10-12 M, while euphausiids (krill) are stim ulated to feed by com pounds such as histidine (10 ’m) an d organic acids (H am ner et al. 1983). A huge range o f com pounds can stim ulate feeding behaviours in different shallow -w ater species. M ost o f the studies have been done w ith low m olecular w eight com pounds such as am ino acids, q u atern ary am m o n iu m com pounds (such as betainc), inosine, nucleotidcs, and organic acids, b ut there is also good evidence for sensitivity to m acrom olecules such as proteins (and peptides), m ucopolysaccharides, lectins, an d glycoproteins. In addition, there m ay be syner­ gistic or antagonistic effects betw een different com pounds, providing an alm ost infinite range o f possible sensitivities in different species (H ara 1993, 1994). T h e experim ental evidence from anim als such as lobsters suggests a very specific exci­ tatory response from each rcceptor, often to ju st a single am ino acid, although it is still uncertain how com plex m ixtures are recognized neurally. T h e reccptors can respond to short (100 ms) pulses o f am ino acids at rates o f up to 4 H z. T h ere is considerable plasticity in the search im age an d it is clear th at previous food experience plays an im p o rtan t role in adjusting sensitivity. T his should be o f no surprise, considering the cultural differences in our own enthusiasm s for different food items an d ou r changes in food preferences from child to adult.

Chemical defences Ju st as the excretions or secretions o f one organism m ay stim ulate the chem oreccptors o f an o th er a n d initiate feeding, so m ay sim ilar products act as feeding deterrents or toxins. C hem ical defences are w idespread in shallow -w ater species, particularly am ong sessile organism s w hich can n o t flee from p red ato rs an d are com peting w ith each o th e r for space. Such com petition an d chem ical defencc is probably equally w idespread in the open ocean an d the deep sea (Wolfe 2000). T h e pressure for p redators to increase the variety o f acceptable prey in a foodlim ited environm ent like the deep sea has probably resulted in a concom itant developm ent o f chem ical m eans o f defence by prey species. In shallow -w ater species it is know n th at toxins an d feeding deterrents in soft-bodied anim als such

THE BIOLOGY OF THE DEEP OCEAN

as soft corals, nudibranchs (cf. Glaucus, C h a p te r 5), an d holothurians are often m etabolites derived from the food, particularly o f algal or b acterial origin. H olothurians, in particular, are ab u n d a n t— often d o m in an t— m em bers o f the deep-sea benthos an d m ay well rely on sim ilar chem ical defence m echanism s. Algal m etabolites affect the suitability o f different phytoplankton spccies as food for grazing copepods. C opepods can not only select different types o f particle b ut also detect qualitative differences betw een individual phytoplankton cells o f the sam e species, presum ably by chem oreception. Acartia tonsa has twice the ingestion rate on fast-grow ing cells o f Thalassiosira weissflogi as on slow'-growing cells at the sam e concentrations, an d can select the faster-grow ing cells in m ixtures o f the two (Cowles et al. 1988). C hem oreception is o f p articu lar im portance in particle dis­ crim ination by herbivores; carnivorous copepods are m ore d ep en d en t upon m echanoreception an d recognition o f the hydrodynam ic disturbances p ro d u ced by prey species (Fig. 7.4). Toxic com pounds in some species o f diatom s, dinofla­ gellates, an d cyanobactcria m ay reducc the grow th rate a n d /o r fecundity or sperm quality o f grazing copcpods, an d could therefore affect the level o f sec­ o ndary production according to their abun d an ce (Wolfe 2000). It is probable that these com pounds have a chcm orcceptor-m ediated inhibitory effect on the feeding activities o f the grazers. Defensive secretions m ay have an alarm function in alerting conspecifics to danger an d in attracting secondary p red ato rs (the ‘b u rg lar ala rm ’ function). T hese responses have been reported from a wide range o f b o th vertebrates an d invertebrates. It has already been noted (C hapter 4) th a t chem ical signals from predators can induce changes in the p attern o f diel vertical m igration behaviour in zooplankton prey. Squid ink contains L -dopa an d dopam ine, an d squid chem oreceptors respond to bo th these com pounds, the result being je ttin g escapc responses. T h e ink o f one squid will therefore w'arn others. It probably has oth er effects, if the observations on octopus arc any indication. T h e ink o f this anim al is recognized not only by its potential p rey the lobster, b u t also by the octopus’ predator, the m oray eel. C hem oreception o f the sam e com p o u n d m ay therefore induce very different behaviours in different species.

Signal range and sex pheromones O nce released, a chcm ical signal is largely beyond the control o f the relcaser, ju st like the m essage in the bottle. In air, volatile com pounds disperse very rapidly but insect pherom ones can nevertheless be detected over distances o f 1 km or m ore. Som e (aerial) m arine chem icals can be perceived at long range: A ntarctic storm petrels feed on zooplankton and are attracted by dim ethyl sulphide (DMS), a volatile chem ical produced by phytoplankton in response to zooplankton grazing. D M S is also involved in clim ate m odulation (Brigg 2000). In the oceans m olecu­ lar diffusivities are hundreds or thousands o f times low er th a n in air and in the deep ocean turbulent diffusion is also generally low. Below the direct surfacc effccts o f w ind m ixing the ocean has a structure ra th e r like a loose pile o f papers,

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w ith thin layers o f w ater stacked one below the oth er in increasing o rd er o f their density, an d sliding slowly over each other. T h e result o f this layering, a n d o f the rel­ atively slow m olecular diffusion, is th a t small m olecular messages released at d epth will spread out slowly, m ore in two dim ensions th a n in three (cf. w hale calls in the SO FA R channel, C h a p te r 6), an d retain th eir identity over longer tim e periods. T h e structure o f the chem ical ‘p lu m e’ th a t trails dow nstream from a source o f food or a m ate will influence the range at w hich it can be detected an d determ in e w hether there is an adequate directional gradient for a recipient to follow. Very little is know n o f plum e shape in situ b u t laboratory w ork suggests th a t there is consider­ able small-scale spatial structure even in conditions o f m inim um turbulence (Zim m er-Faust 1989; Vickers 2000; Z im m er a n d B utm an 2000). C hem ical messages are the only ones th a t can be left b eh in d by an anim al, th a t is th a t continue to wrork (retain their inform ation content) b o th long after their release a n d at considerable range. In conditions w here individuals o f a species m ay be few an d far betw een, chem ical messages can m ake it m uch easier to search for a m ate. U nfortunately, b u t not surprisingly, direct observations o f these sorts o f p herom onc-induced behaviours in the deep o cean are totally lacking. T h ere are, however, observations o f shallow -w ater crustaceans such as copepods, am phipods, an d decapods th a t indicate pherom one-initiated behaviours (K atona 1973; Boxshall 1998). E laborate sw im m ing p attern s w ere induced in m ales o f the copcpods Calanus a n d Pseudocalanus by exposing th em to w ater p reconditioned by adult females, an d organic m aterial from radioactively labelled females w’as taken up preferentially by the aesthetascs (chem oreceptors) o f m ales (Griffiths an d Frost 1976). T h e sam e results w ere achieved in sim ilar experim ents w ith am phipods. T h e interpretation is th a t a phero m o n e released by the fem ale is recognized by the m ale chem oreceptors. T h e hydrodynam ic a n d chem ical inform ation in the ocean can be co u n terin tu ­ itive; the hydrodynam ic trail an organism leaves in the w ater is recognizable for a m uch longer tim e th an one m ight im agine (C hapter 6) an d chem ical trails persist for even longer periods (P. Lenz 2000). Specific sexual behaviours have been analysed in detail in several copepods (Boxshall 1998; L onsdale et al. 1998) w ith the rem arkable results th a t males clearly recognize the sw im m ing tracks of females an d follow them closely over distances o f several centim etres. M ales of the copepod Calanus marshallae search for an d then follow the vertical scent trails laid by sinking females, ju st as the shrim p Acetes follows a food trail (Fig. 7.5). T h e copepods can recognize w hen they are travelling in the w rong direction an d adjust their behaviour to search for the right direction. T h e behaviour o f females o f an o th er copepod (Temora longicornis) changes w hen exposed to m ale exudates. T h ey swim w ith little hops w hose hydrodynam ic footprint m ay b e recognized by the m ale an d m ake the female easier to find. T h e m ales follow fem ale trails, up to 10 s old, as far as 13 cm (130 body lengths) an d can backtrack up th eir own trails if they go in the w rong direction. At the tem poral an d spatial scales o f copepods, lam in ar stracture in the w ater can be retained even in the face o f larger-scalc tu r­ bulence becausc m olecular diffusion is relatively slow.

THE BIOLOGY OF THE DEEP OCEAN

Fig. 7.5

Mate-attraction/mate-search behaviour in Calanus marshallae. The sequence of events is: (1) a female generates a vertical pheromone trail; (2) a male alerted by the pheromone swims in smooth horizontal loops; (3) on crossing the pheromone trail he (usually, not always) performs a dance; (4) the male chases down the pheromone trail to the female; (5) the female jumps away repeatedly with the male in pursuit, sometimes bumping her; (6) a mating clasp is established and the male transfers the spermatophore to the female. (From Tsuda and Miller 1998, with permission from The Royal Society.)

T hese very small anim als clcarlv use both m echano- an d chem oreccptors in these elaborate tracking routines (P. Lenz 2000). M ale copepods, particularly o f oceanic species, increase the nu m b er o f chcm oreccptive acsthctascs at their final m oult, readying themselves for the sexual search ahead. Several groups have non-feeding m ales w ith atrophied m outhparts. The}' lose the prey-sensing systems an d con­ centrate instead on the sexual aesthetascs an d p redator-detecting m echanorecep­ tors. For small anim als whose predators h u n t largely by m echanorcception, chem ical signals m ay be a safer m eans o f facilitating sexual encounters th an random -search swimming. P hotographs o f the ocean floor show the tracks an d trails o f m any bo tto m dwellers (C hapter 3); we need to recognize th at the m id­ w ater environm ent is criss-crossed in three dim ensions by sim ilar tracks an d trails, b o th m echanical an d chem ical, albeit m ore ephem eral in nature. Sexual pherom ones, akin to those in copepods noted above, are assum ed be im p o r­ ta n t in m ate location in m any other deep-sea anim als, particularly in fish. T his assum ption is based on the different degrees o f developm ent o f the olfactory lam el­ lae in m ales and females o f m any meso- a n d bathypclagic fishes (M arshall 1967a,b). A nim als w ith en h an ced developm ent o f the olfactory lam ellae are described as m acrosm atic, while those w ith sm aller th an average o r regressed olfactory organs

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are know n as m icrosm atic. In m any bathypelagic fishes the m ales are m acrosm atic w hereas the females are m icrosm atic. Indeed it has been estim ated th a t over 80% o f the fish fauna living deeper th a n 1 km have sexually d im o rp h ic olfactory organs. T his applies particularly to the ceratioid anglerfishes, the ab u n d a n t gonostom atid genus Cydothone (Fig. 7.6), an d certain o th er species such as Gonostoma bathyphilum.. In all these specics the m ales are m uch sm aller th a n the females, yet they have greatlyelaborated m acrosm atic olfactory organs (and associated enlargem ent o f the fore­ brain an d olfactory- lobes). In those species th a t are either facultative or obligatory p rotandrous herm aphrodites (C hapter 10) (such as Gonostoma bathyphilum, the deepest-living species o f its genus), the m acrosm atic m ales becom e m icrosm atic females. T h re e other species o f Gonostoma (G. demdatum, G. atlanticum, an d G. elonga­ tum) are m esopelagic a n d do n o t have m acrosm atic males. In oth er bathypelagic species o f fish bo th sexes are m icrosm atic. Fig. 7.6

Sexual dimorphism o f the olfactory organs (Oo) and brain of the bristlemouth C ydothone microdon. (a) male; (b) female; (c) head o f male. Cc, corpus cerebelli; Fb, forebrain; Ob, olfactory bulb; Ot, optic tectum. (From Marshall 1967b.)

THE BIOLOGY OF THE DEEP OCEAN

M esopelagic fishes in general (including m yctophids a n d slomiatoids) do n ot have any sexual dim orphism o f the olfactory system, n either is it usually m icrosm atic. E xceptions to this rule include the m acrosm atic males in the two small fishes Argyropelecus hemigymnus (200-600 m) an d Valmcimnellus tripunctulatus, b u t in neither o f these is the female m icrosm atic. T h e deeper-living (600-800 m) hatchetfish Stemoptjx diaphana has m icrosm atic males an d females (Baird an d Ju m p e r 1993). Benthopelagic species in general have m oderately developed olfactory systems w ith no sexual dim orphism , w ith the exception o f the halosaurs, some spccics of w hich have m acrosm atic males. T hese generalizations apply even w ithin those families containing both bathypelagic an d benthopelagic species (e.g. M acrouridae an d Brotulidae). It seems likely th at m atu re males o f anglerfishes an d o f Cydothone greatly o u tn u m b er m atu re females (one estim ate puts the ratio o f m ature m ale anglerfishes to females at betw een 15 an d 30 to one). In these cir­ cum stances a heightened sensitivity to female pherom ones will play a key role in com petition betw een males. T h e m acrosm atic freshw ater eel is know n to be able to detect p articular chem icals at extrem e dilutions. Sim ilar sensitivities can be cxpccted in m acrosm atic m ales o f bathypclagic species. T h e probability o f a m ale/fem ale en coun ter is related linearly to the sw im m ing speed an d population density an d exponentially to the p erception distance, an d these can all be m odelled. T his has been done for the hatchetfishes A. hemigymnus (m acrosm atic males) a n d S. diaphana (both sexes microsmatic) w ith the m odel based on gradual horizontal expansion o f a p h ero m o n e pulse pro d u ced by a drift­ ing female (Jumper an d B aird 1991; B aird an d Ju m p e r 1995). A ny increase in the perception distance will greatly enhance the probability o f enco u n ter an d a p e r­ sistent pherom one patch is one m echanism by w hich this can be achieved. M ales m oving random ly (modelled at realistic speeds based on know n capabilities) encounter the patch an d search w ithin it for the female. T h e patch is assum ed to dissipate w ithin 1 day an d at the observed population densities an d speeds a fem ale should be detected w ithin 1 h o u r o f p herom one production; it wras calcu­ lated th a t female detection w ould take some 8 days if the o th er senses were used instead. A t the slow'er sw im m ing speeds an d sparser populations o f S. diaphana an individual w ith a perception range o f less th an 2 m w'ould take days to weeks to find a mate. T h e perception range w ould need to be at least 4 m in o rd er to find a m ate w ithin f day. Such barriers to finding a p a rtn e r m ay well determ in e the reproductive success o f the species. Sex pherom ones m ay have oth er effects. In shallow species they regulate a variety o f spaw-ning an d endocrine events related to reproduction, including the stim ula­ tion o f female ovulation by m ale pherom ones. Sim ilar events m ay well be taking place in the deep sea, b u t at present w'e have no w'ay o f investigating them . Facultative h erm aphrodites such as Gonostoma bathyphilum m ight, for exam ple, have the m ale to female ratios controlled by population densities, operating through the concentrations o f pherom ones in the water. Similarly, the exam ples o f hom ing, territoriality, an d trail-following know n in the shallow -w ater benthic environm ent will surely have their chem oreceptive parallels am ong the anim als o f the deep-sea floor. Im m ense m igrations are involved in the hom ing o f m idw ater

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fishes such as the eel or salm on. T hese can n o t be directed wholly by chem oreceptive cues b u t the final approaches to particu lar river or stream systems are very probably based on hom e-stream phero m o n e recognition. T h e olfactory sense has been show n experim entally to be necessary for ho m ing in salmon-like fishes an d no d o u b t the sam e is true for eels. We do n o t yet know' w h eth er sim ilar large-scale m igrations occur am ong deep-sea specics.

Aggregation and settlement O n e critical stage in the life history' o f m any shallow -w ater sessile species is the settlem ent o f planktonic larvae. D eep-sea anim als such as sponges, molluscs, polychaetes, tunicates, an d barnacles face precisely sim ilar problem s. T h e settle­ m en t process in shallow -w ater molluscs, such as abalone, requires th a t the larval chem oreceptor be stim ulated by a substrate-specific co m p o u n d or inducer (some­ tim es a tripeptide w ith G -term inal arginine), w hich is associated w ith ap propriate settlem ent surfaces. T his inducer (which m im ics the effect o f the n eu ro tran sm it­ ter gam m a-am inobutyric acid, or GABA) is often a p ro d u ct o f the specific alga on w hich the adult feeds. T h e receptor m olecule in the larval ch em oreceptor cap ­ tures the m olecule o f inducer an d the stimulus is transduced th ro u g h in term ed i­ ate cell messengers, w hich m ay include adenosine triphosphate (ATP). T h e sensitivity o f the larva to the inducer m ay be regulated by o th er com pounds in the w'ater such as the am ino acid lysine; high levels o f lysine greatly en h an ce the post­ recep to r sensitivity o f the system to the inducer (M orse 1991). Adult-specific chem ical messages (pherom ones) m ay be involved in gregarious settlem ent w here larvae are attracted to settle am ong existing adult populations (Burke 1986). A ggregations o f species are frequently recorded am ong deep-w ater populations, perhaps indicating sim ilar gregarious settlem ent processes (e.g. o f vestim entiferan tubew orm s an d mussels at hydrotherm al vents a n d seeps). A lthough there is no algal grow th on the deep-sea floor to provide equivalent inducers, nevertheless algal com pounds m ay still be involved. R ecent w ork has show n th a t algal cells sed­ im ent to the seafloor m uch m ore rapidly th a n was previously thought, particularly in seasonal tem perate areas following spring bloom s (see C h a p te r 10). Algal p ro d ­ ucts certainly stim ulate spaw ning in some deep-w ater species (e.g. the snow crab Chionoecetes) an d they m ight also induce larval settlem ent. Bacterial products, at sites o f high chem osynthetic activity, m ight have the sam e effect. D eep-sea b a r­ nacles will settle as effectively on discarded b eer bottles an d clinker as on seabed rocks. T h e settlem ent cue for these anim als is p robably as m uch tactile (m echanoreceptive) as chem oreceptive, providing an o th er exam ple o f the close functional association betw een the two types o f sensory system. Trail-following is a well-known p h en o m en o n in some shallow'-w'ater anim als (e.g. gastropod molluscs). T h e follower usually uses the chem ical trail o f its prey as a guide to a m eal (or a mate) a n d the phen o m en o n is a tw o-dim ensional exam ple o f the three-dim ensional trail-following n oted above. G iven the extensive a n d persist­ en t netw ork o f trails visible on the deep-sea floor, it is very likely th at chem ical

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trail-following is a n o rm al com ponent o f benthic behaviour. It m ight, for example, be the m eans w hereby echinoderm s achieve the pairing w hich is frequently seen p rep arato ry to reproduction (Fig. 7.7). C hem ical trails are likely to last longer, an d suffer slower diffusion, if adsorbed on to the sedim ent particles rath e r th an dis­ persed into the water. A ny anim al that deposit-feeds across the sedim ents is bo u n d to leave a chem ical trail, as well as (often) a series o f faecal pellets. W here trails have an intraspccific value, the effective range o f the p h ero m o n al co m p o n en t will be m uch less if adsorbed on to the sedim ent particles, b ut this m ay be a w orthw hile trade-off for a reduction in the risk o f alerting distant predators.

Conclusion T h e relative stability o f the deep-sea environm ent and the pressures o f m ate- and food-finding in this vast h abitat provide great scope for the em ploym ent o f chem ­ ical cues by a wide range o f organism s. C hem oreceptors are frequently associated w ith m echanoreceptors; the two senses work closely together an d em phasize the synergy o f the suite o f these (and other) receptors th at each anim al employs. B ehavioural observations on planktonic copepods are opening o u r eyes to the sig­ nificance o f chem oreception in the occan, acting on an environm ental m icroscale in concert w ith m echanoreception. T h e elaboration o f recognizable chem ore­ ceptors in deep-sea fishes gives a tantalizing glimpse o f the im portance o f largerscale chem ical signals in their daily lives, from food-fall recognition to sexual enticem ent. Both copepods a n d fishes can clearly read the chem ical messages in the bottles; m any oth er kinds o f anim als are undoubtedly doing so too.

Fig. 7.7

A pair of hermaphroditic deep-sea holothurians Paroriza pallens at 900 m o ff the Bahamas. Pairs of echinoderms (of a variety o f species) are regularly observed on the seafloor. They come together prior to mating, probably using pheromone cues to find each other. (Photo: Craig Young/HBOI.)

*

8

Seeing in the dark

Light in the ocean Vision is ou r m ain rem ote sensing system. 40% o f the sensory connections to the h u m an cortex are those from the visual system. T h e sun illum inates o u r environ­ m en t d uring the day an d at night we sleep, or tu rn on our own artificial light sources (a strategy m atched in the deep sea by biolum inescence, C h a p te r 9), We live in a prim arily tw o-dim ensional environm ent, effectively at the b o tto m o f a deep ‘o ccan’ o f air, the atm osphere. T h e constituent gases an d w ater v apour that m ake up the atm osphere affect the characteristics o f sunlight, attenuating it an d altering its spcctrum . A ir absorbs light so weakly, however, th a t at the e a rth ’s surface wre, an d its oth er inhabitants, enjoy high intensities o f light covering a b ro ad spectrum o f wavelengths, from ultraviolet (300 400 nm) to infrared (> 1 3 0 0 nm) w ith a peak ph o to n flux at about 600 nm . D a y /n ig h t an d seasonal changes are superim posed upon this by the e a rth ’s rotation an d orbital tilt. T h e visual systems o f m ost terrestrial anim als are sensitive to a b an d w id th from about 350 to 700 nm , spanning the p h o to n flux m axim um at the b o tto m o f o u r atm os­ p heric ‘ocean’ (Fig. 8.1). C hlorophylls an d their accessory pigm ents absorb light w ithin the sam e bandw idth. C onditions in the real occan, however, are very dif­ ferent an d daylight never penetrates m ost o f its volume. Fig. 8.1

Sunlight above the sea surface (s) has a broad spectral distribution in all conditions but at a depth of 500 m in clear oceanic waters (cf) the processes of absorption and scat­ tering result in blue-green light with a very narrow bandwidth. (From Denton 1990, with permission from Cam bridge University Press.)

Wavelength (nm)

THE BIOLOGY OF THE DEEP OCEAN

D ow nw ard illum ination at the ocean surface is sim ilar to th a t experienced by ter­ restrial organism s on a beach o r in a field, although the upw ard reflected an d scat­ tered light is quite different (Denny 1993). Ju st as in air, light is atten u ated in seaw ater by absorption a n d scattering, an d b oth processes are w avelength dependent. Blue light o f w avelength 4 7 0 -4 8 0 n m travels furthest through clear ocean water, b u t even these wavelengths are red u ced by an o rd er o f m agnitude for every 70 m depth. O th e r colours (wavelengths) disappear even m ore rapidly (Fig. 8.1). S cattering by very small particles is inversely p ro p o rtio n al to the fourth pow er o f the w avelength. Blue light at 470 n m is therefore scattered five times m ore th an red light at 700 nm . T his is why the backscattered light gives the clear ocean its blue colour. T h e result is th a t the clearest ocean w ater attenuates visible light 2 -5 orders o f m agnitude m ore strongly th an air. For light o f wavelength 500 nm , the b eam attenuation length (the inverse o f the b eam atten u atio n coefficient) o r the distance at w hich light passing through a m edium is reduced in intensity by the natu ral logarithm e, to 36.8% o f the initial value, is 55 km in p ure air a n d 28 m in pure w’ater. In the night sky the lights o f an aircraft are visible m any kilom etres away; the sam e lights u n d er w ater w'ould vanish at ranges o f 100-200 m even in the best conditions. A n o th er im p o rtan t difference betw een daylight in the ocean an d daylight on lan d is the directionality. O n land u n d er clear skies the position o f the sun d eter­ m ines the direction o f m axim um light intensity an d objects throw strong shadows. T h e large difference betw een the refractive indices o f w ater an d air causes sunlight to be b o th reflected an d refracted at the air-se a interface. W hen the sun is directly overhead (vertical or ‘n o rm a l’ incidence) 98% o f the light is transm itted through the interface an d only 2% is reflected, b u t w hen the sun is low on the horizon m ost light is reflected an d little direct sunlight enters the sea. Sunlight is refracted at the surface an d its direction becom cs closer to the verti­ cal. A n anim al looking up to the surfacc on a calm day sees the w hole 180° of sky com pressed into a small circular patch, called Snell’s window, representing a cone o f view w ith a solid angle o f 97°. Beyond this circlc all th a t is visible from below is upw ardly scattered light reflected back off the undersurfacc by total internal reflection. T h e result o f these processes is that the position o f the sun in the sky is o f little relevance to the angular distribution o f light in the sea, o th er th a n very n ear the surface. A t greater depths the light field rapidly becom es sym m etrical ab o u t the vertical axis (Fig. 8.2). Sm all particles in the w'ater produce some upw ard backscatter b u t the intensity o f dow nw clling daylight is always some 200 times g reater th an the upwelling light (D enton 1990). T h e n earest approx­ im ation to these conditions on land is to be found u n d er a single street lam p in a night-tim e fog; the illum ination is brightest im m ediately overhead b ut an observer looking at any p articular angle o f view' sees the sam e intensity in all directions. A nimals living ju st below' the surface experience daylight th a t is n ot very differ­ ent from that ju st above it, b u t anim als in the m esopelagic zone experience fight

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Fig. 8.2

The angular distribution of radiance in the ocean at the point О is radially symmetrical about the vertical axis, with the downward intensity some 200 times that o f the backscattered upward radiance. The length of the arrows is an indication o f the radiance in each direction. The distribution of radiance is unaffected by either the overhead daylight con­ ditions or the depth, though both greatly affect its intensity. (From Denton 1970, with per­ mission from The Royal Society.)

conditions o f relatively constant colour an d direction b u t exponentially dim in­ ishing intensity. Below ab o u t 1000 m there is effectively no residual daylight an d it is no longer relevant to the lives o f the bathypelagic fau n a (at 2000 m a shrim p eye looking upw ards w ith an apertu re o f 1 m m 2 m ight in tercep t ab o u t 100 photons o f blue light p er day). Yet there are m any anim als below 1000 m w ith functional eyes, ad ap ted solely for the detection o f biolum inescence. In J a n u a ry 1960 Jacques P iccard an d D o n W alsh reached the deepest p o in t on the ocean floor in the bathyscaphe Trieste. Peering o ut o f the p o rt at the b o tto m of the Challenger Deep (35 800 feet, alm ost 11 000 m , below the surface), Piccard ‘saw a w onderful thing. Lying on the bottom ju st b en eath us was a type o f flat­ fish, resem bling a sole . . . Even as I saw him , his two ro u n d eyes on the top of his h ead spied us— a m onster o f steel— invading his silent realm . Eyes? W hy should he have eyes? M erely to see phosphorescence?’ (Piccard an d D ietz 1961), Vision is by no m eans restricted to those anim als w ithin the reach o f daylight. T h e com parative d a ta on optic an d olfactory nerves in rattails an d catfish (C hapter 7) indicate th a t vision is ju st as im portan t to the deep-sea rattail as it is to the shallow -w ater catfish.

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Eyes and their design conflicts T h e visual systems o f all anim als dem onstrate trade-offs an d com prom ises in their capabilities. Photons are captured by specific pigm ents, w hose molecules then isomerize, changing their conform ation. T h e change triggers a cascade o f reactions, resulting in an electrical signal. T h e pigm ents are located in the m em ­ branes o f spccial receptor cells a n d the recep to r cells are usually grouped together to form a light-sensitive layer or retina. Such receptor cells, w hether g rouped or separate, can be present anyw here on the body, but are m ore usually grouped together in special optical structures (eyes). We know m ore ab o u t the visual systems o f deep-sea anim als th an ab o u t their oth er sensory systems because it is m uch easier to infer the capabilities o f an eye (based on its optical anatom y an d retinal structure) th an it is for a chem o- or m echanoreceptor. T h e optics deliver the light to the receptors in a spatially defined w ay so th a t different parts o f the field o f view' are sam pled by different receptors an d an im age is form ed. T h e quality o f the im age depends on a whole host o f factors, chief am ong them being the quality o f the optics, how m uch light reaches (and is absorbed by) the receptor layer in a given tim e, an d w hat degree o f overlap there is betw een the fields o f view' o f neighbouring receptors. H igh visual acuity (fine-grain sam pling o f some or all o f the field o f view--) can only be achieved if the im age is sharply focused on a retin a w ith a high density o f in d e­ p en d en t receptors. It also requires a high p h o to n flux to each receptor and exten­ sive neural processing o f the pho to recep to r signals. At low environm ental light levels this m ay not be possible. In contrast, the detection an d location o f a small w eak light source does not need high acuity but it does need high sensitivity. T h e eye needs to capture as m uch o f the ph o to n flux from the source as possible an d to sam ple it w ith the m inim um n u m b e r o f receptor cells so th a t each receives enough photons to exceed its signal-to-noise threshold. T h e delicate balance betw een these two con­ flicting re q u irem en ts—acuity an d sensitivity—is m ain tain ed by the selection pressures o f the light environm ents at different depths in the ocean, the am o u n t o f tim e a species spends at each depth, an d the different tasks it undertakes there (Land 1990). Solutions to som e o f the conflicts are achieved by different parts o f the eye doing different things or by changes to the eye as the anim al changes its habitat depth. H ow does this translate into the visual adaptations recognizable in different animals?

Fish Basic eye design Like other vertebrates, including ourselves, fishes have a ‘ca m e ra’ type o f eye in w hich a single lens focuses an im age on to the retina. R efraction at the corneal surface does m uch o f the focusing in air, thereby reducing the am o u n t left for the

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lens to do. T h e lens can be thin an d soft; attached muscles can change its shape an d accom m odate to bring b o th n ear an d far objects into focus. In w ater there is no significant corneal refraction an d the lens does all the focusing. To gain the necessary focusing pow er a fish’s lens is spherical an d projects th ro u g h the iris. It is com posed o f v ery concentrated proteins th a t give it a high refractive index and m ake it hard. A ccom m odation is achieved by moving the lens to a n d fro, rath er th an by changing its shape. A spherical lens w ith a u niform refractive index (like a glass m arble) suffers very badly from spherical ab erratio n an d the result is a very b lu rred im age- —b u t a p h o to g rap h taken through a fish lens is perfectly sharp, th at is there is little spherical aberration. T his rem arkable achievem ent is only possi­ ble because the lens has a refractive index th a t varies across its diam eter, w ith the highest value at the centre. T h e m aterials available (protein an d water) lim it the achievable refractive index to ab o u t 1.56; the resulting lens has a ratio o f focal length to radius ( / / r) o f ab o u t 2.55, know n as M atthiesscn’s ratio. T h e ‘f-n u m b er’ o f a lens is an indication o f the brightness o f the im age o f an extended light source at the focus; it is defined a s f / A w here A is the ap ertu re diam eter, so at full aperture a fish lens has an f-num ber o f 2 .5 5 /2 o r ab o u t 1.25. T h is f-num ber is not as low as th a t o f a cat (0.9) b u t b etter th a n th a t o f a h u m an (2.1). Epipelagic fishes live in a bright daytim e environm ent an d experience a b ro ad spectrum o f am bient light. T h e ir eyes look sideways an d ten d to be large, p ro ­ viding enough space for a fine-grain retina covering m uch o f the potential field o f view. A tu n a eye, for exam ple, has a resolution o f 4 arcm in, n o t far short o f that o f a m an (1 arcm in) an d m uch better th a n m ost o th er fishes (~20 arcm in). T h e retina contains two kinds o f receptor cells, rods a n d cones. Rods require a lower p h o to n flux th a n cones, an d consequently are o f p articu lar value d u rin g periods o f dim light (dawn, dusk, or at night). Both recep to r types are m odified ciliary cells. Rods are norm ally only a few m icrom etres in diam eter; the visual pigm ent is in the outer segm ent, w hich takes the form o f a stack o f closely packed m em ­ branous discs. D ifferent kinds o f receptor cells have different visual pigm ents, each w ith a characteristic absorption curve. T his gives the fish a b ro ad -b an d spec­ tral sensitivity. T h e visual pigm ents are m ade up o f a pro tein (opsin) an d a chrom ophorc derived from either vitam in Aj (retinal) or A 2 (3-dehydroretinal). T h e com binations are know n as rhodopsins and porphyropsins, respectively; rhodopsins absorb at shorter wavelengths th a n do their porphyropsin partners. D ifferent deep-sea species m ay have one or m ore pairs o f pigm ents (with differ­ en t opsins) o r the porphyropsin p artn ers m ay be missing an d the fish have several rhodopsins. T h e distribution o f recep to r cells over the retina m ay n ot be even an d m any species have a fovea, a small pit w ith exceptionally high recep to r densities, p ro ­ ducing a region o f particularly high visual acuity. D ark pigm ent cells provide a screen betw een individual receptors during periods o f high light intensity. M ovem ent o f the pigm ent, lengthening o r shortening o f the rods a n d cones, an d changes in pupil diam eter provide shallow -w ater vertebrate eyes w ith m eans o f adapting to both high an d low light intensities. D eep-sea eyes lack this flexibility.

THE BIOLOG Y OF THE DEEP OCEAN

Tubular eyes As w ater d ep th increases the light intensity falls exponentially b u t the residual light always rem ains brightest from above. Typical m esopelagic fishes such as the hatchetfishes an d gonostom atids have m edium -sized eyes an d m any o f them look m ore upw ards th an sideways. By looking upw ards prey can be seen silhouetted against the brightest available background. To obtain the brightest im age on the retina the apertu re o f the lens needs to be as large as possible. B ut if the lens increases in size so does the focal length (because M atthiessen’s ratio rem ains the same) an d therefore so does the size o f the eye— w hich m ay no longer fit on the top o f the head! T h e evolution o f tubular eyes has provided a com prom ise; at one end o f the tube is a large-aperture lens w hich focuses light on to the small area o f retina at the other end o f the tube (Locket 1977). In practice, a tu b u lar eye is simply the central portion o f a n o rm al eye (Fig. 8.3). T h e parallel optical axes o f two tubular eyes give their ow ner a wide binocular overlap, allowing accurate range-finding o f prey targets (and providing a small increase in sensitivity). T h e disadvantage is that the enhanced upw'ard vision is gained at the expense o f m uch o f the rest o f the field o f view, b u t clearly for some species the benefits are w orth it. Low'er m esopelagic fishes an d astronom ers have developed the sam e solution to the problem o f viewing small objects at very low light levels— b o th use a verylarge lens focused on a small region o f the sky. Fishes o f the m esopelagic com m unity show every grad atio n from wholly spheri­ cal eyes looking sideways to wholly tubu lar eyes gazing fixedly upw ards. Little Fig. 8.3

Diagram o f the outline o f a tubular eye (1) superimposed on a normal eye (2), both con­ taining a lens (3) of the same size. The main retina of the tubular eye (4) corresponds to the central portion of retina of the normal eye and receives focused images of the same size. The narrow visual field o f the tubular eye is partly extended by the accessory retina up the side of the tube (5) but the image on this retina will be unfocused. (From Locket 1977, with permission from Springer-Verlag.)

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fishes such as Valenciennellus have som e degree o f upw ard vision an d some hatchetfishes even m ore so. Laterally flattened fishes such as these have a p articu lar problem in achieving large dorsal eyes because the head is so narrow. Flatfishes w ould n o t have this problem . All m esopelagic fishes whose eyes face upw ards have tubular eyes. T ubular eyes have evolved in 11 families o f fishes (M arshall 1971), including the everm annellid, giganturid, an d scopclarchid fishes, Stylephorus, one lanternfish (Hierops), the m ales o f som e anglerfishes, an d various argentinoids such as Dolichopteryx an d the spookfishes Opisthoproctus an d Winteiia. A few o f these fishes paradoxically have forw ard-pointing tubular eyes; their ow ners probably h ang vertically upright in the water. F u rth er evolution o f tubular eyes has even involved the recovery o f som e lim ited lateral vision by m eans o f accessory light collectors. T ran sp aren t refractive fibres form a p a d ben eath the lens in scopelarchids an d everm annellids an d act as light guides to transm it light from the side into the eye (the pads give the scopelarchids their com m on nam e o f ‘pearl-eyes’) (Fig. 8.4). Dolichopteryx has gone even further by developing a retinal diverticulum , a blister o f retin a sticking o ut o f the side o f the eye. Light from below is reflected into it off the silvery side o f the eye. N one o f these extraordinary adaptations produces an im age on the retina because the ventrolateral light is not focused. T h ey can only give an indication o f the presence

Fig. 8.4

Adaptations to extend the visual field o f the pearl-eye Scopelarchus. The main retina of each eye has a dorsal field o f view (A), which provides binocular overlap (B) in the central part of the field. The more ventral part of the accessory retina has an (unfocused) monoc­ ular and lateral field of view (C) and the ventral field of view (D) is served by the dorsal part of the accessory retina, which views light passing unfocused through the lens pad (arrow). (From Locket 1977, with permission from Springer-Verlag.)

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o f a light source and some inform ation ab o u t its direction. N one o f th em w ould be o f any use in conditions o f bright light from the side, w hich w ould continu­ ously fog the m ain image. T h ey only work at all for a dark background contain­ ing a b rief bright spot— such as th at prod u ced by a biolum inescent anim al.

Retinal adaptations N um erous retinal specializations have been identified in tubular-eved an d oth er deep-sea fishes (Locket 1977). T h e m ost obvious one is the absence o f cones in response to the low' light levels. A nother is an increase in the length o f individual rods, or the presence o f m ultiple banks o f rods (up to 3 0 -4 0 rows) stacked one above the oth er (Fig. 8.5). Both adaptations increase the length o f the light p ath through the receptor cells containing the visual pigm ent, an d hence the likelihood

Fig. 8.5

Diagram o f a multibank retina, which increases the light path for photon absorption, in the figure light travels through the retina from bottom to top. The inner bank of rods (1) are like those o f normal retina, the middle (2) and outer banks (3) are connected to the cell bodies containing the rod nuclei (5) by slender myoid filaments; only the outer bank reaches the pigment epithelium (4). (From Locket 1977, with permission from Springer-Verlag.)

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o f p h o to n capture. T h e length o f the light p ath can be doubled by having a m irror or tap etu m b ehind the retina th a t reflects back any light th a t has n ot been absorbed on the first pass. In bright light such a tap etu m produces a characteris­ tic evcshine. If a specular (mirror-like) tap etu m is aligned flat across the end o f the receptors the light will be reflected back along the incom ing light p ath with m inim al degradation o f the image. Reflector caps p laccd ro u n d the o u ter seg­ m ents o f individual rods, or groups o f them , also reduce ran d o m reflections. Diffuse reflectors scatter the light m ore random ly through the p h o to recep to r layer, reducing the im age quality. T h e reflector elem ents m ay be crystalline (usually o f guanine) or form ed o f granules o r fat droplets. If the crystals are arran g e d in m ultiple stacks the reflection is specular an d can be highly m o n o ­ chrom atic (C hapter 9). T h e probability o f ph o to n absorption depends on the absorbance, o r optical density (concentration), o f visual pigm ent. Increasing the absorbance will increase sensitivity, an d the densities o f pigm ent in the rods o f m any deep-sea fish are indeed very high. S pontaneous isom erization o f visual pigm ents (without the absorption o f a photon) causes ran d o m noise. M ore pigm ent will p roduce m ore noise so there is a trade-off betw een pigm ent density an d signal-to-noise ratios. T apetal m irrors m ay have the additional benefit o f increasing the signal (by d o u ­ bling the p ath length) w ithout increasing spontaneous noise. Sharks w ith tap eta have h alf the optical density o f visual pigm ent, co m p ared w ith those w ithout tapeta. T h e absorption spectra o f the visual pigm ents need to be closely m atch ed to the entering light for efficient ph o to n capture. M ost deep-sea fishes have only one visual pigm ent in their rods, an d only rods in their retinas. W h en co m p ared with shallow'-water species the absorption m axim a o f these deep-sea pigm ents are shifted to shorter wavelengths (clustered aro u n d 485 nm) b u t are still at longer wavelengths th an w'ould be expected if they w'ere solely for viewing the blue dow'nwclling daylight. T h ey are closer to the m axim a th a t -would be p redicted for viewing biolum inescence (Fig. 8.6). T h e close spectral sim ilarity betw een m ost oceanic biolum inescence and dow nw elling daylight m ay be a consequence o f the pressure to achieve m axim um range w ith a biolum inesccnt signal, as well as effec­ tive cam ouflage (C hapter 9). It m ay also in p a rt be a response to oceanic visual systems th a t evolved initially to w ork in dim dow nw elling daylight. M axim um effective range depends ju st as m uch on the capabilities o f the observer as on the characteristics o f the water. In assessing the evolutionary sequence o f adaptations such as these it is n o t always clear w hich is the chicken an d w hich the egg. For a given pigm ent density the probability o f p h o to n cap tu re by a single receptor will increase w ith its cross-sectional area (just as m ore raindrops fall into a w ider bucket) but so will the ran d o m noise. In practice, receptor’ cells are rarely o f large diam eter an d the sam e effect is achieved instead by wiringseveral small reccptors together in parallel. If they all converge on a single n euron they will function as one unit. O n e o f the m ain features o f the retinas o f m an\' deep-sea fish is the small n u m b e r o f cells in the in n er neuronal layers

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Fig. 8.6

A histogram showing the wavelengths o f maximum absorption of the visual pigment in those deep-sea fish with a single rhodopsin. Above is shown the range o f wavelengths predicted to confer maximum sensitivity either to downwelling light or to fish biolumines­ cence; the match with bioluminescence is much closer. (Reprinted from Douglas et al. 1998, with permission from Elsevier Science.)

25 у Predicted range for downwelling light 20ф о

Predicted range for bioluminescence

10--

5”

440

450

460

470 Xmax (nm)

480

490

500

o f the retina, indicating high levels o f convergence w hen co m p ared w ith shal­ lower species. G roups o f receptors w ithin their own reflective cups typically connect to a single ganglion cell, th a t is they function as single units. A larger functional receptor cell unit inevitably has a low'er packing density th an a sm aller u nit an d sensitivity is gained at the cost o f p o o rer im age resolution. R ecent studies o f the retinal structure o f deep-sea fishes, b o th pelagic an d d em ­ ersal (near-bottom ), have show'n an unexpected variety o f retinal organization (W agner et al. 1998). D ifferent regions o f the retina m ay have very different d en ­ sities o f ganglion cells, indicative o f different degrees o f resolution an d special­ ization in different parts o f the visual field. Some fishes have an alm ost uniform ganglion cell density over m ost o f the retin a (.Notacanthus bonapartei)\ others have regions o f higher density (called arcae retinae). In several u n related pelagic species, including lanternfishes, the num bers o f ganglion cells increase towards the outer edge o f the retina, suggesting increased acuity at the edge o f the visual field. T his m ight m ake the fish m ore aw are o f prey o r a p red a to r entering the field o f view. In other species there are one or m ore regions (acute zones) w here the ganglion cell densities increase to four or five times those in the m ain retina. In the hatchetfish Sternoptyx diaphana (which does not have tu b u lar eves) this region is in the low'er p a rt o f th e retina, w hich views the upw ard p a rt o f the visual field. In the tripodfish Bathypterois dubius there are two such regions covering the low er visual fields to the front an d rear, perhaps for surveillance o f potential prey ah ead an d p redators behind. Foveas are special kinds o f areae retinae associated w ith a pit an d they

SEEING IN THE DARK

171

have been m entioned earlier as present in m any shallow -w ater fishes. Surprisingly, they are also found in deep-w ater species. T h e pits usually have high recep to r cell densities an d low' convergence, resulting in the highest acuity over a lim ited field o f view. A few' species wdth m ultiple banks o f rods at the fovea (e.g. Baiacalifbrnia) p robably have increased sensitivity at this location, ra th e r th a n acuity. T h e benefit o f foveas in deep-sea species m ay be n o t so m uch their increased acuity but rath e r their heightened ability to detect m ovem ent. T h e im age o f an object m oving across the visual field will scan across m any m ore receptors per u n it tim e as it passes dow n an d up the sides o f the foveal p it th a n if th a t region were flat. In the deep dem ersal fish Conocara macroptera the ganglion cell density in the fovea is ~ 1 0 tim es g reater th an in the adjacent retina. Its fovea subtends a region o f binocular overlap to the front o f the fish w ith a resolution as high as 5—6 arcm in, 10 tim es b etter th a n the eyes o f m ost deep-sea fish an d close to th at o f a tu n a (Fig. 8.7). How'ever, it is m uch easier to determ in e the detail o f the deep-sea retinal variety th an it is to find o u t how it is used. We are forced to

Fig. 8.7

Retina] specialization occurs even in deep-sea fishes. A profile across the retina of Conocara macroptera shows a region of high densities o f both photoreceptor cells (open squares) and ganglion cells (GCs) (filled circles). This region provides the potential for high visual resolution over a limited retinal area. (Reprinted from Wagner et al. 1998, with permission from Elsevier Science.) Conocara macroptera

t

E W О

c ф ■о

о о

JZ

а.

THE BIOLOGY OF THE DEEP OCEAN

interp ret observed sam pling w hat ou r

function from structure, generally w ithout the ad d ed benefit o f behaviour. We can only guess at the advantages for deep-sea fishes of particu lar parts o f the visual field in different ways (which is exactly retinas do).

In conditions o f very dim light it is im p o rtan t to achieve the brightest possible im age by using the full diam eter o f the lens to collect light a n d focus it on the retina. However, because the lens is spherical the iris m ay obscure some o f the light from oblique directions. A n u m b e r o f deep-sea species have developed w hat is called an aphakic gap betw een the lens an d the iris to overcom e this problem . Typically this is to the front o f the eye, rendering the pupil p ear-shaped an d opening the region o f binocular overlap to the full lens ap ertu re (Fig. 8.8). In wellillum inated w aters this w ould be disastrous, because light entering the eye through the aphakic gap from other directions w ould reach the retina w ithout being focused an d w ould fog the image, ju st like a light leak in a cam era. In the d ark­ ness o f the deep sea, how’evcr, a fish lining up a biolum inescent target for a p re d a ­ tory strike does not have this problem .

Fig. 8.8

The slickhead Baiacalifornia drakei has a pronounced anterior aphakic aperture. The upper figures show the sighting grooves in front of the eye (1), and the anterior (rostral) aphakic gap (2), which allows almost the whole diameter of the lens to be exposed to light from the front of the fish. In an excised eye (below) it is clear that the fovea (3) gains the maximum benefit from the brighter image that results from use of the full aperture of the lens. (From Locket 1985, with permission from The Royal Society.)

SEEING IN THE DARK

173

Som etim es there are striking exceptions to the general rules. O n e o f these is the presence o f red-sensitive visual pigm ents in several deep-sea fishes (Aristostomias, Pachystomias, an d Malacosteus) (Douglas et al. 1998). In a w orld do m in ated by blue light this m akes no sense— until we discover th a t all three produce n ot ju st blue biolum inescence b u t red biolum inesccnce as well (C h ap ter 9). Malacosteus has. in addition, a scarlet retinal tap etu m com posed o f carotenoid pigm ent dissolved in lipid droplets. Its specialized visual system enables it to see its ow'n red an d blue light— o r the lights o f an o th er Malacosteus. D ifferent visual m echanism s achieve the sam e rem arkable result in the other fishes: Aristostomias an d Pachystomias probably each have four visual pigm ents (two rhodopsins an d two m atching porphyropsins) providing effective overlap w ith their biolum inescence spectra. Malacosteus has only two, w ith negligible overlap, b u t these arc coupled in the rods to a stable photosensitizing pigm ent th a t absorbs close to the biolum inescencc em ission m axim um . Yellow pigm ents in the lenses o f Malacosteus an d Aristostomias fu rther enhance the ability to perceive red biolum inescence by fil­ tering out short-wave light (in Pachystomias there is a yellow- filter pigm ent in the retina). Several oth er deep-sea fishes have yellow- lenses, including some w ith tu b u lar eyes (Scofielarckus, Stylephorus, Argyropelecus), b u t they do n o t have red-sensitive visual pig­ m ents. T h e function o f these short-wave filters m ay be to en hance the contrast betw een the biolum inescence o f countcrillum inating anim als (C hapter 9) an d the dow nw elling daylight, th a t is to break the cam ouflage. Bioluminescence spectra often have m ore long-wave light th an does dow'nwelling daylight. By filtering out m ost o f the short-w'ave light com m on to both, the contrast betw een the two will be enhanced. A less easily explicable fact is that one species o f fish m ay have a yellow- lens while a closely related one does not. O n e rem arkable deep-sea fish, Omosudis lowei, has a retina th a t contains num erous cones, alm ost exclusively so in one ventral area, an d m any o f them arc opticallyisolated in their ow n tapetal cups. We have no ad equate explanation for this ap p a ren t anom aly o f high photon-flux receptors in low- photon-flux conditions. A few other deep-sea fishes also have som e cones bu t they are never the d o m in an t receptor, although in the benthopelagic notosudids Scopelosaums an d Ahliesaurus they p opulate the foveas. T h e larvae o f m any deep-sea fish live n earer the surface an d their optical environm ent will alter during their ontogenetic descent into deeper w-aters. M ight their visual characteristics changc too, w ith cones beingp resent in the very early stages? As yet there is no general evidence for this sup­ position b u t there are exam ples in some shallower fishes. T h e E u ro p ean eel, the pollack, an d the lem on shark, for exam ple, com pensate for changes in their visual environm ents d uring developm ent by acquiring new visual pigm ents th a t absorb at shorter wavelengths. T h e eel changes its visual pigm ents in the transition from freshw ater elver to oceanic adult an d the o th e r two in the transition from shallow juvenile to deep er adult. In the eel an d pollack the new? visual pigm ents arise from the developm ental expression o f a second opsin. In o th er m igrators the vitam in A 2 chrom ophore on an opsin (as a porphyropsin) is substituted by vitam in A ( on the sam e opsin (giving a shorter -wavelength rhodopsin).

THE BIOLOGY OF THE DEEP OCEAN

T h e re is a strong positive correlation in m esopelagic an d dem ersal teleosts betw een retinal adaptations such as convergence, recep to r density, length o f receptors, loss o f screening pigm ent, developm ent o f tapeta, etc., an d the depth o f habitat. Species th a t move deeper as they grow larger show a sim ilar increased retinal specialization d uring their descent. Ju st like the bony fishes, deep-w ater elasm obranchs lack cones, have retinal tap eta, rods w ith long o u ter segments, an d a reduced pigm ent epithelium . However, there m ay com e a visual level at w hich increased specialization is no longer physiologically viable. T his has led to the concept o f a ‘quit zone’ in the occan, below w hich visual function declines an d eye structure diminishes. Sm aller eyes are certainly a feature o f m any o f the deepest-living species. Abyssal species o f bottom -dw elling rattails an d brotulids have sm aller eyes th a n those living on the u p p er slope (< 1 0 0 0 m), an d bathy­ pelagic Cydothone, anglerfishes, whalefishes, an d gulper eels all have very small eyes, b u t they have hardly ‘q u it’. A small eye is n ot necessarily a ‘d eg en erate’ eye, although the two are frequently confused, ‘Specialist’ w ould often be a m ore appropriate description. Nevertheless, there are some species in w hich alm ost all the optical elem ents have been lost, leaving either a plate o f b are retina (Ipnops) or simply a parabolic reflector an d overlying retin a (.Nyhelinella). N eith er o f these eyes can form an im age but they rem ain specialist photom eters. W h at pu rp o se this serves can only be conjectured, b u t there are parallels am ong the shrim p (see below). C ertainly there are a nu m b er o f deep-sea fishes whose eyes, like these, cannot form good images, but they do retain a light-sensing role. T h e small eye o f Bathypterois was assum ed to be degenerate b u t the recent w'ork outlining its retinal specializations encourages a less dismissive view. O th e r senses, such as the lateral line system or chem oreception (C hapters 6 an d 7), can act as surrogates to take on some o f the roles o f vision in the deep sea (Lythgoe 1978). Trade-offs betw een the senses are inevitable an d relate to differ­ ences in the lifestyles o f deep-sea anim als, b o th fishes an d invertebrates.

Invertebrates T h e eyes o f deep-sea fishes show how the visual system can ad ap t to life in the depths yet still undertake a wide variety o f different tasks. A re the eyes o f inver­ tebrates equally adaptable? Fish eyes evolved only once b u t eyes in o th er groups have evolved quite independently som e 4 0 -6 0 tim es (Salvini-Plaven an d M ayr 1977).

Cephalopods C am era-tvpe eyes are present in relatively few invertebrates b u t they reach p in ­ nacles o f adap tatio n in the cephalopods, closely paralleling those in fish. It is not surprising that w ith an alm ost identical optical system in b o th groups o f anim als the eye should evolve in sim ilar directions in response to the sam e deep-sea

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175

selection pressures. It is the m ore surprising that Nautilus, a m idw ater cephalopod w ith an impressive evolutionary ancestry, should have a quite different eye (Land 19846). Its near-spherical large eye has no lens b u t an extensive retin a w ith verylong receptors. T h e apertu re is a variable pinhole 0 .4 -2 .8 m m in diam eter, w ithout any oth er focusing device, a n d is open to the sea. T h e result is a p o o r im age w ith a stopped-dow n retinal brightness equivalent to an f-num ber o f ab o u t 25 (Table 8.1). Nautilus still has a cam era eye b u t it is a pinhole cam era, w hereas all other cephalopods have m oved on to at least a lens. It lives at relatively shallow' depths in clear ocean w aters so there is still an adeq u ate p h o to n flux at the recep­ tors, b u t alm ost any? lens w ould have given a visual advantage over the pinhole eye. Nautilus an d all other cephalopods have the retinal arran g em en t reversed w hen com pared w ith vertebrates, th a t is the light reaches the receptors first rath e r th an having to pass through the n euronal layer on the way. T h e surprise is th a t the vert­ ebrates followed any o th e r route, seeing that this is such an obvious optical advantage, b u t the constraint is d eterm ined by the w ay the vertebrate nervous system develops. A p art from this feature the eyes o f o th er cephalopods are verysim ilar to those o f fish, w ith a single large spherical lens. T his is m ade o f two dis­ tinct halves b u t still fully corrected for spherical ab erratio n an d has a focal length conform ing to M atthiessen’s ratio. A lmost all invertebrates have photoreceptors based on microvillous cells rath e r th an the rod an d cone ciliary receptors o f vertebrates. T h e retina in squid is com ­ posed o f groups o f four tall cells (retinula cells) w ith a central space; the in n e r­ m ost side o f each cell bears innum erable microvilli. E ach microvillous region is called a rhabdom ere. T h e rhabdom eres fill the central space betw een the retinula cells; they are oriented at right angles in adjacent cells an d interleave to form the rhabdom . T h is orthogonal arran g em en t o f the microvilli provides th e basis for sensitivity to polarized light. Visual pigm ents are m em b ran e-b o u n d in the microvilli a n d based on the sam e vitam in A t an d A 2 chrom ophores as in fish. Shallow cephalopods have a highly' m obile pupil th a t acts as an iris d iap h rag m in variable light intensities. C ephalopods m ay have m ore th a n one visual pigm en t an d different ones may7be located in different parts o f the retina. In a few squid, including the m esopelagic firefly squid Watasenia, a third visual pigm ent ch rom ophore (4-hydroxy retinal, A '1,’)> has been found x(k m a x 471 nm)I in addition to the n o rm al A,1 V(k m a x 484 nm)> an d A 2 (^max 500 nm), related to vitam ins Aj an d A 2. In Watasenia it is preferen­ tially located in the ventral (upward-looking) region o f the retina w here the rctinula cells are two to three tim es as long as those elsewhere (M atsui et al. 1988). Perhaps this helps the squid to distinguish the biolum inescence o f its fellow's from the dow nw elling background. T h e few oceanic squid th at have been investigated have visual pigm ents absorbing at blue w avelengths sim ilar to those o f deepsea fish. D espite the occasional presence o f m ore th an one visual p ig m e n t- -and frequently' o f spectacular colour changes— all the evidence indicates that cephalopods do not have colour vision.

Table 8.1

Comparative optical parameters o f the eyes of some invertebrates and man

Species

C ephalopods Nautilus pompilius Octopus vulgaris O stracod Macrocypridina castanea Isopod Cirolana borealis A m phipod Phronima sedentaria Euphausiids Meganyctiphanes norvegica Stylocheiron maximum Nematobrachion boopis

Eye type

Component

Pin-hole Lens/water Apposition

3.6-25 1.25

Refracting superposition Refracting superposition Refracting superposition

Focal length (ц т) 10 000 10 000

Largest cones Smallest cones

Apposition Apposition

f-number

1.00 Upper eye Lateral eye

Upper Lower Upper Lower

eye eye eye eye

Shrimp Oplophorus spinosus Reflecting superposition Apposition

Light adapted Dark adapted

Man

Lens/air

Light adapted Dark adapted

(д т) 2800-400 8000

Recepto r Receptor diameter length (ц т) (ц т) 450 200

7.5 3.8

Interommatidial Sensitivity Field angle units of view (deg) (deg) 1.15-8 0.011

0.05-2.6 4.23

220 120

350 200

200 200

6 20

1849 4994

150

100

100

15

4181*

2.20 1.10

403 110

183 100

350 50

18 20

0.44 10

70 130

10 180

0.50

340

680

63

17

2.9

266

235

0.50 940 0.50 376 0.50 1229 (Rudimentary)

1880 752 2458

50 50 50

20 17 20

1.2 2.6 1.2

278 201 278

51 120 48

600

100

32

8.1

3300*

45 45

170 170

5 5

1.5 1.5

2000 6000

30 30

2 20

0.50

Shore crab Leptograpsus

Aperture

8.30 2.10

226

1670 1670

* Based on presence of a tapetum. References: Land 1980a, 1981, 1984a; Land et al. 1979; Land and Nilsson 1990; Dusenberry 1992.

0.007 0.07

1 3.2 0.023 37.1

169 169

SEEING IN THE DARK

177

A few m esopelagic cephalopods have tubular eyes (Sandalops, Amphitretus) an alo ­ gous to those o f fishes, a n d the rhabdom s m ay be very long, increasing the light path. D eep-sea cephalopods do not have retinal tap eta, despite having specular an d diffuse reflecting systems elsew here in the p h o to p h o res an d skin. T h e eyes o f deep-w ater cranchiid squids m ay be very large (e.g. leuthowenia megalops) and that o f the giant squid Architeuthis reputedly reaches 400 m m in diam eter. T h e juveniles o f som e species (e.g. Batholhauma) have stalked eyes, w hich becom e sessile in the adults. Stalked eyes in the pelagic octopod Vitreledonella are highlysilvered an d vertically elongate. T h e sam e eve-shape occurs in the upper m esopelagic larvae o f the squids Sandalops an d Taonius, p erh ap s as an aid to cam ­ ouflage (C hapter 9). As the juveniles o f these two genera m ove deeper, the eyes becom e first tubular an d finally hem ispherical in the bathypelagic adults (Young 1975). T h e m esopelagic genus Histioteuthis is rem arkable in th a t the squid has one large tubular eye w ith a yellow lens an d one small n o rm al eve. Perhaps it looks up w ith the large eye, breaking the cam ouflage o f biolum inescent coun­ terillum inators above it, an d looks dow n w ith the sm all-aperturc eye at dim objects below. T his idea is consistent w ith the pho to p h o re p attern . T h e anatom ically tubular eyes th a t occur in som e species o f an o th er group o f pelagic molluscs, the hctcropods, are quite different. H eteropods are tran sp aren t upper-m esopclagic anim als an d voracious predators. T h e eyes are usuallydirected forw ards, have a spherical lens w ith a focal length close to M atthiessen’s ratio, an d considerable binocular overlap. T h ey have a curious retina in w hich the p h otoreceptor cells are arran g e d in a horizontal rib b o n only a few cells wide. T his works in ‘line-scan’ m ode, the eyes m aking regular vertical sweeps, scanning the retinal strip across the field o f view (Land 19846). T h e eyes o f abyssal octopods (Cirrothauma, Cirroteuthis) are m uch reduced in size, like those o f some abyssal fish. In Cirrothauma there is no lens o r iris an d the optic ganglion is very small. Curiously, the bathypelagic squid Bathyteuthis has w hat appears to be a fovea but, like th a t o f the fish Baiacalifornia n oted above, the lengthened retinula cells at the fovea suggest th a t it is a region o f heightened sensitivity rath e r th a n resolution. T h ere have been few studies o f the eyes o f deep-sea species b ut it is likely th at the very different lifestyles o f different species will have resulted in visual subtleties on a p a r w ith those in fish an d crustaceans (below). T h e cxtraocular photoreceptors, or photic vesicles, sited close to the stellate ganglion o r optic nerve tract in, respec­ tively, m any octopods an d squid, have a light-sensing rath e r th a n a visual function an d they m ay m onitor the m atch betw een ventral biolum incsccnt cam ouflage an d dow nw elling daylight (Young 1978).

Crustacea C rustacean eyes are o f tw'O types, simple an d com pound. Simple eyes have their origin in the larval nauplius eye, w hich has three pigm ent cups, each w ith a few

THE BIOLOGY OF THE DEEP OCEAN

microvillous receptors. C o m p o u n d eyes are p aired structures com posed o f m any sim ilar units (om m atidia) that are optically isolated from one an o th er to varying degrees, as in m ost insects. B oth types o f eye m ay be present in the sam e anim al. T h e nauplius eye is always sessile but the com p o u n d eye can be cither sessile (am phipods an d isopods) or stalked an d m ovable (decapods, mysids, an d euphausiids). C rustaceans have an astonishing variety o f optical design in their eyes (Land 1984a), far m ore diverse th a n in any o th er group o f animals.

Simple eyes T h e te rm ‘sim ple’ in this context is a com plete m isnom er because near-surface pontellid copepods, in particular, have taken the nauplius eye to extraordinary heights o f design, w ith m ultiple-lensed a n d scanning systems. D eep-sea copepods have very small eyes w ith few obvious special adaptations except th a t m ost have a reflective m irro r behind the receptors. In the genus Cephalophanes (literally ‘head lights’) two o f the three nau p liar elem ents an d their reflectors are greatly enlarged, a n d w hen seen from above the h ead seems to be taken up w ith two large dish m irrors. A n even m ore extensive developm ent o f the nauplius eye has taken place in the deep-sea ostracod Gigantocypris (Land 1978). A gain two o f the ele­ m ents are hugely enlarged to form a p air o f forw ard-looking parabolic m irrors. A group o f receptors hangs lightbulb-likc at the region o f focus o f each m irror. This eye can n o t form a good im age b u t it has the best light-collecting ability o f any anim al eve, w ith an f-num ber o f 0.25. M ost other deep-sea ostracods have very reduced nau p liar eyes. O n e group o f largely shallow-w'ater species also has m obile lateral co m pound eyes, very like those o f water-fleas. O n e o f these ostra­ cods, A'lacrocypridina castanea, is bathypelagic (see below).

Compound eyes O s tr a c o d s , a m p h ip o d s , a n d is o p o d s : a p p o s itio n e y e s

C o m p o u n d eyes are com posed o f m any structurally sim ilar units. T h e receptor units are m ade up o f a group o f five to eight retinula cells whose microvillous rhabdom ercs interweave at the centre o f the group to form the rh ab d o m , an d provide sensitivity to polarized light. Light is focused by a refracting corneal lens a n d crystalline cone to form an im age at the top o f the rhabdom ; in the sim ­ plest cases the bo tto m o f the cone m eets the top o f the rh ab d o m . T his is called a n ‘apposition’ eye; axial and near-axial light entering the cone is trap p ed by the optical system an d transferred solely to its associated rhab d o m . T h e crystalline conc has a rcfractivc index gradient across its w idth, highest in the ccntrc, an al­ ogous to the system in the fish lens. Off-axis light is absorbed by distal screening pigm ent round the conc a n d /o r proxim al screening pigm ent ro u n d the rhabdom ; the screening m ay be partly w ithdraw n during dark adaptation. T his pigm ent gives the eyes o f shallow'-w'ater shrim ps th eir typical black appearance. T h e effective apertu re o f the eye is the diam eter o f the corncal lens an d the

SEEING IN THE DARK

179

acceptance angle o f each om m atidium is d eterm in ed refracting lens/crystalline cone com bination, a n d rh ab d o m (Fig. 8.9). W hen refracting om m atidia are honeycom b-like arrays, visible as a hexagonal p a tte rn the eye.

by the focal length o f the by the diam eter o f the tightly p acked they form o f facets on the surface o f

T h e deep-sea ostracod Macrocypridina has an eye o f this type containing 27 sep­ arate om m atidia, w ith cones o f different sizes. T h e largest ones have the sm all­ est acceptance angles a n d look anteroventrally. T his gives a region o f higher

Fig. 8.9

Com pound eye types and their optical components. In an apposition eye (a) the omma­ tidia are optically isolated from one another by pigment (p) and a receptor (rhabdom, rh) receives only axial light through its associated lens and crystalline cone (cc). In super­ position eyes (b, c) a 'clear zone' (cz) separates the receptors from the crystalline cones, with the result that light from a number of ommatidia can be focused on one or a few receptors, greatly increasing the image brightness. The focus can be achieved either (b) by refraction in cones with a variable refractive index (lens cylinders), as in mysids and euphausiids, or (c) by reflection in mirror (m) boxes, as in most deep-sea decapod shrimp. (Reprinted from Land 1980b, copyright Macmillan Magazines Ltd.) (a)

Light

Light

THE BIOLOG Y OF THE DEEP OCEAN

resolution (an acute zone) com pared w ith the rest o f the eye, b u t resolution is still very lim ited (Table 8.1) (Land an d Nilsson 1990). M ost anim als w ith com pound eyes have m any m ore om m atidia. Isopods are typical exam ples an d im portant m em bers o f the deep-sea fauna. T h e five fam i­ lies th at are m ost ab u n d an t in shallow w ater all have eyes, w hereas the prim arily deep-sea families all lack eyes. Loss o f eyes in deep w ater seems irreversible, because species from the sam e families th at later m oved up into shallow w ater (particularly into cold fjords) also lack eves. Cirolana borealis is a deep-w ater species w ith w ell-adapted apposition eyes. Its om m atidia have acceptance angles o f about 45°, very sim ilar to those o f the small om m atidia o f Macrocypridina, short fat rh ab dom s, an d a reflecting tapetum (Nilsson an d Nilsson 1981). Cirolana an d m ost oth er deep-sea crustaceans have, like deep-sea fishes, very little screening pigm ent in their eyes. T h e large acceptance angles in Cirolana and Macrocypridina are cor­ related w ith very high sensitivity. T hey have calculated sensitivities o f 4000- 5000 units (based on the nu m b er o f photons absorbed p e r square m icrom etre; a lightadapted crab w ith an acceptance angle o f 2° has a sensitivity o f 1 unit) (Table 8 . 1).

O n e o f the consequences o f this high sensitivity is th a t it renders the eye very vul­ nerable to light dam age. A b rie f exposure to daylight irretrievably blinds Cirolana an d m any other deep-w ater crustaceans— b ut this is not, o f course, a h az ard to w hich they w ould norm ally be exposed! T h e deep-w ater lobster Nephrops (betterknow n on a plate as scampi) is the subject o f a large fishery. U ndersized live speci­ m ens caught in baited traps o r trawls are throw'n back. T h o se exposed to daylight during this process are perm an en tly blinded. Strangely, tagged individuals suffer­ ing this dam age have subsequently been found to survive an d grow ju st as well as sighted specimens. W h en deep-sea shrim p at hydro th erm al vents are exposed to the floodlights o f visiting subm ersibles they too are vulnerable to p erm a n en t dam age. A m phipods are an o th er large group o f crustaceans w ith sessile apposition eyes, living in bo th deep- an d shallow -w ater habitats. T h e d eep er fau n a has a higher p roportion o f eyeless specics. A study o f some 4240 species o f gam m aridean am phipods found 18% o f them to be eyeless. Above 200 m only 8% are eyeless, but far m ore o f these eyeless species occur at high latitudes th an elsewhere, perhaps in response to the long periods o f polar darkness o r to reinvasion o f shallow polar w aters by eyeless deep-sea forms. T h e pro p o rtio n o f eyeless species increases w ith dep th dow n to ab o u t 1000 m , below w hich it rem ains steady at 75-85% dow n to 5000 m (T hurston an d Bett 1993). (Eyclessness is n ot solely related to a deep-sea habitat; there is also an evolutionary tren d tow ards eycless­ ness in burrow ing species, w hether in shallow w ater or in the deep sea.) G am m arid ean am phipods are not prim arily pelagic b ut the 300 o r so species o f hyperiid am phipods are. T h e y too, have apposition eyes b u t these are greatly m odified for the light regim e o f their meso- an d bathypelagic environm ents. If the eyes o f spccics living at the surface an d those at u p p er an d low er m esopelagic depths arc com pared, several depth-related trends can be recognized (Land 1989,

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2000). T h e first is th a t there is an increase in eve size w ith increasing d ep th an d at the sam e tim e the eyes becom e m ore asym m etric as the u p p er p a rt o f the eye becom es increasingly enlarged (Fig. 8.10). T h e om m atidia o f the u p p er eye increase in diam eter w ith depth, while the field o f view declines from 40° to 60° in u p p er m esopelagic species to 10° in low er m esopelagic species. T his is func­ tionally analogous to the upw ardly directed tu b u lar eyes o f fishes an d is p articu ­ larly ap p a ren t in Phronima (Table 8.1). To increase the resolution (acuity) in the upw ard direction the eve m ust have m ore om m atidia p er degree o f view; w ith a sm aller angle betw een each one. If m ore om m atidia w ere to be packed into one small region o f a spherical eye they w ould necessarily be m uch sm aller an d each

Fig. 8.10 Fields of view and binocular overlap of the medial eyes of four hyperiid amphipods viewed from the front (left) and from the left side (right), arranged in order of their depth distributions, with Platyscelus the shallowest and Cystisoma the deepest. Thus in Platyscelus each medial eye has an anterodorsal field of 42°, a lateral field o f 55°, and a 15° binocular overlap. The medial or upper eyes (heavy stipple) have larger facets than the lateral or lower eyes (light stipple) and, as the habitat depth increases, the field of view becomes narrower. Cystisoma has no lateral eye. The scale bars to the right repre­ sent 1 mm. (From Land 1981, with permission from Springer-Verlag.)

THE BIOLOGY OF THE DEEP OCEAN

receive less light, giving a dim m er image. Instead, the u p p er om m atidia becom e w ider an d their radius o f curvature m uch greater th an th at o f the rest o f the eye. T h e ir apertures rem ain at least as large as those o f the original om m atidia b ut at a m uch sm aller angular separation, giving a higher resolution w ith no loss of im age brightness. N orm ally at m esopelagic depths dark pigm ent betw een the om m atidia would ensure their optical isolation b u t if the dorsal om m atidia are greatly lengthened and pigm ent-screened the eye w ould becom e a very conspicuous d ark blob. To avoid this the retina m ust either rcduce its screening pigm ent (as in Cystisoma) or be condensed to a m uch sm aller blob {Phronima). In the latter case the eye retains its transparency by having p igm ent only ro u n d the small rhabdom s at the base o f the long om m atidia. T h e focused im age is transferred from the distal crystalline cone to the rh ab d o m several m illim etres away, across a tran sp aren t space an d w ithout any light loss or interference from unfocused light entering from the side. T his optical m iracle is achieved by stretching the lower en d o f the crystalline cone into a thin fibre, w hich links it to the top o f the rhab d o m . T h e cone filam ent acts as a fibre optic, keeping the focused light im age trap p ed w ithin by total in tern al reflection. Superficially Phronima appears to have two eyes on each side, one looking up an d one looking sidew'ays an d dow'n, b ut structurally they are differ­ ently m odified portions o f the sam e eye. T h e whole u p p er p a rt o f the eye has a field o f view' o f ab o u t 10°- -approxim ately the sam e as th a t o f a single om m atidium in the low er eye! W illiam Beebe (1926) describes Phronima delightfully: ‘Its overbalanced appearance rem inded m e faintly o f a term ite, b u t its eyes w ere well w'orthy o f the cranium in w hich they were placed . . . It seems th at Phronima is especially blessed w ith eyesight.’ T h e deep er am p h ip o d Cystisoma has ab an d o n ed the low'er p a rt o f the eye an d greatly enlarged the u p p er p o rtio n so th at it covers the whole o f the top o f the head, w hereas in shallower anim als such as Platyscelus the u p p er an d low er eyes arc less clearly differentiated an d their resolutions are very sim ilar (Fig. 8.10). At abyssal depths hyperiid am phipods greatly reduce the eye size, optics, an d the n u m b e r o f om m atidia, ju st like the g am m arid ean am phipods. T h u s Scypholanceola has an alm ost naked retin a w ith a couple o f large reflectors b ehind it.

E u p h a u s iid s a n d m y s id s : r e fr a c tin g s u p e r p o s i t io n e y e s

E uphausiid an d mysid shrim ps are m ost ab u n d a n t in the u p p er 500 m b ut extend into abyssal depths. T h e eyes o f m any o f the shallower species have becom e bilobed like those o f the hyperiid am phipods, w ith the upw ard p a rt o f the eve becom ing increasingly' separated from the rest o f the eye. How'ever, the optical design o f the eyes is fundam entally different from th at in am phipods an d isopods. Euphausiids an d mysids still have eyes in w hich the light is focused by refraction in the crystalline cones, an d the facets retain their hexagonal packing, but they are ‘superposition’ eyes, not apposition ones. In superposition eyes the cones and rhabdom s are not in direct contact but are separated by' a b ro ad ‘clear zo n e’. Light ray's from m any facets can now be brought to a com m on focus on a single rh ab d o m across the clear zone, instead o f the im age being transferred from a

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single cone solely to its own rh ab d o m (Fig. 8.9). T h e key result is th a t the ap ertu re is no longer ju st one facet but a w hole group o f facets (up to 3000), giving a huge increase in im age brightness an d therefore in sensitivity. T h e resulting f-num ber for such an eye is ab o u t 0.5. T h e shallower species o f bo th groups (e.g. Meganyctiphanes a n d Siriella) usually have eyes w hich are spherical a n d the cones an d rhabd o m s are separately screened by dark pigm ent, b u t those low er in the w ater colum n have optical adaptations w hich are sim ilar to those o f hyperiid am phipods an d fishes, w ith regions o f the eye spe­ cialized for upw ard viewing. O n e optical constraint o f th e superposition eye is that the om m atidia m ust be concentric for it to work, because they are no longer optically independent. E uphausiids an d mysids w ith divided eyes (e.g. Slylocheiron an d Euchaetomera, respectively) m ust retain this feature in b o th regions o f the eye, despite differences in facet size. In effect, bo th parts o f the eye are still concentric but w ith different centres o f curvature an d corrected for spherical aberration. T hese eyes are highly m obile a n d can be tu rn e d th ro u g h 90° so th at the ‘u p w ard ’ region faces forw ard. T h e relative w idth o f the u p p er p a rt increases w ith h ab itat dep th an d is alm ost the only p a rt o f the eye rem aining in the euphausiid .Nematobrachion boopis (cf. the am ph ip o d Cystisoma, above) (Table 8.1). T h e aperture o f the u p p er eye is defined by the nu m b er o f cones; specics o f the euphausiid Slylocheiron live at different depths an d the nu m b er o f cones in the u p p er eye increases w ith d ep th o f habitat, providing an enlarging ap ertu re as the light becom es dim m er. D eeper-living euphausiids an d mysids have m uch less screening p ig m en t an d mysids often have a thick tapetum giving a brig h t eyeshine; euphausiids never have this feature. V isual acuity in euphausiids is lowest in the bathypelagic species o f Thysanopoda. Relative to the eye size these deep species have long, wide, crys­ talline cones an d long rhabdom s, giving high sensitivities, calculated at 4 7 5 -8 6 4 units (Hiller-A dam s an d Case 1984). T h e eyes o f Bentheuphausia amblyops arc reduced in size an d the arran g em en t o f the facets is m ore h ap h a za rd th an in any other species. Its nam e appropriately translates as ‘D eep euphausiid w ith w eak sight’. Thysanopoda mmyops, the deepest euphausiid know n (3500-5000 m), has m inute eyes w ith very few crystalline cones, although they are o f sim ilar size to those in other species o f Thysanopoda. Eye grow th slows w ith increasing hab itat depth, so the very large adults o f deep-w ater euphausiids have relatively small eves, but their shallow er juveniles have eyes o f a size com parable w ith those o f adults o f shallower, sm aller species. In general, less is know n ab o u t mysid eyes b u t in m ost bathypelagic species the eyes are either absent, greatly reduced, o r hugely m odified. In some o f these specics the eyes m ay be very large relative to the body size (.Meterythrops picta, Boreomysis megalops)', in others the optical elem ents are entirely lost an d only the rhabdom s are left, w ith or w ithout som e residual p igm ent a n d /o r tapetum (e.g. Boreomysis scyphops, Pseudomma spp., Petalophthalmus). In these anim als the rh a b d o m ’s microvilli lose their n o rm al orderly arran g em en t an d they becom e alm ost random ly oriented aggregates. T h e m ost ab u n d a n t bathypelagic mysids

THE BIOLOGY OF THE DEEP OCEAN

(species o f Eucopia) have greatly reduced eyes (which look superficially rath e r like those o f Bentheuphausia) in w hich facets are n o t recognizable. T h e giant lower mesopelagic mysid Gnathophausia has large, norm al, superposition eyes w ith a very thick tapetum an d high convergence in the n eu ral linkages from the rhabdom s, providing it w ith large receptive fields an d high sensitivity. T h e rhabdom s have a visual pigm ent w ith A, at ab o u t 495 nm , sim ilar to th a t o f Eucopia. T h e deeper specics G. gracilis an d G. gigas have sm aller eyes th an their shallow er relatives G. zoea an d G. ingens.

D e c a p o d s : a p p o s it io n e y e s , r e fr a c tin g a n d r e fle c tin g s u p e r p o s it io n e y e s

D ecapod crustaceans (shrimps, praw ns, crabs, an d lobsters) have an extraordinary variety o f optical systems, w hich include b oth apposition an d several different types o f superposition eyes. A pposition eyes in adults arc found only in a few' true crabs, h erm it crabs an d their relatives. T h ey use lens-cylinder optics an d usually have considerable am ounts o f screening pigm ent. T h e eyes o f deep-sea crabs arc small but have not been investigated in detail. T h e vast m ajority o f adult decapods have superposition eves.

P e la g ic e y e s

O nly a very few' pelagic decapods have refracting superposition eyes like those of euphausiids an d mysids, an d they arc im m ediately recognizable by the same hexagonal arran g em en t o f facets. T h ey include som e w idespread deep-sea shrim ps (Gennadas, Benthesicymus, Bentheogennemd). T hese specics all have small eyes, bright tapeta, an d tiny individual faccts. T h e eyes o f Gennadas elegans (800 1000 m) are sm aller th a n those o f two shallow er species o f Gennadas. M ost decapods have a quite different type o f superposition eye, a reflecting one, whose optical design w'as not recognized until 1975 (Land 19806). In these eves the crystalline conc is square in section, has little refracting power, an d is lined -with reflecting m aterial (guanine o r pteridine granules) to produce a m irror-box. T his has the sam e optical result as the refracting system: light entering the box from above at an angle is reflected o ut o f it below in the same vertical plane an d at the sam e angle (Fig. 8.9). T h ese eyes necessarily have square, not hexagonal, packing o f the facets. In Lipper-ocean species the eyes have a lot o f screening pigm ent w hich, if it extends below' the m irror-box into the clear zone, will absorb any off-axis reflections an d limit the optics to a functionally apposition eye. In deeper-w ater species there is less pigm ent an d it is not mobile. D eep species o f the w idespread an d ab u n d a n t genus Acanthephyra have smaller eyes th an shallow er ones; the abyssal A. microphthalma has the smallest o f all, as its nam e implies. Low er-m esopelagic species (A. purpurea, A. pelagica) have some dark pigm entation b u t the deeper A. curtirostris an d A. stylorostralis have sm aller eyes an d no screening pigm ent. Like m ost meso- an d bathypelagic decapods they have a diffusely reflecting tapetum . In the shrim p family O p lo p h o rid ae as a w hole eve size decreases as species live deeper. T h e rhab d o m s are sm aller in the sm aller eyes,

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an d in deeper species eye grow th slows w ith increasing body size, ju st as in euphausiid shrim p (Hiller-A dam s an d C ase 1988). In the deep genus Hymenodora the eyes are small, the optical elem ents are lost, an d the eye consists o f h ypertro­ p hied rhabdom s em bedded in a tapetum . Large superposition eyes have a larger aperture an d hence a higher potential sensitivity th an sm aller ones (the large eye o f the m esopelagic shrim p Oplophorus spinosus has a sensitivity o f 3300 units, at an f-num ber o f 0.5, Table 8.1). T h ey have b etter contrast discrim ination th an sm aller eyes b u t incur a g reater m c ta­ bolic cost in their construction an d operation. A large eye renders d ark objects m uch m ore visible against a dim background light, b ut the visual contrast betw een object a n d background rapidly decreases w ith depth. However, the con­ trast o f a bright object (e.g. a lum inescent source) against the background will increase w ith depth, as the background becom es darker. T h u s the decline in eye size w ith dep th m ay be at least partly com pensated for by the increased contrast o f the likely visual targets, as well as the benefits o f m etabolic savings on eye construction an d m aintenance.

B e n th ic e y e s

So far we have only considered pelagic decapods. T h e eyes o f bottom -living decapods have different relationships betw een size an d d ep th (Hiller-Adam s an d C ase 1985). In these anim als bo th the relative eye size an d its relative grow th rate increases w ith depth. R h a b d o m length an d w idth ten d to increase w ith eve size (and therefore w ith depth). T h e differences betw een b enthic an d pelagic species are m arked; som e abyssal bcnthic species have larger eyes th an any pelagic specics o f sim ilar body size. T h e im plication o f these differences is th a t g reater sensitiv­ ity (and the potential for g reater acuity provided by a larger eye) is m ore valuable in the benthic environm ent. T h e re arc probably m ore biolum inescent visual targets on o r n e a r the bottom th an in midw'ater an d the m etabolic cost o f a large eye (in term s o f d rag an d density) is m uch less for an anim al th a t can rest on the bottom . T h ere rem ain, o f course, a n u m b e r o f benthic decapods th at have com ­ pletely lost their eyes (e.g. Munidopsis crassa, Polycheles), w hereas there are no totally blind pelagic decapods. In one particu lar group o f benthopelagic decapods (the bresiliid shrimps) evolu­ tion o f the eyes seems to have favoured eye reduction an d loss o f m ost o f the optical elem ents, resulting in small fused eyes largely com posed o f rh ab d o m s (cf. some mysids an d Hymenodora). Som e o f these shrim p have becom e associated w ith hydrotherm al vents (where they m ay be hugely ab u n d an t, C h a p te r 3, Fig. 3.11); they have uniquely extended the naked retin a out from the reduced eyestalk an d b ac lw ard s into the carapacc, w'here it forms a m uch-enlarged sheet o f rhabdom s em bedded in reflecting m aterial (Rimicans exoculata). Such an eye is sim ply a largearea p hoto d etecto r (cf. the retinal plates o f the fishes Ipnops an d .Nybelinelld), equiv­ alent to the film w ithout the cam era. T h e value o f this specialization in the vent environm ent is n o t clear; it is possible that it m ay be able to detect the infrared a n d /o r ehem ilum inescent ‘light’ that is know n to be em itted bv the h o t vents.

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Larval decapods usually live m uch shallower th an adults. T h o se species w ith small eggs a n d small larvae, even the hydrotherm al vent shrim p, all begin life w ith tran sp aren t apposition eyes and acquire their respective refracting or reflecting superposition eyes later in developm ent. A dults w ith square-faceted reflecting eyes thus start life w ith hexagonal facets. Species w ith large eggs (such as Oplophorus), in w hich m uch o f the larval developm ent takes place before hatching, em erge w ith the changeover to the superposition eye already partly u n d er way. A third type o f superposition eve (parabolic), whose optical design incorporates bo th reflection a n d refraction, is present in some crabs b u t is n ot know n in any deep-sea species. V is u a l p i g m e n t s

M ost deep-sea decapods have a single visual pigm ent w ith ^ max at 4 8 0 -5 0 0 nm , slightly blue-shifted relative to m ost o f their shallow -w ater relatives an d the same in bo th benthic an d pelagic species. T hese pigm ents will en hance the visual sen­ sitivity for b o th residual dayiight an d m ost biolum inescence. Very unexpectedly, however, all six species o f the genera Systellaspis an d Oplophorus th a t have been studied also have a visual pigm ent w ith к 400- 415 nm , sensitive to very short­ wave near-ultraviolet light, an d they have a dem onstrable behavioural response to the sam e wavelengths. M ost o f these are vertically m igrating mesopelagic species w ith ventral photophores, an d they could experience some residual n ear­ ultraviolet light dow n to ab o u t 600 m , but there is one species (S. braueri) w hich is bathypelagic, living at depths well below any significant U V p en etration, an d has no photophores. N o com pletely satisfactory ecological explanation has yet been proposed for the extra visual pigm ent, but the m ost plausible ideas are th a t the two pigm ents m ight be used for discrim inating betw een different sources o f bio­ lum inescence, for exam ple those o f oth er individuals an d o f o th e r species, or for d ep th discrim ination by assessing the ratio o f the two w-avelengths in the dow n­ welling light (Cronin a n d Frank 1996). D espite their two visual pigm ents these deep-sea shrim p do n ot even appro ach the visual complexity? o f the reef-dwelling m antis shrim ps (stomatopods) w hich have an extraordinary array o f up to 16 com binations o f visual pigm ents, colour filters, an d polarization sensitivities in their om m atidia! T h e re are no really deep-w ater m antis shrim ps b u t there are a few th a t live at 100 m or so. Shallow species have several colour filters in their retinas. T h e deep species have the sam e set o f visual pigm ents as the shallow er ones but the colour filters vary' in individuals in relation to their dep th (and therefore light environm ent), thus d em onstrating y'et an o th er visual refinem ent o f these rem arkable anim als (Cronin et al. 2000).

Conclusion T h e visual systems o f oceanic anim als are finely tu n ed to the differing light co n ­ ditions at different depths. At m esopclagic depths the tu b u lar eyes o f fishes and

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cephalopods, the divided apposition eyes o f am phipods, an d the divided super­ position eyes o f euphausiids an d mysids provide three different optical solutions to the challenge o f sighting dark objects against the brightest available back­ ground. Anim als w hich choose to live at different depths at different stages o f their life history ad a p t the eye structure a n d /o r the visual pigm ents to th eir dif­ ferent habitats. Below the influence o f sunlight there is a very high p rem iu m on sensitivity, achievable equally in cam era-type eyes an d in b o th apposition and superposition com pound eyes, though w ith a trade-off in resolution. A t the greatest depths eyes are often (but by no m eans always) reduced in size or com ­ plexity but are still largely retained. Vision is only one o f several senses an d it m ay be regarded as a ‘bon u s’ sense in deep water. Som e species m anage w ithout vision th ro u g h o u t their adult lives an d if others (e.g. undersize Jfepkrops) are acci­ dentally deprived o f it the result need n o t be fatal. T h e only visual stimuli at bathypelagic depths are the biolum inescent signals o f o th er organism s; the c h a r­ acteristics o f these light sources are explored in the next chapter. T h e eyes of many, probably m ost, deep-sea anim als are overw helm ingly dedicated to the detection an d interpretation o f such signals.

9

Camouflage, colour, and lights

Camouflage and colour We have seen in C h a p te r 8 how the light environm ent in the ocean is fun­ dam entally different from th a t on land. O nly at the edges o f the ocean arc there any real similarities to the small-scale structure an d optical com plexity present in fields, woods, or streams. It is here th a t the w ater is shallowenough, an d the light bright enough, for bottom -living plants to flourish as thickets o f algae an d sea-grass, an d for corals to exploit th eir photosynthetic sym bionts in the exuberance o f tropical reefs. Prey an d p redators in these environm ents seek constantly to outm anoeuvre each o th er by disguise an d subterfuge. Vision is such a dom inan t sense in these well-lit habitats th at m uch o f the survival strategy is tuned tow ards seeing yet n o t being seen— except w hen necessary T h e bright, broad-spectrum light, w ith its changing directions, an d the clut­ tered space w ithin w hich cach anim al moves present b oth challenges an d opportunities for individual cam ouflage or display. O n a single tree the colours an d shapes o f the green bug on a leaf, the brow n caterpillar on a twig, or the m ottled m o th on the bark attest to the variety o f background w ith w hich each has to cope. T h e options for cam ouflage arc either to persuade the observer th a t you are not there at all or to persuade th em th a t you are som ething quite different. D isplay is the converse, in th at it is a deliberate attem p t to attract attention (usually o f the opposite sex) an d to em phasize your presence. T h e purely visual elem ents o f b oth cam ouflage and display are often reinforced by appropriate behaviour patterns. T h ere are spectacular terrestrial exam ples o f b o th strategies, epitom ized by the insects th a t m im ic bird droppings an d the flam boyant displays o f birds o f paradise, an d they have their parallels in the reef an d shallow -w ater faunas. A nim als here, as on land, have the additional option o f hiding in the nooks an d crannics o f the habitat, w hich m ay also prove m ore defensible refuges. T his is n ot an option for oceanic animals; throughout their lives they have no cover or hiding-place from the eyes o f others yet still need briefly to signal o r display their sexual w ares (McFall-Ngai 1990; H a m n e r 1996). Background is a w ord im bued w ith all the overtones o f terrestrial life. O nly at the b ottom o f the occan is there ‘g ro u n d ’ in the terrestrial sense, an d m ost m idw ater anim als are likely to encounter it only as sedim enting post-m ortem particles. T h e

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background against w hich they live their daily lives is provided by the light envi­ ronm ent and, as discussed in C h a p te r 8, this changes rapidly w ith depth. T h e key features for cam ouflage in the m esopelagic realm (just as for vision) are the u n i­ form ity o f the light environm ent in all lateral directions, w ith the highest intensity com ing from above (Fig. 8.2) an d the restriction o f the spectrum to blue wave­ lengths. In deep er w ater the uniform ity is com plete, w ith darkness all around. At the start o f this book I em phasized the vertical separation o f recognizable h ab i­ tats in the occan; the grad ien t in the quantity an d quality o f am b ien t light plays a m ajor role in setting the habitat levels an d determ in in g their characteristics. So m uch so that, w ith a little experience, it is possible to judge from the colours o f the anim als in a daytim e traw l ju st w here in the u p p er 1500 m they have been living.

Upper-ocean camouflage In the bright light close to the surface o f the tropical ocean m any anim als are blue, closely m atching the blue o f baekscattered daylight. T h e blueness is achieved in m any different ways. C rustaceans, particularly pontcllid copepods, achieve a royal-blue colour w ith a carotenoprotein pigm ent. T his is very sim ilar to the blue colour o f a (live) lobster an d consists o f a red carotcnoid pigm ent (usually astaxanthin) com bined w ith a protein. I f any o f these anim als are cooked they tu rn red: the carotenoid is released from the d en atu red protein an d the blue colour is lost. R ed carotenoids colour everything from carrots to flamingos; they arc accessory photosynthetic pigm ents in plants an d can n o t be synthesized by anim als. Ju st as flam ingos get their carotenoids from their diet, so do oceanic anim als. Blue carotenoproteins are to be found in m any o th er near-surface anim als particularly the cnidarians Velella an d Porpita w hich float at the surface (C hapter 5). T h e related siphonophore Physalia, the Portuguese M an o ’ War, is also blue, but this colour is p roduced by a biliprotein, a com bination o f a bile pigm ent an d protein. A blue colour can also be achieved structurally, w ithout any blue pigm ent. T h e near-surface oceanic isopod Idotea metallica is pow der blue over its u pper surface. In this anim al the colour is produced bv the g reater backscattering o f the shorter (blue) w avelengths o f sunlight by tiny crystals in the epiderm is, while a dark pigm ent ben eath the crystals absorbs the longer (red) wavelengths. S cattering by very small reflective particles is pro portional to I /А / (C h ap ter 8) an d the colour o f the anim al is p roduced by m uch th e sam e process as the colour o f the sea, no d oubt helping it to achieve a m atch. T h e entirely differ­ ent m echanism s by w hich different anim als achieve a sim ilar blue en d-product em phasize th a t the visible (reflected) colour is w hat m atters. Its cam ouflage value is easily appreciated, bo th for the crustaceans avoiding visual predators an d for the siphonophore traw ling for eyed prey w ith its long blue tentacles. Blue reflectance m ay also provide some protection against potentially dam aging short-w avelength radiation.

THE BIOLOGY OF THE DEEP OCEAN

Transparency M any anim als in the u p p er ocean are highly transparent. T his is potentially the best cam ouflage o f all, but the ways o f achieving it are b o th lim ited an d lim it­ ing (C hapm an 1976; Jo h n sc n an d W idder 1999). Perfect cam ouflage by tran s­ parency requires the object to have the sam e transm ission characteristics as those o f the surrounding m edium . A n anim al m ad e entirely o f seaw ater would be perfect— b u t im practicable. C ellular organization an d tissues require m ore th an ju st seawater. However, if a large volum e o f seaw'ater-equivalent is incor­ p o rated into the tissues the anim al m ay get very close to the ideal. T his is exactly w hat m any gelatinous anim als do. A thick layer o f acellular w atery m aterial of uniform refractive index (the m esogloea in jellyfish) separates the very thin cel­ lular layers. It is always strange to recognize the presence o f such an anim al in a plankton sam ple not by seeing it directly b ut by being awrare o f an unexpected space betw een the o th e r animals! T h e additional associated benefits o f buoy­ ancy (C hapter 5) an d increased size (C hapter 10) m ake this an attractive evolu­ tionary option, exem plified particularly by jellyfish, siphonophores, salps, an d som e crustaceans, squid, an d pteropods. T h e dow nside is the relative im m obil­ ity o f this inert w atery mass. By incorporatin g w'ater the refractive index o f the additional m aterial is g uaranteed to be sim ilar to th at o f the surrounding sea­ water. T his is im portant, because even if the m aterial is highly transparent, reflections will still occur at the interface betw een the anim al tissues an d the sur­ rounding ocean water, if there is a significant difference in refractive index betw een them . O th e r tissues such as muscle, nerves, an d cartilage have a differ­ en t an d m uch m ore com plex com position b u t as long as th eir com ponents do not absorb or scatter light m uch m ore than seawater, they too will be effectively transparent. Tissues can also be m ade tran sp aren t if the cellular com ponents are arran g ed in a regular way. T h e lens an d cornca o f the vertebrate eye achieve their rem arkable clarity by regular arrangem ents o f the fibrils o f the proteins crystallin and colla­ gen, respectively, w hich result in destructive interference o f scattered light (Johnsen 2000). T h e regularity o f muscle fibrils probably m akes a sim ilar co n tri­ bution to the transparency o f anim als such as fish larvae, chaetognaths, an d larvaceans. I f the fibrils or particle diam eters are very small w hen co m p ared w ith the w avelengths o f visible light (i.e. m uch less th a n 500 nm) it is relatively u n im ­ p o rta n t how they are orientated. T h e m easured transparencies o f a variety o f gelatinous planktonic anim als range from 50 to 90% . T h e effectiveness o f different levels o f transparency depends on the m inim um contrast that the observer’s visual system can detect. T his is greatly affected by the light intensity. T h e contrast threshold o f a co d ’s eye, for example, increases from an optim um o f 0.02 at light intensities equivalent to those in the top 200 m o f the open ocean to 0.5 at the light intensity prevailing at 650 m in the clearest ocean waters. A t this depth the cod would be unable to detect any tissues w ith a transparency o f 50% or m ore at any distance above it. Because the contrast threshold falls rapidly with light intensity, the effectiveness of

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transparency cam ouflage increases dram atically w ith d ep th (Johnsen an d W idder 1998; Joh n sen 2000). T ransparency o f cellular tissues requires active m aintenance. It is quite rem ark ­ able how w hole tran sp aren t anim als such as arrow w orm s an d fish larvae rapidly becom e milky a n d opaque as they die, an d how the muscles o f shrim p blanch u n d er severe stress, w hereas jellyfish, in general, a n d the acellular m esogloea, in particular, rem ain tran sp aren t for long periods after death. In a few species transparency is reversible. T h e siphonophore Hippopodius is glass-clear m ost of the tim e b u t can blanch rapidly if stim ulated. T h e blanching is caused by small granules spreading throughout the m esogloea an d scattering the light. It may help to p rotect the anim al against further accidental collisions w ith fish an d o th e r anim als. T h e siphonophore regains transp aren cy in 15-30 m in if left undisturbed. T ransparency o f muscle an d o th e r active tissues, an d o f w hole anim als, is m ore easily achieved if one dim ension is very thin. T h e w afer-thin phyllosom a larva o f the lobster is a prim e exam ple. A blade-like o r leaf-like body form is quite consistent w ith m uscular sw im m ing by m eans o f lateral waves an d is exem pli­ fied by the tails o f larvaceans an d fish larvae. M ost striking am ong the latter are the leptocephalus larvae o f deep-living eel-like species; som e o f these larvae m ay exceed 25 cm in length an d 5 cm in height yet be only a few' m illim etres in w idth an d com pletely transparent, ju st occasionally given away in b rig h t light by a reflective sheen from the muscle sheaths. T ransparency m ay n ot always be as effective a ploy as it appears. Passage o f light th ro u g h a tran sp aren t anim al affects the polarization characteristics an d anim als w hose eyes can detect the polarization, such as cephalopods, m any crustaceans, an d some fishes, m ay be able to break the cam ouflage th a t transparency otherw ise provides (Shashar et al. 1998; Joh n sen 2000). Som e tissues can n o t be m ade tran sp aren t an d others are deliberately opacjue. T h e siphonophore Agalma okenii has opaque nem atocyst batteries on the tips o f the tentacles b u t is otherw ise transparent. T h e nem atocyst batteries are used to attract prey by m im icking the ap pearance o f copepods. Eyes m ust contain lightabsorbing pigm ent an d therefore can n o t be wholly tran sp aren t. E xperim ents w ith freshw ater planktonie crustaceans have show n th a t those w ith large dark evespots are the first to be eaten by fish predators. T h e sam e is u n doubtedly true in the open ocean. We have seen already how m ost o f the volum e o f the enlarged eyes o f som e hyperiid am phipods (e.g. Phronima) can rem ain almost tran sp aren t because o f their optical design (C hap ter 8), an d the sam e is true for the large an d often elongate eyes o f the larvae o f m any decapod shrimps. It is n ot possible to m ake a large cam era-type o f eye even p artly tran sp aren t, so in fish a n d squid, for exam ple, these organs are particularly vulnerable to detection by visual predators, no m atter how tran sp aren t the rest o f the anim al m ay be. Food is usually opaque (and even if it was originally tran sp aren t it becom es opaque d uring digestion), w ith the result th a t the stom ach a n d liver arc organs w hich need to be cam ouflaged.

THE BIOLOG Y OF THE DEEP OCEAN

Silvering T h e solution for a necessarily opaque structure is for it to m im ic transparency; this can be done w ith silvering. In the predictable light distribution o f the m esopelagic environm ent a vertical m irror will be invisible from all angles o f view, except im m ediately above and below (Fig. 9.1). T his is solely because the light environm ent is sym m etrical ab o u t the vertical axis; the effect is in d ep en d en t o f the dow nw elling intensity an d therefore applies al all depths. A n anim al has only to tu rn itself into a vertical m irror and it, too, will be invisible from the side. T his is how m ost uppcr-ocean fishes cam ouflage themselves (e.g. sardines an d silversidcs). T h e m esopelagic hatchetfishcs arc am ong the best exam ples o f this strat­ egy. T hese fish are so laterally flattened th at their flanks are vertical in the W’ater, their bodies arc only a few m illim etres thick, an d th eir height is ab o u t the same as their length. T h e w hole flank is extensively silvered so th a t a fresh specim en has the m irror-like appearance o f alum inium foil. T h e silvering is achieved by tiny reflective crystals o f guanine precisely arran g ed parallel to the surface in m ultiple stacks o f defined orientation and spacing (D enton an d L an d 1971; L and 1972). T h e constructive interference produced by only 5 - 1 0 appropriately spaced layers o f altern ate high- an d lowrrefractive-index m aterial (in this case guanine an d cytoplasm) can produce alm ost 100% reflection o f incident light (Fig. 9.2). T h e colour th a t is best reflected by any particu lar crystal stack is d eterm in ed by the crystal separation. For a given w avelength the m ost efficient reflection is achieved w hen each layer in the stack has an optical thickness (i.e. actual thickness X refractive index) of one-q u arter o f the incident wravelength. T h u s a stack in w’hich each layer has

Fig. 9.1

Diagram to show how a dark object can be camouflaged in the radially symmetric radi­ ance distribution of the ocean (Fig. 8.2) by making it reflective. A fish looking at a reflec­ tive vertical mirror (M) cannot distinguish between reflected rays (R) and direct rays (D), so the mirror (or silvered fish) is invisible. (From Bone et al. 1995, after Denton 1970, with kind permission from Kluwer Academic Publishers.)

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an optical thickness o f 125 nm m ost efficiently reflects 500 n m blue light at n o rm al (90°) incidence. It is an ‘ideal’ quarter-w avclength reflector because constructive interference betw een the reflections occurs at every interface. Similarly constructed crystal stacks produce the tapetal reflections in the eyes o f m any fish, as noted in C h a p te r 8 (H erring 1994). As the angle o f incidence o f the light becom es m ore acute the best-reflected w avelengths shift further into the blue (i.e. tow ards shorter wavelengths). T h e spectral b an d w id th o f the reflected light is d eterm ined by the optical thicknesses an d regularity of spacing o f the stacks. In the near-m onochrom atic blue light experienced by hatchetfishcs the stacked reflectors have only to reflect blue light, b u t for com plete cam ouflage n ea rer the surface all wavelengths need to be reflected. In the h errin g each scale has areas in w hich th e stacks arc differently spaced an d therefore reflect different colours. T h e overlapping arran g em en t o f the scales ensures th a t at any location the dif­ ferent areas overlay one another, giving com plete spectral coverage an d silver reflection (D enton an d N icol 1965). An alternative solution is for different crystal stacks to reflect different colours; this ‘pointilliste’ effect is on too small a scale to be detected by an observer a n d the result is th a t the overall reflection appears silvery. T h e high refractive index m aterial need not be guanine. M any squid, cuttlefish, a n d octopods also have m irror-like silvery regions but they use stacks o f proteinaceous discs or ribbons in their reflectors, again frequently in very regular Fig. 9.2

Arrangement of a constructive interference reflector: light incident on a thin layer o f high refractive index (R.l.) n and thickness t (left) is partially reflected at the upper and lower interfaces. Light reflected at the upper interface, between low- and high-refractive index media, undergoes a phase change of half a wavelength. For a given wavelength X, if n t = %I4 the tw o reflections will be in phase and show constructive interference. An alternat­ ing stack of such layers (right) is a very efficient reflector, with maximum reflectance at wavelength A. when = n2t2 = л/4. (Reprinted from Herring 1994, with permission from Elsevier Science.)

THE BIOLOGY OF THE DEEP OCEAN

arrays (Fig. 9.3). T h e reflective cells are know n as iridophores an d the reflective stacks as iridosomes. A great advantage o f these m ultilayer reflective structures is th a t they can be p u t anyw here. In an anim al w hich is largely tran sp aren t b u t still has the problem o f cam ouflaging the dark eyes an d liver, the reflectors can be placed on the organs w hich are at m ost risk o f detection. Single organs o r body regions can be treated in ju st the sam e w ay as w hole anim als. T ran sp aren t fish larvae, like squid, usually have silvering over the w hole o f the eyeball. M aking the organ m ore nearly vertical will enhance the effect o f the silvering an d this is the reason for the spindle-shaped livers an d vertically elongate eyes o f som e larval an d juvenile squid noted in C h a p te r 8. M irro r cam ouflage requires th at the m irro r be vertical. W hile this is easily achieved in hatchetfishes an d a few other fishes in w hich the flanks are vertical, it is n o t practicable for a muscular, active fish such as a tu n a o r h errin g to flatten the body to the sam e degree. In these fishes the bodies are w ide an d the flanks are curved. T h e crystal stacks no longer lie parallel to the body surface b ut are independently oriented so that each individual stack is aligned vertically. T h e fish effectively has m yriad tiny vertical m irrors em b ed d ed in its sides (Fig. 9.4). O nly specular (mirror-like) reflectors will do for this kind o f cam ouflage; a

Fig. 9.3

Electron micrograph of a group of multilayer interference reflectors in the photophore of the squid Selenoteuthis. The platelets (dark) are spaced about 120 nm apart. In cephalopods the high refractive index material in the platelets is proteinaceous; in fishes it is usually guanine.

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diffuse reflector com posed o f granules o r o f uno rien ted crystals w ould n ot reflect incident light at the angle required to m im ic the background. Diffuse reflection is utilized in a m ore general w ay by sharks, for exam ple, for w hich it provides a w hite ventral countershacling against the d ark dorsal surface. L ateral m irrors ca n n o t cam ouflage the u p p er surface o f a fish; were the silver­ ing to be continuous over the u p p er surface o f a hatchetfish the reflection o f the dow nw elling light w ould m ake it horribly conspicuous w hen viewed from above. T h e hatchetfish reduces the problem by being so thin an d by having a dark pig­ m ented u p p er surface. T h e reverse problem applies from im m ediately below; the anim al will be seen as a silhouette against the dow nw elling light. T h e crosssectional profiles o f epipelagic fishes tap er ventrally which, w ith silvering, reduces the visibility b u t does not elim inate it completely. In d eep er w aters perfect cam ouflage can be achieved by the positioning o f lights along the u n d er­ side o f the fish to provide m atching counterillum ination (D enton 1970; see below7).

9.4

Reflectors aligned to the curve of the body surface would not be an effective camouflage for the flanks o f a muscular fish o f elliptical cross-section. The diagram shows how in a cross-section of a herring the individual reflectors are aligned vertically, providing an effective vertical mirror surface. (From Denton and Nicol 1965, with permission from Cambridge University Press.) Dorsal

\

i

Ventral

THE BIOLOGY OF THE DEEP OCEAN

Camouflage in deeper water At m esopelagic depths dow nw elling daylight an d its diel changes have a m ajor effect on the fauna. Unless they move up an d dow n at rates ap p ro p riate to m ain ­ tain themselves at a constant light intensity (or isolume) they will experience daily fluctuations in illum ination. M any anim als do n ot slavishly ride the isolumes (C hapter 4) an d they therefore need to a d a p t their ap p earan ce to m aintain cam ­ ouflage. T h e lateral silvering o f hatchetfish, so effective by day, could be a liabil­ ity at night w hen flashes o f biolum inescence m ight com e from any angle an d be reflected off the m irro r surface. In order to reduce this risk some o f them disperse dark chrom atophores over the silvering at night to reduce the reflectance. C rustaceans have never evolved body silvering. L arger shrim ps at mesopelagic depths are ‘half-red’, that is partly tran sp aren t an d partly pigm ented by a few very large, dorsal, red chrom atophores. T hese prevent upw ard reflection o f dow n­ welling light a n d the pigm ent can disperse or aggregate in accordance w ith the changes o f light intensity. T h e red pigm ent is the sam e carotenoid, astaxanthin, as th a t present in the blue carotenoproteins o f the near-surface fauna. Below about 600 m the appearance o f the fau n a changes quite rapidly. Silveriness in fishes becom es first m ore bronze an d then disappears; the ‘half-red’ o f shal­ low er shrim p becom es m ore nearly all-red; tran sp aren t m edusae are replaced by species w ith red, brow n, or p u rp le hues. A t bathypelagic depths (> 1 0 0 0 m) the fauna is alm ost uniform ly dark. Fish are velvet-black, uniform ly p igm ented by m elanin granules located in tiny chrom atophorcs whose distribution can n o t be altered. Shrim ps are uniform ly scarlet an d also unable to change th eir ap p e ar­ ance. T h ey have a m ultitude o f tiny red chrom atophores spread all over the body as well as pigm ent em bedded in the cuticle. M edusae are chocolate-brow n or purple, m any o f them containing large quantities o f po rp h y rin pigm ents. T h e key factor is that the pigm entation is uniform , m att, and in all cases absorbs blue light. T hese anim als arc not black, scarlet, or purple: they are all effectively black in the light environm ent in w hich they live. T h e ir pigm ents cam ouflage them by p re ­ venting the reflection o f any flashes o f blue biolum inescencc; the anim als will still m atch the background darkness regardless o f the direction from w hich the biolum inescence m ay come. T h e ir ‘colours’ do n o t exist w ithin their ow n h ab itat— they only ap p e ar w hen the anim als are exam ined on deck in daylight by som eone w ith colour vision (or are pickcd out in the ‘w h ite’ floodlights o f a submersible). N ot all anim als fit the group stereotypes: there are a few' black an d p urple crus­ taceans as well as a few scarlet fish, but they arc the exceptions. O th e r kinds of bathypelagic anim als, w hether ncm ertinc w orm s, pelagic holothurians, com bjcllies, or cephalopods, have sim ilar characteristics; the)' are orange, scarlet, purple, brow n, or black— but never blue. D uring the developm ent o f m any bathypelagic specics the juveniles live at m uch shallow er depths th an the adults (C hapter 4). T h e colours o f the different stages arc appropriate to their depths an d change as the anim als descend. Juvenile mesopelagic shrim p such as Systellaspis debilis are half-red in th eir early stages and becom e uniform ly scarlet w hen adult an d living deeper. Shallow-living near-

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tran sp aren t fish larvae rapidly acquire black chrom atophores during their devel­ opm ental descent to the bathypelagic depths o f the adults. T h e even pigm entation o f anim als continues thro u g h o u t the bathypelagic zone an d changes only' w hen the seabed is reached. H ere the d ark colours o f the b athy­ pelagic spccics often m ake way for a paler, m ore anaem ic appearance. O n the abyssal floor grey-brow n rattails, chalky-white squat lobsters, an d pale h ydrother­ m al vent shrim p take over from the black anglerfishes an d scarlet decapods n ot far above, ju st as pale sedim ents replace the infinite blackness o f deep water. D espite the ap p a ren t correlation betw een pale sedim ents an d the lack o f anim al colour it seems unlikely th a t there is enough biolum inescencc at d ep th for these colour differences to be adaptive in term s o f cam ouflage against the pale sedi­ m ent background. Nevertheless, there are m any specics th a t still have functional eyes. Perhaps there is so little biolum inescence th a t the light environm ent is closer to that o f a cave, w ith its typically unpigm ented fauna. But this still docs not explain why the faunas are so unpigm ented, unless a light stimulus is necessary to stim ulate the deposition o f pigm ented m aterial. All the red carotenoid pigm ent in bathypelagic crustaceans an d oth er anim als has to be acquired through the food chain, because anim als can n o t synthesize these pigm ents. It is possible th a t the food preferences o f some seafloor crustaceans (e.g. the vent shrim p Rimicaris exoculata) m ay not contain en ough carotenoid residues to colour the body. T his hypothesis cannot, however, explain the paleness o f oth er anim als such as fish, w hich are perfectly capable o f synthesizing the m elanin w hich cloaks their bathypelagic relatives ju st above. M id w ater rattails such as specics o f Odontomacrurus an d Cynomacnirus, for exam ple, arc m uch darker th an their benthopelagic cousins. Pale colouration is an adaptive feature in shallower, illum inated benthic habitats so perhaps as the b o tto m fauna gradually spread downw’ards into the deep sea they simply retain ed the character, never having cause to acquire the dark cam ouflage o f the m idw ater inhabitants. Nevertheless, there is light in the depths o f the ocean a n d there are eyes to sec it.

Lights in a dark environment: bioluminescence T h e ability to em it visible light (bioluminescence) is one o f the m ost characteris­ tic features o f m any deep-sea organism s. Relatively' few' terrestrial organism s have this capability; fireflies an d glow'-worms are exceptional an d d ram atic cases. O ceanic life is different; biolum inescent species occur in at least 12 anim al phyla as w'ell as in the E ubacteria an d Protista. U nfortunately, many7 o f the deep-sea fauna arc know7n mainly' from specim ens w hich either w ere already dead w hen recovered from nets o r trawls o r w ere quickly preserved for later identification. As a consequence their physiological systems arc little know n an d th eir potential for biolum inescence mostly unexplored. C areful exam ination o f freshly' caught spe­ cimens, captu red w ith less-dam aging sam pling techniques (C hapter 1), has steadily increased the range o f oceanic organism s know n to be biolum inescent. In

THE BIOLOGY OF THE DEEP OCEAN

recent years, for exam ple, octopods, arrow w orm s, sea squirts, starfish, sea cu cu m ­ bers, sea lilies, larvaceans, an d m any families o f cnidarians, crustaceans, an d fish have been ad d ed to the list (H erring 1978, 1987; H astings an d M o rin 1991). Biolum inescence has always h a d a fascination for m ankind, far beyond its lim ited terrestrial expression. T h e earliest observers found the p ro duction o f cold light by living organism s particularly bew ildering because in their lives light was norm ally inseparable from heat. It was only later in the seventeenth century th a t chem ical light production (chemilumincscence) was recognized, in the form o f a blue light produced by the air oxidation o f phosphorus (itself o b tain ed from distilled urine). As a consequence, for m uch o f the eighteenth an d n ineteenth centuries biolum inesccnce an d phosphorus wrere assum ed to be somehow7associated. T h e biolum i­ nescence o f the surface waters, witnessed a n d m arvelled at by every seafarer, was therefore routinely b u t inaccurately described as phosphorescence— a nam e that has stuck ever since. T h e biolum inescent abilities o f m any deep-sea anim als are largely inferred from the presence o f com plex photophores or light organs. In m any cases (probably most) their biolum inescence has not been observed directly b u t is assum ed, based on the structural sim ilarity to photophores o f oth er anim als o f proven light emis­ sion. U sing these criteria the abundance an d distribution o f biolum inescent species can be assessed. A t depths greater th an 500 m in the eastern N o rth A tlantic m ore th a n 70% o f the specics o f fish, an d 90% o f the individuals, arc lum inous. C om parable figures for decapod crustaceans are alm ost 80% b o th o f species an d individuals from the surface to 500 m , an d 65% o f the species an d 41% o f the individuals at 500 -1 0 0 0 m. All b u t one o f the 87 species o f euphausiid shrim p (> 9 9 % o f individual euphausiids in the u p p er 1000 m) is b io­ lum inescent. A dd to these figures the fact th at 2 0 -3 0 % o f all copepods dow n to 1000 m arc also lum inous (as are m ost o f the ostracods) an d the overw helm ing im portance o f biolum inescence in the deep sea is im m ediately obvious.

Bioluminescence chemistry Biolum inescence is the biological harnessing o f p articu lar chem ilum inescent reactions to produce visible light. T h e reactions are oxidations in wiiich a small organic m olecule, know n generically as luciferin, is raised to a chem ically excited (higher energy) state in the presence o f an enzym e (luciferase). T h e cxcited-state luciferin th en decays to the stable ground state an d the energy released appears as light, rath e r th an as heat w hich is the m ore usual p ro d u ct o f o th er oxidation reactions (Fig. 9.5). T h e energy can alternatively be tran sferred to another, fluor­ escent, m olecule w hich then emits light o f its ow n characteristic colour. T h ere are m any chem ically different luciferins an d each species m ay have its own luciferase. Strangely, one p articular type o f luciferin is widely em ployed by oceanic anim als, an d occurs in organism s from at least seven phyla. It is know n as coelenterazine because it was first identified from coclenterates. It is form ed from a tripeptidc, containing two residues o f tyrosine an d one o f phenylalanine,

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Fig. 9.5

Diagram of the bioluminescent reaction system. A molecule of luciferin is oxidized in the presence o f the enzyme luciferase and raised to an unstable excited state (*), from which it decays to a stable product (oxyluciferin) with the emission o f a photon of a particular wavelength. Alternatively, the energy from the reaction can be transferred to a fluor, which then emits light at its own characteristic wavelength. Accessory fluor

whose ends link to produce a cyclic molecule. In som e anim als the luciferin an d luciferase can be com bined in the form o f a single extractable protein, know n as a photoprotein. T h e photoproteins o f cnidarians (e.g. aequorin from the m edusa Aequorea) contain coelenterazine a n d require only the addition of calcium ions to em it light. T h ey have been m uch used as experim ental tools to follow' the m ovem ent o f calcium in the cells o f o th er organisms.

Luminous bacteria T h e sim plest lum inescent organism s in the oceans are bacteria. T h ere are ab o u t h a lf a dozen species o f lum inous bacteria (variously assigned to the genera Photobacterium, Vibrio, an d Sheivanella) w hich have been cultured from seaw'ater samples. T h ey have different tem p eratu re preferences; som e species are found only in w-'arm surfacc w aters (Photobacterium (— Vibrio) fscheri, P. leiognathi) while others are present in colder a n d /o r deeper w'aters (P phosphoreum). T h e ir relative ab u ndance n ea r the surface changes wdth the seasons, reflecting the changes in w ater tem perature. A lthough they can be cultured from seaw ater it is n ot d e a r w hether they are truly free-living or are norm ally associated w ith particles such as m arine snow. B iolum inescent bacteria are also found on the skin an d in the gut flora o f m any m arine anim als a n d the ‘free-living’ ones are som etim es considered as basically in transit betw een host sites. In the best-studied species (e.g. P. fischeri) individual b acteria do n o t lum inesce in isolation but only at high population densities. T his is because the cellular m achinery th a t controls luciferase production is only sw itched on w hen an ex tra­ cellular ‘autoin d u cer’ (produced by the b acteria itself) reaches a high enough con­ centration in the surrounding m edium . T h e luciferase tu rn s on the light an d the b acteria glow continuously. T h e ir luciferin is a flavin, quite different from the luciferin o f any o th e r m arine organism . O n e potential benefit o f biolum inescence to the bacteria is th a t their glow ing accum ulation on particles such as faecal pellets o r m arine snow m ay encourage anim als to eat these particles, thereby transferring the bacteria to the nutritionally rich environm ent o f the h o st’s gut. Even if they w'ere sw itched on, one o r two bacteria w ould n ot produce enough

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light to be visible. T h e delay produced by the au toinduction process ensures that the cells are sufficiently num erous for their light to be seen.

Bacteria as luminous symbionts A few groups o f anim als have harnessed lum inous b acteria as th eir light sources an d do n o t m ake their own luciferins an d luciferases. T h e symbiotic b acteria are cultured in special organs an d their light is used for a variety o f purposes. B acterial light organs are present in several u n related groups o f shallow -w ater an d deep-sea fishes (Haygood 1993). T h e m ost num erous o f the form er are the flashlight fishes (Anom alopidae) an d pony fishes (Leiognathidae). In the deep sea the ccratioid anglerfishes a n d som e argentinoid fishes (e.g. Opisthoproctus, Winteria) provide m idw ater exam ples, while the slope-dw elling rattails (M acrouridae) an d some deep-sea cods (M oridae) are benthopelagic fishes w ith lum inous bacteria (Fig. 9.6). A few shallow -w ater squid also em ploy lum inous bactcria. E conom ical though it m ay seem to have an in d ep en d en t source o f light, the culture o f lum inous sym bionts presents its own problem s (H erring 1977). First, the bacterial culture has to be m aintain ed in optim um condition, or the light goes out. Second, the bacteria m ust be localized and n o t allowed to spread throughout the h ost’s body. T h ird , unless the light is to be on all the tim e its emission m ust be u n d er the host’s control, an d finally the right species o f b ac­ terium m ust be either transferred to the next generation or acquired anew

Fig. 9.6

Several deep-sea species have luminous bacterial symbionts as their source of light. Female anglerfishes, such as this 55-mm Chaenophryne draco, culture the bacteria in lures that are often extraordinarily elaborate. In this species some o f the light produced by the bacteria in the main lure is conducted along an anterior light pipe and emitted from its tip. (Photo: P. 1. Herring.)

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from the environm ent. M any fishes th a t use b acteria have light organs th at develop as diverticula from different parts o f the gut. O esophageal, pyloric, rectal, an d anal diverticula all form bacterial light organs in different species. T ransfer o f sym bionts directly from one generation to the next is probably unnecessary because they can be acquired anew from the gut flora. T h ese gutassociated light organs each contain ju st one species o f lum inous bactcrium . T h e sym bionts are identical to certain know n free-living species an d can be grow n in artificial culture m edia. T h e sym bionts o f shallow, w arm -w 'ater fishes {P. leiognalhi) have a sim ilar tem perature preference to their host (i.e. pony fishes), the sym bionts o f tem perate specics are usually P. Jischeri, while the sym­ bionts o f the deep-sea cods, rattails, an d argentinoids are the cold-w ater spccies P. phosphoreum. T h e opening betw een the light organ an d the gut allows dead or surplus bacteria to be continually vented. A nim als whose light organs do not link w ith the gut have special problem s. Typical exam ples are the shallow' flashlight fishes, w hich have a large light organ u n d er each eye, an d the deep-sea anglerfishes whose b acteria are located in a bulb at the tip o f the specialized fin-ray that form s the rod an d lure. T h e light organs o f bo th groups open to the seaw^ater via one o r m ore pores through w hich the bactcria are shed, but we do n ot know- w here the bacteria com e from. T h ey cannot yet be cultured in isolation from the fish an d genetic analysis has show'n th a t they are n o t identical to any described spccics (but they are related: all fall w ithin the genus Vibrio). It is possible th a t each species o f anglerfish has a separate species o f bacterium but how-’ they are acquired is still a com plete mystery. T h e light organs o f young anglerfish contain no bacteria until they are several weeks old. Squid w ith lum inous sym bionts have light organs seated on the ink sac an d unconnected to the gut. T h e newly h atched young o f Euprymna have no bacteria in their light organs b u t w aft in bacteria {Photobacterium fisckeri) from the surrounding sea w ater using special, tem porary, ciliated lobes situated at the entrance o f the du ct to the organ. T h e m ech a­ nisms by w hich this squid achieves bacterial specificity are gradually being unravelled (M cFall-Ngai 2000). A nim als w ith bacterial light organs have only a very few' such organs, usually ju st one or two. T h e organs o f fish an d squid always o pen to the exterior, either directly or via the gut, an d the bacteria are always extracellular; in the symbiosis they lack the flagclla that characterize the free-living form s o f the sam e species. A lthough their ow ners have so few' bacterial light organs, they can nevertheless be p u t to m any uses (sec below). T h ere is one o th er group o f anim als whose light organs contain bacteria-like inclusions; these arc the pyrosomes, colonial pelagic tunicates. T h e p air o f light organs in each individual are usually tu rn ed off b u t w hen stim ulated they becom e brightly lum inescent. T h e light-em itting structures ap p e ar to be bacteria an d are intracellular. T h e light organs do n o t open to the exterior an d no th in g is know n ab o u t how the light is controlled.

THE BIOLOGY OF THE DEEP OCEAN

Self-luminous species M ost oceanic anim als do not use bacteria b u t have their own luciferin (frequently coelenterazine). It is generally assum ed that they can synthesize it themselves, b ut there are exceptions to this rule. A few species need to obtain it in the diet, rath e r like a vitam in. T his has been best dem onstrated in the coastal fish Porichthys, whose luciferin is a cyclic tripeptide (tyrosine, arginine, an d isoleucine) identical to th a t o f the ostracod Vargula. Unless Porichthys has Vargula in its diet it will not biolum inesce. T h e deep-sea mysid Gnalhophausia appears to have a sim ilar dietary need for coelenterazine as its source o f luciferin, an d there are probably other cases in w hich lucifcrins are norm ally acquired in the diet. C oelenterazine is certainly w idely distributed am ong oceanic anim als an d has been identified in b o th biolum inescent and non-biolum inescent deep-sea animals. It has been found, for exam ple, in the livers o f anglerfishes whose ow n biolum inesccncc is produced by bacteria, as well as in p red ato ry non-lum inous am phipods. In bo th exam ples it will have been acquired in the diet b u t in neither case is it involved in biolum inescence. T h e luciferins o f euphausiids an d dinofla­ gellates are chem ically quite different to coelenterazine. T h ey are both tetrapvrrolcs wiiose structures suggest th at they are ultim ately derived from chlorophyll. A dietary link betw een the luciferins o f the two groups o f organism s is possible, b u t it is difficult to reconcile the vast populations o f lum inous euphausiids in the S o uthern O cean w ith the hypothesis th a t they acquire all their luciferin from the lim ited n um bers o f lum inous dinoflagellates in the sam e region. A nim als that have their owm luciferin, an d do not use bacteria, can have any n u m b e r o f photophores. H undreds to thousands o f p h o tophores are present in m any species o f squid an d fishes (M arshall 1979; H errin g 1988). A n o th er contrast is that m ost such photophores do n o t open to the surrounding seaw'ater (or gut lum en) but are closed systems (unless they are secretory glands). T h e re is an im m ense variety o f biolum incsccnt structures, ranging from single biolum incscent cells (or photocytes) to com plex photophores w ith elaborate accessory optical devices. B acteria em it light uniform ly in all directions (isotropically) an d the sam e applies approxim ately to the intracellular light sources o f protists such as dinoflagellates an d radiolarians. Photocytes located in tran sp aren t tissues in larger anim als also effectively em it in all directions (e.g. those in larvaceans an d some crustaceans) an d these cells m ay be scattered widely over the body surface o f m any cnidarians an d holothurians. T h e biolum incsccncc o f sm aller crustaceans (e.g. copepods an d ostracods) appears in the form o f glandular secretions squirted into the sur­ rounding seaw^ater. Secretory biolum inescence is also p ro d u ced by som e cnidari­ ans, ctenophores, m any w orm s, some molluscs (including a few squid), m any shrimps, and a few fish. Few; o f these lum inous glands are particularly com plex. R eal structural com plexity is largely restricted to the in tern al p h o tophores of fishes, squid, shrim ps, an d euphausiids (H erring 1985). T h e optical com plexity usually serves to lim it the apertu re o f the photophore, while at the sam e tim e

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increasing th e efficiency an d defining the spatial an d spectral characteristics of the em itted light. T h e sim plest m odification is the provision o f a hem ispherical pigm ent cup aro u n d the photocytes; a reflector (specular o r diffuse) m ay be inserted betw een the photocytes an d the p igm ent a n d the light m ay be focused or collim ated w ith a lens o r a reflective surface in the aperture. T h e light from a small group o f photocytes can be spread over a large solid angle w ith light guides o r the light m ay be em itted at som e distance from the source after being tran s­ m itted dow n a light pipe. T h ere m ay additionally be absorption or interference filters in the apertu re o f the pho to p b o re (Figs 9.7, 9.8). M ost biolum inescence in the ocean is blue, as one W'ould expect if selection is for m axim um range, b u t there is some variability (H erring 1983; W idder et al. 1983; see also below). Benthic an d coastal species tend to have greener light (and terrestrial ones yel­ lower light).

Functions of oceanic bioluminescence T h e variety an d com plexity o f structure in biolum inescent organism s m ust surely be p u t to equivalent variety o f use. In order to recognize these uses it is necessary to study the biolum inescent behaviour o f the deep-sea fau n a— still an alm ost impossible task. M uch o f the in terpretation o f the functions o f biolum inescence in the deep sea depends on com parisons w ith those o f better-studied shallower organism s (H erring 1990). M any specific functions have been ascribed to biolu­ m inescence (some m ore by im aginative guesswork th an by observation) b ut they can be conveniently grouped into three categories: interactions w ith predators, interactions w ith prey, an d interactions w ith others o f the sam e species (M orin 1983; Young 1983).

Interactions with predators (defence) F la s h e s a n d s q u ir ts

M ost deep-sea biolum inescence is defensive. In a d ark environm ent a flash or a squirt o f light can distract or inhibit a visual p red a to r long enough for the prey to escape. For delicate anim als which are unable to escape because they are either sessile (sea-pens) o r slow-moving (ctenophores) it m ay also serve to prevent dam age being caused by repeated accidental collisions w ith larger anim als (M orin 1974). Because the intensity o f biolum inescence is m any orders o f m agnitude less th an that o f daylight, biolum inescence will be ineffective in near-surface w ater d uring the day. M ost species th a t live there are n o t biohim inescent, w ith the special exception o f m any dinoflagellates, whose buoyancy o r photosynthetic needs keep th em n ea r the surface. T h ey conserve th eir lum inescence for the night by having it u n d er the control o f a circadian rhythm . I f stim ulated d u rin g the day they do not flash, b u t at night they becom e fully com petent. H erbivorous cope­ pods feed on dinoflagellates (am ong oth er organisms) an d lab o rato ry experim ents

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Fig. 9.7

O ptical structure o f photophores: (a) point source emission o f a group o f photocytes (ph); (b) a pigment cup (p) restricts the angle of emission; (c) a reflector (r, specular or diffuse) increases the efficiency; (d) colour filters (f, either pigment or interference) in the aperture tune the spectral emission; (e) a lens (I) collimates the light output; (f) a reflec­ tive lamellar ring (Ir) further collimates light at the periphery o f the lens; (g) light guides (g) spread the emission from a small source over a wide solid angle; (h) a light pipe (Ip) trans­ fers light from the photocytes to a point of emission some distance away (as in Fig. 9.6). (From Herring 1985, with permission from the Company of Biologists.)

have show n that the flashes o f dinoflagellates can reducc the grazing pressure o f the copepods by changing their sw im m ing p attern . T his is a ‘startle’ response (Buskey et al. 1983). T h e re is an o th er positive benefit for the dinoflagellate in th at its flash acts as a ‘burglar ala rm ’ w'hich m ay alert secondary p red ato rs to the pres­ ence o f the copepod. A gain there is good experim ental evidence th at this really

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Fig. 9.8

Three means whereby a photophore can be occluded (either to shut off the light from a continuous source or to obscure a reflective surface): (A) chromatophores are expanded or dispersed; (B) the photophore is rotated so that light is directed inwards; (C) an opaque shutter is drawn across the aperture. All three methods are found in different fishes; some cephalopods use chromatophores. (From Herring 1985, with permission from the Company of Biologists.)

Open

Occluded |

works (Fleisher and Case 1995). D inoflagellates do n ot occur in the ocean depths, b u t the ‘burglar ala rm ’ value o f defensive biolum inescence by any anim al can apply at any depth. Its effectiveness, however, will dim inish w ith d ep th because the reducing num bers o f anim als deeper in the w ater colum n will m ean th at there are likely to be fewer individuals w ithin visual range o f any interaction. M any larger anim als produce defensive flashes, particularly cnidarians, ctenophores, an d dragonflshes such as Astronesthes. T h e flashes m ay serve to illu­ m inate the outline o f the anim al, perhaps as an intim idatory indication o f its size. T h e am ph ip o d Scina flashes brightly at the distal extrem ities o f p articu lar elong­ ated limbs, giving an im pression o f large size. M an y black dragonflshes have photocytes all dow n the fin rays an d tail fins an d these flash brightly w hen the anim al is disturbed. A t first the large postorbital photophores o f these fish m ay flash alone, then the fin photophores an d the o th e r epid erm al groups are also brought into play, all o f them flashing in synchrony. Repetitive flashes are a com m on phenom enon. Patches o f lum inous tissue on the heads o f fishes like Astronesthes produce repeated volleys or trains o f flashes at frequencies o f up to 5 s ' . Repetitive flashing at sim ilar frequencies is a feature o f m any cnidarians, ophiuroids, an d w orm s. In these anim als the flashes m ay spread from the source to sweep over the body surface as a prop ag ated wrave, which, w hen com bined with repeated flashing at the source, can produce a m ost d ram atic display lasting for m any scconds. In colonial anim als such as sea-pens an d siphonophores the lum i­ nous wave travels over the colonies. Such displays are particularly impressive in m any deep-sea m edusae (Atolla), siphonophores (Agalma), ctenophores (Reroe), seapens (Pennatula), brittle-stars (Ophiacanlha), an d holothurians (Pannychia). T hese anim als do not have im age-form ing eves and the biolum inescence can only be

THE BIOLOGY OF THE DEEP OCEAN

directed at oth er species. Very bright flashes m ay even have the effect o f tem ­ porarily stunning a p red a to r (M orin 1983; Y oung 1983). Som etim es the flashing is associated w ith the shedding o f p articu lar parts o f the body (arms in brittle-stars, scales in scale-worms, sw im m ing bells in siphonophores). T h e autotom izcd tissues continue to flash independently, acting as decoys o r distractions, while the rest o f the anim al escapes. Biolum inescent secretions p o u red into the w ater can have the sam e distractive effect and, if large enough, will also provide a lum inous cloud b eh in d w hich the p ro d u cer can escape, exactly paralleling the effects o f the cloud o f ink p ro d u ced by a squid in well-lit surface waters. B iolum inescent secretions are characteristic o f copepods an d ostracods and d uring an escape response are left b eh in d as gobbets o f light. M any deep-sea copepods have lum inous glands on their feet or ab d o m en an d flick o r kick the secretions away. In one copepod (Disseta) the lum inescence has a tim e delay o f a few seconds so th a t the secretory droplets ‘explode’ like an ti­ aircraft fire aro u n d the predator! Several species o f ctenophore an d the m edusa Periphylla em it a scintillating secre­ tion, apparently com posed o f thousands o f in d ep en d en t particles, each o f w hich flashes repetitively for up to a m inute. Platytroctid fishes also squirt o ut a scintil­ lating secretion from a g land ju st b en e ath the operculum . T h e m aterial consists o f groups o f cells each o f w hich contains m any lum inous granules. T h e secretion o f decapod shrim ps (e.g. Opbphorus) is pu m p ed into the exhalant respiratory cu rren t an d appears as a lum inous jet; this p articu lar shrim p can produce en ough biolu­ m inescence to brightly illum inate a w hole bucket o f seawater. T h e mysid Gnathophausia does the same, an d the effect in situ can be im agined. W illiam Beebe w atched a shrim p (Systellaspis) in an aquariu m tan k produce a ‘sm oke-ring’ o f bio­ lum inescence th a t was blow n across the tank an d th en stuck to the opposite wall. T h e squid Heteroteuthis mixes its biolum inescence w ith m ucus an d ink so th a t w hen squirted out, it too m aintains its spatial integrity for m any m inutes. If secretions o f this type produce a direct hit on a p red a to r they will en hance the b urglar alarm effect. Physical contact w ith m any w orm s an d cnidarians produces a sticky lum i­ nescent m aterial, either by secretion from gland cells or by direct adhesion of ab rad ed lum inous epiderm is, an d this will also m ark a p red a to r (Young 1983). M any secretors have oth er types o f biolum inescence as well. T h e deep-sea m edusa Periphylla, for exam ple, produces rep eated waves o f light over its u p p er surface, as well as its scintillating secretion, while the shrim p Oplophoi'us an d the platytroctid fishes have com plex photophores in addition to their secretions. T h e large bacterial suborbital pho to p h o re o f the flashlight fishes can be used defensively to m islead a predator. U sually it is rhythm ically closed (or blinked) by m eans o f a shutter, producing a sequence o f long flashes along the fish’s path. Following the direction o f the flashes w ould allow a p red ato r to anticipate the position o f the fish for a feeding strike. In w hat has been described as a ‘blink-andru n ’ escape response, the flashlight fish w hen th reaten ed turns off the light an d changes direction while it is dark, reap p earin g at an unexpected location w hen it turns it on again (M orin et al. 1975). T h e analogous b u t self-lum inous postorbital

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photophores o f m any dragonflshes (Fig. 9.9) could perh ap s be involved in sim ilar behaviour patterns, b u t we have no m eans o f observing them in their n atu ral environm ent. L u m in o u s c a m o u f l a g e

All the biolum inescent defences described above are designed to be seen. T h ere is an o th er defensive use o f biolum inescence whose purpose is n o t to be seen, or at least not to be recognized. It is the use o f ventral biolum inescence to elim inate the silhouette o f an anim al w hen seen from below against a b ackground o f dim dow nw elling daylight o r m oonlight. It is described as counterillum ination, by analogy w ith the principle o f countershading em ployed by m any terrestrial (and u pper ocean) anim als. In countershading a paler underside serves to reduce the overall contrast o f the anim al by lightening the shaded p a rt o f the body. Biolum inescent counterillum ination w ould serve no purp o se in the uniform d ark­ ness at bathypelagic depths; it will be o f greatest value to those m iddle-sized mesopelagic anim als th a t live at depths w here the daylight is still a factor an d whose silhouette w ould be very visible, yet are not large enough or swift enough to disregard the risk from p redators below (particularly those w ith upw ardly directed tubular eyes; C h a p te r 8). T h ere are very close links betw een the dep th distribution an d size o f an anim al an d the ventral distribution o f its photophores. A m ong the bathypelagic fauna ventral photophores are rare a n d tiny, probably only o f use in the shallower-living

Fig. 9.9

Large postorbital photophores in fish such as the black dragonfish Melanostomias are used both to illuminate prey and for sexual signalling; males have larger ones than females. M ost of these photophores can be rotated (Fig. 9.8). (Photo: P. 1. Herring.)

THE BIOLOGY OF THE DEEP OCEAN

juveniles, but ventral photophores pred om inate in the m esopelagic fauna (M arshall 1979). Typical exam ples are those o f fish, squid, an d euphausiid and decapod shrim ps, all w ith daytim e hab itat depths o f ab o u t 3 0 0 -7 0 0 m. C am ouflage from the side is partly achieved by silvering or colour p attern s an d cam ouflage from below by biolum inescence. T h e hatchetfishes present the best exam ples o f this tactic; their entire ventral projected area is covered by' groups o f large tubular photophores. T h e light is p ro d u ced in a heavily silvered cham ber above each group o f photophores; it is em itted th ro u g h ventral apertures in the cham ber into the individual p hotophore tubes, each o f w hich is silvered on its in n er surface an d half-silvered on its outer surface (D enton a n d L an d 1971). In m ost species a m agenta-coloured filter plugs the ap ertu re from the photocytc cham ber. T h e result o f this elaborate arran g em en t is th at the p h o tophores em it light whose spectral content an d angular distribution is exactly the same as th a t of dow nw elling daylight. T h e fish will be invisible if the intensity also m atches the dow nw elling light. T his is achieved w ith a p air o f very' small p h o tophores th a t do not point dow nw ards; instead they point into each eye. T h e hatchetfish sets its ventral intensity' by m atching the o utput o f these p hotophores w ith downwelling daylight. By appropriately- adjusting the intensity o f its biolum inescence it can rem ain perfectly cam ouflaged while still being able to changc its depth. Partially successful attem pts were m ade to use the sam e principle to cam ouflage torpedo bom bers during the early stages o f W orld W ar II. Lights w ere m ounted u n d er the wings an d fuselage and a photocell-controlled feedback system m atched their o utput to th a t o f the sky above. T h e pow er requirem ents w ere lim ­ iting b u t the system did greatly decrease the range at w hich the plane becam e visible from its target, a surfaced subm arine. T h e developm ent o f ra d a r overtook the system ’s usefulness before it becam c operational. A lm ost all the u p p er m esopelagic fishes have counterillum inating photophores, often to the exclusion o f any oth er photophores, a n d the sam e is true o f m anv squids (e.g. Abralia, Histioteuthis), decapod shrim ps (Oplophorus, Sergestes), an d all euphausiids. H atchetfishes have relatively few large photophores, lanternfish have sm aller ones, enoplotcuthid squid have hundreds o f tiny ones, an d m idw ater sharks (Jsistius) have thousands o f m inute ones. Lanternfish, squid, an d shrim p have been observed to change the intensity o f their ventral biolum incscence in response to changes in overhead light an d to m atch the light intensity over a wide dynam ic range (Young 1983) (Fig. 9.10). We have already seen how opaque organs in otherw ise tran sp aren t anim als can be cam ouflaged by individual silvering. T h e cam ouflage can be com pleted by7the placem ent o f photophores ben eath the organs. T ran sp aren t cranchiid squids have opaque b ut silvered eyes an d livers; they' all also have photophores b en eath the eyes an d a few species have photophores ben eath the liver. M odified liver tubules in ‘half-red’ sergestid shrim ps form ventral photo p h o res to cam ouflage the rem ain d er o f this opaque organ. Perfect cam ouflage depends on the photophores pointing dow nw ards; if the anim al changes its orientation in the w ater the cam ouflage value is rapidly

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Fig. 9.10 The ventral counterilluminating bioluminescence o f the squid Abraliopsis closely matches the overhead light intensity over a considerable dynamic range. The solid line indicates the expected value for a perfect match. At high overhead light levels the animal can no longer match the ambient intensity. (Reprinted from Young et al. 1980, with permission from Elsevier Science.)

dim inished. S hrim p an d euphausiids cope w ith this by being able to rotate the photophores in the plane o f pitch, so th a t they rem ain directed vertically dow n­ w ards even w hen the body tips up or dow n in the water. C ran ch iid squid tend to stabilize their eye orientation, so that the photophores ben eath the eye m ain ­ tain the cam ouflage even w hen the body axis tilts. M any o f these squid have only a few subocular photophores but their light is evenly diffused by an elabo­ rate sheet o f light guides to ensure that they illum inate the w hole ventral surface o f the eyeball. A m ong the m ost extraordinary o f counterillum ination arran g em en ts is th a t o f the spookflsh Opisthoproctus. It has a flat ventral sole an d an anal diverticulum containing lum inous bacteria. T h e light from the bacterial o rg an shines through a coloured filter a n d into a very reflective light pipe w hich illum inates the whole length o f the sole, elim inating its silhouette. O th e r fishes such as the pearl-eye Benthalbella an d the paralcpidid Lestidium have a few large p h o to p h o res at in ter­ vals along the belly. T hese will not achicve perfect cam ouflage b u t will success­ fully break up the outline an d greatly reduce the an im al’s visibility. Slope-dw elling rattails have ju st one bacterial p h o to p h o re shining through one or two ventral lenses. T h ey are large benthopelagic fishes an d the light is

THE BIOLOGY OF THE DEEP OCEAN

unlikely to have any cam ouflage value. It is possible they m ay be able to vent a cloud o f bacteria or use their light for sexual com m unication, although there is no sexual dim orphism o f the photophores (M arshall 1979). Curiously, abyssal rattails lack a light organ. T h e success o f all ventral cam ouflage depends ultim ately on the visual acuity an d the range o f the observer. A system th a t m ay seem only partially effective to our eyes m ay be perfectly adequate against a p re d a to r’s eye w ith low er resolution. T h e sam e applies to the spectral m atch betw een counterillum inating photo p h o res an d dow nw elling light. I f the spectral m atch is precise, the contrast betw een belly an d background will be negligible, w hatever the spectral sensitivity o f the predator. I f the spectral m atch is only close, then the contrast will d ep en d very m uch on the spectral sensitivity o f the observer. As noted in C h a p te r 8, the em ploym ent o f a yellow lens m ay enhance that contrast. W h en an anim al has m ore th a n one type o f biolum inescence their colours m ay differ. T h e shrim ps Opkphorus an d Systellaspis have counterillum inating photophores whose biolum inescence colour closely m atches dow nw elling light, w ith a narrow' b an d w id th an d a A. at ab o u t 475 nm . T h ey also have a bright secretion th a t is b o th bluer (Я. 460 nm) an d has a b ro ad e r b andw idth (H erring 1983). T h e only spectral selection pressure for this secretion is th a t it m ust be brightly visible to a range o f potential predators.

Interactions with prey T h e m ost basic use o f biolum inescence in feeding is to illum inate the prey. N ightfeeding flashlight fishes have been seen by scuba divers to take p lankton caught in the b eam o f their lum inescence, a n d aquariu m -m ain tain ed fish behave in exactly the same way. T h e re is every reason to believe th a t the large, similarly placed p h o to ­ phores in black dragonflshes have the same role (Fig. 9.9). A p h o to p h o re whose light is designed to illum inate prey is m ost effectively placed close to the eye so th a t the beam o f illum ination (and the reflections off potential prey) are as close as possible to the line o f sight. For m ost purposes a blue light will be best because it has the m axim um effective range in clear seawater. M ost o f the large black dragonflshes (stom iatoid fishes) have postorbital light organs th at em it light w ith a ^max about 475 nm , m aking excellent headlights, albeit aim ed sideways. A few fishes have another, larger, suborbital pho to p h o re w hich is coloured brow'n, red, or orange. T his em its red light, while the postorbital p h o to p h o re em its blue light, as in oth er dragonflshes. Malacosteus has a red light w ith a ^ max o f 708 nm , alm ost into the infrared region. T hese wavelengths are rapidly absorbed by sea­ w ater a n d can have only a very lim ited useful range. N evertheless they have the great advantage th a t m ost oth er anim als can n o t see the light because they have only blue-sensitive eyes (C hapter 8). Malacosteus has visual pigm ents th at allow it to detect bo th blue an d red light. R ed light will be reflected off a red anim al (e.g. a red shrim p) allowing Malacosteus to see its prey w ithout the prey being aw are th at it is being w'atched. T h e fish has in effect its own private w aveband, w hich could also be used to send ‘secret’ signals to others o f the same species. T h e red light is

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probably produced by energy transfer (Fig. 9.5), w ith the basic blue-lightproducing lum inescent reaction transferring its energy to a red fluorescent protein th a t is p resent in large am ounts in the red photophore. T his produces b ro ad -b an d red light, w hich is further filtered through the brow n surface layer o f the p h o to ­ phore. T h e filter absorbs all w avelengths shorter th an ab o u t 600 nm , leaving a narrow -bandw idth biolum inescence em ission in the far red (Fig. 9.11). T h e filter absorbs som e 80% o f the light b u t the loss is com pensated by the heightened advantage th e narrow; far-red, bandw idth gives to the red-sensitive visual pigm ent w hen com pared w ith the blue-sensitive one available to the illum inated prey (D enton et al. 1985). Two other genera o f fishes (Aristostomias an d Pachystomias) have the sam e capability. Biolum inescence can also be used to lure prey. T h e best exam ples are the lures o f female anglerfishes. Shallowr-w atcr anglerfishes have tasselled b u t non-lum inous

Fig. 9.11 The loosejaw fish M alacosteus (a) has a blue-emitting postorbital photophore and a redemitting suborbital photophore. The photocytes in the suborbital photophore contain a large amount of red fluorescent material. A vertical section o f the suborbital photophore (b) shows how the red light produced in the photocytes is further modified by a brown filter. The resulting spectral emission o f the suborbital photophore (c) has a maximum at 708 nm (solid line), very different from the typical blue emission (dotted line) of the post­ orbital photophore. (From Denton e t al. 1985, with permission from The Royal Society, and W idder e t al. 1984.)

W avelength (nm)

THE BIOLOGY OF THE DEEP OCEAN

lures. T h e fishes wave them ab o u t to attract p rey w hich are presum ably deceived into thinking that they m ight be edible. It is n ot possible to observe a deep-sea anglerfish feeding at depth, but the parallels betw een the lures o f deep an d shallow7 species are so close th a t the bacterial lum inescence is certain to have the sam e function. Female anglerfishes have a globular shape th at is designed for rem aining m otionless m uch o f the time; only Gigcmtactis an d its relatives have the elongate form th a t is suitable for (brief) bursts o f swimming. T h e light a n d the m ovem ent o f the lure attract the prey to w ithin reach o f the gaping jaws. Cryplopsaras can slide the ‘ro d ’ p a rt o f the app aratu s back into a groove, draw ing the lure (and prey) closer to the m outh. It can also rotate the lure tip an d produce a flash from it, as well as a glow. T h e lures o f different anglerfish are extraordinarily elaborate, with sensory filaments, papillae, light pipes, an d shutters. It m ay be that different species m im ic different kinds o f prey— b u t th at is pure speculation. O n e anglerfish (Caulophryne) has a ‘lu re’ o rn am e n ted w ith m any filam ents (probably free lateral-line neurom asts, see C h a p te r 6) b ut it is not believed to be lum inous. T h e re is one genus o f anglerfish (Linophryne) in w hich the female has not only a lum inous bacterial lure on the h ead b ut also a m ulti­ bran ch ed barbel hanging from the lower jaw (Fig. 9.12). T h e b arb el filaments contain m any m ore biolum inescent organs w ithin th em but, quite remarkably, the light o f these is n o t bacterial but intrinsic. T his fish really seems to have a beltand-braces approach to luring its prey.

Fig. 9.12 The anglerfish genus Linophryne is unique in having tw o luminous systems. The lure con­ tains typical luminous bacteria whereas the barbel has many tiny photophores with their own intrinsic luminescence. (From Bertelsen 1951.)

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T h e chin barbels o f Linophryne arc m atched an d surpassed by those present in m any o f the long black dragonflshes, particularly species o f Eustomias. Som e have short, simple barbels, others long, m u ch-b ran ch ed ones; w ithin them are nodules o f biolum inescent tissue o f all colours an d sizes (but we do n ot know w 'hether the observed reflected colours have any relevance to the em itted colours). T h e barbels and postorbital organs can flash in synchrony as p a rt of the defensive response noted earlier, but it is likely th a t they are norm ally lit up independently to attract prey. A gain there is the intriguing possibility th a t their com plexity an d variety som ehow m im ic different kinds o f organism s— b ut that is m ore speculation. I f the fish hangs still in the w ater the p a tte rn taken up by the spread barbel filam ents m ay be repeatable enough to have some m im icry value, b u t if it moves in the w ater any such spatial p a tte rn m ust surely be lost. T h e elaboration o f the barbels often varies considerably as the fish develops, so the spatial p a tte rn o f the lights m ust changc considerably too, m aking a detailed m im icry unlikely. O n e alternative is th a t they sim ply rep resen t glowing faecal pellets. T h e deploym ent o f filam entous lures, w hether by anglerfishes o r dragonfishes, carries a risk. T h e bait m ay be taken an d the lure b itten off before the prey pays the price for succum bing to the deception. In these circum stances wc m ight expect to find a significant n u m b e r o f fishes th at have lost the tip o f th eir lures, but such cases arc vanishingly rare. T h e squid Chiroteuthis has two im m ensely long an d filam entous tentacles, each w ith a p hotophore at its tip. T his, too, seems likely to be a biolum inescent lure; lum inous arm tips o f o th er squid (e.g. Oclopoteuthis) m ay have the sam e function (in this anim al they are easily shed, so they m ay also act as decoys). Several kinds o f fish have photophores inside the m o u th (e.g. Sternoplyx, Chauliodus, Pseudoscopelus) an d this is an o th er site from w hich the light m ay act as a lure. C ountcrillum ination cam ouflage (e.g. in som e m idw ater sharks) could potentially be used to allow the p red a to r to rem ain hidden from prey species below it. A further twist in a very speculative tale is given by the ‘cookie-cutter’ shark (Isistius), so-nam ed because it bites n eat biscuit- or cookie-sized chunks out o f large fish an d m arine m am m als. It glows brightly from over its w hole underside exccpt for a dark collar region. T his region, w hen set against the rest o f the glowing belly, m ay perhaps m im ic the silhouette o f a small fish. T his in tu rn m ight attract a larger anim al, giving Isistius the chance to cut an o th er cookie (W idder 1998).

Intraspecific functions: schooling and sex Schooling or aggregating specics use vision an d biolum inescence to m aintain their aggregations, ju st as species in well-lit w ater use vision an d reflected light. O bservations o f the behaviour o f n o ctu rn al near-surface schools o f the flash­ light fish Photoblepharon support this concept, b u t it is n o t possible to validate it for deeper species (M orin et al. 1975). S eparate m a le/fem ale pairs o f flashlight fish m ay also use their biolum inescence to m aintain their relationship. T h e ir

THE BIOLOGY OF THE DEEP OCEAN

photophores are o f sim ilar size an d shape so either the inform ation is som ehow encrypted in the kinetics o f a biolum inescent dialogue or sexual identification is achieved through some other sensory system. O th e r species have different degrees o f sexual dim orphism in their biolum inescent organs an d this implies (but does n o t prove) th at biolum inescence is used for sexual signalling (H erring 2000). T h e deep-sea anglerfishes are perh ap s the m ost extrem e such case, for the m ales have no lum inous organs at all while the females have the characteristic lures. D oes this m ean th a t the lures provide (specific?) sexual signals to a m ale anglerfish or arc they simply a m eans o f luring prey for the females? I f a m ale is attracted to the fem ale’s biolum inescence how' does he avoid being eaten? T h e larger relative size an d b etter organization o f the eyes in males gives a strong h int that vision is m ore im p o rta n t for th em th a n for the females, encouraging the idea th a t the female lure m ay be involved in obtaining b o th a m eal an d a m ate. A lm ost all the ab u n d a n t m esopelagic lanternfishes have counterillum inating p h o ­ tophores (much sm aller ones in the deeper species) b ut m any have additional p h o ­ tophores on the head, tail, o r body that are o f different sizes o r differently positioned in m ales an d females. In species o f Diaphus the huge forw ard-directed p hotophores at the front o f the head are larger in m ales th an females. In m any oth er lanternfish genera there are special photophores on the u p p er an d lower m argins o f the tail. T h eir size, num ber, an d location differ in m ales an d females, a n d there are usually m ore o f them in the males (Fig. 9.13). In black dragonflshes the postorbital photophores are usually large in males b u t reduced o r even absent in females. Sexual differences in the light organs arc n o t restricted to fishes. A m ong the squids, m ales o f the tassel-finned squid Ctenoptayx siculus develop a large abd o m i­ nal pho to p h o re an d m ales o f Lycoleuthis diadema were originally described as a

Fig. 9.13 Many lanternfishes have sexually dimorphic photophores; in Myctophum spinosum there are dimorphic photophores on the upper caudal region in males (a) and lower caudal region in females (b), in addition to the ventral counterilluminating photophores shown in the upper diagram. (From Nafpaktitis and Nafpaktitis 1969.)

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com pletely different genus, in p a rt because o f the differences in their p h o to p h o re patterns. A dult females o f som e cranchiid squid develop large p h o tophores at the tips o f p articu lar arm s. M ost specim ens o f the m idw ater octopod Japetella have no light organs, but m ature females develop a large ring o f lum inous tissue ro u n d the m outh; this atrophies once they have spaw ned. T hese p hotophores m ust surely be used for signalling to the males. M any decapod shrim ps have ventral, presum ably counterillum inating, ep id er­ m al photophores, as noted above for Oplophorus. Sexual differences in th eir dis­ tributions have been noted in some species o f Sergia, though the num bers are not very different in the two sexes (in S. lucens, for exam ple, there are up to 182 in m ales a n d 184 in females). T h e re are also sexual differences in the photophores o f som e euphausiid shrimps. O n e or m ore o f the four ab dom inal photophores are enlarged in males o f species o f Mematoscelis, an d in the A tlantic populations o f J\rematobrachion flexipes m ales lack one o f these p hotophores an d females lack two. D o these differences indicate th a t the sexual p attern s are recognized o r could there be some oth er feature o f the biolum inescence th a t is sexually im portant? In the case o f the lanternfishes the flash characteristics o f the caudal photophores are very different from those o f the counterillum inating ones. T h e caudal organs produce fast brig ht flashes, often in trains, an d it m ay be th a t the sexual in fo rm a­ tion is as m uch in the flash kinetics as in the p hoto p h o re patterns. T h e sam e m ay be the case in the orbital photophores o f dragonflshes. We know noth in g ab o u t differences in o u tp u t o f the sexual photophores o f decap o d an d euphausiid shrim ps but it seems unlikely th a t the (to o u r eyes) trivial differences in p h o ­ tophore p attern s in Sergia are the sole way by w hich the sexes recognize each other. T h e sexual photophores o f female squid are m ore easily accepted as defin­ itive signals in their ow n right, b u t there m ay well be additional sexual in fo rm a­ tion inherent in their flash kinetics. N one o f these questions can be resolved w ithout in situ observations o f their behaviours. O u r know ledge o f the com plex sexual language in the flashes an d glows of m ating fireflies dem onstrates how elaborate som e biolum inescent dialogues can be. G iven the com plexity o f the photophores o f deep-sea anim als it is almost inconceivable th a t sim ilar dialogues are n o t p a rt o f their n o rm al com m unication (H erring 1990). It is ironic th a t the only m arine anim als (other th a n the flashlight fishes) in w hich dialogues are know n to take place are shallow -w ater species with simple light organs. Syllid firew orm s use biolum inescence in m ating rituals an d ostracods o f the genus Vargula have quite astonishingly com plex sexual biolum i­ nescence behaviour, w hich has been established only by divers observing them in situ over long periods o f tim e (M orin 1986). In these tiny anim als the m ales release little puffs o f biolum inescence along specific sw im m ing trajectories ju st above the seafloor. T h e p attern o f puffs, an d their timing, tells the females sitting on the b ottom w hich species is signalling an d allows them to swim up to the right male. It w ould have been quite impossible to anticipate this specificity simply from knowledge o f th eir (very similar) distribution o f lum inous glands. In d eed the

THE BIOLOGY OF THE DEEP OCEAN

biolum inescent behaviours o f two m orphologically indistinguishable populations o f one ‘species’ of' Vargula are so different th a t they m ay prove to be cryptic specics.

Conclusion T h e struggle for survival in the open occan is m ade m ore intense by the absence o f refuges. All anim als are potentially exposed to the sight o f their predators, and cam ouflage in this environm ent relates directly to the conditions o f illum ination. A t shallow depths blue pigm ents m atch the background colouration. T ransparency achieves the sam e result. Tissues th a t are necessarily o paque can be disguised by m im icking transparency w ith m irrors. D eep er in the w ater anim als becom c progressively m ore uniform ly pigm ented, b u t th eir different colours, so strikingly conspicuous to ou r eyes, ren d er th em critically invisible to the eyes of alm ost all their neighbours a n d /o r predators. T h e eternally dark conditions o f the deep sea have en couraged the developm ent o f biolum inescence in a huge variety o f anim als. In fishes a n d squid, in p articu ­ lar, a single species m ay have m any structurally different p h o tophores at different sites on the body. Yet we know (from observations on shallow -w ater species) th at even those w ho have only a single p air o f bacterial photophores can nevertheless use the light in a m ultitude o f different ways. As we struggle to in terp ret the func­ tions o f those m any biolum inescent structures w hich we know are present in deep-sea anim als, the one certainty is th a t these anim als have a m uch g reater range o f biolum inesccnt defence, prey attraction, an d sexual display th a n w’e have yet im agined. All the uses to w hich light an d colour are p u t in the shallows, o r on land, can also be achieved in the dark environm ent o f the deep sea by using biolum inescence.

10 Size, sex, and seasonality

Life histories G row th an d reproduction are the keys to the success o f individuals an d the evo­ lution o f species. H ow are they affected by life at depth? T h e deep sea is n o t a uniform habitat, either in its physical features (C hapter 1) o r in the consequent p atterns o f biogcographv an d variations in biodiversity (C hapters 4 a n d 11). It is therefore wholly unreasonable to expect the deep-sea com m unities to conform to any single lifestyle or exhibit any one reproductive strategy. A fter all, we accept a variety o f habits as com m onplace on land, including those as diverse as budding in tapew orm s, rap id asexual m ultiplication and altern atio n o f gen­ erations in aphids, an d sexuality, long gestation, an d p aren tal carc in elephants. It is no surprise to find sim ilar variety in oceanic organism s. T h e life history o f a species is d eterm ined by num erous physiological characteris­ tics, or traits, whose total is som etim es described in term s o f a life-history strategy. T hese traits determ ine the rates at w hich individuals grow an d at w hich p o p u la­ tions m ultiply an d the study o f their consequences is know n as dem ography. T h e m athem atical clfects o f different traits provide the basic m aterial for dem ographic theory. N atu ral selection is assum ed to act independently on individual life-history com ponents o r traits, w hich therefore can evolve independently o f each other. Selection optim izes adaptive strategies in different environm ents. R eproductive traits in the ocean include such factors as egg size, egg num ber, b ro o d frequency broods p e r lifetime (semelparity—ju st one, o r iteroparity— many), generation tim e, body size, sexuality, developm ent type, a n d ‘reproductive effort’ in term s o f the am o u n t o f energy allocated to reproduction. M any o f these traits ‘co-vary’, th a t is to say a change in one will have inevitable consequcnces for another. T h e differences betw een traits such as these are therefore often described in term s o f trade-offs (e.g. m ore sm all eggs or fewer large eggs).

Trade-offs T h e life history o f a species is inevitably constrained by the resources available to it. T h e w av the energy resources are allocated betw een grow th, rep ro d u c­ tion, activity an d m etabolic m aintenance will determ in e the life history o f the individual (Fig. 10.1). T h e p roportion o f the resources th at arc allocated to

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reproduction will affect three factors. T h e first is lifetime fecundity (the n u m b er o f eggs p roduced in a lifetime), the second is the survival probability o f ju v e­ niles versus parents, an d the third is lifc-cycle tim ing, w hich includes b o th the tim e to reach sexual m aturity an d the d u ratio n o f reproductive com petence (Sibly an d C alow 1986). If unlim ited resources w ere to be allocated for rep ro ­ duction they w ould potentially increase b o th fecundity an d juvenile survival an d w ould decrease the tim e to m aturity, b u t because resources are lim ited trade-offs will occur betw een the three term s. A llocating m ore resources to im m ediate reproduction leaves less for body grow th in the future. T his has a cost for the parent(s) in term s o f reduced grow th, low er survival, an d conse­ quently fewer future offspring. A t any age o f an individual there is therefore a tradc-off betw een curren t reproductive o u tp u t an d residual reproductive value— betw een definite eggs now an d possible eggs later (Sibly an d Calow 1986; B arnes et al. 1988). T h e balance betw een these two determ ines the organism ’s lifetime reproductive output.

Fig. 10.1 A diagram representing the competing physiological energy sinks in a deep-sea organism illustrates the potential trade-offs between growth, reproduction, and activity. (From Clarke 1980.)

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Development patterns: larvae or not? It seems intuitively likely th a t a tropical copepod, a deep-sea fish, a n d a w hale will have different life histories. T h e problem is to try a n d separate the different factors th a t contribute to the life history o f any given organism (e.g. evolutionary con­ straints, reproductive strategy, size, an d tem perature), an d particularly to assess how com binations o f these factors are related to p articu lar environm ents. D evelopm ent in m any m arine anim als lakes place through a series o f sw im m ing o r floating larval stages. T h ey provide a variety o f po ten tial benefits, the m ain one o f w'hich is dispersal (G raham e an d B ranch 1985). For attach ed anim als such as barnacles a n d tunicates there is no oth er way o f getting about. Even for swim­ m ing adults, or m obile bottom -dw ellers, dispersal o f small larvae by w ater cur­ rents increases the potential range an d the gene flow in the populations. D ispersal is m ore effective if the larvae an d adults are vertically sep arated because the currents at their respective depths are likely to be m oving at different rates in different directions. L arvae either feed in the plankton (planktotrophic) or rely on reserves o f egg yolk for their early developm ent (lecithotrophic). It follows th at species w ith planktotrophic larvae have sm aller eggs th a n relatives with lecithotrophic larvae. T h e m ain risks attached to having a larval stage are th at it will be eaten (or starve) before it m atures, o r that it will be swept aw ay from an appropriate adult habitat. T h e latter risk is greater for the larvae o f adults th a t are restricted to slope habitats th an for those from abyssal environm ents. O th e r species reduce this risk by elim inating the larval stage altogether an d instead having direct developm ent. In these anim als the young em erge as sm aller form s o f the adults (e.g. arrow w orm s an d squids), are often brooded, som etim es even live-born, an d are nourished by yolky eggs or placentas. In the deep-sea fauna the em phasis is m uch m ore on this direct developm ent or on lecithotrophic larvae th a n it is in shallow er waters. Is there a theoretical fram e­ work or m odel th a t can m ake accurate predictions ab o u t these kinds o f lifehistory differences in term s o f different com binations o f environm ental features? Are there different theoretical life histories particularly suited to the shallow- an d deep-sea environm ents? H ow do they com pare w ith the reality o f w'hat we observe in the oceans?

Theory T h e rate o f change in a population th a t is grow ing exponentially can be described m athem atically by the grow th equation: cL\7d/ = rJV o r JVf — jVJ, ef/ w here Л'i s the n u m b e r o f individuals in the population, jVy is the n u m b er at tim e О, Л ' is the n u m b e r at tim e t, an d the exponent r determ ines the rate o f p o p u la­ tion increase w ith tim e. B ut the num bers can n o t increase like this for ever, w hether the organism s are bacteria o r whales; the environm ent will have only a

THE BIOLOGY OF THE DEEP OCEAN

finite carrying capacity. T his can be expressed m athem atically by introducing a factor К into the equation so that: d N / d t= iN { K -J V )/K T his logistic equation describes how the population grow th rate declines as the num bers . V tend tow ards K.] the carrying capacity o r level at w hich the environm ent is ‘satu rated ’ (Fig. 10.2). Several theories have been proposed w hich link the evolution o f the dem ographic (life history) characteristics o f organism s w ith the selection pressures im posed by particu lar environm ents. T h e theories have been m atched m ostly against terres­ trial or freshw ater d ata but can equally be applied to the oceanic fauna an d flora. A n early theory was based on the differences betw een tropical an d tem perate regions, arguing th a t in tem perate regions physical factors are the m ain source o f mortality, w hich is therefore in dependent o f population density T his should select for early reproduction an d high fecundity, th at is rep roducing as soon an d as fast as possible. In the tropics, so the theory went, the physical environm ent is m ore stable an d therefore biological interactions p red om inate (i.e. com petition); selec­ tion should be for com petitive ability a n d p red ato r avoidancc (i.e. fewer, larger, m ore-advanced young). T his idea was expanded an d codified in the qualitative concept o f r- an d Kselection (M acA rthur an d W ilson 1967; Pianka 1970) w hich supposed that selec­ tion w orked to m axim ize either r or К in the logistic equation (above) an d th a t the reproductive traits o f species could be classified according to w hether they were rselected or ^Г-selected. T h e concept visualized a continuum in w hich the theoreti­ cal r endp oint is an ecological vacuum , w ith no density effects an d no com petition, an d at the other extrem e (the К endpoint) the environm ent is saturated, all resources are fully exploited, an d the result is intense com petition. In reality, o f Fig. 10.2 Population growth over time in a resource-limited environment with a population maximum K, according to the equation d/V/df = rN {K - N)/K. (Fig 9.3 p. 185 from Pianka 1994 Copyright © by HarperCollins College Publishers. Reprinted by permission of Addison Wesley Longman Publishers, Inc..)

Time (t)

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course, even if the concept is correct, no environm ent w ould be entirely r-selccting or /f-selecting for any one species; each w ould fall som ew here in betw een, based on the degree o f density dependence. T h e two types o f selection w ere assum ed to lead either to increased productivity (/-selection: density-independent, unpredictable environm ents, high (‘prodigal’) reproductive effort) or to increased efficicncy (Kselection: density-dependent, stable environm ents, low' (‘p ru d e n t’) reproductive effort). T h e dichotom y for the populations is based on density' dependence. In practice, r- an d iT-selection theory describes the w ay in w hich populations are density regulated but does not identify the m echanism . Its som ew hat em pirical predictions ab o u t reproductive traits arc by no m eans always observed (Stearns 1992). N atural selection acts at the level o f the individual, an d the fitness o f indi­ viduals w ithin a population is determ ined by the survival an d num bers o f their offspring. T his provides two alternative selective routes to en h an ced fitness, nam ely increased survival or increased fecundity. I f age-specific m ortality is incor­ p o rated into the theory a b etter m atch is achieved w ith the observed reproductive traits. In this ‘bet-hedging’ scenario the particu lar predictions o f r- an d ^ s e le c ­ tion simply becom e the special cases o f variable adult m ortality (Table 10.1; Stearns 1976 provides a detailed analysis). N evertheless, different organism s expe­ riencing the sam e climatic conditions m ay have different developm ental responses. In high latitudes, for exam ple, some copepods respond to the variable food supplies by' having short life cycles an d by overw intering as d o rm a n t eggs, w hereas others take longer to grow, store m ore energy, an d reduce the im pact of periods o f starvation w ith resting juvenile stages (Conover et al. 1991). T h ere is a feedback betw een som e o f the reproductive traits th at m ay be selected in an organism (e.g. age at first reproduction, or generation time) an d the tem p o ­ ral level o f variability in the environm ent th a t will be o f significance to it. Seasonal changes will im pinge little on a species w ith a generation tim e o f days or weeks, while short-term fluctuations in w eather will be o f less consequence to a spccics w ith a lifetime o f several years, ju st as the ability' to accum ulate a n d store energy reduces the effective spatial patchiness in the environm ent (C h ap ter 4).

Table 10.1

The reproductive predictions o f bet-hedging (Stearns 1976) Stable environments

Fluctuating environments

1. With variable adult mortality

Slow development/late maturity Single reproduction Small reproductive effort Few young Long life

Rapid development/early maturity Repeated reproduction Large reproductive effort Many young Short life

2. With variable juvenile mortality

Early maturity Repeated reproduction Large reproductive effort More young per brood Fewer broods Short life

Late maturity Repeated reproduction Smaller reproductive effort Fewer young per brood More broods Long life

THE BIOLOGY OF THE DEEP OCEAN

222

Juvenile m ortality is a key factor in the success o f a population or species. So an o th er w ay o f looking at reproductive tactics is to classify the environm ent as to how well it can support grow th (G) an d juvenile survival (S). T his gives the four possible environm ental com binations o f low a n d high G (prim arily food-based) w ith either low o r high S (survival-based). Som e reproductive predictions that derive from this theoretical base are shown in T able 10.2. In low-survival envi­ ronm ents anim als should not p u t all their eggs in one brood; semelparity, o r m ore picturesquely ‘big b a n g ’ reproduction, m a y prove term in al for the population as well as the individual. T h e contrast betw een high G /h ig h S an d low G /lo w S rep ­ resents the sam e scenario as th a t envisaged by the r—K hypothesis.

Real animals H ow do these predictions m atch the observed features o f oceanic anim als? In the surface w aters many' anim als are faced w ith a very patchy (variable) food environm ent (C hapter 4). A dense patch o f phytoplankton provides an alm ost unlim ited resource, b u t only for a very lim ited time. Salps w hich graze these patches provide p erh ap s the best anim al exam ple o f the high S /h ig h G situation. T h ey can have phen o m en al indi­ vidual an d population grow th rates: Thalia democratica has a length increase at 30°C of up to 25 % h 1, equivalent to w eight increases o f 35 % h 1, an d a population increase o f up to 2.5 day 1(Borgne a n d M oll 1986). T h e appendicularian Oikopkum dioica has a generation tim e o f ab o u t 1 day an d rates o f population increase sim ilar to those o f Thalia. Field populations o f Oikopleura show a biom ass increase o f up to 1000% day'"1! T hese pheno m en al rates o f grow th an d m ultiplication are akin to those o f the phyto­ plankton on w hich these anim als feed, an d in the case o f the salp are achieved by asexual reproduction. T h e anim als arc spectacular opportunists m aking the m ost o f a fleeting, non-com petitive ecological near-vacuum , the ultim ate oceanic expression o f density'-independent population growth. In the deep sea the data are far m ore lim ited. Probably the best data relate to the giant bathypelagic mysid Gnathophausia ingens, largely because it has been m aintained in the laboratory for up to a year an d its grow th a n d reproductive investm ent m onitored for com parison w ith field samples (Childress an d Price Table 10.2 Some reproductive traits predicted for environments with different potentials for growth G and survival S (Barnes et al. 1988, after Sibly and Calow 1986)

Low

Survival rate (S) High

Low

Investment per brood: low Large eggs Few eggs

High

Investment per brood: low Small eggs Moderate number of eggs

Potential (G) for growth

Investment per brood: high Large eggs M oderate number of eggs

Investment per brood: Small eggs Very many eggs

high

SIZE, SEX, AND SEASONALITY

223

1978, 1983). Individuals live for about 8 years at adult depths o f 9 0 0 -1 4 0 0 m an d at a tem perature o f ab o u t 3.5°C. Larvae (as m any as 350) are carried by the females in the brood pouch (or m arsupium ) for up to 15 m onths. Gnathophausia has an exponential grow th curve w ith long intervals betw een instars, an d breeds only once (semelparity) (Fig. 10.3). T h e females invest as m uch as 75% o f the energy accum ulated during their lifetime in egg-laying an d brooding. In life-history term s the authors conclude th at ‘the greatest fitness should result from delaying reproduction until the cost-benefit relationship betw een individual fecundity (increasing w ith size) a n d m ortality reach an optim um . . . sem elparity m ay allow the allocation o f a m uch larger fraction o f the body’s energy into reproduction, thus allowing increased individual fecun­ dity com pared to iteroparous species’ (Childress an d Price 1978). T his appears to be a good exam ple o f a /Г-selected specics yet the single reproductive event an d reasonable n u m b e r o f young do not m atch the p redicted traits o f this group n o r do they fit a bet-hedging tem plate (Table 10.1). In practice, they conform m ore closely to the low G /h ig h S characteristics (Table 10.2). A study o f shallow -w ater brooding crustaceans has also found a p o o r fit betw een the theoretical predictions o f r—K selection o r bet-hedging an d the observed lifehistory traits (Fenwick 1984). M ost anim als have hyperbolic grow th curves; the exponential one in Gnathophausia m ay be linked to sem elparity in th a t the fastest rate o f size increase occurs tow ards the end o f its life an d larger size is linked to increased fecundity. Som e deep-sea fish have sim ilar grow th curves. T h e lifehistory adaptations o f G. ingens m ay thus have evolved in response to the low food levels in its environm ent, an d these extrem e adaptations are m ade possible in the deep sea by the environm ental stability. Fig. 10.3 Growth of the giant deep-sea mysid Gnathophausia ingens from the egg through the final moult to sexual maturity. Each step indicates a separate instar and the overall curve is hyperbolic. (From Childress and Price 1978, with permission from Springer-Verlag.)

Age ( days)

THE BIOLOG Y OF THE DEEP OCEAN

Fecundity and egg size D eeper species o f crustaceans o f all groups generally produce larger an d fewer eggs th a n do shallow er species w ith planktotrophic larvae. Planktonic food o f very small particle size is lim iting at dep th an d m ost deep-sea species have lecithotrophic larvae or direct developm ent. T h e volum e o f the entire brood, however, rem ains approxim ately constant w ith increasing depth, at 10-15% of body volum e (M auchlinc 1988). In seven spccics o f Pacific shrim p, w hose ab u n ­ dance m axim a range from the surface to 625 m , the body length, egg size, an d reproductive lifespan all increase w ith h ab itat depth. T h e shallower spccics breed once an d the deeper ones are iteroparous. It seems th at the im pact o f lim ited food resources on larval survival at greater depths is offset by the increased egg sizes in the deeper species, an d th a t the decreasing adult m ortality w ith increasing d epth allows a longer lifespan, an increased nu m b er o f broods, an d an overall increase in lifetime reproductive effort (K ing an d Butler 1985). T his is closer to the high S /lo w G predictions (Table 10.2). A lthough m any life-history traits are constrained by the phylogenetic history of a species (e.g. no m alacostracan crustaceans have any form o f asexual rep ro ­ duction), closely related specics m ay nevertheless differ m arkedly in reproductive traits. C arid ean shrim p carry their eggs until they hatch. In deep-sea caridcan shrim p o f the w idespread family O plophoridae, for exam ple, the egg size varies very greatly. Species o f Acanthephyra, Notostomus, an d Meningodora all have h u n ­ dreds o f small (< 1 mm) eggs, w hich hatch as planktotrophic early larvae, w hereas Systellaspis, Oplophorus, Hymenodora, an d Ephynna all have 10—30 larger eggs w hich support a m uch longer em bryonic life an d hatch into lecithotrophic larvae at a m uch later stage o f developm ent. T hese generic differences b ea r no relation to h abitat dep th no r to adult size b u t seem to reflect different responses to apparently sim ilar selection pressures, supporting the idea th at com pletely dif­ ferent strategics m ay be equally satisfactory in dealing w ith the sam e environ­ m ental challenges. Phylogenetic differences are p erhaps involved in the fact that all pasiphaeid shrim p have large eggs while all p an d alid shrim p have small ones, yet b oth groups are com m on in the deep sea. Phylogenetic constraints probably also determ ine the fact that deep-sea sergestid an d pen acid shrimps, such as species o f Sergestes, Sergia, an d Gennadas, w hich occupy the sam e d epth horizons as the oplophorid shrimps, simply broadcast their tiny eggs into the w ater with no elem ent o f paren tal brooding. Each strategy is different vet each is (equally?) successful, Mysids an d euphausiids also divide into small- an d large-egged species. C opepods, too, divide into two analogous groups, one o f w hich com prises the broadcast spaw ners an d the other the sac-spawners; in the latter the eggs are carried in a sac by the female until they hatch. B roadcast spaw ners are m ore likely to be herbivorous, but otherw ise there are no obvious ecological correlations with the two life histories. Sac-spaw ning cyclopoid copepods have a lower feeding rate an d fecundity w hen com pared w ith broadcast spaw ning calanoids (K iorboe and S abatini 1994). T his life cycle is an ad aptatio n to the potentially higher m ortality

SIZE, SEX, AND SEASONALITY

225

o f egg-carrying females, w hile that o f broadcast spaw ners reflects the very high egg m ortality rate. Skewed sex ratios, w ith a pred o m in an ce o f females, serves to com pensate for the high female m ortality o f sac spaw ners T h ere m ay be a m inim um viable size for a crustacean egg; if this is so, small crustaceans can only increase fecundity by m ore broods, w hereas large ones can increase the n u m b er o f eggs by reducing egg size. Inform ation from other anim als, especially deep-sea fishes tells a story o f similar variety (M auchline 1991; Childress et al. 1980). In nine species o f meso- an d bathypelagic fishes from C alifornian w aters the m esopclagic spccies w ere gener­ ally small, w ere all vertical m igrants (C hapter 4), an d h ad slow grow th an d early; repeated, reproduction. T h e non-m igratory bathypelagic ones w ere larger, h ad faster grow th an d late reproduction, possibly a single event. T his p attern m ay be successful only in an environm ent w here juvenile survival does n ot have m uch variation. Studies on meso- an d bathypelagic species o f Cyclolhone in Jap an ese w aters provide a different com parison (Miya an d N em oto 1991), because Cydothone do n o t verti­ cally m igrate. T h e m esopelagic spccies C. alba is small, has separate sexes and reproduces after 2 years, spaw ning once to release a few h u n d red eggs. T h e bathypelagic species C. atraria is larger, an d is a p rotandrous h erm ap h ro d ite in w hich the females m ature at 5 -6 years and then have rep eated spawnings of several thousand eggs (Fig. 10.4). T h e egg sizes o f the two species are sim ilar but the duration o f the egg an d larval stages increases w ith adult depth. Specics of Cydothone, like 75% o f oth er bony fishes, have buoyant eggs th a t float tow ards the rich surfacc w aters w here the larvae develop. Like m any o th er deep-sea fishes the larvae then undertake an ontogenetic m igration from the surface w aters back to adult depths. T h e deeper species need to be m ore fecund if longer ontogenetic m igrations pose a greater risk to the survival o f the larvae. T h eo ry dictates that the intrinsic (or p e r capita) rate o f increase r is m ore sensi­ tive to changes in generation tim e th an to changes in fecundity. T his m eans th at

Fig. 10.4 O f tw o species of bristlemouth the 30-mm shallower species Cydothone alba (above) has a different reproductive lifestyle (see text) to that o f the 50-mm darker and deeper Cydothone atraria (below). (From Grey 1964.)

THE BIOLOGY OF THE DEEP OCEAN

226

breeding younger (and smaller) is generally a m ore effective m eans o f increasing r th an delaying reproduction an d producing m ore eggs p e r batch. C. alba can therefore breed earlier at a sm aller size (increasing r) a n d achieve a lifetime rep ro ­ ductive success com parable with th a t o f C. atraria. Sim ilar depth-related trade-offs in reproductive traits are found am ong o th er species o f Cydothone in the Pacific a n d A tlantic, b u t curiously the deeper o f the two species present in the M ed iterran ean (С. pygmaea) is the smaller. Population-specific reproductive traits show the effects o f selection pressures in different environm ents. In the Pacific the populations o f the fish Vinciguerria nimbaria in the low -productivity regions o f the central gyres (C hapter 4) have larger eggs an d lower fecundity th an do populations in the less-im poverished equatorial regions. L arger eggs yield larger larvae w ith m ore num erous fin-rays, vertebrae, etc. (this is know n as m eristic variation). L arger size at h atching increases the success o f the larva in finding food an d avoiding starvation in this desert-like region o f the ocean (Fig. 10.5). Cave fishes provide a parallel exam ple o f a foodrestricted environm ent; they, too, tend to be sm aller b u t have larger eggs than their relatives in the outside world. E ach species has its individual response to the environm ental selection pressures. Vinciguerria nimbaria shows one reproductive response to the productivity differ­ ences betw een the central an d equatorial w aters in the Pacific; lanternfishes in the sam e study show others. Som e species o f lanternfish are present in b o th areas an d the populations in the central w aters carry m ore eggs. However, w hen one o f a closely related p air o f species is present in central w aters an d the o th er in eq u a­ torial w aters the reverse is the case: the equatorial species has the higher n u m b er o f eggs (Clarke 1984). T h e num bers o f eggs in small- an d large-egged species o f stom iatoid fishes differ little; indeed in this study the highest n u m b e r (> 10 000 eggs) was observed in the large-egged Idiacanthusfasciola. T his large-egged species thus seems to invest m ore effort p e r egg w ithout sacrificing egg num bers, so the overall reproductive effort p e r spaw ning is g reater th an in small-egged species. M ost o f the tropical species o f m idw ater fishes (m ainly lanternfishes) are small, spaw n in rep eated batches, an d live for less th an 1 year. T h e n u m b er o f eggs p er batch is so low w hen com pared w ith higher latitude species th a t despite m ore fre­ qu en t spaw ning the lifetime fecundities o f these fishes are also m uch lower. Nevertheless, the lanternfish populations in b oth environm ents rem ain stable, w hich implies th a t larval survival is higher in the tropics. Perhaps the tropical oceanic environm ent has fewer physical fluctuations to th reaten larval life (cf. C h a p te r 4), as envisaged in the early r - K debate.

Fig. 10.5 Specimens of Vinciguerria nimbaria (20 mm) living in the impoverished central gyres have larger, fewer, eggs than similar sized individuals in richer waters. (From Grey 1964.)

SIZE, SEX, AND SEASONALITY

227

L anternfishes in the G u lf o f M exico have two breeding p atterns. Som e species have typical tropical lifespans o f less th a n 1 year an d spaw n a few h u n d red or thousand eggs every few days for a perio d o f 4—6 m onths, while their fecundity increases linearly w ith size. O th ers live for 1-2 years an d spaw n thousands to tens o f thousands o f eggs only once o r twice a year, while their fecundity increases exponentially w ith size (G artner 1993). T hese strategies m ay be the m eans w hereby b o th groups o f species m aintain populations equivalent to (or larger than) those o f larger stom iatoid com petitors such as Gonostoma elongatum, w hich has a higher batch fecundity (about 50 000 eggs) b u t spawns only once.

Body size V ariation in the batch fecundity o f b o th repeated an d single breeders is related to body size (because there are generally only small differences in egg size betw een the two). L arger individuals produce m ore eggs at each spawning. Indeed, the size o f an organism is closely linked w ith m any physiological characteristics an d in responding to selection pressure a change in size will inevitably move it one way o r the other on the r—K continuum (Southw ood 1981). T h ere is a strong positive correlation betw een size an d generation tim e in organism s ran g in g from bacteria to whales. G eneration tim e is correlated w ith longevity, an d longevity is inversely proportional to total m etabolic activity p er unit weight. M etabolism is effectively a m easure o f the ‘rate o f life processes’; the low er it is p e r unit w eight the longer the organism is likely to live an d the larger it will grow. Anim als in the deep sea tend to have a low m etabolic rate (C hapter 5); this will tip th em tow ards a longer life an d generation tim e an d a larger size as a consequence o f positive feedback (Fig. 10.6). A detailed study o f the reproductive traits o f over 1000 specics o f oceanic fishes in the N o rth A tlantic, alm ost equally divided into dem ersal (near-bottom ) an d pelagic (midwater) species, has show n th a t although the two habitats contain fishes from very different orders an d families, the relationships betw een m axim um size an d m axim um fecundity rem ain very sim ilar (M errett 1994). Fecundity increases w ith size in bony fishes (teleosts) b u t this is n o t the case in cartilaginous fishes. T h e relationship betw een fecundity an d size is sim ilar for m yctophids, stom iatoids, an d other pelagic fishes, an d contrasts m arkedly with the relationship in pelagic a n d dem ersal sharks (Fig. 10.7). D em ersal teleosts show a m uch g reater scatter in the relationship th an do pelagic species (indeed in the dem ersal large-egged eelpouts (Zoarcidae) there is no increase in fecund­ ity w ith size). It is im m ediately obvious from these d ata that there is no single reproductive ‘style’ w hich guarantees success in the deep sea. Increased size provides increased lifetime fecundity for ‘big b a n g ’ (semelparous) spaw ners (e.g. gulper eels), b u t if success is indicated by ab u ndance then the success o f p articu lar species o f rattail fishes (M acrouridae), for exam ple, is unrelated to fecundity, size, o r iteroparity

THE BIOLOGY OF THE DEEP OCEAN

Fig. 10.6 Diagram to illustrate the positive feedback between large size and other life-history traits that contribute to the /("-selection hypothesis. Arrows point from causes to effects; heavy arrows represent actual selection. (From Horn 1978.)

(M crrctt 1994). O n the sam e criterion successful species m ay have either small eggs (e.g. m acrourids) or large eggs (e.g. alepocephalids), again showing parallels w ith the situation in the crustaceans (e.g. oplophorid shrimp). T h e p aren tal investm ent strategy o f live-bearing fishes parallels th a t o f broodbearing crustaceans. W ithin the dem ersal ophidiiform fishes one group is livebearing and the oth er egg-laying yet their weight-specific fecundities are n o t very different. M crrctt (1994) has listed the size classes an d reproductive traits o f the deep-sea dem ersal fishes in the Porcupine Seabight, southw est o f Ireland, w hich is probably the best-sam pled region o f the N o rth A tlantic. T his dem onstrates (1) th a t viviparity is found in bo th very small an d very large fishes b u t not those o f interm ediate size, (2) th a t small-cggcd spccies usually have high fecundity an d largc-eggcd species low fecundity, an d (3) th a t there are successful exceptions to every generalization! L arge eggs are not confined to crustaceans an d fishes; o th er invertebrate groups in the deep sea, particularly the bivalve molluscs an d echinoderm s, also have spccics w ith cither large or small eggs (with correlated low or high fecundity an d lecithotrophic o r planktotrophic developm ent). M any o f the echinodcrm s carry precocial developm ent even further and b ro o d the young in special pouches. T h e deeper bivalves have sm aller gonads th an the shallower ones. I ’hc deepest o f seven species o f Nucula, for exam ple, is the smallest an d has the lowest fecundity w ith just two large eggs (the bathypclagic copepod Valdiviella also carries ju st two large eggs). In general, sm aller deep-sea species presum ably experience growthlim iting conditions (low G in T able 10.2) in w hich it will pay them to produce larger offspring that will cope better. A lm ost all deep-sea bivalves have yolky eggs

SIZE, SEX, AN D SEASONALITY

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Fig. 10.7 The relationship between the maximum fecundity (egg number) and size (weight in grams) for oceanic fishes in the North Atlantic. In both the pelagic species (a) and the demersal species (b) fecundity increases with size in teleosts (triangles) but not in elasmobranchs (circles). (From M errett 1994.)

3

5

7

9

11

13

15

17

19

21

Log 2 weight class (b) D em ersal fishes ▲

▲ I

A

A A *

A A

^

А

A

! A

^

A

I

/

▲ •

a ! A A A

A

«

±

• • • • • »

-3

-1

1

3

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7

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21

Log 2 weight class

or (less frequently) direct developm ent, w hereas alm ost all shallow -w ater ones have planktotrophic larvae. A m ong deep-sea gastropods, on the o th er han d , the p roportion o f species w ith planktotrophic larvae increases w ith depth. T h e b en e­ fits o f larval dispersal clearly differ for different groups. T h e benefits will be p a r­ ticularly im p o rtan t for species in relatively ephem eral habitats, such as hydrotherm al vents, w here dispersal failure will result in extinction. Size is ultim ately d eterm ined by the availability o f food. In the deep sea there are the conflicting options o f cither becom ing sm aller to reduce the nutritional requirem ents o r becom ing larger to im prove foraging ability, an d these options tend to со-vary w ith the reproductive strategy. T h ere is evidence for an ecological variation in the adult size o f some m idw ater specics, w ith sm aller specim ens present ben eath oligotrophic surfacc w aters (despite the larger size o f som e early larvae, noted above). In the benthic fauna these regions favour anim als o f large size b u t low caloric density (‘caloric dw arfs’) such as hexactinellid an d dcm osponges, kom okiaceans an d xenophvophores, m uch o f w hose tissue is inert. Similarly, deeper w aters (> 4 0 0 m) have a m uch lower available food biomass th an the surfacc an d the fauna are generally smaller, fam ously described by M u rray an d H jort (1912 ) as a ‘Lilliputian fau n a’. T h ere m ay perhaps be a lower lim it to

THE BIOLOGY OF THE DEEP OCEAN

the effective abundances necessary for sexual encounters, w hich w ould p u t a p rem ium on the production o f m ore num erous sm aller individuals rath e r th an fewer large ones. Paradoxically, giant species o f m any invertebrate groups arc also present in the bathypelagic or benthopelagic environm ents (e.g. mysid Gnathophausia, euphausiid Thysanopoda, am ph ip o d Paralicella, isopod Glyptonotus, ostracod Gigantocypris, pycnogonid Collossendeis, squid Architeuthis, m ed u sa Deepstaria, siphonophore Apolemia, appendicularian Bathochordeus, etc.) while the largest vertebrates (whales, w hale sharks, m a n ta rays, sunfish) live an d feed at shallower depths (with the notable exceptions o f the sperm w hale an d the m eg am o u th shark). G igantism is prevalent at bo th abyssal depths an d in polar waters. A m ong g am m arid ean am phipods, giant spccies (defined as m ore th a n twice the m ean size o f species o f the group) account for 31% o f A ntarctic spccies, 21% o f A rctic species, an d 8% o f ‘abyssal’ (2500—6000 m) species. T h e h ad al faun a (> 6 0 0 0 m) contains relatively few species but frequent giant ones (29% o f the g am m arid ean am phipods) (De Brover 1977). Large size gives the benefit either o f g reater fecundity or o f larger eggs (which hatch into larger larvae, to w'hom a w ider range o f food is accessible). It also gen­ erates adults that are m ore mobile, thus benefiting in the search for food or m ates, have a w ider size range o f potential food (thereby dim inishing ap p a ren t environ­ m ental patchiness) an d arc less vulnerable to predation. Large size also implies an increase in longevity an d hence a potentially longer perio d o f sexual m aturity (Fig 10.6). T his size increase in pelagic specics usually involves some buoyancy com ­ pensation; the in corporation o f buoyancy aids, w’hich are m etabolically relatively inert (lipid, w ater; C h a p te r 5), will also decrease the m etabolic rate p er unit w eight providing a positive feedback loop to fu rth er size increase. T h u s bathy­ pelagic fishes ten d to be larger th an related m esopelagic ones a n d achieve this by m ore rap id grow th rates. T h e high grow th efficiencies are achieved as a con­ sequence o f low' m etabolic rates (Childress et al. 1980). A lthough dem ersal fish species often have a m arked ‘d e e p e r-la rg e r’ (or ‘sm aller-shallow er’) relationship (Fig. 10.8) this is not the case for either echinoderm s or decap o d crustaceans, whose sizes show no p articular trends w ith depth. Large size, large eggs, low'-fecunditv, brooding a n d /o r viviparity, a n d slow' grow th rates similarly characterize the bottom -living anim als o f the A ntarctic. M ight it not be the low7tem peratures com m on to b o th the A ntarctic an d the deep sea that determ ine these traits? Low tem perature by itself is no b a r to fast absolute growth rates. In polar w aters the com bination o f slow grow th rates an d low' m etabolic rates is seen as p a rt o f a suite o f adaptations to the long periods o f low food avail­ ability in the po lar winters. T his is the real d eterm in a n t o f life history, rath e r th an the low tem perature alone (Clarke 1987). Low7 tem perature docs encourage large size because the energy directed tow ards m etabolic m aintenance is reduced. T his will result in h igher grow th efficiencies a n d /o r higher reproductive investm ent (Fig. 10.1). Even w ithin a single spccies the deeper adults m ay be the larger ones. T h e copepod Euchaeta marina has a

SIZE, SEX, AN D SEASONALITY

231

Fig. 10.8 The size of demersal fishes tends to increase with depth, as indicated by the mean weight o f fishes taken in the same semi-balloon otter trawl at depths down to 5000 m in the eastern North Atlantic. (Adapted from Haedrich and M errett 1997 with kind permission of Kluwer Academic Publishers.)

d ep th range o f 400—1800 m an d its body length increases w ith d ep th o f occur­ rence. In a com parison o f 12 species o f Euchaeta, the egg size, sperm atophore length, a n d generation tim e are all positively correlated w ith h ab itat d ep th (M auchline 1995). Similarly, the epi- an d m esopelagic species o f the copepod Pareuchaeta produce 40 to m ore th an 50 small eggs, w hereas bathypelagic species have only 4 -1 9 larger, energy-rich eggs (and a sm aller energetic investm ent p er clutch) (Auel 1999)" Both polar a n d deep-sea anim als have h ad to develop m eans o f surviving long periods o f very low' food resources, driving bo th faunas tow ards sim ilar life-history strategies, including large size. R a p id grow th rates do occur in the deep sea w here food is abundant. T his has been show n by tim e-lapse cam era observations of abyssal xenophyophores an d barnacles, w hich h ad up to 10-fold increases in volum e an d length, respectively, over periods o f 6—8 m onths. T h e x eno­ phyophores h a d short pulses o f grow th separated by long quiescent periods, so the grow th rates during the pulses w ere very high (G ooday et al. 1993). D eep-sea pres­ sures are no b a r to high grow th rates either; the reco rd ed grow th rate o f the giant vestim entiferan w orm Riftia pachyptila at 2500 m at a h ydrotherm al vent on the E ast Pacific Rise was m ore th an 85 cm p er year an d was claim ed to be the highest for any m arine invertebrate! T his is achieved entirely th ro u g h the activities o f its endosym bionts— it has no m outh, gut, o r anus (Lutz et al. 1994). C ontrasting figures for an o th er vestim entiferan (Lamellibrachia) from a cold seep in the G u lf o f M exico give a grow th rate o f less th an 8 m m p e r year, an d a probable age o f adult p opulations o f m ore th an 100 years.

Sex M any bathypelagic spccies do achieve large size, b u t food resources are never­ theless severely lim ited at all depths below the surface. Intraspecific partitioning o f the available resources is often ap p aren t in disparities betw een the biomass

THE BIOLOGY OF THE DEEP OCEAN

allocated to males an d females. T his can be seen either in num erical differences in the abundances o f the two sexes o r in size differences (sexual dim orphism ). T h e re are m any exam ples o f species in w hich females are m ore ab u n d a n t th an males; typically; in deep-sea copcpods males are very uncom m on, sometim es even unknow n. C onsidering the deep-sea fishes, m atu re females are considerably m ore ab u n d a n t th an m ature males am ong several mvctophids, stom iatoids, m acrourids, halosaurs, an d notacanths (Clarke 1983; M errett 1994). O f course this can result not only from a skewed sex ratio at h atching b ut also from a g reater longev ity in females. M any copcpods have males th at do not feed an d are therefore likely to have shorter lifespans th an do the females an d in these anim als the m ales are generally sm aller th an the females. In one study o f deepsea fishes the m ales o f two spccics o f m elam phacids w ere m ore a b u n d a n t th an females; these fishes have no sexually dim orphic com m unication systems (olfac­ tory, acoustic, or lum inescent) an d the increased n u m b e r o f m ales m ay enhance the likelihood o f m ating b u t at the expense o f a decreased n u m b er o f egg p ro ­ ducers in the population. A lthough greater longevity o f females, w ith continuing grow th, can produce an ap p a ren t size dim orphism , m any species o f deep-sea fish have a true sexual dim orphism o f size, in w hich the males m atu re at m uch sm aller sizes th an females. In shallow -w ater an d reef environm ents m ales are som etim es the larger sex, enhancing their abilities to defend territories or m ain tain a h arem , b u t this is never the case in the deep sea, w here the challenge for the m ale is to find an d m ate w ith a relatively im m obile female at very low population densities (Ghiselin 1974). Packaging the m ale biom ass into m ore, smaller, units increases the likeli­ hood o f successful sexual encounters, assum ing th at the m ales are the active searchers an d th a t their size is not so small th at they lack the en d u ran ce for the search. T his is w here the em ission o f sexual signals by the female (pherom ones, lum inescence, etc.) will m ake a crucial difference to the succcss o f the outcom e by guiding the m ale tow ards her. Anglerfishes represent an extrem e exam ple o f this strategy’ (Pietsch 1976); all species have d w arf males w ith large olfactory organs. In m ost spccies the males m ay attach briefly d uring m ating b u t in som e the attach m en t is p erm an en t, so th a t effectively they becom e parasitic. In these cases the gonads o f u n attach ed m ales an d unparasitized females do n o t develop: the association seems essen­ tial in order to initiate sexual maturity. Females m ay occasionally have m ore th an one attached m ale (Fig. 10.9). D ocs this m ean th at males were m ore ab u n d a n t locally— or th a t her scent was particularly potent? It has also been know n for a m ale o f one spccies to attach to a female o f another, presum ably through failure o f the specific recognition factors- or desperation. Anglerfishes include m ore species (> 100) th an any' other group o f bathvpclagic fishes. W hale fishes, w hich are the next m ost diverse (—35 species), also have d w arf males. M ales o f the small live-bearing tclcost Parabrotula are sm aller th an the females an d produce sperm atophores; this sperm storage device m ay be an adap tatio n to the low population densities in the deep sea an d enables a female to utilize the sperm over long periods o f time. By this m eans she can have

SIZE, SEX, AND SEASONALITY

233

Fig. 10.9 A female of the small anglerfish Haptophryne (45 mm) bearing tw o attached males. (Photo: P. M. David.)

several broods w ithout the uncertainty involved in finding an o th er m ale each time. Anglerfish m ales reach sexual m aturity soon after m etam orphosis but females take m uch longer (indeed m ature females o f some species have n ot yet been caught); one estim ate is th a t overall there are 15-30 ripe m ales to every ripe female. T his discrepancy also occurs in som e species o f Cydothone w here ripe males are far less a b u n d a n t th an females overall, b ut nevertheless o ut­ nu m b er ripe females by m ore th an 10 to 1. A n alternative response to the problem s o f successful m ate finding is th at o f h e rm ­ aphroditism . T h e added cost to the individual is in the m ain ten an ce o f b oth sets o f gonads. S eparate sexes have an advantage in situations w here population d en ­ sities are high enough for m ating encounters to be frequent. At low population densities, w hich m ake encounters less likely, herm ap h ro d itism will be favoured. Conversely, as the m obility o f species increases, the en co u n ter probability will also increase an d the extra cost o f herm aphroditism is likely to becom e a g reater b urden th an the lim itations o f separate sexes. T h e low population densities at w hich m any species occur, com bined w ith the reduced m obility o f the w atery deep-sea fauna, enhance the value o f herm aphrod itism (Calow 1978). M esopelagic p redators in the fish families N otosudidae an d A lepisauridae are synchronous herm aphrodites; so are the deep benthic tripod fishes (Ipnopidae), lizard fishes (Bathysauridae), an d green-eyes (C hlorophthalm idae). In contrast, all the shallow -w ater green-eyes have separate sexes. A lthough there are no synchronous herm aphrodites am ong the benthopelagic or bathypelagic fishes, there are several protandric herm aphrodites. T hese fish m ature first as males an d later becom e females. Som e p rotandrou s h erm ap h ro d itic species of Cydothone (e.g. C. atraria, C. microdori) are extrem ely ab u n d an t. A lthough the shal­ lowest-living species o f the related genus Gonostoma (G. atlanticum) has separate sexes, the deeper m esopelagic species G. gracile an d G. elongatum are obligatory

THE BIOLOG Y OF THE DEEP OCEAN

p rotandrous herm aphrodites. T hese fishes invariably change sex a n d the males are therefore always sm aller th an the m atu re females, w hich consequently have a higher fecundity th an if the sequence was reversed (as it is in some reef fishes) or if the sexes were separate an d b o th were the size o f males. T h e closely related but deep er living G. bathyphilum is a facultative p ro tan d ric h e rm ­ aphrodite, th a t is it can change from m ale to female, b u t does n ot always do so; once m ales reach a certain size w ithout changing sex they usually continue as males (Badcock 1986). In other environm ents the presence o r ab u n d an ce o f one sex m ay determ ine w hether o r n o t a facultative h erm ap h ro d ite changes sex, an d it is possible that the sm aller m ales o f G. bathyphilum m ay change sex if the ratio o f males to females in an area exceeds a certain level, p erh ap s indi­ cated by chem ical cues. Elsewhere the sex o f an individual fish, am phipod, copepod, or shrim p m ay be irreversibly d eterm in ed by factors such as n u tri­ tion, tem perature, o r day length, but there is no evidence th a t any such factors are involved in the deep sea.

Duvenile characters (progenesis) M any deep-sea fishes, particularly m esopelagic species, have red u ced size an d early sexual m aturation, com bined w ith reduced ossification an d a general sim­ plification o f body structure, interprctable as a response to low food conditions (C hapter 5). C onsideration o f a w hole range o f deep-sea fishes, from m any fam ­ ilies, led M arshall (1984) to the conclusion th a t this general m orphology was the result o f progenesis— the precocious or accelerated assum ption o f sexual m atu ­ rity before com plete som atic developm ent has taken place. Progenesis contrasts w ith neoteny, in w hich juvenile characters are retained into adult life b u t w ithout early maturity. M any o f the features o f fishes such as species o f the non-m igrants Cydothone an d anglerfishes are readily explicable as typical larval characters w hich are present as the result o f precocious sexual maturity. In contrast, active vertical m igrants such as m yctophids show no such tendencies. Cyclothone’s econom y of structure m ay enable it to achieve b oth m aturity w ithin a year an d a fecundity com parable to th a t o f its m yctophid com petitors (M arshall 1984). O th e r pelagic fishes show ing sim ilar tendencies include giganturids, aphyonids, m onognathids, and, to a lesser degree, some m elam phaeids, scopelarchids, notosudids, an d cyemid eels. Progcnesis is m uch less com m on in benthic an d benthopelagic fishes, w here it is recognizable only in liparids an d alepocephalids. Progenetic ten d en ­ cies, particularly in m idw ater fishes, allow a g reater p ro p o rtio n o f the lim ited available energy' to be diverted into gonadal developm ent. T h ey allow n o n ­ m igrant m esopelagic species to com pete w ith vertical m igrants; in bathypelagic species they p erm it the developm ent o f a g reater fecundity th an w ould otherw ise be possible for a given size.

SIZE, SEX, AN D SEASONALITY

235

Seasonality T h e d ata for m ost epipelagic fishes indicate th a t they spawn in p articu lar seasons, w hether they spaw n once or repeatedly. Epipelagic invertebrates have sim ilar sea­ sonal cycles m ost clearly recognizable in the tem perate regions w here seasonality in th e w eather is translated into m arkedly cyclical phytoplankton an d zooplank­ ton populations n ea r the surface (Fig. 2.3). In the deep sea, far from the surface fluctuations, it has long b een assum ed that continuous rep ro d u ctio n is the n orm , fed by the continuous rain o f m aterial slowly sedim enting through the w ater colum n an d being frequently recycled along the way. Tw o early dogm as, O rto n ’s rule a n d T h o rso n ’s rule, predicted, respectively, th a t deep-sea populations w'ould have continuous reproduction a n d w'ould brood (i.e. have yolky developm ent). Tw o m echanism s m ay result in continuous reproduction w ithin an abyssal p o p u ­ lation. E ither a few individuals at any one tim e release all th eir gam etes (i.e. they have asynchronous cycles (am phipods, ophiuroids)), or m any individuals spawn frequently an d repetitively, releasing only some o f th eir gam etes at once (bivalves, polychaetes). A n analysis o f benthic samples from 1240 m in the S an D iego T rough found only two species w ith annual cycles o f rep roduction (a lam p shell an d an elep h an t’s tusk mollusc, w hich spaw ned in different m onths). T h e conclu­ sion was th a t year-round reproduction is indeed th e com m o n p a tte rn in the deepsea benthos (Rokop 1974). L ater studies o f m ore extensive samples from the Rockall T rough at depths of 2900 m provided evidence, based on grow th increm ents, o f seasonal grow th in a nu m b er o f species o f echinoderm . Seasonal grow th rings have also been rep o rted in the otoliths o f deep-sea rattails an d in the shells o f p ro to b ran ch bivalves. A lthough these d ata indicate seasonal grow th they do n ot directly indicate sea­ sonal reproduction. Evidence for seasonal repro d u ctio n on the deep-sea floor com es from two sources. T h e first is an analysis o f the size distributions o f p o p u ­ lations o f echinoderm s. Som e species o f deep-sea brittle-stars an d sea urchins show a sum m er influx o f juveniles, w hich results in a reduction in the m odal size o f the population. A n even m ore direct indication o f reproductive activity on a seasonal basis com es from studies o f oocyte size or egg brooding in a n u m b e r of groups o f benthic anim als. In samples o f deep-sea isopods, taken from sites off the C arolinas an d in the Scotia Sea south o f the Falldands, m ore gravid females w ere present in the late sum m er an d early au tu m n th a n at o th er tim es o f the year. T h e samples an d the seasonal cover w ere lim ited an d the in terp retatio n o f the data as seasonal breeding was view ed w ith som e scepticism. However, in the early 1980s, d ata from a long tim e series in the Rockall T rough confirm ed the results for isopods an d show ed clear evidence (extending over several years) o f seasonal ovarian m aituration an d spaw ning in som e bivalves an d echinoderm s. In a study o f 14 species o f echinoderm , five (a starfish, an urchin, an d three brittle-stars) prod u ced num erous small (~0.1 mm) eggs w ith a m arked seasonality. T hese small eggs develop into small plankton-feeding larvae a n d the five species show m arked reproductive synchrony, b o th betw een individuals an d

THE BIOLOGY OF THE DEEP OCEAN

betw een spccies (Tyler 1988). T h e result is th a t they all send th eir larvae into the plankton at the sam e tim e, in Ja n u a ry an d February, to reach the surface w aters at the start o f the spring burst o f phytoplankton growth. Clearly n eith er O rto n ’s n o r T h o rso n ’s ‘rules’ always apply, although the o th er nine species pro d u ced a few large (> 1 mm) yolky eggs an d show ed no evidence o f seasonality. T h e large eggs are in terpreted as indicating direct developm ent to a small adult form , w ith no larval stage. Such irrefutable evidence for seasonality (at a d epth o f alm ost 3 km) begs the question o f w hat signal controls the reproductive cycle. I f the m aterial from the surface w aters drifts very slowly dow n as a fine nutritional drizzle, swept h ith er and thither by currents at different depths, any surface seasonality will rapidly be dissipated. Tim e-lapse cam eras placed on the seafloor o f the Porcupine Seabight in 1981 and 1982 told an extraordinary an d wildly different story. Pictures o f the sam e area o f seafloor, taken at intervals o f a few hours over periods o f a year or m ore, show dram atic changes. In early sum m er flocculent m aterial appears, accu­ m ulating particularly in any depression. It then increases rapidly, to cover the seafloor an d obliterate m any o f the sm aller m ounds an d pock-m arks, before dis­ persing later in the sum m er (Fig. 10.10). Sam ples o f this m aterial show th a t it is form ed o f fluffy aggregates full o f diatom s an d o th er phytoplankton, as well as debris, all glued together w ith mucus. Som e o f the phytoplankton has been eaten and is present as faecal pellets, b u t m uch o f it rem ains intact. T h e spring bloom at the surface has aggregated in large gobbets an d sedim ented m uch m ore rapidly th an w ould otherw ise have been the case (Billett et al. 1983). S edim ent traps

Fig. 10.10 The seafloor at 2000 m in the Porcupine Seabight in May. A darker layer of phytodetri­ tus, rapidly deposited from the surface waters, covers much o f the pale sediment (cf. Fig. 3.4). A starfish (Bathybiaster) ploughs across the field o f view. A current indicator throws a long shadow at lower right. (Photo: R. Lampitt.)

SIZE, SEX, AN D SEASONALITY

237

deployed in the area following this revelation show ed a corresponding ‘cap tu re’ o f this scdim enting fluff (or phytodetritus) in early summer. H ere is a strong seasonal signal to the deep-sea floor. T h e pulse o f food to the sedi­ m ent feeders is assum ed to be the trigger for the observed seasonal reproduction. It is well know n th a t phytoplankton-derived chem ical cues can initiate spaw ning in shallow -w ater sea urchins an d mussels, an d th a t phytodetritus triggers larval release from deep-w ater crabs, so there is no reason whv it should n o t provide chem ical as well as nutritional cues to developm ent in abyssal species (Starr et al. 1994). In recent years the pulse o f scdim enting m aterial has been found to be cor­ related w ith the reproductive cycles o f other anim als, including sponges, sea anem ones, lam p shells, an d cum acean crustaceans. T h e cam eras have also shown th at the m obile sea cucum bers an d urchins are m uch m ore activc during the p eriod w hen detrital aggregates arc visible on the bottom . T h e sedim ent com m u­ nity respiration rates also rise sharply following the arrival o f the m aterial. T his rapid deposition o f m aterial has been seen in w ater depths o f up to 5 km in m any regions o f the ocean. It is a p articular feature o f tem p erate regions w ith their m arked spring bloom o f near-surface phytoplankton. It does n ot seem to be sig­ nificant in tropical regions, w here surface productivity is m ore seasonally uniform . T h e deep-sea fauna has often been characterized as having typically ^ s e le c te d characteristics, w ith r-selected features present only in shallow -w ater spccies. Studies o f the responses o f the sm aller benthos to the arrival o f phytodetritus on the seafloor explode this dogm a (G ooday an d Turley 1990). B acterial grow th on the phvtodetritus is rap id an d is followed by the developm ent o f large populations o f bacterial-feeding flagellates. Two or three p articu lar species o f foram iniferans (of the tens o f species present in the sediments) rapidly colonize the m aterial an d becom e dom inant. O ne, Alabaminella weddellensis, com prised 75% o f the speci­ m ens in the Porcupine Seabight m aterial in 1982 (Fig. 10.11). A nother, Epistominella exigua, has a very w idespread distribution, typical o f opportunist col­ onizers w ith high values o f r. T hese anim als feed both on the b acteria an d directly on the fluff. O th e r m eiofauna such as nem atodes, kinorhynchs, an d h arpacticoid copepods also respond to the phytodetritus, thou g h less rapidly. T h ese o p p o r­ tunists, analogous to the salps in surface waters, lie in w ait on the deep-sea floor an d rapidly colonize the new m aterial w hen it arrives. L arger anim als gobble it up an d convert it into eggs an d larvae that are sent back up into the surface w aters in the following year. Yet despite this seasonal b o n an za the m ajority o f m egafaunal specics still reproduce thro u g h o u t the year, m any w ith yolky eggs. Both O rto n a n d T h o rso n w ere m ostly right.

Conclusion G row th, size, sex, a n d seasonality c,o-vary in the life histories o f deep-sea anim als, though n o t in any consistently predictable way. T h e selection for p articu lar traits takes place w ithin the context o f b o th the physiological lim itations o f the species

THE BIOLOGY OF THE DEEP OCEAN

238

Fig. 10.11 Many benthic animals respond rapidly to the deposition of phytodetritus. The numbers o f three species o f foraminiferan change from the relatively few present in the bare sediments at 4550 m in the eastern North Atlantic early in the year (April 1988 data) to very high numbers later in the year when phytodetritus is present (August 1986 data). The numbers in the sediment change little, but there is a massive increase within the phytodetritus. (From G ooday and Turley 1990, with permission from The Royal Society.) 140

«

I

120

I phytodetritus

H i sediment

ю 100 CO

Alabaminella weddeliensis

Tinogullimia riemanni

Epistominella exigua

Ф ■Q E

Apr. ’88 Aug. ’86

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Apr. ’88 Aug. ’86 Samples

Apr. ’88 Aug. '86

an d the variability in the environm ent. A variety o f life-history p attern s can be achieved by different arrangem ents o f the physiological an d environm ental pieces; these p atterns result from different trade-offs in different species. T h ere is no single deep-sea life-history p attern , n o r is there yet a theoretical m odel w hich adequately encom passes the know n variety. O n e o f the reasons for this is p ro b a ­ bly that ou r know ledge o f the im pact o f the physical environm ent, o f com peti­ tion, o f resource utilization, a n d o f m etabolic effort in the deep sea is still too lim ited to prevent ou r assum ptions about th eir relationships being simplistic. Existing dem ographic theories are useful in rationalizing the life-history traits (and their relationships) in deep-sea anim als b u t too m any p aram eters rem ain unquantified for the theories to be reliably predictive. We see the variety o f results that n atu ral selection has achieved in the deep sea over long periods o f tim e and we trv to in terp ret them . It is akin to looking at a com plex piece o f sculpture an d trying to deduce from the end-product the history o f its construction, w hat kind o f tools were used, in w hat order, an d for how long. T h e task is certainly difficult, b u t n o t wholly impossible.

11 A wonderful variety of life: biodiversity of the deep-sea fauna

Origins and habitats Life probably arose in the earliest seas some 4 billion years ago (4000 M a), perhaps close to hydrotherm al springs. T h e re is fossil evidence for the existence of prokaryotic (bacteria-like) organism s 500 million years later an d m ats o f cyanobacteria-like organism s or strom atolites w ere ab u n d a n t 3 billion years ago (3000 Ma). E ukaryotes ap p eared after an o th er billion years (2000 Ma) b u t it was an o th er 1.4 billion years before the great expansion in the variety o f m ulticellular anim al life (metazoans) becam e recognizable in the E d iacaran (575 M a) and Burgess Shale (525 M a) faunas. T h is expansion probably occurred in the w arm shallow w aters o f the pre-C am b rian seas a n d the present m arin e fau n a is the p ro d u ct o f the subsequent h alf a billion years o r so o f evolution. Living organism s have until recently been grouped into five kingdom s (Barnes et al. 1988; M argulis a n d Schw arz 1988) an d each kingdom divided into a n u m b er o f phyla. In this classification the kingdom A nim alia contains the m etazoan phyla (Sorensen et al. 2000 discuss their phylogeny). T h e oth er kingdom s are the Plantae (green plants), the Fungi, the Protista (unicellular eukaryotes), an d the M o n era (prokaryotes or bacteria). R eccnt discover)' o f the very unequal genetic divergence betw een these groups has led to a new consensus com prising three m ajor ‘d om ains’ o f equivalent divergence, the B acteria (Eubacteria), the A rchaca (A rchaebacteria), an d the E ukaryota (Eukarya), w ith the last do m ain subdivided into a n u m b e r o f kingdom s including the A nim alia, Plantae, a n d Fungi (Doolittle 1999, 2000). Biological diversity encom passes all three o f the dom ains an d recent genetic d ata em phasizes the vast (and largely unknow n) scale o f the dom inance an d diversity o f the m icrobial populations in the oceans, including b o th pro k ary ­ otes an d eukaryotes (K arn er et al., 2001; L opez-G arcia et al. 2001; M o on-van der Staay et al. 2001). M ost detailed studies o f m arine diversity have h ith erto focused on m etazoan diversity; although the kingdom A nim alia is also the focus for this chapter, it is im p o rta n t to recognize th a t m etazo an diversity provides only a lim ited n u m b e r o f the pixels in the w hole m arine image. I f the process o f evolution leads to m ore variety th en we m ight expect a g reater variety o f life in the oceans th an there is on land, w here the evolutionary process is m uch younger an d the h abitat are a is m uch smaller. T his seems to be supported

THE BIOLOGY OF THE DEEP OCEAN

by the fact th a t 95% o f the 250 000 species in the fossil record are m arine. Paradoxically, however, m ost o f the 1.5 m illion living spccics th a t have been form ally described are terrestrial (dom inated by the 240 000 species o f flowering plants an d the 750 000 species o f insects w hich have co-evolved w ith them). Yet there is m ore variety o f anim al life in the oceans, as dem o n strated by the greater nu m b er o f m etazoan phyla (or ‘kinds’ o f anim al) living in the occans com pared with those on the land. O f the 34 m etazo an phyla, 33 include m arine species (Table 11.1). O f these phyla, 16 have only m arine species, th at is they are endem ic to the oceans. By contrast, terrestrial a n d freshw ater habitats support species from no m ore th an 17 phyla, an d ju st one o f these phyla is endem ic.

What is biodiversity? T h e variety o f organism s present in the oceans (outlined above an d described in the A ppendix) provides the starting point for discussions ab o u t ‘biodiversity’, b u t before joining the discussion we m ust be sure w hat we are talking about. ‘Biodiversity’ was introduced in about 1985 as a contraction for ‘biological diver­ sity’. It is a term that is now em otively pow erful b ut only elusively m easurable (H ulbcrt 1971). It has high profile b u t low precision. Biodiversity now encom ­ passes the levels o f genetic diversity (between individuals), species diversity (between species), an d ecological diversity (between com m unities), but its use needs to be clearly defined for any particu lar com parison. Species richness is the cornerstone o f biodiversity studies. It describes the n u m b er o f species in a given region. However, at any scale o f sam pling some species will be ab u n d a n t an d others rare, an d these differences also need to be taken into account. T h e ‘equitability’ o r evenness o f the sam ple describes the num erical distribution o f individ­ uals betw een the identified species, an d various m athem atical form ulae are available to m erge this w ith the n u m b e r o f species an d to generate a ‘diversity index’ (M agurran 1988; see also H u lb ert 1971). A nother w ay o f looking at biodiversity is to consider the n u m b er o f species in a given area (species richness p e r u nit area) as a-diversity; or w ithin-habitat divers­ ity, an d to describe the distribution o f these species in space (spatial pattern) as pdiversity, or betw een-habitat diversity. T hu s if all the spccies in one are a occupy large overlapping ranges |3-diversity will be very low; on the o th er h an d if their ranges are small an d adjoining the P-diversity will be high. M ost o f the basic concepts involved in the m easurem ent o f biodiversity a n d the assessment o f its significance w ere developed for terrestrial habitats, frequently in the context either o f organism s that did n ot move ab o u t m uch (e.g. plants) or o f anim als whose ranges w ere reasonably well-defined. N eith er context applies to the oceans, w ith the result that studies o f m arine biodiversity have been the poor relation in the family. Nevertheless, the very scale an d continuity o f the oceans decreases the chances o f local extinction an d therefore helps to m aintain a higher diversity. T h e general assum ption has been th at deep-sea specics diversity is low, on the basis that the described m arine fauna represent only aro u n d 10—15 % o f

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241

the nu m b er o f global species an d ranges are g reater in the oceans th a n on lan d (cf. L onghurst 1998). E xplanations for these faunal differences vary, how ever (M ay 1994). Benthic organism s, a n d particularly those living w ithin the sedim ents, represent the nearest approxim ation to a com parable terrestrial fauna. Sim ilar m ath ­ em atical treatm ents can be applied to d ata sets from the two environm ents. T h e total n u m b e r o f species present in any area o f interest can be estim ated from the dim inishing rate at w hich additional species are add ed to the list as

Table 11.1 Distribution of animal phyla (as adults) between marine pelagic, marine benthic, and terrestrial/freshwater habitats (modified after Pearse and Buchsbaum 1987 and May 1994). Phyla that are solely parasitic are shown as P Phylum Acanthocephala Annelida + Arthropoda Brachiopoda Bryozoa Chaetognatha Chordata Cnidaria + Ctenophora Cycliophora Echinodermata Echiura Entoprocta/Kamptozoa Gastrotricha Gnathostomulida Hemichordata Kinorhyncha Loricifera Mesozoa/Dicyemida Mollusca + Nematoda Nematomorpha Nemertea Onychophora Orthonectida Phoronida Placozoa Platyhelminthes Pogonophora Porifera Priapulida Rotifera + Sipuncuia Tardigrada Totals 34 Endemic

Marine pelagic

Marine benthic

Terrestrial/freshwater

P + +

P + + + + + + + + P +

P

+ + + + + + +

+ + + +

+

+ P + + + +

P + + +

+

+

+ +

+ + + +

P + + + + +

15 Marine: 16

+ + + + + + +

+

33

17 Terrestrial/freshwater: 1

+

THE BIOLOG Y OF THE DEEP OCEAN

242

the nu m b er o f samples from the area increases. T hese relationships are expressed graphically as ‘rarefaction’ curves, w hich describe em pirically how the n u m b e r o f species present in the samples scales w ith the n u m b er o f indi­ viduals collected (Fig. 11.1). T h e first few samples will contain m any new species b u t in later sam ples m ost o f the species present will already have been sam pled an d fewer and fewer new nam es will be ad d ed to the list. R arefaction curves express the ‘evenness’ o f the species distributions; they do n ot directly indicate the total nu m b er o f species present, b u t extrapolations from them are som etim es used for this purpose. T h e accuracy o f such extrapolations depends very m uch on (1) how far along the rarefaction curve the sam pling has p ro ­ gressed, (2) how uniform the com m unity is w ithin the area, (3) a variety o f assum ptions ab o u t the representative natu re o f the samples, an d (4) the dom i­ nance o f different species w ithin the samples (Flulbert 1971; G age an d M ay 1993). T h e scale o f the extrapolations used (and the consequent u n certainty in their accuracy) is dem onstrated by a terrestrial exam ple in w'hich 1200 species o f beetle were knocked out o f the canopies o f 19 specim ens o f one p articular species o f P anam an ian tree. W hen the relevant assum ptions have been m ade these num bers scale up to predict som e 30 m illion species o f tropical forest insects (Erwin 1982; 0 d e g a a r d 2000)!

Fig. 11.1 A rarefaction curve derived from Grassle and Maciolek's box-core data (see text) shows the rate at which new species are found as more and more individuals are sampled. The distances mark the transition between successive stations along the sampled transect. (From May 1992, after Grassle and Maciolek 1992.)

A WONDERFUL VARIETY OF LIFE: BIODIVERSITY OF THE DEEP-SEA FAUNA

Biodiversity on the deep-sea floor Historically, the deep-sea floor has been viewed as a relatively uniform an d undis­ tu rb ed environm ent w ith a low biodiversity w hen com p ared w ith terrestrial h ab i­ tats. N evertheless, since the 1960s detailed studies o f the anim als sam pled in sedim ent cores from a n u m b e r o f deep-sea sites have dem o n strated high num bers o f species (i.e. spccies richness) in the m acrobenthos (0.25-0.5 m m size range) and in the m eiobenthos (0.05-0.25 mm). T h e deep-sea cat was p u t am ong the terres­ trial pigeons by the results o f an intensive survey o f the b cnthic m acro fauna o f one particu lar area (Grassle an d M aciolek 1992). T h e authors looked at a total o f 233 box-core sam ples (covering a total o f 21 m 2 o f the ocean floor) along a 176km track at depths o f 1500—2500 m off the coast o f New'Jersey. O n e o f the g reat­ est problem s in this sort o f study is the difficulty o f identifying the anim als, com bined w ith the laborious nature o f the tasks o f sorting an d processing the samples. In the deep sea, in particular, m any o f the species taken are likely to be new to science. G rassle an d M aciolek identified 798 species from the almost 91 000 individuals w hich were retained on a 0,3-m m sieve (Table 11.2 an d Fig. 11.1): 58% o f them w ere new' species. In the later stages o f the analysis ab o u t 100 furth er species were being ad d ed to the list for every 100 km distance along the slope contour. T h e researchers assum ed th a t they w ould have add ed species even faster h ad they been sam pling across the contours and suggested th a t a rate o f one additional species for every extra square kilom etre o f seafloor was reasonable. W ith 300 m illion km 2 o f ocean floor deeper th an 1000 m, this translates to a global total o f 300 m illion b enthic m acrofaunal species! Yet as recently as 1971 T h o rso n estim ated th a t the

Table 11.2 Number o f species by phyla in 90 677 macrofaunal animals sorted from 233 box-core samples taken at depths between 1500 and 2500 m o ff New Dersey (from Grassle et at. 1990) Phylum

Number of species

Annelida Arthropoda Brachiopoda Bryozoa Chordata Cnidaria Echinodermata Echiura Hemichordata Mollusca Nemertea Pogonophora Priapulida Sipunculida

385 185 2 1 1 19 39 4 4 106 22 13 2 15

Total

798

THE BIOLOGY OF THE DEEP OCEAN

total nu m b er o f species in the oceans, at all depths, was ab o u t 160 000, In fact, G rassle an d M aciolek considered (arguably) th a t the oligotrophic n atu re of m uch o f the ocean w ould greatly reduce the num bers o f species in m any areas a n d suggested a conservative estim ate o f 10 million o r m ore m acrofaunal species (mainly molluscs, crustaceans, an d worms). T his conclusion tu rn ed the potential global inventory o f species on land an d in the sea on its head, an d raised the issue th a t the biodiversity o f the deep sea m ay challenge th at o f coral reefs an d rain forests. T h e issue hangs on the validity o f extrapolating from the 21 m 2 sam pled to the 300 X 10(> km 2 o f ocean floor th a t exists at equivalent depths. Som e biologists have even suggested th a t w hen the m eiofauna arc included, particularly the n em ­ atode w orm s, the nu m b er o f global m arine specics could be n earer to 100 million th a n the 10 million suggested from the m acrofaunal study (Lam bshead 1993). T hese very high estim ates for m acrofaunal species num bers w ere soon chal­ lenged. M ay (1992) argued th a t because ju st over h alf the identified species were new7it was likely that the sam e proportion w ould apply to a world inventory o f the fauna, in w hich case a total o f aro u n d 0.5 X 10(’ species could be expected. S u pport for the higher figure cam e quickly from the w ork o f two crustaccan tax ­ onom ists (Poore an d W ilson 1993). T h ey n oted th a t in samples taken in different ocean locations an d basins (but at depths sim ilar to those sam pled by Grassle an d Maciolek) the nu m b er o f spccies o f isopod crustaceans to be expected from every 100 specim ens w'as v ery variable, ranging from 7 to 39. In Grassle an d M aciolek’s d ata the value w-Tas only 12, suggesting th a t estim ates o f w orld species o f isopods based on the N o rth A tlantic d ata alone were likely to be too low. T h e controversy served to stim ulate interest in m arine biodiversity (and the m ethods o f assessment) an d several com parative studies have attem p ted to assess w hether the deep-sea results are unique to that environm ent. O n e study took sedim ent samples at depths o f 7 0 -3 0 0 m along a 1200-km stretch o f the N orw egian continental shelf an d looked at the m acro fau n a w hich w ere retained on a 1-mm sieve (Gray 1994). T his shallower fauna yielded 620 species from 39 582 individuals. From the rarefaction curve o f G rassle an d M aciolek the sam e n u m b e r o f individuals w ould have included only 550 species. T h e conclusion to be draw n is that the deep sea is n ot unique in its diversity an d th at spccies diversity on the shelf m ay be at least as high. T h e d o m inance p a t­ terns were sim ilar in bo th locations, w ith the single m ost ab u n d an t species m aking up 7% o f the individuals. A n earlier study o f the deep N orw egian Sea had, in m arked contrast, show n extrem ely low diversity, although this m ay in p a rt be a consequence o f the massive sedim ent flows know n to have occurred there some 5000 years ago an d now recognizable as turbidites (C hapter 3). A further com parison o f biodiversity in coastal an d deep-sea habitats (G ray el al. 1997) concluded that there was little discernible difference betw een the tw7o envi­ ronm ents and th a t the conclusions th a t could be draw n from existing d ata were very sensitive bo th to the num bers o f individuals collected an d to the areas sam pled in different program m es.

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245

E xtrapolation (or scaling up) from collected samples is only one w ay o f getting answers to the question ‘How' m any species are there?’ O th e r m ethods involve extrapolation from know n faunas an d regions, o r m ethods using ecological m odels, o r an integration o f the opinions o f expert taxonom ists, o r (theoretically) counting all specics. D em ersal fish have been used as a test o f the deep-sea m ethod o f extrapolation because they are m uch b etter know n by taxonom ists th an are the invertebrate m acrofauna (Koslow et al. 1997). T h e ir num bers were analysed from 65 com m ercial trawls fished betw een 200 an d 1400 m off W estern A ustralia (Fig. 11.2). T h e global species num bers predicted by extrapolating from the samples w ere th en com pared w ith the know n dem ersal fish fauna. T h e survey found 310 species from 89 families. U sing the sam e extrapolation criteria as for the deep-sea box-core d ata ab o u t 60 000 dem ersal species w ould be expected worldwide. A m ore realistic estim ate is 3000-400 0 global specics, based on the 2650 species currently know n, an d falling far short o f the 60 000 extrapolation. T h e authors therefore conclude th a t the extrapolation m eth o d is n o t appropriate for estim ates o f deep-sea global biodiversity. Fig. 11.2 The actual (circles) and predicted (line) number of species at 65 stations on the continental slope off western Australia. is indicated below by the estimated area o f the continental 20°S and, respectively, 24, 28, 32, and 35°S. (From Koslow sion o f Kluwer Academic Publishers.)

of demersal fishes collected The spatial scale o f sampling slope (km2) between latitude et al. 1997 with kind permis­

Number of individuals

,------,------1----- •,----- 1----- j----- 1------ 1 0

10

20

30

40

50

60

Number of samples 0

28,000

69,000

Slope area (km^)

87,000

104,000

70

THE BIOLOGY OF THE DEEP OCEAN

C learly there is plenty o f scope for further debate, b u t the p o in t has been forcibly m ade th a t deep-sea biodiversity is considerably higher th an h a d been thought. C om parisons w ith rain-forest biodiversity are nevertheless som ew hat tendentious because the size o f the organism s studied an d the spatial heterogeneity o f the environm ents are very different. W h en exam ined below the global scale there are substantial differences in the distributions o f biodiversity betw een latitudes, betw een ocean basins, and betw een depths. In the deep N o rth A dantic there is a general polew'ard reduction in the biodiversity o f the deep-sea benthic m acro ­ fauna, yet this is n o t so clear in the shelf fauna, n o r is it ap p aren t in the m eiofaunal nem atodes (Lam bshead et al. 2000) whose diversity increases polew ard, perhaps in response to a grad ien t o f increasing surfacc productivity. In the south­ e rn hem isphere there is m arked basin-to-basin variation a n d very high species richness in some coastal an d slope regions a n d any latitudinal correlation is m uch less ap p a ren t (Rex et al. 1993) (Fig. 11.3). T h e variation results from the different tectonic an d evolutionary histories o f the different oceanic basins. O n e explana­ tion proposed for the polew ard changes is th a t the geographical ranges o f species at high latitudes are greater, in response to the extrem e seasonal changes, w hereas organism s in the tropics are ad ap ted to m uch m ore constant conditions an d their ranges are therefore m uch m ore restricted. T his is know n as R a p o p o rt’s rule an d was originally proposed for terrestrial species. T h e relative abundances (evenness) o f m arine species in three shallow (30-80 m) soft-bottom com m unities from Arctic, tem perate, and tropical sites show ed no indication o f any latitudinal tren d (Kendall an d A schan 1993), so any effects o f latitude are by no m eans applicable to all benthic com m unities. T h e species diversity o f the benthos is also affected by depth. In the N W Atlantic the values for m acrobenthos on the shelf are relatively low (though n o t in the N E A tlantic, as noted above) but they increase rapidly dow n the slope to reach a m axim um at m id-slope depths (~2000—3000 m) before declining again dow n to the abyssal plains (Rex et al. 1993). In the Porcupine Seabight the m egabenthos has highest diversity at ab o u t 1000 m. T h ere is, in general, no link betw een the vertical profiles o f benthic biom ass (Fig. 3.9) an d biodiversity (Fig, 11.4). T h e first interpretations o f high biodiversity in the deep-sea sedim ents were built on a stability/tim e hypothesis, in w hich environm ental stability (and uniform ity) over long periods o f tim e allows a high degree o f niche separation an d p artitio n ­ ing o f food resources, an d therefore high specics diversity. M ore recent analyses suggest that the ap p aren t uniform ity o f the deep-sea floor is largely illusory an d th at there is considerable small-scale h abitat structure (m icroheterogeneity) in the environm ent. T his patchincss is associated w ith biological activity or disturbance (burrows, tracks, m ounds, faecal deposits, projecting structures, etc.) w hich m ay persist for long periods o f tim e (Gage 1996). S uperim posed on this are tem poral an d local differences in food deposition from above, in the form o f either phy­ todetritus (C hapter 10) or larger food falls. T h e present consensus is th a t the deepsea floor is m uch m ore a m icro-patchy environm ent th an -was previously appreciated an d th a t this is the m ain factor d eterm in in g its biodiversity. Sites w hich are subject to high levels o f disturbance (high cu rren t flow; for exam ple in

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247

Fig. 11.3 Variability in the biodiversity o f different oceanic basins is shown by the differences in the numbers of species of (a) isopods, (b) gastropods, and (c) bivalves expected in, respectively, 200, 50, and 75 specimens. There is a tendency for higher diversity at lower latitudes. (Reprinted from Angel 1996, with permission from Manson Publishing, after Rex et al. 1993, with permission from Macmillan Magazines Ltd.)

’S

"N

the H E B B L E area, C h a p te r 3) have a low er species diversity th a n do m o re stable ones, an d there are great differences in the ways different kinds o f anim als respond to these stresses. T h e overall p atterns o f biodiversity are p robably a com ­ prom ise betw een the level o f food resources available to the fau n a a n d the degree o f environm ental disturbance th a t they experience (this is know n as the D ynam ic E quilibrium hypothesis). Studies o f polychaete species diversity at three depths (1700, 3100, an d 4600 m) in, respectively, oligo-, meso-, an d eutrophic regions o f the tropical A tlantic

THE BIOLOG Y OF THE DEEP OCEAN

248

Fig. 11.4 Depth profiles of the numbers of species o f four megabenthic taxa in the Porcupine Seabight o ff southwest Ireland: (a) fish; (b) decapod crustaceans; (c) holothurians; (d) starfish; (e) the four groups combined. The maximum number of species in three o f the four groups occurs at a depth of between 1 and 2 km. (From Angel 1996, with permission.) (a) 60-1

(e) 100

2 3 Depth (km)

(20—2 1°N) have show n th a t the diversity peaks at ab o u t 2000 m (CossonS aradin et al. 1998). Species diversity is highest at the eutrophic site, an d g reater th an the values at sim ilar depths in tem perate latitudes, b ut the results do n o t conform entirely to the predictions o f the D ynam ic E quilibrium hypothesis. T h e conclusion is th at for the polychaetes alone the relationship betw een resources (surface productivity) an d disturbance is a com plex one, an d is always likely to be bo th locality- an d taxon-specific. T h e m osaic o f different conditions p roduced by differential food availability an d disturbance (whether physical o r biological) is prim arily responsible for the patchiness o f the benthic fauna on a variety o f scales, an d for the consequent biodiversity. T h e greatest disturbance is th a t im posed by massive m ud-slides or turbidites (C hapter 3). A large area o f the M a d eira Abyssal Plain is covered by turbidites an d the divers­ ity o f the polychaete fauna is m uch reduced, com prising a few com m on species (Glover et al. 2001).

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249

A n extrem e situation is th a t o f the populations at hydro th erm al vents (C hapter 3): there is very high endem ism at these dynam ic sites (~550 global species are know n only from hydrotherm al vents an d ~ 220 only from seeps) b ut the high levels o f physical disturbance lead to relatively low levels o f biodiversity. Nevertheless, the num erical abundance o f the lim ited n u m b er o f species th a t can flourish in these conditions is astonishing. T h e frequent description o f vents an d seeps as biological ‘oases’ in the ocean ‘desert’ is som ew hat misleading; they are indeed oases in term s o f biom ass density b u t no t in term s o f biodiversity. Low levels o f benthic diversity arc also characteristic o f the H E B B L E region in the eastern n o rth A tlantic, w here energetic bottom eddies b en eath the G u lf Stream lead to occasional benthic ‘storm s’ w hich scour a n d resuspend the sedim ents in the area. H ere a single species o f polychaete accounts for 5 0 -6 5 % o f the bcnthic m etazoan fauna. Seam ounts provide relatively small, geographically isolated seafloor environ­ m ents, analogous to hydrotherm al vents. A recent study o f the larger benthic fauna o f seam ounts off eastern A ustralia has show n b o th a very high endem ism (~30% o f species are know n only from the seam ounts) an d a high biodiversity (de Forges el al. 2000). T h e faunal overlap is greatest betw een seam ounts in p articu ­ lar clusters o r ridges an d is greatly reduced betw een those on different ridges. A sim ilar situation applies to the faunas o f bo th hyd ro th erm al vent sites an d deep trenches. A lthough m ost o f the curren t debate is about w hat produces the high biodiversity am ong the benthos, geological evidence has show n th a t it is historically m o d u ­ lated by clim ate (Rex 1997). T h e historical diversity o f ostracods (sampled in seabed cores) has varied directly w ith clim ate over 11 glaciation cycles. T h e species are basically the sam e throughout, b u t w ax an d w'ane in abundance. It seems likely that the clim atic cycles at the surface are linked to the deep-sea b io­ diversity through shifts in surface production an d its subsequent deposition on the seafloor. T h e determ inants o f deep-sea biodiversity thus o p erate at scales w hich range from local an d ep hem eral to global an d m illennial.

Biodiversity in midwater So far we have only considered the 300 X 10() km 2 o f seafloor below-' 1000 m. W h a t ab o u t the 1.4 X 10 9 km 3 o f the ocean volume? D oes this scalc similarly? Should w e therefore assume a total species n u m b e r o f several billion? All the evi­ dence points in the opposite direction, w ith the num bers o f pelagic species being orders o f m agnitude low er th an those o f their b enthic counterparts. T his is reflected in the fact th a t no phyla are solely pelagic (Table 11.1). T h e reasons for this disparity are not clear b u t it is likely th a t it is d eterm in ed largely by the global circulation o f the m idw ater environm ent an d the resulting w idespread dispersal capability o f pelagic anim als a n d their larvae, coupled w ith the relative lack o f structural heterogeneity in m idw 'ater (Angel 1997). Spatial structure is generated by the oceanic circulation, an d is often recognizable in th e form o f mesoscale

THE BIOLOGY OF THE DEEP OCEAN

eddies h undreds o f kilom etres in diam eter. T em poral structure is provided by the seasonal changes in the p rim ary production at the surface an d its subsequent transfer throughout the w ater colum n. M u ch o f the spatial structure is too ep hem eral to encourage isolation an d speciation, an d the high biom ass associated w ith the m arked seasonality at high latitudes derives from relatively few species w ith very large ranges. D espite these lim itations the pelagic fau n a o f the ocean is by no m eans uniform in space a n d tim e an d biogeographical regions (or faunal provinces) can be recognized (C hapter 4), corresponding in general to the exist­ ing circulatory p atterns w hich in tu rn are superim posed upon the geological history o f the ocean basins. Speciation requires som e separation o f populations, either by physical isolation (allopatric speciation) or by som e form o f reproductive isolation (sympatric speci­ ation). Oscillations in clim ate (e.g. glaciation cycles) have p ro d u ced m ajo r changes in sea level, sufficient to open o r close some seaways (largely east-w est) an d tem ­ porarily isolate ocean basins an d seas. T hese events (known as vicariance events) provide p articular opportunities for allopatric speciation. In the absence o f phys­ ical barriers allopatric speciation m ay still occur if gene flow rates are very slow an d the h ab itat distances very large. Prolonged vertical separation o f populations will be ju st as effective a form o f isolation as horizontal separation. Sym patric spe­ ciation, on the other h an d , implies some degree o f niche separation, perhaps linked to the seasonal periodicity o f production or to changes in the p attern s o f vertical m igration. W hatever the m echanism s, speciation in the pelagic occan has been lim ited. O ne factor, w hen com paring biodiversity w ith th at on land, is th a t there are only some 5000 species o f (very small) m arine phytoplankton w hereas there are 50 tim es as m any large terrestrial green plants. M any o f the latter have their own associated com m unities o f specialist anim als (mostly insects). In the ocean, w here the h erb i­ vores are generally m uch larger th an the phytoplankton on w hich they graze, sim ilar associations are the exception an d particle size is o f g reater im portance in determ ining feeding relationships. T h e global n u m b e r o f species in the dom in an t m idw ater groups is n o t large (e.g. 2200 copepods, a few h u n d red jellies an d comb-jellies, 115 chaetognaths, 187 ostracods, 87 euphausiids, an d less th a n 1000 fish). G iven the inverse pyram id o f biom ass density from the surface to the seafloor (C hapter 4), we m ight expect th at pelagic species diversity w ould show a sim ilar declinc w ith d epth an d th at the bathypelagic fauna w ould have a particularly low species diversity. Analyses o f net samples from the surface to 2000 m show th at in fact the spccies diversity declines m uch m ore slowly th an does the biom ass density, sim ilar to the results for the benthos (i.e. in deep w ater there are far fewer individuals b u t n ot equivalently fewer species). Studies o f planktonic ostracods in the u p p er 2000 m o f the N E A tlantic from 11 -60°N along longitude 20°W, for exam ple, show an increase in species diversity at m id-depths (Fig. 11.5). T h e ostracod d ata also show a m idlatitude peak in specics richness (at 18°N); the same applies to the fish, decapods, an d euphausiid shrim p taken in the sam e hauls (Fig. 11.6). T h e peak m ay

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251

represent the overlapping o f two faunal provinces (C h ap ter 4) at this latitude. A recent study o f planktonic foram iniferans, sam pled from the shells deposited in surface sedim ents, found a sim ilar m id-latitude p eak in diversity. O f the observed geographical variation, 90% was explicable on the basis o f satellite-m easured sea-

Fig. 11.5 Vertical profiles of the numbers o f species o f planktonic ostracods in the upper 2000 m at seven stations along longitude 20°W. There are more species at all depths southwards from 40°N (filled symbols) than there are at higher latitudes (open symbols). (From Angel 1996, with permission.)

0

10

Species (number) 20

30

40

1__________ 1___________ I___________ I___________ I

THE BIOLOGY OF THE DEEP OCEAN

Fig. 11.6 The total numbers of midwater species of four taxa taken at six stations along 20°W in the eastern North Atlantic. The number o f species decreases with increasing latitude; the maximum at 18°N reflects a boundary between tw o faunal regions. (From Angel 1996, with permission.)

Latitude (“N)

surface tem peratures a n d led to the conclusion th at the zooplankton diversity (at least o f this group o f animals) is directly controlled by the physical characteristics o f the near-surface ocean (R utherford et al. 1999) (cf. the identification o f faunal dom ains, C h a p te r 4). T h e plankton samples at 18°N, noted above, contained 4 0 -5 0 % o f the globally know n species o f pelagic ostracods and euphausiids, dem onstrating w hat a large p roportion o f all oceanic species m ay be present at any one locality (Angel 1997). A t one station in the central Pacific over 200 species o f phytoplankton were recorded in the photic zone an d 175 species o f copepod in the u p p er 500 m. Clearly, local species richncss can be very high. T h e picture o f pelagic biodiver­ sity is therefore prim arily one o f a lim ited n u m b e r o f species w ith extensive geo­ graphical ranges (i.e. low P-diversity). T his picture is, however, based on classical taxonom y in w hich species are recognized by their m orphological differences. G enetic inform ation on one spccies o f deep-sea fish suggests th a t the criteria o f classical taxonom y m ay be inadequate (Miya an d N ishida 1997). T h e genus Cyclothone com prises 13 species o f ubiquitous an d num erically d o m in an t small m esopelagic fishes. Cydothone alba occurs in the tropical A tlantic, Pacific, an d Indian oceans. T h e ribosom al R N A o f specim ens from different regions d em o n ­ strates quite distinct but robust genetic differences betw een the populations. T hose in the central a n d w estern N o rth Pacific are m ore related to the Atlantic an d Ind ian O ccan populations, respectively; th an they are to o th er Pacific p o p u ­ lations. T h e lineages seem to have been historically linked across the P an am an ian

A WONDERFUL VARIETY OF LIFE: BIODIVERSITY OF THE DEEP-SEA FAUNA

253

isthm us an d S trait o f T im or, w hich now present physical barriers to mixing. T h e m axim um intraspecific genetic differences in C. alba w ere sim ilar to the m inim um interspecific differences betw een C. alba an d C. signata. T h e separate genetic iden­ tity o f three Pacific populations o f C. alba over very long periods o f tim e indicates how allopatric speciation can occur in the deep sea th ro u g h the persistence o f genetically distinct populations (or cryptic species). I f these results are applicable to the rest o f the pelagic fauna (and d ata from oth er taxa suggest th a t they are) it is very likely that pelagic biodiversity based on classical taxonom y seriously u n d er­ estim ates the real situation. T h e pelagic fauna is not unique in this respect; cryptic species in the benthos are also likely to produce underestim ates o f diversity (Etter et al, 1999).

Conclusion Benthic, an d pelagic biodiversitics in the deep sea are on quite different tim e an d space scales. Present diversity is a consequence o f the evolutionary build-up o f species inventories, the effects o f dispersal processes an d the b arriers to them , an d the curren t environm ental conditions th a t allow species to m aintain their populations. It is therefore highly dynam ic. As yet we do n o t really know w hat ‘value’ biodiversity represents to different ecosystems. T h e original belief that higher biodiversity (with a m ore com plex w eb o f interspecific linkages) represents a m ore resilient com m unity has been show n to be naive. M ath em atical analytical techniques have show n th a t sim pler ecosystems w ith lower biodiversity m ay be the m ore robust. E xperim ental m anipulations o f m icrobial com m unities have indicated, however, th a t the m ore species th a t are present in different functional groups (autotrophs, decom posers, prim ary consum ers, etc.) the m ore stable are the com m unities (Naeem an d Li 1997). T h e consequences o f the disturbance o f deep-sea ecosystems th at activities such as the m ining o f m anganese nodules m ight produce have been investigated exper­ im entally by ‘ploughing’ an area o f the abyssal Pacific floor an d following the recovery o f the benthic fauna. T h e experim ent is still in an early stage o f recolo­ nization b u t all the indications so far are th a t the recovery process is extrem ely slow. It is w orth noting th a t this sort o f disturbance is sim ilar to th a t inflicted alm ost continuously on the benthic populations o f the N o rth Sea by com m ercial b eam trawls (some areas are estim ated to be swept m ore th an 300 times p er year!). N atu ral disturbance o f pelagic deep-sea populations has n o t yet been identified, n o r has it been attem p ted experimentally. Following a local disturbance, there is little d oubt that although the populations arc fragile they w ould probably retu rn to their previous level if given sufficient recovery time. T h e consequences o f con­ tinued or w idespread disturbance (such as m ight be p ro d u ced by changes in the speeds or p attern s o f ocean currents im posed by clim ate change) cannot be p re ­ dicted. T h e pelagic biodiversity in the low-oxygen regions o f the N W Indian O cean and the eastern tropical Pacific is low com p ared w ith th at o f oxygenated w aters at com parable latitudes. W ere these low oxygen conditions to spread (in

THE BIOLOGY OF THE DEEP OCEAN

response to changes in circulation), the effects on biodiversity w ould be b oth severe an d long term . C onservation o f the biodiversity o f the deep sea m ay n o t seem a high priority at the m om ent. C onservation effort is focused on individual (large) species o f the u p p er ocean, such as whales a n d com m ercial fishes. W e do n ot know how the b io­ diversity o f different p arts o f the ocean affects the w ay the ecosystem functions as a whole. W hich are the key species? A re they the m ost num erous ones o r the ones th a t eat the most? O r do som e rarer species have critical roles in the m aintenance o f ecosystem stability? Ju st as on land, it m ust surely be m ore im p o rtan t to m a in ­ tain the long-term integrity o f the h abitat th a n simply to focus on the short-term survival o f a few em otionally a n d /o r com m ercially satisfying species. B ut therein lies the problem , because the physical continuity o f the h ab itat an d the m otion o f the fluid w ithin it will ultim ately transfer the effects o f a p ertu rb atio n at one location ro u n d the entire system. T h e saving grace at present is th a t the volum e o f the oceans an d the area o f the ocean floor buffer the effects o f local pertu rb atio n s an d provide the species reser­ voir from w hich recovering populations can generally draw. M an k in d ’s globalscale activities, however, w hether they be com m ercial fishing or carbon dioxide emissions, p u t a severe pressure on this buffering capacity. It is these kinds o f pres­ sures th a t need to be addressed to m aintain the existing biodiversity o f the oceans through this m illennium .

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Appendix

The marine phyla

Introduction T h e g reater p a rt o f the biodiversity exemplified by the phylum distributions show n in T able 11.1 is hidden in the structural an d physiological variety w ithin each phylum . B rief outlines o f the different phyla an d their m ain habitats are given below. T h e em phasis here is on the anim al phyla; they are all heterotrophs in th a t they d ep en d upon the photo- or chem osynthetic abilities o f other o rg an ­ isms to convert inorganic carbon into the organic m aterial on w hich they feed. M ost o f this organic carbon derives from photosynthesis in the surface w aters by the protist o r bacterial phytoplankton (photoautotrophs) b ut som e com es from chem osynthesis by free-living or sym biotic b acteria (chem oautotrophs) either in the sedim ents o r at special sites such as h ydrotherm al vents an d cold seeps (C hapter 3).

'Kingdom' Protista: some important heterotrophs By no m eans all unicellular organism s are either p h o to au to tro p h s or chem o au ­ totrophs, i.e. fix inorganic carbon. M any protists require dissolved or particulate organic carbon for their nutrition (i.e. they are heterotrophs), ju st like the A nim alia (or m etazoans). Som e o f these protists are very im p o rtan t in the econom y o f the oceans, an d specifically the deep oceans, nam ely the ciliates, foram iniferans, an d radiolarians. T hese w ere once all classified as ‘P rotozoa’. I use the form er K ingdom Protista as a convenient receptacle for a genetically h et­ erogeneous group o f organism s involving from 27—45 phyla, or h igher taxa, according to different authors (M argulis an d Schw arz 1988; D oolittle 2000). W ithin this K ingdom fall arguably b o th the m ulticellular ‘algae’ or seaweeds an d the larger photosynthetic, or photoau to tro p h ic, m icroorganism s (diatoms, dinoflagellates, flagellates, coccolithophores, etc.), as well as the heterotrophs. In the five kingdom classification the ciliates, foram iniferans, an d radiolarians were separated into the phyla C iliophora, Foram iniferida, an d A ctinopoda, respec­ tively (M argulis an d Schw artz 1988; C apriulo 1990). Ciliates are im p o rtan t in bo th the sedim ents an d the plankton. T h e m eiobenthos contains 10-15% o f all know n spccies and they are extrem ely ab u n d an t, w ith densities o f u p to 50 X 10(> organism s m -. D ifferent species feed on bacteria,

APPENDIX

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detritus, algae, or o th e r anim als, an d the species present in any p articu lar sedi­ m ent vary according to the pore size o f the sedim ent particles. T h e ir an n u al p ro ­ duction to biom ass ratio (or turnover) in this environm ent is ab o u t 250, a very high value w hen com pared w ith 13 for the benthic m eiofauna an d 2 -3 for the b enthic m acrofauna. Ciliates are present in the w ater colum n at densities o f up to 145 X 101’ 1"1 an d are locally enriched on m arine snow. T in tin n id s an d o th er cil­ iates graze on the m icroflagellates an d their role is prim arily as interm ediates in the m icrobial loop (C hapter 2). T h e m icroflagellates w hich eat the b acteria are, of course, also heterotrophs, an d m ay o ccur at densities o f 10°—10' l-1, each m icroflagellate consum ing hundreds o r thousands o f bacteria p e r day. Foram iniferans are exclusively m arine organism s an d are ab u n d a n t throughout the oceans at all depths, bo th in the plankton an d in the benthos. T h ey have single- or m ulti-cham bered shells, form ed o f an organic m atrix reinforced to varying degrees by calcification o r by the agglutination o f sedim ent particles. C ytoplasm ic filaments extend out o f the shell to un d ertak e swimming, feeding, or shell construction. T h ey have m ultiple nuclei an d a haploid—diploid altern atio n o f generations. T h ey are omnivores, ensnaring particles o f all kinds including small copepods. Some, particularly those in oligotrophic areas, have photosynthetic symbionts, b u t these are absent from the deep-w ater species. T h e re is consider­ able structural variety in a single species an d the grow th form reflects the w ater conditions in w hich the individuals live. Foram iniferans can therefore be used as m arkers o f p articu lar oceanic w ater masses an d th eir distribution in the sedim ents provides a valuable historical record o f ancient oceanographic conditions. T h ere are species am ong the m eiofauna th a t live in or on the sedim ents an d som e deepsea species respond very rapidly to the deposition o f m aterial from the surface (C hapter 10). O n e group, the koinokiaceans, com prises large agglutinated foram iniferans th a t are com posed o f a tangled m ass o f tubules. T h ey m ay be very ab u n d a n t on some deep-sea sediments. T h e even larger (to 25 cm diam eter), m uch-branch ed , sponge-like xenophyophores (Fig. 3.6) are superficially sim ilar to the kom okiaceans b u t are giant testate rhizopods (amoebae) a n d not foram iniferans. In som e regions o f the eastern N o rth A tlantic an d Indian O ceans these organism s m ay carp et the abyssal seafloor. Spherical gelatinous am oebae the size o f golf balls are related protists w hich m ay also be very ab u n d a n t on particu lar areas o f the deep-sea floor. R adiolarians form a loose group o f prim arily planktonic actinopodans. T h ey have a lifespan o f ab o u t a m onth a n d are present from pole to pole an d from the surface to the abyss. T h e re are four groups, three o f w hich have silica spines or spicules. T h e fourth group (the acantharians) has a skeleton o f strontium sulphate. R adiolarians have only one nucleus an d a central capsule, w hich m ay be sur­ rou n d ed by a frothy cytoplasm . Som e have a radial symmetry, others a bilateral one. T h ey feed on a variety o f m aterial, including b actcria, detritus, algae, an d small planktonic anim als, captu red by cytoplasm ic stream ers. T h ere arc 400—500 species in the m ain group (the polycystines), 4 0 -5 0 o f w hich can be found over very w idc dep th ranges, although som e occur only below 2000 m. M an y species in this

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group contain num erous photosynthetic sym bionts an d som e are colonial, form ing large gelatinous aggregates, particularly in the near-surface w arm oligotrophic w aters in w hich they are particularly abu n d an t. T h e re are some regions o f the Pacific O ce an w here large masses o f these colonics sedim ent on to the deep-sea floor, w here they look rath e r like a dim inutive form o f m arine tum blew eed.

Kingdom Animalia T h e m arine anim al phyla are o f very uneq u al ecological im portance (e.g. Table 11.2). Som e are o f negligible significance, others arc d o m in an t shapers o f the m arine ecosystem. Som e are wholly benthic, others m ainly pelagic. A b rief in tro ­ duction to each o f them is given below, setting them in the deep-sea context. Phyla w ithout any know n deep-sea species are in sm aller font. M o re inform ation can be found in the references for C h a p te r 10 an d in M arshall (1979), B arnes et al. (1988), H iggins an d T hiel (1988), Brusca an d Brusca (1990), G age an d Tyler (1991), H am m o n d (1992), G iere (1993), H aw ksw orth an d K alin-A rroyo (1995), an d H aedrich an d M errett (1997). T h e first two phyla have no separate tissue layers an d can be co m p ared w ith aggregate protists. P la c o z o a

L ooking ra th e r like a ciliated am o eb a, the one species in this phylum was originally believed to be a sponge o r c nidarian larva. It was first found in m arin e a q u a ria and occurs in the intertidal zone.

Porifera (sponges) Sponges are sessile anim als that lack any tissues or organs an d have no ch arac­ teristic symmetry. Flagellated cells know n as choanocytcs are responsible for w ater filtration an d feeding an d there is an often elaborate skeletal system o f calcarcous or siliceous spicules or o f collagenous fibres. A lm ost all the 10 000 or so species are m arine. T h e re are m any deep-sea species, several o f very large size (up to ~ 1 m diam eter); the glass sponges (hcxactincllids) are prim arily deep-w ater anim als an d large specim ens m ay be m ore th an 200 years old. T h e next four phyla have only two layers o f cells. C nid arian s an d ctenophores used to be com bined as ‘coelenteratcs’ but are now regarded as separate phyla.

Cnidaria (jellyfish, anemones, corals) C nidarians are radially sym m etrical anim als w ith tentacles ro u n d the m o u th an d ‘m edusa’ o r ‘polyp’ body forms. T hey have two layers o f cells (epiderm is an d

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endoderm is) separated by an acellular gelatinous m esogloea. Stinging threadlike nem atocysts (‘cn id a’) are unique to the phylum an d are present in all groups. T h ey are coiled in cells nam ed cnidocytes an d fired by hydraulic eversion. M ost o f the ~ 10 000 cnidarian species arc m arine. T h e A nthozoa (corals, sea anem ones, sea pens, sea fans) com prise 6200 species, occur only as solitary or colonial polyps, are sessile (though som e can move slowly), an d the shallow -w ater species usually contain dinoflagellate symbionts. M any anthozoans have calcareous o r ho rn y skeletons. T h e num erous deep-sea species include sea pens, solitary corals, an d som e stony corals (e.g. Lophelia), w hich m ay form extensive reef-like aggregations. T h e H ydrozoa (3100 specics) usually have a sessile polyp an d a free-living m edusoid form , though either o f these form s m ay be lost. Som e have algal symbionts. T h e polyps form the typical colonies o r ‘hydroids’ a n d different polyps m ay have different form s a n d functions w ithin the colony. H ydroids are typically shalloww ater coastal anim als b u t their m edusae m ay be found in the plankton in all areas o f the ocean. D eep-sea H ydrozoa are know n prim arily from the m edusa forms, an d arc com m on in the m eso- an d bathypelagic zones. O n e group, the siphonophores (150-200 species), are very com plex pelagic colonies w ith individ­ uals m odified as floats, sw im m ing bells, stom achs, etc., an d the colonies m ay som etim es extend to tens o f m etres in length. T h ey are very im p o rtan t m eso- and bathypelagic predators, but difficult to sam ple adequately because o f their fragility; A few' species anchor themselves tem porarily to the b o tto m by th eir ten ­ tacles, looking rath e r like benthopelagic hot-air balloons ready for take-off. T h e Scvphozoa o r true jellyfish (200 species) occur m ainly in the free-sw im m ing m edusoid form . T h e re are m any oceanic specics; they have no polyp stage and occur at all depths in the ocean. T h ey m ay reach a large size (1-2 m diam eter) and, w ith the siphonophores, are very- im p o rtan t pelagic predators. C ubozoa (sea wasps) are shallow -w ater tropical m edusae w ith potentially lethal stings. Som e o f these anim als have surprisingly well-developed ey^es.

Ctenophora (comb jellies) T his phylum shares a com m on ancestor w ith the C nidaria. T h e 100 or so species are exclusively m arine. O n e group has two long tentacles, giving th em a bilateral symmetry. They' do n o t have penetrative nem atocysts like the C n id aria but instead the tentacles b ear sticky lasso cells (colloblasts); they have muscles derived from the m esoglocal layer an d they have eight rows o f com b plates constructed of fused cilia w hich are used for feeding an d locom otion. T h e second group lacks the tentacles an d m any o f these species feed by engulfing o th er ctenophores. T h ey are poorly' know n because they arc extrem ely fragile an d difficult to study; Shalloww ater species m ay occasionally ‘b loom ’ in huge populations an d seriously' reduce the num bers o f the planktonic anim als an d larvae on w hich they feed. T h ey are im p o rtan t in the pelagic ecology o f the deep sea an d are becom ing b etter ap p re­ ciated through the use o f submersibles. T h e deep-sea specics are often ab u n d an t,

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m ay exceed 0.5 m in size, some are o f ex trao rd in ary delicacy o f structure, an d m any are able to swim rapidly by m eans o f m uscular contractions o f their oral lobes, in addition to slower m ovem ents using only the ciliary com b-plates. M esozoa

S quid, cuttlefish, a n d octopods have these sm all (10 m m ) parasitic w orm -like anim als living in th eir kidneys. T h e 70 species have b e en considered as interm ed iates betw een th e p ro ­ tists a n d the m etazo an s a n d have two tissue layers a n d only one org an system , the gonads. R ecent studies o f gene sequences suggest th a t they are secondarily sim plified h igher protostom es (invertebrates including annelids, m olluscs, a n d arthropods). T h e re are no described deep-sea species.

O r th o n e c tid a

O riginally included in the M esozoa, these anim als are parasitic in a n u m b e r o f m arine invertebrates, including flatw orm s, nem ertines, m olluscs, a n d echinoderm s. T h e re are ju st three g e n era a n d few species a n d they infest a range o f tissues.

All other phyla have three layers o f cells an d their relationships hinge on the type o f body cavity (if any) an d on their em bryonic developm ent.

Platyhelminthes (flatworms) Flatw orm s have bilateral symmetry, three body layers, an d occur in all m ain h ab i­ tats. T hey have a m o u th an d gut, b u t no anus. T h ere are ab o u t 15 000 species, m any o f w hich are m arine, bo th free-living turbellarians a n d parasitic trem atodes (flukes) an d cestodes (tapeworms). T h e largest species (whale tapew orm s) m ay achieve a length o f 30 m. T h e turbellarians are n ot known from the deep sea but flukes a n d tapew orm s occur in fish (and other animals) a t all depths. T h e ir eco­ logical im portance in the deep sea is therefore prim arily as the parasitic load on other species. It has been suggested th a t they are related to the nem atodes and gastrotrichs.

Nemertea (ribbon-worms) T hese unsegm ented w orm s are distinguished from the flatworms (Platyhelminthes) by the presence o f an anus, closed blood system, an d eversible proboscis. T h e 900 species are m ainly shallow -w ater m arine anim als an d an intertidal species m ay reach 30 m in length. O n e group o f n em erteans (Anopla) is m ainly benthic. M any species o f the oth er m ain group (Enopla) are pelagic and present in deep water. T h ey m ay som etim es com prise 30% o r m ore o f the pelagic biom ass below ab o u t 1500 m . T hey are p red ato ry anim als an d m an y probably feed on decapod crustaceans or their eggs. In coastal w aters some species present a com m ercial problem as com m ensals o r parasites o f lobster eggs. T h ere arc also 30 or so species o f very small interstitial nem ertines.

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G n a t h o s to m u lid a

T h e 100 o r so species o f these tiny (0.5 -1 m m ) w orm -like acoelom ate anim als are com m on m em b ers o f the m eiofauna o f anoxic a n d sulphidic m arin e sedim ents, extending to depths o f a t least 800 m . T h ey have a ciliated ep iderm is a n d h a rd en e d jaw s for g razing on m icroorganism s living o n the surface o f sand grains.

G a s tr o tr ic h a

G astrotrichs are tiny (< 4 m m ) w orm -like u nsegm ented acoelom ate anim als covered w ith scales, spines, or hooks a n d b e arin g adhesive tubes. T h e y m ove by ciliary' gliding and the m arin e species are p a rt o f the inter- and subtidal interstitial fauna o f oxic sedim ents. Л few species are planktonic. T h e re are ab o u t 450 species. T h e g roup is m ost closely related to the nem atodes.

R o t if e r a ( w h e e l a n i m a l c u l e s )

T h ese little planktonic anim als have at th eir heads a characteristic circlet o f two rings o f cilia, b e atin g in opposite directions, a n d a t th eir tails a n elongate foot w ith an adhesive or spinous tip. T h e ir bodies are enclosed in a chitinous covering o r lorica. They' m ay be round or tru m p et-sh ap ed a n d there are ab o u t 2000 species o f w hich only 50 o r so are m arine. T h e m arin e species feed o n m icroalgac a n d are a n im p o rta n t food source for the plank­ tonic larvae o f o th er specics. T h e re are n o deep-sea species.

Kinorhyncha K inorhynchs are exclusively m arine anim als that pull themselves along by m eans o f hooks on the h ea d an d have 11 trunk segments covered by a spiny cuticle. M ost arc less th an 1 m m in length. T h ere are some 100-150 spccies, an d they co n ­ tribute to the interstitial m eiofauna dow n to at least 5000 m.

Loricifera O nly ab o u t 15 species o f these m inute (< 0 .3 mm) anim als are know n a n d the phylum was erected only in 1983. All are m arine an d have been found am ong the interstitial fauna, from the intertidal to 8000 m an d from the A rctic to the midPacific. T h e anim als have a head w hich is eversible an d bears a n u m b er o f spines, a short arm o u red neck, and a trunk covered by' a cuticular lorica o f six longitu­ dinal plates (or o f num erous folds) bearing anteriorly-directed spines. N o th in g is know n about their ecological significance. C y c lio p h o r a

T h is acoelom ate phylum w as proposed in 1995, based o n the discovery o f the single species Symbian pandora, a tiny anim al w hose fem ales (3 00-400 |im in length) and attached d w a rf m ales (80 ц т ) w ere found o n the up p er lip o f the squat lobster Nephrops norvegicus. T h e fem ales have a ciliated m o u th a n d the phylum has affinities w ith the E n to p ro c ta a n d E ctoprocta.

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E n to p r o c ta (o r K a m p to z o a )

T hese sm all (0.5-5 m m high) m arin e anim als (~ 150 species) superficially resem ble ectoprocts, w ith w hich they w ere once grouped, b u t the body? cavities are o f different origin, b o th the m o u th a n d anus o p e n w ithin the circle o f tentacles (the anus is outside the circle in ectoprocls) a n d there are m an y o th e r differences. Zoologists continue to argue a bout their relationships but they are not tru e lo phophorates a n d are p ro bably m ost conveniently lum p ed w ith o th er enigm atic groups such as the gnathostom ulids, kinorhynchs, a n d loriciferans. Som e are solitary a n d som e are stalked, form ing hydroid-like colonies. T h e plan k ­ tonic larvae resem ble the tro ch o p h o re larva o f annelid w orm s. T h ey are p ro bably all h e rm aphrodites. N o deep-sea species are known.

Acanthocephala (spiny-headed worms) T h ere are at least 600 species o f these gut parasites o f carnivorous vertebrates. T h ey have no free-living stage and the first hosts o f m arine species are usually zoo­ plankton crustaceans. M ost are only a few centim etres in length; the largest is ab o u t 1 m. T h ey are unsegm ented, have no gut an d occur in hosts from the m arine, fresh­ water, an d terrestrial habitats, including seals, dolphins, an d deep-sea fishes.

Nematoda (roundworms, eelworms) N em atodes are unsegm cntcd w orm s w hich have a thick cuticle som etim es bearing hairs, spines, or o ther projections. T h ey have separate sexes, no cilia, a n d no circu­ lar muscles. T h ey are divided into two classes based on the num bers an d types of sense organs. At least 25 000 species have been described, including large num bers o f parasitic species in bo th plants an d anim als an d m any others free-living in soil o r m arine sediments. T h e free-living form s arc small, often less th an 1 m m in length, and their food ranges from b acteria to o th er nem atodes. T h ey are probably the m ost ab u n d a n t m eiofaunal group, m aking up 9 0 -9 5 % o f the individuals an d 5 0 -9 0 % o f the biom ass in m any m arine sedim ents, including those o f the deep sea. M any can survive low-oxygen conditions (or even the presence o f sulphide) an d they are found everywhere from po lar regions to hydrotherm al vents. It is quite pos­ sible that there arc m ore th an a million undescribcd species and even this figure m ay be a gross underestim ate. A nim als o f m eiofaunal size, like nem atodes, are counted from corc samples covering an area o f only a few square centim etres. It has been suggested that scaling up the species diversity from these samples to the global oceans w ould im ply some 10- 100 m illion spccies! N e m a to m o r p h a (h o r s e h a ir w o r m s )

T h e larvae o f these threadlike w orm s are parasitic in a variety o f arthropods, a n d the adults have a b rie f free-living existence. T h e gut is degenerate a n d n o u rish m en t is absorbed th ro u g h the cuticle. T h e adults have som e superficial sim ilarities to the nem atodes, b u t the larvae m o re close!)' resem ble kinorhynchs a n d loriciferans. T h e re are only ab o u t 250 species m ost o f w hich live in fresh water. In the o rd e r N ecto n cm atid a there are some m arin e species w hich parasitize d ecapod crustaceans. N o deep-sea species are known.

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T h re e sedentary or sessile phyla are known as lophophorates because they have the com m on feature o f a lophophore, a ring o r horseshoe o f ciliated tentacles ro u n d the m outh for suspension feeding. T hey all lack specialized gonads, the g erm cells being m erely loose clusters o f cells in the peritoneum . P h o r o n id a ( h o r s e s h o e w o r m s )

T h e 15 species in this phylum are all m arine, a n d know n only from coastal w aters. T h e large lo p h o p h o re has u p to 15 000 tentacles, w hich m ay be a rra n g e d in a spiral coil and the species range in size from 1 m m u p to 0.5 m in length. All b u t the ten ta cu lar crow n is enclosed w ithin a chilinous tube, w hich is eith er b uried in the sedim ents o r a tta ch e d to a rock. T h e actin o tro ch a larvae are ciliated a n d planktonic, resem bling the trochophore larvae o f annelid w orm s.

Brachiopoda (lamp shells) T h e body o f these sessile lophophorates is enclosed in a bivalved shell. T h ey look very like clams but the two halves o f the shell are dorsal an d ventral instead o f left an d right. T h ey have a large an d com plex lo phophore a n d m ay be cem ented to rocks, attached by a stalk, o r lie free on the sediments. All are m arine. T h e ir heyday was in the Palaeozoic era from w hich alm ost 30 000 fossil species are known, but there are only 335 living species, all o f w hich are rela­ tively small (1 m m to < 1 0 0 mm). T h e ciliated larva is different in the tw o sub­ groups o f brachiopod but in bo th eases is planktonic. T h e adults are found at all depths to 4000 m.

Ectoprocta (or Bryozoa) (moss animals) E ctoprocts are small, usually colonial, encrusting anim als th a t look rath e r moss­ like. A lm ost all the 4 0 0 0-5000 species are m arine. T h e colonies are form ed by asexual budding an d the contiguous individuals (zooids) m ay develop into several different form s (polym orphism ), specialized for feeding, defence, reproduction, ctc. T h e small (< 2 mm) zooids are enclosed in tubes o r boxes m ade o f chitin or calcareous m aterial an d form a honcycom b-like array. T h e grow th form s o f the colonies m ay be encrusting, stalked, or leaf-like an d th eir shape is often d eter­ m ined by the local cu rren t speed. A bout 150 species are know n in the interstitial m eiofauna, ranging to depths o f 6000 m.

Priapulida T h e phallic appearan ce o f these m arine w orm s gives the phylum its nam e. T h ere are only 16 living species, ranging from 0.5 to 200 m m in length, b ut m any m ore were present in the C am b rian period. T h ey are carnivorous an d feed on polvchaetes an d other anim als. T h ey have a retractable an terio r p o rtio n o r proboscis

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(prosoma) w ith spines or teeth, an externally segm ented w arty or scaly trunk, an d a tail-like appendage. T h e cuticle is chitinous an d m oulted periodically. T hese anim als occur sporadically from shallow w ater to at least 2500 m. T h e abyssal specim ens m ay all belong to a single species an d m ay be very abu n d an t; densities o f over 200 individuals m 2 were recorded from one location at 1800 m. T h eir larval developm ent links them to the kinorhynchs.

Mollusca (tusk shells, chitons, snails, clams, pteropods, cephalopods) Molluscs have som e affinities w ith particu lar w orm phyla, p erh ap s m ost closely w ith sipunculans. T h ey are soft-bodied anim als in w hich a fold o f body wall, the m antle, secretes the shell. T his is basically o f protein b ut is often hugely reinforced w ith calcareous plates. In the m outh is a to o th ed ribbon, the radula, w hich can be everted to rasp at the food. T h e body form is hugely varied, ranging from linear chitons to spiral snails, bivalved clams, gelatinous pteropods, an d long-arm ed cephalopods. T h e re are probably m ore th an 70 000 species know n, a n u m b er exceeded only by the insects. T h ere are eight classes o f molluscs, dom inated by the gastropods an d bivalves (which m ake up 98% o f the know n species) an d the cephalopods. O f the other classes, one contains a few recently discovered lim pet­ like deep-sea species an d is m uch better know n from the fossil record, two others contain species w ith no shell an d worm -like bodies; they, too, include some deepsea species. T h e re arc also a few deep-sea Polyplacophora (chitons) and S caphopoda (tusk shells) in an d on the abyssal sediments. In the G a stro p o d a the visceral h u m p (which contains the in tern al organs) rotates through 180° during developm ent so th a t the m antle cavity faces forw ard. This process is know n as torsion. M ost o f the m arine snails have retain ed this organiza­ tion, w ith a foot, spiral shell, and one or two gills in the m antle cavity. T h ey have ciliated trochophorc a n d veliger larvae. T h e m ajority have separate sexes though a few are herm aphrodites. M arin e snails com m only browse on algae or sessile anim als, b u t some are deposit feeders an d a few' are voracious predators. M em bers o f one planktonic group, the heteropods, have reduced the shell, developed an o ar­ like sculling foot, an d bccom e active predators. O th e r gastropods have lost or reduced the shell a n d /o r undergone some detorsion. T hese include the nudibranchs (sea-slugs an d sea-hares) and the planktonic pteropods (sea-butterflies). Pteropods typically filter-feed (using large m ucous webs to snare food particles) an d have thin shells. T hey m ay be so ab u n d an t th a t th eir shells accum ulate on parts o f the deep-sea floor as a ptero p o d ooze. O th e r pteropods have lost the shell an d becom e carnivorous. Both types are im portan t an d often a b u n d a n t m em bers o f the plankton, an d there are a few deep-sea species. T h ere are m any deep-sea benthic gastropods. T h ey include deposit feeders, p red ato rs on polychaetes an d on other molluscs, roving scavengers, an d a nu m b er o f ectoparasites o f echinoderm s an d anem ones.

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T h e B iv alv ia (clams, oysters, mussels) arc laterally com pressed molluscs com ­ pletely enclosed w ithin the two shell valves an d they have lost the radula. T h ey are m ore num erous in the deep-sea sedim ents th an are the gastropods an d they have a higher species diversity in som e abyssal regions. Shallow -w ater bivalves m ay reach 1 m in length and belong m ainly in the lam ellibranch subgroup. M ost specics feed on particles brought in on the inhalan t w ater current, sorting them on the enlarged gills; further ciliary food selection m ay take place on the labial palps. Som e lam ellibranchs cem ent themselves to the substrate or attach by threads, m any burrow in the sedim ents, an d others are surface dwellers, even feeding on live prey. A nu m b er o f species are extrem ely ab u n d a n t in the vicinity o f hydrotherm al vent an d cold seep environm ents; these anim als have chem oautotrophic bacterial sym bionts w hich provide their nutrition. Sim ilar sym bionts are also em ployed by shallow -w ater specics in sulphide- or m ethane-rich environ­ ments. C iliary filter-feeding is a less successful strategy in the deep sea and the abyssal species o f lam ellibranch have greatly redu ced gill sorting areas an d may depend on bacterial ‘gardens’ an d extracellular symbionts. T h ey also have a very long gut w hich m axim izes their absorption efficiency. O n e group o f species have bccom e very successful predators, sucking small prey into the m antle cavity or trap p in g it on sticky tentacles. A few deep-sea spccies (closely related to the shallow'-water shipworm ) are specialized w ood borers an d som e live com m ensally w ith other invertebrates. T h e second, m ore prim itive, subgroup o f bivalves, the protobranchs, are very successful deep-sea anim als. T h ey have only a small gill, lim ited ciliary sorting areas, an d long guts. T h ey are deposit feeders an d use the labial palps to collect an d sort the food. Som e have siphon-like feeding systems analogous to those o f shallow er lam cllibranchs. At one sam pling site at 2900 m in the eastern N o rth A tlantic bivalves m ade up 10% o f the m acrofaunal biom ass an d 80% o f them were protobranchs. T h e C e p h a lo p o d a (nautiloids, squids, cuttlefish, an d octopods) include the m ost m obile m arine invertebrates as well as the largest (to 20 m), though n ot the longest. In these anim als the m olluscan foot has developed into the arm s, te n ta­ cles, a n d funnel. In the pelagic squids the m antle cavity an d funnel provide a je t propulsion m echanism , aided to a variable degree by m uscular sw im m ing with the fins. Prey is caught w ith the arm s, to rn up by the h o rn y beak an d then m ac­ erated w ith the radula. Nautilus has a m ulticham bered external shell an d cuttlefish have an internal one. In m ost squids the shell is reduced to a chitinous ‘p e n ’ an d it is absent in octopods. Nautilus has 90 or so arm s; octopods, squid, an d cuttlefish have eight arm s an d the last two groups also have two tentacles. T h e active, pelagic squids arc torpedo-shaped with two large gills in the m antle cavity. Less active deep-sea species have a reduced m antle cavity an d m usculature, sm aller gills, an d the body form is very' varied. T h e eyes, b rain , a n d blood sy'stems o f m ost cephalopods are highly developed. C ephalopods arc the only anim als to have chrom atophores operated by muscles, thus acquiring the capability o f nearinstantaneous colour change. T hese anim als m ay be extrem ely ab u n d a n t an d they occur at all depths in the ocean. M any o f the abyssal octopods have arm s w hich are linked by extensive webbing. T h ey have becom e secondarily pelagic,

THE BIOLOGY OF THE DEEP OCEAN

drifting above the bo tto m an d using the arm s an d w eb to swim like a m edusa. All cephalopods are active predators, feeding particularly on fish, shrim p, an d other cephalopods. D espite their often large size, cephalopods do n o t live long and reproduce only once, at the end o f their lives.

Annelida (earthworms, bristleworms, leeches) A nnelids are segm ented coelom ate w orm s w ith chitinous bristles o r chaetae an d m any have a free-sw im m ing ciliated trochophore larva. T h e coelom ic fluid acts as a hydraulic skeleton against w hich the muscles work. T h ere are ab o u t 9000 species in three m ain groups, the m ainly terrestrial O lig o ch a e ta (earthworms), the largely m arine P o ly ch a e ta (bristleworms, 8000 specics), an d the H iru d in e a (leeches), o f w hich there are a few m arine specics. M ore th an 25 species of oligochaete are know n from depths o f m ore th an 1000 m and, like th eir terres­ trial relatives, they are deposit feeders. Polychaetes, w ith a size range o f less th an 1 m m to 3 m, also live prim arily in or on the bottom . Betw een 50 an d 60 species are perm an en tly pelagic, including som e in the deep sea; all are fiercely carnivo­ rous an d swim w ith elaborate paddle-like appendages (parapodia) th a t b ear the chaetae on each segm ent. M any o f those living on the b o tto m have a sim ilar appearance. R eproduction often involves m ating sw arm s, som etim es w ith a lu n ar periodicity, an d the adults m ay either undergo a com plex change o f form at the tim e or fragm ent into free-sw im m ing gonad-filled segments. M any epibenthic polychaetes are scavengers an d they arc im p o rtan t m em bers o f the deep-sea m acrofauna (see Table 11.2). D eep-sea polychactes ten d to be sm aller th an their shallow er relatives. M ost o f them are burrow ing deposit feeders. T h e ir body form is very varied a n d closely reflects their different lifestyles. Very small (< 1 mm), often ciliated, species are an im p o rtan t p a rt o f the interstitial m eiofauna at all depths. Like their shallower relatives, m any deep-sea polychaetes live in tubes m ade o f chitin o r constructed out o f sedim ent particles an d secretions. Tube dwellers often have elaborate tentacles to sweep the sedim ent surface (like echiuran w orm s (see below) b u t on a sm aller spatial scale) while burrow ers ingest the sedim ent, like the sublittoral lugw orm s. T h e ir subsurface activities, an d ab u n ­ dance, greatly m odify the sedim ent structure an d chemistry, adding to the h et­ erogeneity o f the deep-sea benthic environm ent. M any specics o f scale-w'orm live com m ensally in or on other anim als (including abyssal sea-cucum bers an d h ydrotherm al vent mussels) an d a few polychaetes are specialist parasites of echinoderm s.

Sipunculida (peanut worms) T h ere are ab o u t 300 species o f these unsegm ented w orm s, m ost o f w hich have bushy tentacles ro u n d the m outh. T h e an terio r proboscis is used for burrow ing a n d bears spines o r scales. It can be fully retracted into the trunk. T h e larvae are ciliated trochophores like those o f annelid w orm s b u t the group probably has

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closer affinities to the molluscs. T h e anim als range in length from a few centim e­ tres to nearly 1 m. M ost are deposit feeders, nourished by diatom s an d o th er p ro ­ tists or by detritus. T h ey are present dow n to abyssal depths (in some cases the sam e species are present in bo th abyssal an d shallow water) an d , th ro u g h their burrow ing activities, are im p o rta n t contributors to bio tu rb atio n o f the sediments. T h ey m ay dom inate the macrofauna, in som e areas, occurring, for exam ple, at densities o f up to 355 n r 2 at 1200 m off N ew E ngland.

Echiura (spoon worms) O n ce classified w ithin the A nnelida (they have a p a ir o f ventral chaetae), these w orm s range in length from a few m illim etres to 40 cm an d live in distinctive burrow s in soft sediments. T h ey use their enorm ously extensible proboscis (up to 1.5 m) to collect detrital particles from the surrounding sedim ent. W h en the area surrounding a burrow has been ‘sw ept’ they m ay th en move to a new site. M any o f the peculiar spoke-like p atterns visible on the abyssal sedim ents m ark these swept areas (Fig. 3.3). E chiurans have separate sexes an d trochophore larvae; a few' species have dw arf m ales w'hich live on the females. A group o f three phyla (T ardigrada, A rthropoda, an d O nvchophora) share the two fea­ tures o f pairs o f legs along all or p a rt o f the body an d a pseudocoelom ic body cavity, called a haem ocoel w hen it contains blood. T h e O n y ch o p h o ra (velvet worm s) is the only an im al phylum w ith no living m arine representatives, though a n u m b er o f m arine fossils belong in this phylum .

Tardigrada (water bears) T ardigrades are m inute (0.05—1.2 mm) squat anim als w ith four pairs o f unjointed legs bearin g claws. T h e body cavity form s a hydrostatic skeleton, they lack cilia, and the cuticle is o f protein n o t chitin. T h ey suck p lan t or anim al juices through stylets. T h ey are found in all habitats an d are am azingly resistant, in the lab o ra­ tory surviving desiccation, extrem e pressures, tem peratures o f over 100°C, cold to alm ost absolute zero, an d even X -rays. They' have separate sexes an d there is no larval stage. T h ere are 70 m arine species (out o f —500 in all). T h ey arc com m on m em bers o f the interstitial fauna, present particularly in shallow sandy substrates b u t also in abyssal sediments.

Arthropoda A rthropods are distinguished by having segm ented bodies an d appendages, and an exoskcleton o f chitin. T h ey are by far the m ost a b u n d a n t m em bers o f the anim al kingdom ; over three-quarters o f a m illion species o f insect have already been described. T h ey are grouped into three superclasses (considered by som e to

THE BIOLOGY OF THE DEEP OCEAN

be phyla), the C rustacea (including the parasitic tongue w orm s o r Pentastom a), U n iram ia (millipedes, centipedes, an d insects), an d C helicerata (sea-spiders, horseshoe crabs, scorpions, harvestm en, spiders, an d mites). T h e C r u s ta c e a are the arthropods o f the sea. 97% o f all m arine arth ro p o d species are crustaceans and 85% o f the 52 000 specics o f crustaceans are m arine. M em bers o f this group have cylindrical or leaf-shaped appendages th a t are basi­ cally divided into two branches, usually o f different size an d organization. T h ere are three pairs o f p rim ary m outhparts an d the body has a head, five lim b-bearing segments, and a trunk o f up to 65 segments. T h e h ead an d some tru n k segments are usually fused to form a cephalothorax an d p a rt o r all o f the body m ay be enclosed in the carapace, an outgrow th o f the head. Sexes arc usually separate, eggs are often carried or brooded by the female, an d m any species have a threesegm ented larval stage know n as a nauplius. T h ere are 10 subgroups o f crus­ taceans o f equivalent systematic separation. O f these, the cephalocarids, m ystacocarids, rem ipedes, an d tantulocarids contain few species an d are intersti­ tial, cave-dwelling, o r parasitic crustaceans. T h e bran ch iu ran s or fish-lice are ectoparasites an d the branchiopods (waterfleas an d fairy shrimps) have only a few planktonic m arine species. T h ere are ab o u t 13 000 spccics o f C o p e p o d a , the d o m in an t m em bers o f the m arine plankton at all depths in the occan, occurring at densities o f up to 1 0 ' m 3 an d totalling an estim ated 10is individuals worldwide! C opepods have a variety o f body form , no carapace, an d no com p o u n d eyes. T h ere are benthic, intersti­ tial, parasitic, com m ensal, an d free-sw im m ing species. O n e group o f m idw ater species probably spend m uch o f their tim e brow sing on the surface o f sus­ p en d ed particles such as faccal pellets o r m arine snow. T h e 1800 species of m arine calanoid copepods are the grazers o f the ocean. M ost o f those in the u p p er occan take phvtoplankton, ranging from large diatom s to tiny cyanobac­ teria, while the deep-sea specics are pred ato ry or om nivorous anim als. T h eir faecal pellets provide a m ajor com ponen t o f the biological flux from the ocean surface to the abyssal seafloor, w here it m ay be rew orked by h arpacticoid cope­ pods (> 3 5 0 0 spccics), whose biom ass in the m eiobenthos is second only to that o f the nem atode w orm s. C opepods are interm ediates in the transfer o f p rim ary production through the oceanic ecosystcm; they form the food o f m any other species, especially chaetognaths an d fishes. Som e arc even taken regularly by whales. T h e C ir rip e d ia (barnacles) are very highly m odified sessile crustaceans, m any o f w hich arc parasitic. T h e re are 1000 species, all o f them m arine. T h ey have little segm entation, the head is hugely m odified in adults to provide the m antle a n d shell (and stalk), an d they lack an abdom en. In extrem e parasitic cases they com prise just a fungus-likc mass o f rootlets w ithin the host tissue an d an external sac o f gonads. T h e m ore conventional free-living specics arc p rotected by cal­ careous plates an d use the thoracic legs as food-collecting cirri. T h e nauplius larva is followed by a cypris (ostracod-like) stage w ith a bivalved carapace. T his stage settles from the plankton an d cem ents itself to the substrate by secretions released

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through the antennules. In goose barnacles the pre-o ral region m ay th en enlarge to form a stalk. M ales are reduced or m inute. T h e re are several free-living abyssal species including the ancient genus Neolepas at hyd ro th erm al vents. T h e O s tra c o d a (7000 species, alm ost all m arine) are small (< 0 .1 -3 0 mm) crus­ taceans enclosed w ithin a bivalved carapace. T h e an ten n ae are the m ain swim­ m ing organs an d one group has com pound eyes. T h ere are several h u n d red planktonic species, som e o f w hich are omnivores, others p red ato rs (including bathypelagic ones), b u t m ost species are benthic. T h e latter live in o r on the sed­ im ents at all depths an d are prim arily detritus feeders. K now ledge o f th eir hab itat preferences an d the persistence o f their carapaces in the fossil record have m ade th em very useful for studying the past history o f the oceans an d the associated clim ate changes. T h e largest group o f crustaceans is the M a la c o s tra c a , containing som e 29 000 species showing a great diversity o f body form . T h ey have an eight-segm ented thorax to w hich the h ead is often fused (e.g. crabs an d prawns) an d a six- to seven-segm ented abdom en, w ith appendages on each segm ent. T h e re are a n u m b e r o f small groups o f interstitial o r benthic anim als (e.g. tanaids) an d several groups o f larger an d m uch m ore num erous species. T h e 400 or so species o f m antis shrim ps are prim arily subtidal species w ith th ree-b ran ch ed anten n ae an d subchelate limbs. M any are fearsom e p red ato rs an d there are a few deeper-w ater species. C um aceans are prim arily bottom -dw elling anim als living in the sedim ents, b u t som e o f them venture into the plankton at night. T h ey occur at all depths as do the mvsids (opossum shrim ps, 1000 species), m any o f w hich live close to the bottom . M any mysids are p erm an en tly p lank­ tonic a n d below 1000 m they m ay be a m ajo r co m p o n en t o f the m idw ater biomass. Som e o f these anim als reach 20 cm in length. M arin e isopods are m ainly benthic scavengers; they are im p o rtan t com ponents o f the deep-sea m acrofauna. T h e re are also a n u m b e r o f planktonic an d parasitic species. Isopods are dorsoventrally flattened an d lack a carapace. T h e am phipods simi­ larly lack a carap ace b u t are laterally flattened. O n e group o f ab o u t 250 species is planktonic an d m any o f these species associate w ith th e gelatinous plankton (e.g. salps, m edusae, siphonophores) as com m ensals or parasites. T h e o th er m ain group o f am phipods (> 6 0 0 0 species) is prim arily b enthic b u t does include several planktonic species. E uphausiid shrim ps are pelagic an d look superficially sim ilar to mysids an d decapod shrimps. T hey differ m ost obviously in th a t their gills are easily visible below the edge o f the carapace. T h e re are only 87 species o f euphausiid b u t they have an enorm ous im pact on the pelagic fauna. Some are prim arily herbivores, others are om nivores o r carnivores. O n e species, the A ntarctic krill E uphausia su p erb a. is probably th e pivotal species in the A ntarctic ecosystem, w ith a global biom ass m easurable in hund red s o f millions o f tonnes. Euphausiids occur at all latitudes an d at all d epths an d provide food n ot only for the baleen whales b u t also for m any o th e r predators, especially fish an d squid. T h e decapods include not only shrim ps an d praw ns (2500 species) b u t also crabs an d lobsters (> 6 5 0 0 species). M any species, b o th pelagic an d benthic, are the target o f shallow -w ater com m ercial fisheries. D ecapods are

THE BIOLOG Y OF THE DEEP OCEAN

present dow n to 6000 m (but n o t deeper) an d are one o f the m ain com ponents o f the pelagic biom ass, particularly in the m id-occanic deep-w ater regions. M ost o f them arc prim arily carnivores or om nivores b ut m any are deposit feeders or scavengers, easily attracted to baited traps. As their nam e suggests, the second m ajo r subdivision o f the arthropods, the U n ira m ia (m ainly insects), do n o t have biram ous appendages. T h e re are no wholly m arine representatives o th e r th an species o f the w aterstrider Halobates, w hich are w idespread on the surface o f the tropical an d subtropical oceans. In the th ird arth ro p o d subdivision, the C h e lic e ra ta (horschoe crabs, seaspiders, an d arachnids), the body is divided into two sections. M ost species have six pairs o f limbs, the first o f w hich (the chelicerae) are grasping, the second usually feeler-like o r claw-like, an d the rem aining four pairs are walking legs. O f the three groups o f chclicerates two are wholly m arine. O ne, the shallow horse­ shoe crabs, has only four species, an d the other, the pvcnogonids or sea spiders, ab o u t 1000 species. Sea spiders have a variable n u m b er o f p aired appendages an d their relation to other chclicerates is disputed. T h ey suck the tissues o f sessile cnidarians, sponges, an d bryozoans an d there are several deep-sea species, one o f w'hich m ay reach 75 cm in leg span. T h e rem aining chelicerates (98%) are included in the A rach n id a. am ong w hich are several h u n d red species o f m arine mite. M ost o f these are m em bers o f the shallow m eiofauna b ut the dis­ tribution o f others extends into abyssal depths. T h ey are often found on larger anim als, such as crustaceans, gastropods, a n d even jellyfish. T h e rem aining five phyla are know n as deuterostom es because they share a p articu lar p a tte rn o f cell division in the early em bryo.

Pogonophora (beard worms) T hese w orm s (considered by some experts to be m ost closely related to the poly­ chaetes) are segm ented, 5 cm to 3 m in length, an d live in tubes o f chitin or protein. A lthough know n since 1900, only recently have they been extensively studied, largely because o f their abundance at some h ydrotherm al vents an d cold seeps. A dults have no gut o r m outh an d rely on sym biotic chem osynthetic b actc­ ria. T h e b actcria are housed in an extensive ‘tro p h o so m c’ tissue an d m etabolize reduced sulphur com pounds a n d /o r m ethane. T h e re is a cephalic lobe w ith a crow n o f respiratory tentacles, a short glandular region, an d an elongate trunk ending w ith an attachm ent or burrow ing ‘holdfast’, often w ith chaetae. T h ere are two sub-groups, the Perviata an d V cstim entifera. T h e latter lack chaetae an d are som etim es regarded as a separate phylum . T h e 15 or so species in this group are generally m uch larger an d are associated w ith the hydro th erm al an d seep envi­ ronm ents, particularly in the Pacific O cean. T h ey m ay accum ulate in spectacular beds, an d this, com bined w ith their bright red tentacles, so en tran ced the first sci­ entists to visit the hydrotherm al vents in subm ersibles th a t they n am ed one area the ‘Rose G ard en ’.

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Chaetognatha (arrow worms) T hese enigm atic little anim als (up to 120 mm) have characteristic hooked jaw s on the head for grasping an d swallowing prey a n d are rath e r flattened an d elongate, w ith two pairs o f lateral fins an d a tail. T h ey have a rap id dartin g m ovem ent, achieved by dorsoventral flexing o f the tail. A rrow w orm s are very im p o rtan t planktonic predators; they feed on copepods, fish larvae, m edusae, an d sim ilar prey an d are themselves im p o rtan t com ponents o f the diet o f larger predators, especially fish. T h e ir developm ent suggests affinities w ith the pogonophores, echinoderm s, hem ichordates, an d chordates. All the 100 or so species are m arine an d they are found in all oceans, from the surface to bathypelagic depths.

Hemichordata (acorn worms and pterobranchs) H em ichordates are unsegm ented w orm s, divided into two groups. T h e acorn w orm s includes som e 90 species o f solitary anim als w hich live in U -shaped burrow s and range in length from 25 m m to 0.25 m. T h ey have a proboscis, a collar, an d a trunk, an d num erous pharyngeal gill slits. T h ey are know n mostly from coastal habitats b u t there are also som e deep-sea forms, an d they m ay be ab u n d a n t ro u n d som e hydrotherm al vents. T h e o th er group (pterobranchs) are small (< 1 0 mm), often colonial, tube-dw elling anim als bearing a lophophore-like crow n o f tentacles. T h e re are only ab o u t 10 species. T h ey have a U -shaped gut an d few or n o gill slits an d are found from subtidal to abyssal depths. A corn w orm s have a planktonic, ciliated ‘to rn a ria ’ larva. Both groups have separate sexes b u t the p terobranchs can also reproduce by asexual budding. Both groups use cilia to collect their food.

Echinodermata T h e adults o f these benthic anim als all share a basic five-rayed, usually radial, symmetry. B eneath the skin they have a system o f calcareous plates, w hich often support tubercles or spines. T h e tube feet an d the feeding appendages are hydraulically operated through a unique w ater vascular system w hich opens indi­ rectly to the sea. T h e re is no head, brain, o r body segm entation. E chinoderm s probably h a d a filter-feeding sessile ancestry from w hich m ost o f the existing groups have becom e secondarily free-living. A lm ost 7000 species are know n, all of them m arine. T h ey are grouped into six classes, the C rin o id ea (sea-lilies an d feather-stars), the A steroidea (starfish), the O p h iu ro id ea (brittle-stars an d basket stars), the E chinoidea (sea urchins an d sand dollars), the H o lo th u ro id ea (sea cucum bers), an d the recently discovered Concentricycloidea, All six classes have abyssal species. A further 18 classes are know n from fossils. C rin o id s (625 species) retain the ancestral body posture (with an upw ard m outh). Sea-lilies are sessile deep-sea anim als, often attach ed by a long non-

THE BIOLOG Y OF THE DEEP OCEAN

contractile stalk. Feather stars are m ainly shallow -w ater anim als, they do n ot have a stalk a n d attach only temporarily. Both groups are filter feeders. A stero id s (1500 species) have a flattened body w ith usually 5 b u t up to 40 arm s a n d some o f the spines are m odified as pincer-like pedicellariae. T h ey include deposit a n d suspension feeders as well as scavengers a n d predators. In the ophiu ro id s (2000 species) the central body is a small disc an d the arm s are very long a n d flexible, w ith m uch o f their volum e occupied by the fused skeletal ossicles th a t form articulating vertebra-like structures. T h e re are predators, scavengers, deposit an d suspension feeders. E ch in o id s (950 species) are prim arily globular anim als w ithout arm s. T h e ossicles form a rigid shell w ith m oveable spines an d pedicellariae an d the m o u th has a grazing apparatus o f calcareous plates know n as A ristotle’s lantern. B urrow ing species (heart urchins an d sand dollars) have becom e flatter an d bilaterally sym m etrical. Som e shallow -w ater sea urchins graze on algae o r seagrass (or on sessile animals) b u t m any are deposit feeders, as are all those in the deep sea. H o lo th u ro id s (1150 species) exhibit a second­ ary bilateral sym m etry an d are echinoderm s th a t lack arm s an d have a leathery body w all in w hich the skeleton is reduced to m icroscopic ossicles. Tentacles ro u n d the m o u th are used for suspension or deposit feeding. Som e species are sedentary an d use the tube feet for attachm ent; in others, particularly deep-sea species, the tube feet have becom e greatly elongated a n d the anim al appears to be walking on stilts. H olothuroids are d o m in an t anim als on the deep-sea floor, especially in the deep trenches, an d som etim es occur in large groups or ‘h erd s’ (Fig. 3.5). M any o f the deep-sea species can swim an d one o r two have becom e secondarily planktonic, their elongated oral tentacles a n d web m aking th em look very like m edusae (some ophiuroids an d feather stars can also swim for short periods). T h e co n ce n tricy clo id s (two small species) w ere discovered in 1986 from deep w ater first off N ew Z ealand an d later the B aham as; they have a flat disc w ithout arm s w hich is su rrounded by a circlet o f spines. E chinoderm s reproduce sexually, or asexually by fission; m ost o f th em have planktonic larvae b u t some brood the em bryos w ith direct developm ent. T hey play a very im p o rtan t role in the deep-sea benthos; th eir activities in rew orking the abyssal sedim ents probably enhance the small-scale patchiness in the deep-sea environm ent.

Chordata T h e chordates include a range o f anim al form s u n ited by th e fact th a t at some stage d uring their developm ent all o f them have a single dorsal nerve cord, a cartilaginous rod (the notochord) dorsal to the gut, an d phary n g eal gill clefts. T h ere are four very different subphyla, th e U ro c h o rd a ta (tu n ica te s, s e a s q u irts , salp s) an d the C e p h a lo ch o rd a ta (lan celets), b o th o f w hich lack a b rain , a n d the two ‘v erteb rate’ subphyla, the A g n ath a (lam p rey s and hagfish) an d the G n a th o s to m a ta (fish, a m p h ib ia n s, re p tile s, b ird s, and m a m m a ls ).

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THE MARINE PHYLA

291

T h e body o f u ro c h o rd a te s is enclosed in a secreted test o r house an d has no segm entation a n d a m uch-reduced coelom ic body cavity. T h e gut is U -shaped an d m ost species are herm aphrodites. A dults are sessile o r free-living, solitary or colonial, ciliary filter feeders w ith a free-sw im m ing ‘tadpole-like’ larva. T h e re are some 2000 species. T h e 1850 ascidians (sea-squirts) are sedentary; asexual budding is com m on a n d the individuals m ay rem ain associated as colonies, though there is no polym orphism o f the zooids. Ascidians occur at all depths and filter-feed using a ciliary b ranchial basket. A few deep-sea form s have becom e sec­ ondarily predatory. T h e 70 or so thaliaceans are pelagic an d occur at all depths. O n e group (the pyrosomes) form cylindrical colonies up to several m etres in length an d open only at one end. T h e individual zooids are aligned across the cylinder walls pum p in g w ater into the central cavity, from w here it escapes thro u g h the single orifice. T h e oth er two groups (salps an d doliolids) are p rim a ­ rily solitary an d have alternating sexual an d asexual generations. In salps the asexual ‘solitary’ generation produces a long stolon o f sexual individuals that break aw ay in groups to form chains o f sexual ‘aggregates’. Curiously, the two generations have different kinds o f eyes. In doliolids the solitary generation is sexual an d the aggregate generation multiplies asexually by budding. Both salps an d doliolids are im p o rtan t planktonic groups, able in good conditions to m ulti­ ply very rapidly an d produce huge sw arm s, w ith a corresponding im pact on the p hytoplankton on w hich they feed. T h e ir faecal pellets provide a m ajo r flux of m aterial from the surface to the deep-sea floor. T h e 65 species o f planktonic larvaceans (appendicularians) are generally small (up to 40 m m total length) an d retain the larval tadpole-like body form w ith a short tru n k an d long tail. M ost are u pper-w ater species b u t they extend to depths o f at least 2000 m. G lands on the trunk secrete a relatively huge gelatinous ‘house’ (reaching > 1 m d iam eter in giant deep-sea species) w ith filtering screens o f extrem ely fine m esh (100-200 nm) through w hich the anim al pum ps water, feeding prim arily on the picoplankton retained on the screens. It periodically abandons th e house an d secretes a new one in a m a tte r o f m inutes. L arvaceans reproduce sexually an d are im p o rta n t plank­ tonic anim als, harvesting the picoplankton an d providing food for m any small p redators, w hile at all depths their ab an d o n ed houses are im p o rta n t com ponents o f m arine snow. C e p h a lo ch o rd a te s have laterally com pressed fish-like bodies, are up to 10 cm long a n d are sedentary benthic ciliary feeders w hich swim briefly to change loca­ tion. T h e re are only 25 species, none deep-sea, b u t they can be very a b u n d a n t in coastal waters. T h e ‘cran iate’ chordates have a brain an d skull. M em bers o f the subphylum A g n ath a have no jaw s o r paired limbs; the only living representatives are the hagfishes an d lampreys. H agfishes are ab u n d a n t seafloor scavengers to 2000 m in tem perate areas an d arc easily attracted to a bait, w here they m ay accum ulate in very large num bers (Fig. 7.2). All the o th e r seafloor (benthic, dem ersal, o r benthopelagic) an d pelagic fishes are included in the G n a th o s to m a ta . T h e re are some 11 500 spccies o f m arine fish

THE BIOLOGY OF THE DEEP OCEAN

an d 2900 o f these are deep-sea, roughly equally divided betw een seafloor and pelagic species (C ohen 1970; N elson 1994). T h ey are fu rth er divided into the car­ tilaginous fishes (sharks, skates, a n d rays) an d the bony fishes. T h e pelagic m id ­ w ater species im pinge on the seafloor populations, particularly on the slope. A lthough there is no absolute distinction betw een the two faunas, they are never­ theless ecologically distinguishable. C artilaginous species m ake up some 12% o f the dem ersal fishes in the N o rth A tlantic (M errett an d H aed rich 1997) an d are typified by the black squaloid sharks, the largest o f w hich (the G reenlan d shark) reaches 7 m. T h ey are absent from abyssal regions. T h e m acrourids o r rattails are the m ost diverse o f the bony dem ersal fishes, w ith 250 o r so species, 95% o f w hich occur in the u p p er 2000 m. In com m on w ith m any oth er dem ersal fishes (e.g. brotulids, halosaurs, eels, an d notacanths o r ‘spiny-eels’) rattails have an elongate form w ith long dorsal an d ventral fins m eeting at a tapering tail. T h e m o u th is often ventrally placed an d protrusible for taking benthic food o r rooting in the sediments. A few' specialists such as the tripod fishes an d batfishes sit on the b o tto m w aiting for prey. T h e deep-sea cods (morids) an d slickheads (alepocephalids) are also typical m em bers o f this fauna, w hich shows a tendency for the size o f individuals to increase with depth. Four species o f fishes are know n to be present at the bottom o f the deepest trenches; they do not include the anim al rep o rted by Jacq u es Piccard an d D on W alsh (C hapter 8), w ho reached the botto m at the deepest sounding (~ 11 000 m) only to find an ap p a ren t flatfish illum inated in the lights o f their bathyscaphe. N either observer w'as a biologist an d it has subsequently been suggested th a t it m ay not have been a fish at all b u t a hoiothurian. T h e coelacanth (Latimeria) is a relatively shallow (about 2 0 0 -5 0 0 m) species whose evolutionary' antiquity an d unexpected discovery in east A frican (and very recently Indonesian) w aters excited w orldwide interest. It has some o f the visual attributes o f a deep-sea species (e.g. tapetu m in the eye an d blue-sensitive visual pigm ent) an d is ovoviviparous, w ith a few huge eggs. T h e m idw ater (pelagic) fishes com prise a very different fauna, an d have a differ­ ent lifestyle. T h e M yctophidae (lanternfishes) an d the stom iatoids (hatchetfishes, bristlem ouths, an d black dragonflshes) dom inate the m esopelagic fishes a n d are generally m uch sm aller th an the dem ersal fishes. T h ere are m ore th a n 300 species o f lanternfish, m ost o f w hich occur in the u p p er 1000 m, though a few are bathy­ pelagic. T h ey are small, rath e r sardine-like, m uscular fishes, b u t have in addition row's o f light organs in species-specific p attern s along th eir sides an d bellies. T hey feed m ainly on small planktonic anim als such as fish larvae, copepods, ostracods, euphausiid shrim p, a n d arrow w orm s. T h ey share the m esopelagic h ab itat with the silvery an d laterally-flattened hatchetfishes an d the tran sp aren t or dusky' bristlem ouths. A lm ost all these fishes are small, becom ing adult at 2 5 -7 0 m m , an d m any o f them have anatom ical features m ore characteristic o f larvae an d ju v e­ niles. T h e little bristlem ouths (species o f Cydothone) arc ubiquitous th ro u g h o u t the w orld’s occans an d are som etim es regarded as the w'orld’s m ost ab u n d a n t verte­ brates. T h e ir diet is sim ilar to that o f lanternfishes, i.e. prim arily zooplankton,

APPENDIX

THE MARINE PHYLA

293

p articularly copcpods. O th e r sm all-m outhed silvery fishes include bizarre squat form s w ith tubular eyes such as Opisthoproctus a n d Winteria (C hapter 8). T h e silvery b arracudinas a n d their relatives are m ore conventional m edium -sized m idw atcr p redators w ith large teeth. T h e fearsom ely-fanged scabbardfish, snake mackerel, an d oilfish are even larger. T h e colouration an d appearan ce o f these m idw ater fishes are very m uch related to the depths at w hich they live (C hapter 9). T h e deep-bodied fangtooth Anoplogaster is pale as a m esopelagic juvenile but black as a bathypelagic adult. M idw ater snipe-eels are brow n o r silvery. A few o f the shallow er viperfishes an d dragonflshes are also silvery o r bronze an d they, like the jet-black dragonflshes a little deeper, are elongate fishes w ith large teeth an d jaws. T h e dorsal an d ventral fins arc positioned at the end o f the body, close to the tail fin, an d they swim by sculling w ith ju st this region, keeping the rest o f the body rigid. All have a variety o f light organs, w ith an enlarged one ju st below or b eh in d the eye, an d m any have a very elaborate barbel suspended from the low er jaw. D espite the overall simi­ larity o f their appearances, different species o f these fishes specialize on different prey. Som e concentrate on lanternfishes, others on copepods an d small crus­ taceans, still others on sergestid shrim ps or on squid. T h ey are key predators in the m idw ater environm ent, w ith a very substantial im pact on the o th e r fauna. In the bathypelagic realm the anglerfishes hold sway w ith a great variety o f spccies, the great m ajority o f them no m ore th an fist-sized. A lm ost all the females arc velvet-black in colour an d globular in shape, w ith an elaborate lum inous lure, an d som etim es a barbel too. M ales are m uch sm aller an d have no lure; some attach p erm an en tly to the females. Female anglerfishes are sim ply living baited traps. W hale fishes have a w ide gape an d are an o th er group o f bathypelagic fishes w ith small eyes, though m uch ra re r th an anglerfishes. T h e anglerfishes an d bristlem ouths at these depths are dark brow n o r black b ut unusually som e whalefish are orange or scarlet. A m ong the oddest o f deep-sea fish are the gulpcr eels, som e o f w hich have enorm ous bag-like m ouths. T h ey eat a variety o f prey includ­ ing shrim ps an d squid. T h e dark m elam phaeids have heavily arm o u red heads an d large m ouths but only small teeth, an d they have large gelatinous scales w hich are easily shed. Little is know n about the detailed habits o f m any o f these deep bathypclagic species, least o f all how they m anage to find one an o th er in the dark em ptiness o f the deep oceans. O th e r m arine vertebrates are air breathers an d largely restricted to the u p p er few' h u n d red metres. M arine reptiles w ere ab u n d a n t in the M esozoic era (exemplified by plesiosaurs, ichthyosaurs an d mosasaurs) b u t living species are restricted to some 61 Indopacific species o f sea snake (5 sea kraits an d 56 tru e seasnakes), 2 iguanas an d 8 turtles. T ru e seasnakes have laterally flattened tails an d are viviparous, w ith the young released directly into the sea. Iguanas are lan d based a n d b o th turtles an d sea kraits com e ashore to breed. Turtles prey especially on gelatinous anim als an d m ost species undertake ocean-w ide m igrations (C hapter 6). T h e leatherback turtle is the largest, reaching 1.9m an d 900kg, an d lacks the h ard shell plates present in the oth er specics. Olive R idley turtles are probably the m ost abu n d an t.

THE BIOLOGY OF THE DEEP OCEAN

All oceanic birds breed ashore b u t m any spend m uch o f their life at sea. T h e 17 species o f p enguin are flightless b u t use their wings to “fly” underw ater. T h ey m ay forage hundreds o f km from the ice edge an d the E m p ero r penguin, at ~ lm the largest species can dive to depths o f up to 500m . Auks such at the m urres can also swim underw ater, while albatrosses, petrels, prions an d shearw aters, in particular, forage at the surface on oceanic prey. M arin e m am m als include the o rd er Sirenia (seacows) w ith four species o f m anatee an d dugong, large herbivores th a t live in shallow, w arm w ater habitats w here they give birth. In the order C arnivora, the large su border Fissipedia includes 2 species o f sea o tter a n d the polar bear. T h e suborder P innipedia com ­ prises 19 species o f seal, 14 o f sealion (“eared seals”) an d the walrus. All have fore a n d hindlim bs m odified as flippers an d they m ay feed on clams, squid, shrim p or fish, an d even penguins in the case o f the leo p ard seal. L arger species (the S outhern E lep h an t seal reaches 3-4 tonnes) m ay dive to 1000m o r m ore b u t all com e ashore to breed. T h e order C etacea contains the whales, dolphins an d p o r­ poises, all o f w hich breed in the op en sea a n d extend th ro u g h o u t the world oceans. T h e ir forelimbs are m odified as flippers an d they lack hindlim bs. Baleen whales (Mysticeta) lack teeth a n d filter small prey (including copepods, krill an d small fish) through the ho rn y baleen plates w hich take the place o f teeth. T h e 11 species range from the small pygmy right w hale to the huge blue w hale, the largest anim al th a t has ever lived, up to 33m in length an d w eighing over 100 tonnes. Female baleen whales are generally larger th a n the males an d the species u n d er­ take im m ense seasonal m igrations. T h e 67 species o f too th ed whales an d dol­ phins (O dontoceta) feed on larger prey, usually fish o r squid an d m ales are usually larger th a n females. K iller whales (m axim um length alm ost 10m) are fearsom e predators, hunting in packs a n d taking fish, seals, sealions an d even small whales. T h e sperm w hale at 25m is by far the largest o f the to o th ed whales. It can dive to at least 1500m an d som e o f the beaked whales are probably capable o f sim ilar feats. Sea otters an d po lar bears rely largely on h air for insulation b u t cetaceans an d pinnipeds have lost m ost o f their hair a n d are insulated by thick layers o f fat or blubber.

Index

Abralia, 208 Abraliopsis, 209 ab so rp tio n levels different feeding types, 42 a b u n d an c e, 24, 199 at h y d ro th erm al vents, 249 bacteria, 16, 46 b en th ic anim als, 62 biolum inescent species, 198 calculation from nets, 22 cycles, 249 estim ates from im ages, 53 increase o f g ra ze r in a food p a tc h , 85 sex d e te rm in a tio n , 234 Synechococcus, 35 zooplankton, 37 abyssal plains, 2, 50, 52, 54, 57, 62, 246 sedim entation rates, 61 abyssal sam pling, 20, 70. See also benthos: sam pling abyssal species distributions, 56 abyssal zone, 50 Acanthephyra, 184, 224 A c an th o cep h ala, 241, 280 Acartia, 94, 154 feeding, 84, 85 Acetes, 152, 153, 155 acoustic backscatter, 13, 14, 83 vertical variability, 86 acoustic im pedance, 13, 14, 125 acoustic lenses, 109 acoustic pressure wave, 134, 135, 137. See also far field o f vibrations acoustic size discrim ination by odontocetes, 144 acoustic system in fishes, 126-138 acoustic tags for fishes, 151 acoustic techniques, 12-15, 22, 87 acoustico-lateralis system , 126, 127

active tra n sp o rt o f fauna, 80, 8 1 -8 3 , 87, 96 advection. See active tran sp o rt o f fauna Aequorea, 108, 199 aesthetascs, 149, 150, 151, 155, 156 Agalma, 191, 205 aggregations sw arm s a n d schools, 86, 87, 139, 159 See also holothurians: herds; schooling Aglantha, 138 A gnatha, 290, 291 Ahliesaurus, 173 Alabaminella, 237 Aldrovandia, 128 A lepisauridae, 233 alepocephalid fishes, 59, 228, 235 algal m etabolites, 154, 159, 237 A lpheidae, 142 Alvinella, 66 am m o n ia as a n itrogen source, 35, 39 co rrelated w ith chlorophyll, 85 am m o n iu m ion. See buoyancy am phibians, 126, 131 am phipods, 56, 70, 150, 287 eyes, 180 Amphitretus, 177 am p u llary organs, 145 anem ones, 55, 57 anglerfishes, 3, 133. See also sexual d im orphism bacterial specificity, 201 chem oreception, 157, 158 feeding, 100, 101 free neurom asts, 128, 130, 132 lures, 212 a n g u lar distribution o f light, 192 a nim al colours, 196, 208. See also cam ouflage

THE BIOLOG Y OF THE DEEP OCEAN

296

anim al phyla, 197, 239, 274, 276 h a b ita t distribution, 241 a nnelid w orm s, 64, 241, 243, 284 Anoplogaster, 99, 129, 293 A ntarctic. See S o u th e rn O c ca n A nthozoa, 277 Aphanopus, 23 Apolemia, 230 appendicularian. See larvaceans apposition eyes, 178 -182 184, 186, 187 A ra b ian Sea upwelling, 37 A rchaea, 239 arch aeal num bers, 36 Architeuthis, 24, 177, 230 A rctic a n d A ntarctic surface cooling, 11 A rctic O c ca n , 38, 40 co p ep o d herbivores, 46 Argyropelecus, 158, 173 Aristostomias, 173, 211 a rth ro p o d eyes c o m p o u n d eyes, 178-186 sim ple eyes, 178 arthropods, 64, 241, 243, 285- 288 ascidians, 55, 56 asexual re p roduction, 222, 224, 281, 289, 290, 291 assim ilation efficiency, 283 a m bush a n d stealth predators, 102 in different trophic regions, 103 asteroids, 289, 290 Astronesthes, 205 Astroscopus, 146 A tlantic O c ea n a b u n d an c e o f biolum inescent specics, 198 biodiversity'; 246 Calanus, 89 c arb o n a te chim neys, 64 c arb o n a te solubility, 62 circulation, 72, 80, 81 co n trastin g abyssal sites, 60 Cyclothone, 226 deep water, 8 fish reproductive traits, 227 fish size a n d d e p th , 231 m acrourids, 62 M e d ite rra n e a n input, 8 m id w ater traw ls, 20 m ixing d ep th , 32

o stracod diversity, 250 pelagic biodiversity'. 252 prim ary' p ro d u ctio n , 36 scattering layers, 15 subtropical carb o n flux, 38 vent fauna, 68 vertical biom ass, 88 Atolla, 205 a u d ito ry systems o f fishes, 132 A U V s (autonom ous u n d e n v a te r vehicles), 12

b acteria, 15, 27, 35, 37, 202, 237, 239. See also chem osynthetic b acteria aggregates at new' vents, 66 barophilic, 62, 70 biolum inescence, 199-201, 206, 209, 212

culture m ethods, 16 m icrobial loop, 4 3 -4 5 num bers, 36 b acterial m ortality, 45 b acterial sym bionts. See chem osy'nthetic sym bionts: lum inous sym bionts Baiacalifornia, 171, 172, 177 b a ite d cam eras, 149 baleen whales, 99, 14-3, 294 Barathrodemus, 136 Bargmannia, 22 barnacles, 55, 111, 286 basin size a n d circulation, 80 Bathochordeus, 99, 230 Bathothauma, 111 bathyal zone, 50 Bathybiaster, 236 Bathygobius, 136 Bathylagus, 106 Bathymicrops, 55 bathypelagic fauna, 60, 71, 87, 100 colours, 196 energy adaptations, 122 bathypelagic fishes n eurom ast organs, 128, 129 bathypelagic, zone, 2, 3, 20, 49 light, 163 Bathypterois, 55, 170, 174 B athysauridae, 233 bathyscaphe Trieste, 69, 163, 292 Bathyteuthis, 111 Benthalbella, 209

INDEX

297

Bentheogennema, 184 Benthesicymus, 184 Bentheuphausia, 183, 184 benthic b o u n d a ry layer, 51 benthic crustacean eyes, 185 b enthic environm ent, 50 52 benthic fauna. See b en th ic m ega-, m acroa n d m eiofauna a n d benthos b e n th ic fishes, 55 be n th ic m acrofauna, 53, 55, 56, 58, 61, 243, 244, 245, 246, 275, 284, 285, 287 be n th ic m eg afau n a, 52, 53, 55, 56, 58, 71, 237, 246, 248 biom ass, 56 b enthic m eiofauna, 53, 55, 58, 237, 243, 244, 275, 279, 281, 282, 284, 286, 288 b cnthic p lankton, 52 b enthic rccolonization, 67 b enthic storm s, 85, 249. See also seafloor currents b enthic topography; 50 Benthogone, 61 benthopelagic fauna, 50, 5 9 -6 0 , 62, 71 biolum inescence, 209 benthopelagic fishes, 20, 55, 59, 117, 137, 158, 173, 200, 233 colours, 197 sw im bladders, 114 benthos, 46, 5 1 ,6 1 ,7 1 , 99, 229 aggregations, 87 biodiversity7 6, 24-3, 246, 248, 249, 253 biom ass, 62, 280, 286 chem oreception, 158 colours, 197 definition, 2, 50 h a d al, 69 m etabolism , 62 rep ro d u ctio n , 235 respiration rate a n d d ep th , 119 sam pling, 15, 5 2 -5 5 size divisions, 55 Benthosema, 77 B ering Sea, 86 Beroe, 108, 205 bet-hedging, 221 biliprotein, 189 billfish heaters, 104 biodiversity, 6, 26, 58, 71, 239, 240 254,

262, 274, 280, 283, 287 b enthic, 2 4 3 -2 4 9 coastal a n d deep-sea com parison, 244 d e p th effects, 247, 248, 250 disturbance, 248, 249 latitude, 2 4 6 -7 , 251 pelagic, 249 253 biogeochem istry, 41 biogeography, 1, 7 2 -7 5 , 96, 250. See also faunal provinces biological pum p. See export flux biolum inescence, 21, 100, 133, 161, 163, 169, 170, 173, 175, 186, 195-216, 232, 293 bacteria, 199-200 cam ouflage, 207 chem istry, 198-199 colour, 198, 199, 203, 208, 210, 211 defence, 2 0 3 -2 1 0 , dinoflagellate, 33 functions, 2 0 3 -2 1 6 intensity' changes, 208 interactions w ith prey, 2 1 0 -2 1 3 intraspecific functions, 2 1 3 -2 1 6 rhythm s, 203 biolum inescent flashes, 168, 205 biolum inescent lures, 99, 100, 101, 200, 201, 2 1 2 -2 1 4 biolum inescent secretions, 202, 206, 210 biom ass, 3, 6, 7, 29, 36, 42, 222, 24-9 bathypelagic fishes, 60 b enthic, 28 b enth opelagic fishes, 60 bivalves, 283 con trib u tio n o f n em atodes to m e io ­ fauna, 58 D V M effects, 91 e n h an c em e n t o n m arin e snow7, 46 lan d a n d ocean, 38, 49 lan d plants, 5 m ark e r o f large-scale distributions, 87 m icrobial loop, 43 planktonic a n d pelagic decline w ith d ep th , 87 transfer from p rim a ry to secondary p ro ­ duction, 41 values at h y d ro th erm al vents, 68 vertical distribution, 88, 250 zooplankton, 28 biom es. See faunal provinces

THE BIOLOG Y OF THE DEEP OCEAN

298

biotic provinces. See faunal provinces b io tu rb a tio n , 54, 246, 285 bivalve m olluscs, 65, 66, 67, 70, 283 bloom s. See p h y to p lan k to n bloom blue light environm ent, 189, 193 b ody size, 4, 5, 6, 13, 16, 17, 18, 43, 74, 217, 226, 2 2 7 -2 3 1 , 234, 237, 243, 246 abyssal gigantism , 230 acoustic discrim ination, 14 benefits o f larg er size, 230 diet, 86 fecundity, 223, 227, 229 food size, 99 oligotrophic regions, 45, 229 m o u th size, 101 te m p e ra tu re /d e p th , 230, 231 bony fishes, 117, 128, 2 9 2 -2 9 3 . See also teleost fishes Boreomysis, 183 b o tto m currents, 56 b o tto m traw ls, 59, 69. See also benthos: sam pling b o tto m u p control, 39, 41 b o u n d aries in th e o cean, 2, 7, 10, 26, 73, 75, 76, 95 Boyle’s Law, 111, 113 brachiopods, 55, 241, 243, 281 Branchiostoma, 130 breed in g frequency, 217 Bregmaceros, 77 bresiliid shrim ps, 6 5 -6 7 , 180, 185 brin e seeps, 63, 67 bristlem ouths. See Cydothone British C o lu m b ia coast, 84 brittle-stars. See ophiuroids b ro o d in g o f eggs a n d larvae, 228, 235 brotulids, 59, 136, 137 B ryozoa, 241, 243, 281 buoyancy' 103—117 a m m o n iu m ions, 107 changes in w a ter a n d ionic content, 105-109 eggs, 106 hydrocarbons, 110 m am m als and birds, 110 stressed phytoplankton, 34 sulphate exclusion, 107, 108 sw im bladders in fishes, 112 use o f fat a n d oil, 109-110

using gas, 111-117 buoyancy adaptations, 17, 23, 55, 122, 142, 144, 190, 203, 230, 258, 259. See also n e u tra l buoyancy b uoyant plum e, 64 b u rg lar a la rm hypothesis, 154, 204, 205 burrow s, 52, 53, 54, 55, 61, 71, 180, 246, 284, 285, 289 14C tracers m ea su re m e n t o f p rim a ry p ro duction, 37 Calanoides, 89 Calanus, 42, 85, 86, 89, 93, 155, 156 susceptibility to patchiness, 84 C alifornia C u rre n t upwelling, 37 c am era eyes, 187 in cephalopods, 174 in fishes, 164 transparency, 191 cam ouflage, 93, 169, 177, 188-197, 216 biolum inescence, 2 0 7 -2 1 0 u p p e r ocean, 189-195 deep water, 196-197 visual acuity, 210 can al neurom asts, 128, 131, 132 canyons, 51, 52, 71 c arb o n dioxide, 10, 11, 64, 254 c arb o n fixation, 29, 40, 45 p a rtial pressure, 40 C ariaco T rench, 76 carnivores, 42, 56, 62, 98, 287, 288 caro ten o id pigm ent, 173, 189, 196, 197 cartilaginous fishes, 292. See also elasm o­ branchs; d eep-sea sharks Caulophryne, 130, 212 cell size, 39, 40, 86 Celtic Sea prod u ctio n , 36 Centropages, 84 Cenlroscymnus, 110 C e p h alo ch o rd a ta, 130, 290, 291 Cephalophanes, 1 78 cephalopods eyes, 174gas cham bers, 112, 113, 142 statocysts, 141 reflectors, 193, 194 visual pigm ents, 175 Ceratium, 34 Ceratocorys, 34 Ceratoseopelus, 95

INDEX

299

Cestus, 108 cetaceans, 294 acoustic lenses, 144 m agnetic navigation, 147 m echanism o f sou n d p ro d u ctio n , 144 sound prod u ctio n , 142-145. See also echolocation Chaenophryne, 200 Chaetoceros, 34 chaetognaths, 78, 84, 241, 289 Chauliodus, 100, 106, 213 C helicerata, 286, 288 chem ilum inescence, 198 chem o au to tro p h s, 27, 274, 283 c h em oreception, 48, 94, 148-160 aggregation a n d settlem ent, 159-160 defence, 149, 153-154 feeding, 61, 149-153 p herom ones, 154 -1 5 9 spaw ning, 159, 237 stim ulatory com pounds, 153 toxic com pounds, 154 tracks a n d trails, 156 chem oreceptors, 140, 149-157, 159, 160 chem osynthesis, 2 7 -2 9 chem osynthetic b a cteria, 27, 29, 71, 159, 274, 288 chem osynthetic sym bionts, 6 4 -6 9 , 231, 283 Chiasmodon, 101 chiasm odontids, 100 Chilomycterus, 136 Chionoecetes, 159 Chiroteuthis, 213 C h lo ro p h th a lm id a e, 233 Chlorophthalmus, 55 chlorophyll, 36, 40, 72, 161 deep m axim um , 34 fluorescence, 12, 83, 85, 86 light absorption, 31 chlorophyll-linked luciferins, 202 chordates, 241, 243, 2 9 0 -2 9 5 c h rom atophores, 196, 197, 205, 283 ciliates, 17, 4 3 -4 5 , 48, 274, 275 Ciona, 141 circulation, 5, 6, 10, 26, 249, 254 m atch w ith biological p attern s, 73, 74, 80 relation to oxygen, 76 Cirolana, 176, 180

cirrate octopods, 59, 177, 283 G irripedia. See barnacles Cirroteuthis, 177 Cirrothauma, 17 7 clam s. See bivalve m olluscs classical food chain, 43, 45 clim ate, 40, 41, 80, 154, 249 change, 11, 37, 253, 287 cycles, 249, 250 lan d a n d sea, 5 clupeid fishes, 129 coupling o f e a r a n d sw im bladder, 134, 135, 138, 147 C n id aria , 241, 243, 276 coastal regions, 43 coccolithophores, 11,13, 33, 34, 35 coelenterazine, 198, 199, 202 Coelorhynehus, 128, 129 cold a d ap tatio n , 121 cold seeps, 27, 29, 63, 6 7 -6 8 , 70, 71, 159, 249, 274, 288 Collossendeis, 230 c olour changes w ith d e p th , 196 colours o f anim als, 175, 188, 189, 197, 216 com b-jellies. See ctenophores com pensation d e p th , 30, 31 c o m p o u n d eyes, 178—186 C oncentricycloidea, 290 conductivity. See salinity Conocara, 171 conservation, 254 constructive interference, 192, 193 continental rise, 52 con tin en tal slope, 50, 51, 59, 62, 71, 81, 137, 245 sedim entation rates, 61 continuous sam pling m ethods, 83 contrast discrim ination a n d cam ouflage, 190 convective m ixing, 32 convergences, 73, 75, 76, 84, 89 copepods, 36, 39, 47, 78, 89, 286 aggregations, 139 ch em oreception, 1 3 8 - 139 egg a n d body size a n d d ep th , 231 feeding currents, 138 feeding in different regions, 46 flow field, 152 food selection, 151-152, 154

THE BIOLOGY OF THE DEEP OCEAN

300

copepods (conl.) grow th o n different diets, 42 life histories, 221 m ech an o recep tio n , 138-139 num bers, 36 sensory m odel, 152 sensory sexual dim o rp h ism , 156 sexual pherom ones, 156 trail following, 138 corals, 55 core. See sedim ent cores core zone for species distribution, 78, 79 Coryphaenoid.es, 120, 128 c o u n te rcu rre n t systems, 104, 116, 117 co unterillum ination, 173, 195, 2 0 7 -2 1 0 , 214, 215 countershading, 195 coupling o ccan physics a n d biology, 5, 6, 73, 74,

Cystisoma, 181-183

Daphnia, 94 daylight in the sea, 8, 94, 119, 161-163, 169, 177, 180, 186, 188, 189, 196, 203, 207, 208. See also light; dow n­ w elling daylight spectral distribution, 161 d ecap o d shrim ps, 55, 59, 60, 80, 91, 92, 208, 287 biom ass, 288 eyes, 184-186 respiratory adaptations, 121 statocysts, 141 deep scattering layers, 14, 90 deep-sea biodiversity, 2 4 0 -2 5 3 d eep-sea cods, 59, 137 deep-sea fishes, 4. See also fishes diet, 102 elongate bodies, 133 252 progenesis, 234 crabs, 55, 66 respiratory adaptations, 120 c ranchiid squids, 107, 108, 209 Crangon, 139 retinal cones, 173 crinoids, 55, 84, 289 sex ratios, 232 critical d ep th , 3 0 -3 4 sexual pherom ones, 156 sound p ro duction, 137 crustaceans, 56, 286 visual adaptations, 170 a d ap tatio n s to large m eals, 102 Deepstaiia, 230 buoyancy; 107, 108 dem ersal fishes, 59, 227, 228, 231, 245, eyes, 177-186 lipid levels, 110 292 density sexual pherom ones, 155 organism s, 4, 103, 104 v ib ratio n sensitivities, 139 cryptic species, 70, 216, 253 w atery tissues, 105, 106 Crypiopsaras, 212 density g radients, 8 density' o f air Ctenolabrus, 105 ctenophores, 21, 100, 138, 241, 276, 277 effect o f tem p e ra tu re a n d pressure, 4 density o f gas, 137 Ctenopteryx, 214 C u b o zo a, 277 density o f seawater, 2, 4, 5, 8, 10, 21, 32, cum aceans, 56, 58 33, 35, 37, 51, 67, 87, 104 cupula, 127, 129, 131, 133, 138, 141 density' layers, 155 effects o f pressure, 7 currents, 4, 8, 11, 21, 28, 65, 73, 76, 81, 83, 87, 96, 235, 253. See also circula­ interfaces, 64, 96, 99 deposit feeders, 51, 55, 56, 58, 61, 160, tion 282 -285, 288, 290 Cyanagrea, 66 d e p th o f occurrence c yanobacteria, 35, 36, 39, 45 C ycliophora, 241, 279 fishes, buoyancy a n d m etabolism , 106- 107 Cydothone, 157, 158, 174, 252, 292 rep ro d u ctio n , 225, 226, 233, 234 enzym e activity in fishes, 119 respiration rates, 117-118 Cymbulia, 108 Cynomacrurus, 197 rete length, 11 7

INDEX

301

sam pling, 17, 19 d e p th range o f species by day7a n d night, 90 detritivores, 42, 47, 287 deuterostom es, 288 diapause-like w inter dorm ancy, 89 Diaphus, 77, 214 diatom s, 3 3 -3 7 , 39, 40 fish as grazers, 98 upw elling regions, 36 diel vertical m igration, 15, 19, 78, 9 0 -9 6 , 107, 114, 125, 154, 225, 234, 250. See also D V M diffuse flow a t vents, 64 diffusion processes, 96 chem oreception, 155 dispersion o f patches, 83 n u trie n t uptake, 35 dinoflagellates, 3 3 -3 5 , 154, 2 0 2 -2 0 4 , 274direct developm ent, 219 discontinuities, 75 dispersal o f larvae, 219, 229 at h y d ro th erm al vents, 66, 68, 88 m idw ater, 249 Disseta, 206 dissolved organic c arb o n , 27, 35, 43, 44 diversity. See biodiversity7 diversity index, 240 diving capabilities o f m arin e m am m als, birds a n d reptiles, 25, 110, 144, 294 Dolichopteryx, 167 dolphins, 23, 142. See also cetaceans c o m p a red w ith bats, 144 dow nw elling daylight, 162, 170, 173, 195, 196, 210 biolum inescence m atching, 2 0 8 -2 0 9 spectral quality, 161, 169 drag, 4, 103, 106, 122, 185 in air a n d w'ater, 4 dragonfishes, 99, 210, 292 diet, 102 lures, 213 D V M 9 0 -9 6 causes a n d consequences, 9 1 -9 6 chem ical cues, 94 energetic c o st/b e n efit, 93 escape from visual p re d ato rs, 91 genetically based differences, 94 light control, 94, 95 m ig ratio n rates, 91, 95 Pleuromamma spp, 93

sam pling strategies, 90-91 subm ersible observations, 95 variability a n d d em o g rap h ic value, 93, 94 variations in tim e a n d space, 91 d w a rf m ales, 232, 279, 285 D y'nam ic E quilibrium hypothesis, 247, 248 dynam ic lift in a ir a n d w ater, 4 E ast Pacific Rise, 63, 66, 67, 231 echinoderm s, 55, 64, 241, 243, 2 8 9 -2 9 0 echinoids, 61, 290 ech iu ran w orm s, 54, 56, 70, 241, 243, 285 echolocation, 5, 124, 138, 143- 145 echosounder, 15 ecological efficiency; 38, 42, 49 ecological processes, 40, 49 lan d a n d ocean, 6, 26 ecosystem disturbance, 253 ecotrophic efficiency, 38, 41, 42 E ctoprocta, 281 eddies, 5, 8, 12, 13, 51, 76, 83, 249 vent plum es, 67, 88 eelpouts. See zoarcid fishes egg size, 186, 217, 224, 225, 226, 227, 228, 235 in d e ca p o d shrim p, 224 relation to d ep th , 224, 231 El N ino, 36, 37 elasm obranchs, 130 ears, 133 electroreception, 131, 146 eyes, 174 fecundity', 229 electric organs, 145-146 electroreception, 127, 131, 145-146 Emiliana, 13, 34 endem ism , 76, 249 h ad al fauna, 70 energy m an a g em e n t, 98, 122 m axim izing inp u t, 9 8 -1 0 2 m inim izing energy o u tp u t, 103-105. See also buoyancy7 energy transfer efficiency, 41 E nglish C h a n n el, 81 Engraulis, 85 E n to p ro cta, 241, 280 enzym es pressure sensitivity, 121

THE BIOLOGY OF THE DEEP OCEAN

302

Ephyrina, 224 epipelagic zone, 2, 8 Epistominella, 237 E u b acteria, 197 Euchaeta, 230 D V M , 93 feeding currents, 1 5 1 receptors, 138, 139 size a n d d ep th , 231 Euchaetomera, 183 Eucopia, 184 eukaryotes, 16, 35, 239 Euphausia, 75, 77, 89, 287 euphausiid shrim ps, 75 - 78, 85, 287 euphotic zone, 2, 11, 29, 34, 37, 46, 49, 63 Eurytemora, 93 Eurythenes, 60, 70, 102 d e p th distribution, 60 Eustomias, 213 eutrophic regions, 3 2 -3 4 , 37, 49, 103, 247, 248 ex p o rt flux, 27, 31, 34, 36, 38, 39, 41, 46, 48, 49, 69, 87, 96, 286, 291. See also sinking ex trao cu lar p h o to rec ep to rs in cephalopods, 177 extrap o latio n o f biodiversity, 242, 244, 245 eye size a n d body size, 185 a n d d e p th , 70, 174, 177, 1 8 1-185, 187 eyes, 164-186 acuity a n d sensitivity, 164 cephalopods, 174-177 crustaceans, 177-186 design conflicts, 164 epipelagic fishes, 165 f-num ber, 165, 175, 176, 178, 183, 185 fishes, 164 -1 7 4 h u m an , 176 im age quality, 164, 170 invertebrates, 174-186 m ale anglerfishes, 214 p h o to n flux, 164 retina, 164 182, 185 retinal a d ap tatio n s in deep-sea fishes, 168-174 retinal convergence, 170, 184 rods a n d cones, 165 screening pigm ent, 165

spherical a b erra tio n , 165 transparency, 182, 190, 191 tubular, 166-168 f ratio, 39 faecal pellets, 11, 34, 46, 61, 96, 160, 199, 213, 236, 286, 291. See also export flux far field o f vibrations, 124, 125, 133, 138, 142, 147 faunal provinces, 73, 77, 79, 250, 251 A tlantic, 80 fecundity, 218, 220, 2 2 3 -2 2 8 feeding types relative im portance, 4-6, 47 filter feeders, 36, 46, 141, 282, 289, 290, 291 a t the surface, 98 in deep w ater, 99 p re d ato ry b enthic species, 99 firefly squid, 175 fish larvae, 21, 85, 127, 190, 191, 197 sam pling, 20 fish lateral line, 1 2 5-133, 135, 136, 138, 140, 141, 147, 174, 212, 257, 259 canals, 128, 130 com parison w ith aud ito ry system, 132 m ode o f action, 131 hearing, 137 fish lens, 165 M atthiessen’s ratio, 165 fish p ro duction, 43 fisheries, 12, 13, 22, 23, 59, 98, 254 fishes, 78. See also deep-sea; benthic; b e n ­ thopelagic; dem ersal etc acoustic reflection, 14 as filter feeders, 43, 98 e nlarged teeth a n d jaw s, 99 hearing, 126 heaters, 104 h e art size, 120 olfactory sexual d im orphism , 148, 156-158 sound p ro duction, 136-1 38 vibration receptors, 136 Fissipedia, 294 flagellates, 17, 43, 45, 48, 237 flashlight fishes lum inous behaviour, 206 flatw orm s, 64, 278

INDEX

303

flow field over chem oreceptors, 151 fluxes to the seafloor. See ex p o rt flux flying energy' cost, 4 food webs, 7, 36, 4 1 -4 4 food-chain. See food webs foram iniferans, 11, 53, 57, 58, 78, 237, 275 foveas, 165, 170-173, 177 free neurom asts, 129-132, 151, 212 frequency responses o f h a ir cells, 127 fronts, 5, 76, 83 Fundulus, 129 Fungi, 239 Gadus, 134 g a m m a rid e an am phipods, 180 gas buoyancy, 111-117 gas bubble e n h an c em e n t o f acoustic p res­ sure wave, 125, 134-135 gas gland, 111, 114-116 gas p a rtial pressure, 112-116 gas space, 14, 105, 111, 112, 122, 142 gastropods, 282 gastrotrichs, 241, 279 Gazza, 137 gelatinous anim als, 14, 19, 59, 60, 106-108, 111, 190, 276, 287, 291, 293 gene flow, 67, 96, 219, 250 g eneration tim e, 39, 217, 221, 222, 225, 231 a n d body' size, 227 genetic diversity o f m icrobes, 16 genetic inform ation, 67, 70, 252, 278 Gennadas, 184, 224 g e o th e rm a l processes, 64 g iant squid, 24. See also Architeuthis Gigantactis, 212 Gigantocypris, 178, 230 Glaucus, 111, 154 global c arb o n budgets, 12, 41 global w arm ing, 4 1 ,8 1 .See also clim ate change Glyptonotus, 230 Gnathophausia, 153, 184, 202, 206, 222, 223, 230 G n a th o sto m a ta, 290, 2 9 1 -2 9 4 G nath o sto m u lid a, 241, 279 Gonostoma, 101, 105, 157, 158, 227, 233

buoyancy budget, 114-115 h e rm a p h ro d itism , 2 3 3 -2 3 4 Gonyaulax, 34 gorgonians, 55 gravity' 4, 7, 103 receptors, 133, 141 grazing by zooplankton, 31, 34, 37, 3 9 -4 3 , 46, 47, 49, 8 3 -8 6 , 154, 204, 286 dim ethyl sulphide, 154 on surfaces, 46, 58, 64, 279, 290 patchiness, 84 physiological flexibility o f Neocalanus, 86 secondary' p ro d u ctio n , 4 1 -4 3 tem p erate a n d oligotrophic sites, 41 grow th efficiency, 38, 42, 230 grow th rates, 231 g u an in e crystals, 112, 184, 192, 193 G u lf o f M exico, 68 G u lf S tream , 81, 85 G u lf S tream rings, 81, 82, 83 g ulper eels, 128, 293 gyres. See oceanic gyres h a d al fauna, 6 9 -7 0 , 230 h a d al zone, 2, 50, 6 9 -7 0 H aem ulidae, 136 hagfishes, 55, 60, 133 h a ir cells, 123, 126-128, 131, 133, 134, 136, 138, 141, 145, 147 Flalobates, 288 halosaurs, 59, 128 Flaplophryne, 233 h a rp ac tic o id copepods, 58 hatchetfishes, 292 biolum inescence, 208 diet, 102 olfactory systems, 158 silvering, 192 tu b u la r eyes, 167 h e at capacity o f water, 5 Helicocranchia, 108 hem ichordates, 241, 243, 289 herbivores, 5, 33, 41, 42, 46, 47, 154, 250, 287, 294 particle size, 47 h e rm ap h ro d ites, 157, 158, 160, 225, 2 3 3 -2 3 4 , 280, 282, 291 herring, 93, 114, 135 heteropods, 106, 177, 282

THE BIOLOG Y OF THE DEEP OCEAN

304

Heleroleuthis, 206 heterotrophs, 16, 27, 39, 41, 4 3 -4 5 , 49, 274, 275 phytoplankton, 35 Hierops, 167 Hippopodius, 191 Hirondella, 70 H iru d in ea , 284 Histioteuthis, 107, 108, 177, 208 H N L C regions, 40 H olocephali, 110 holothurians, 55, 61, 289, 290 dom inance a t h a d al depths, 70 herds, 56, 87 sw im m ing, 59 hom eoviscous a d ap tatio n . See pressure: biochem ical effects h o m ing a n d ch em oreception, 158—159 h orizontal distributions, 7 2 -8 6 , 96 hu m p b ac k w hale songs, 143 hydrocarbons buoyancy, 109 vents a n d seeps, 67, 68 hydrodynam ic disturbances, 124, 138, 151, 154 hydrodynam ic lift, 103, 104, 110, 114, 117 hydrodynam ic receptors fishes, 126-136 invertebrates, 138-142 hydrography' 7 Hydrolagus, 145 hydrosphere, 7 h y d ro th erm al vents, 27, 29, 6 3 -6 9 , 71, 88, 159, 180, 185, 231, 249, 274, 281, 283, 284, 287, 288, 289 at hadal depths, 69 chem osynthetic bacteria, 63 fish m etabolism , 120 gene flow, 67, 70 new Pacific vent site, 67 plum es, 64, 67, 88 plum e sam pling, 22 shrim p. See bresiliid shrim p species dispersal, 67 H y'drozoa, ‘1 11 Hygophum, 78, 95 Hymenodora, 185, 224 hyperiid am phipods, 183 eyes a n d d e p th , 180-181 Hyporhamphus lateral line, 132

icefishes, 110, 120 Idiacanlhus, 226 Idotea, 189 im aging techniques, 20, 52, 53. See also sam pling: p h o to g rap h ic a n d video surveys In d ia n O c ca n , 75, 80 oxygen m inim um , 76—78 upwelling, 76, 89 vent fauna, 66 inhibition o f h a ir cells, 127 in n er ear, 133-136, 147 interstitial fauna, 278, 279, 281, 282, 284, 285, 286, 287 Ipnopidac, 233 Ipnops, 55, 174, 185 iridophores, 194 iron, 11, 27, 43 lim iting p ro d u ctio n , 40—41 Isistius, 208, 213 isopods, 56, 58, 287 ey'es, 180 Janthina, 111 Japetella, 215 juvenile characters, 234. juvenile survival, 225 kairom ones, 149 K a m p to z o a, 241, 280 kinorhynchs, 58, 241, 279 Kolga, 56 K olm ogorov scale, 12 krill. See also euphausiid shrim ps biom ass, 13, 287 K uroshio C u rre n t, 81 lactic acid secretion in the sw im bladder, 115 L ag ran g ian drift, 8 Lamellibrachia, 68, 231 lam preys, 133 lanternfishes, 3, 59, 77, 78, 292 biogeographv, 80 breeding p atterns, 227 diet, 101, 102 D V M , 91 schooling, 132 sexual d im orphism , 214 large food-falls, 60

INDEX

305

large food particles p re d a to r adaptations, 99 larvaceans, 16, 36, 46, 47 larvae dispersal at vents, 67 eyes, 186 lecithotrophic, 219, 224, 228 p lan k to tro p h ic,65, 219, 224, 228, 229, 235 settlem ent, 159 lateral line. See fish lateral line Latimeria, 292 Lepas, 111 Leptograpsus, 176 Lestidium, 209 life history, 94, 121, 2 1 7 -2 2 3 , 238 A ntarctic anim als, 230 deep-sea a n d polar, 231 fecundity a n d egg size, 224 -2 2 7 larvae, 219 phylogenetic constraints, 224 pop u latio n density, 220, 221 positive feedback processes, 2 2 7 -2 2 8 potential for grow th a n d survival, 222 theory, 2 1 9 -2 2 2 trade-offs, 217, 218, 226, 237 life-cycle tim ing, 218 lifetim e fecundity, 218 light. See also daylight in the sea; biolum inescence a n g u la r distribution, 162, 163 as a n energy source, 27 a tten u atio n , 5, 7, 29, 48, 162 m ax im u m transm ission, 162 quality at d ep th , 29, 30, 31 reflection a n d refraction, 162 scattering, 162, 189, 191 light d am age shortw ave, 31, 189 visible, 180 light intensity, 3, 8, 32, 34, 39, 40, 87, 190, 196. See also critical d e p th com pensation d e p th , 30 d e p th zones, 2 light organs. See p h o to p h o res Linophryne, 212, 213 L iparidae, 55 lipids buoyancy, 109 effects o f pressure a n d tem p eratu re, 122

Lolliguncula, 141 long distance m igrations, 147 Ioosejaws. See m alacosteids Lophelia, 277 lophophorates, 281 loriciferans, 58, 241, 279 luciferase, 198-199 luciferin, 198 199, 202 I Jidda, 66 lum inous bacteria. See bacteria: biolum inescence, lum inous p atches on fishes, 205 lum inous secretions, 202, 206, 210 lum inous sym bionts, 200- 201 Lycoteuthis, 214 m acrobenthos. See b enthic m acro fau n a Macrocypridina, 176, 178-180 m acro p lan k to n , 43 m acrourids, 59, 60, 84, 120, 200, 227 abu n d an ce, 62 body form , 59 diet, 60 drum m ing, 136-137 lateral line, 128 m acrozooplankton, 36 m agnetic senses, 146-147 Malacocephalus, 137 m alacosteids, 99 Malacosteus, 173, 210, 211 M alacostraca, 287 m am m als, 23, 24, 110, 213, 2 9 3 -2 9 4 insulation, 104, 110, 294 sounds, 142-145 m antis shrim ps, 186 m arin e phyla, 2 7 4 -2 9 5 m arin e snow, 16, 46-4-7, 48, 61, 87, 199, 275, 286, 291 M atthiessen’s ratio, 166, 175, 177 m ech an o recep tio n , 48, 124-145, 147 m ech an o recep to rs, 123, 133, 149, 151, 156, 160 fishes, 126-136 invertebrates, 138-142 M e d ite rran e a n w ater, 8, 9, 88 m edusae, 21, 138, 277 m egabenthos. See b enthic m eg afau n a m egafauna. See b e n th ic m egafauna Meganycliphanes, 176, 183 m eiobenthos, 274. See b enthic m eiofauna m ela m p h a eid fishes, 101, 129

THE BIOLOGY OF THE DEEP OCEAN

306

m ela m p h a eid fishes (cont) p re d ato rs o n gelatinous anim als, 102 Melanonus, 130 Melanostomias, 207 m em b ra n e a d ap ta tio n to d ep th , 122 m en h a d en , 85 Meningodora, 224 m esh size o f nets, 17 o f sieves, 56 m esopelagic fauna, 71, 87, 100 sam pling, 20 m esopelagic fishes, 292 eyes, 166, 167 m esopelagic zone, 2, 3, 8 cam ouflage, 189 c o unterillum ination, 207 light, 162 m eso p elag ic/b en th o p elag ic interactions, 59 m esoscale eddies, 12, 83, 96, 249 M esozoa, 241, 278 m esozooplankton, 36, 43, 45 m etabolic dorm ancy, 30 m etabolic rates, 93, 102, 117-122, 150, 227, 230 cold a d ap tatio n , 118-119 decline w ith d ep th , 118,121 d e p th a n d pressure effects, 119 h e at re tention in fishes, 104 locom otory reduction w ith d ep th , 119 o f bacteria, 62 reductio n in winter, 89 m etazoans, 2 3 9 -2 4 0 , 274, 278 Meterythrops, 183 m eth an e, 27, 64, 67 m eth a n e ice, 67, 68 m eth a n o tro p h s, 67, 68 m icrobial loop, 34-, 4-3-45, 46, 49, 275 energy flow, 43 m icrobial populations, 239 com m unity stability, 253 m icroflagellates, 35, 43, 275 m icroorganism s. See viruses; bacteria; picoplankton m icroplankton, 36 m icrozooplankton, 3 9 -4 2 , 45, 48 m id-A tlantic R idge vents a n d fauna, 6 5 -6 7 m id-ocean ridges, 51, 52, 71 m im icry, 213, 216

m igrations. See vertical m igrations; season­ ality/: m igrations m irro r cam ouflage, 192, 194 Misophria, 150 m ixed layer, 3 0 -3 4 , 39, 76 stability, 30, 33 w ind forcing, 34 m ixing processes, 10, 11, 32, 33, 36, 80, 96 at fronts, 76 diffuse n u trie n t, 34 m olecular biology p a tte rn s o f dispersal, 84 molluscs, 55, 56, 64, 241, 243, 2 8 2 -2 8 4 Molpadia, 56 Monacanthus, 136 Monomitopus, 137 m orids, 59 m ortality, 221, 225 life histories, 222 Munidopsis, 185 mussels, 55, 65, 66, 67, 68 Mustelus, 146 my'ctophid fishes. See lanternfishes Myctophum, 214 my'sids, 222, 287. See also Gnathophausia biom ass, 287 eyes, 182-183 statocysts, 141 mysticetes. See b aleen whales Myxine, 133 Nannochloris, 35 nan o p lan k to n , 36, 44 nauplius eye, 17 7 Nautilus, 112, 142, 175, 176, 283 n e a r field o f vibrations, 124, 126, 136, 140, 147 Nebaliopsis, 102 nekton, 16, 50, 91 definition, 2 Nematobrachion, 176, 183, 215 nem atocysts, 111, 191 ,2 7 7 nem atodes, 58, 64, 241, 280 diversity' 58 N e m ato m o rp h a , 241, 280 Nematoscelis, 215 nem ertines, 241, 243, 278 Neocalanus, 86, 89 Neolepas, 287

INDEX

307

neph elo id layer, 51 Nephrops, 180, 187, 279 nets, 15-26, 57, 87, 88, 250. See also trawls avoidance, 19, 20 ben th ic, 52 d e p th range, 17, 18 drag, 20 flow m eters, 21 high speed, 20 lim itations at h a d al depths, 69 L o n g h u rst-H ard y P lankton Recorder, 19, 83 m esh size, 17 m ultiple, 18, 19, 90 o p e n in g a n d closing, 18 p op-up, 18 pressure wave, 17 signals, 17, 18, 52 size bias, 20 vertical, 17, 18 neu ro m a st organs, 1 2 7-135, 145, 151 sensing o f currents, 131 stru ctu re a n d distribution, 127-131 n e u tra l buoyancy, 4 ,8 8 , 104-106, 110, 112, 113, 117, 122, 133. See also buoy'ancy h y d ro th erm al plum es, 64 w ater co n ten t, 105, 107 nitrate, 10, 32, 35, 39, 40 nitrogen, 27 fixation, 35 N o rth Pacific co p ep o d feeding, 46 gyre, 36, 37, 41 N o rth Sea co p ep o d patch, 84 N orw egian Sea, 8, 10 benthic biodiversity, 244 notacan th s, 59 Notacanthus, 170 Notostomus, 1 0 7-109, 224 N otosudidae, 233 N'ucula, 228 nudib ran ch s, 111 nutrients, 7, 10, 11, 33, 35, 37, 40 lim itation, 31, 35, 39, 40, 48, 84 rem ineralization, 47 re plenishm ent, 32, 34, 76 Nybelinella, 174, 185 Oasisia, 68

ocean colour, 162 ocean currents, 4. See also circulation electric fields, 146 ocean m odelling, 41 ocean processes, 5 ,8 , 11, 16, 2 7 ,3 1 ,4 1 , 73, 74, 76, 81, 96, 262 oceanic ecosystem , 2, 3, 26, 38, 45, 48, 49 com parison w ith terrestrial ecosystem , 3 -7 , 38 feeding types, 47 m easurem ents, 7 scale, 1 stru ctu re a n d m ain ten an ce, 77 oceanic gyres, 5, 29, 36, 42, 53, 79, 226 octopods, 53, 177 Octopoteuthis, 213 Octopus, 176 odontocetes, 143, 294 Odontomacrurus, 197 o d o u r plum es, 149, 155 Oikopleura, 141, 222 olfactory organs, 151, 156, 157 anglerfishes, 232 Cyclothone, 157 O ligochaeta, 284 oligotrophic regions, 29, 3 4 -4 3 , 45, 49, 53, 58, 103, 237, 244, 247, 275, 276' om nivores, 275, 287, 288 Omosudis, 173 Oncaea, 47 ontogenetic m igrations, 89, 173, 225 O n y ch o p h o ra, 241, 285 Ophiacantha, 205 ophiuroids, 53, 289, 290 Opisthoproctus, 167, 200, 209, 293 O p lo p h o rid ae , 224 Oplophorus, 176, 185, 186, 206, 208, 210, 215, 224 optical particle counter, 20 optical techniques, 12, 14, 18, 20, 83, 87 Orchomene, 150 O rth o n e ctid a , 241, 278 O rto n ’s Rule, 2 3 5 -2 3 6 Ostereococcus, 35 ostracods, 58, 178, 287 otoliths, 123, 125, 127, 132-137, 235 oxygen in seawater, 7, 10—12, 53, 95 blood capacity, 120, 121 d e te rm in a n t o f biological distribution, 76

THE BIOLOGY OF THE DEEP OCEAN

308

oxygen in seaw ater (cont.) from photosynthesis, 29, 65 in sw im bladder, 112-116 m ea su re m e n t o f p rim a ry prod u ctio n , 38 m in im u m layers, 76—79, 1 19, 253 oxvcline, 10 source lor chem osynthesis, 27, 63, 65 Pachystomias, 173, 211 Pacific O c ca n . See also N o rth Pacific biogeography, 7 7 -8 0 c arb o n a te solubility, 62 circulation, 72, 73, 80 Cydothone, 226, 252 D V M , 91 Eurythenes, 70 H N L C region, 40 lanternfishes, 226 Neocalanus, 89 oxygen m inim um , 76 phytop lan k to n a n d copepod diversity; 252 seafloor d isturbance experim ent, 253 trenches, 69 vent fauna, 66, 68 Vinciguerria, 226 Pagolhenia, response to vibrations, 132 Palinurus, 142 Pannychia, 205 Parabrotula, 232 Paralicella, 102, 150, 230 parasites, 241, 278, 280, 282, 284, 286, 287 parasitic m ales, 232, 236 Pareuchaeta, 231 Paroriza, 160 particle displacem ent, 123, 125, 126, 133-135, 147 particle flux, 62. See also export flux feeding, 51 particle size, 46, 224, 250 sam pling, 20 sedim ents, 71 surface feeding o f larvae, 89 zooplankton grazing, 39, 41, 42 particle velocity. See p article displacem ent patchincss, 7, 14, 40, 87, 96, 221, 230, 246, 290 benthos, 248 breed in g cycles, 84 causcs, 83

coupling to ocean processes, 84in the open ocean, 74 m etabolism , 84 phytoplankton, 33 storm s, 84, 85 vertical, 86 Pelagia, 108 pclagic biodiversity; 249, 250, 252, 253 pelagic biom ass, 46, 278 pelagic com m unities, 6 pelagic fauna hadal zone, 6 9 -7 0 penaeid shrim p, 140, 224 penguins, 24, 294 Pennatula, 205 pennatulids, 55 Periphylla, 206 P eruvian w aters, 43 El N ino, 37 Petalophthalmus, 183

pH carb o n dioxide budget, 11 gas gland, 115 116 pherom ones, 149, 154-159 P h o ro n id a, 241, 281 p hosphate, 10, 32 ph o to au to tro p h s, 16, 3 5 -3 7 , 40, 274. See also phy'toplankton Photobacterium, 199, 201 Photoblepharon, 213 p h o to g rap h s 52, 83. See also sam pling:photographic. a n d video survey's photophores, 177, 186, 194, 198, 200, 202 216. See also light organs cam ouflage, 2 0 8 -2 0 9 control, 205 optical design, 204 orien tatio n , 208 rotation, 209 size a n d h a b ita t d ep th , 207 photosynthesis, 2, 10, 11, 27, 29 31, 33, 36, 3 8 ,4 0 ,4 1 ,4 8 ,6 0 ,6 3 ,6 4 , 71, 81, 274 inhibition, 31 p h otosynthetic sym bionts, 188, 2 7 5 - 277 Phronima, 176, 181, 182, 191 Phrynichthys, 130 Physalia, 111, 189 physical factors a n d biological p atterns, 75 physiological decline in cold-core rings, 82 phytodetritus, 55, 60, 236, 246

INDEX

309

p h y todetritus (cont) responses o f the benthos, 237 -238 phytoplankton, 5, 10-12, 16, 17, 2 7 -4 8 , 80, 87, 237 biom ass, 36 from satellites, 72 light a n d shade species, 31, 34 patches, 8 3 -8 5 seasonal cycle, 32 tu rb u le n t m ixing a n d species, 36 phytop lan k to n bloom s, 13, 33, 37, 39, 40, 84, 89, 236, 237, 277 b cn th ic effects, 235 causes, 34sinking, 159 virus effects, 45 picoplankton, 16, 33, 3 5 -3 7 , 39, 44 4-6, 49 con trib u tio n to prim ary' p ro duction, 36 P innipedia, 294 Placozoa, 241, 276 plankton, 19, 50, 91. See also phyto p lan k ­ ton a n d size fractions (pico-, etc) a d ap tatio n s to increase drag, 4 definition, 2 sam pling m ethods, 12, 16—22 size categories, 16 spatial p attern s, 84 Platy'helm inthes, 241, 278 Platyscelus, 181, 182 platytroctid fishes, 128, 206 Plesiopenaeus, 60 Pleuromamma, 93, 151 pleuston gas buoyancy, 111 Plotosus, 145 pogonophores, 56, 64, 67, 241, 243, 288 polarized light, 175, 178, 186 polychaete w orm s, 56, 66, 68, 70, 284 Polycheles, 185 Polyplacophora, 282 p opulation cycles, 39 po p u latio n density-dependcnce, 2 1 9 -2 2 3 po p u latio n m ixing b arriers, 253 Porcupine S eabight, 55, 56, 58, 61, 228, 2 3 5 -2 3 7 , 246, 248 Porichthys, 202 Porifera. See sponges Poromitra, 129-130, 151 p o rp h y rin pigm ents, 196

porphyropsins, 165, 173 Porpita, 189 p o ten tial grow th a n d survival, 218 pred ato rs, 10, 29, 38, 47, 59, 91, 95, 141 defence, 137-139, 189, 203, 210 D V M , 9 3 -9 4 p atch feeding, 85 pressure, 64 biochem ical effects, 121 -122 d e p th relationship, 7 clfcct o n w ater density, 2 effects o n organism s, 62, 11 7 gas density, 113, 137 rigid gas cham bers, 112 sensors, 17 sw im bladders, 113 priapulids, 56, 64, 241, 243, 281 p rim a ry producers, 5, 6 p rim a ry 'p ro d u ctio n , 15, 2 6 -4 9 , 50, 72, 73, 76, 89, 98, 221, 226, 237, 258 coastal, 38 com pensation a n d critical depths, 31 consum ption by' bacteria, 43 control in oligotrophic regions, 45 conversion to tertiary' p ro duction, 42 definition, 27 export from euphotic zone, 34 global budget, 36, 38 global distribution, 28 hyd ro th erm al vent co ntribution, 68 lan d a n d ocean, 6, 38, 49 lim itations, 39 -41 m easurem ents, 3 7 -3 8 new a n d regenerated, 35, 39, 47, 84 regional differences, 38 seasonal effects, 48 size fractionation, 36 Prionace, 146 Prionotus, 136 Prochlorococcus, 35 -36 progenesis, 234 prokaryotes, 35, 239 protists, 45, 48, 64, 197, 239, 274 -276, 278 p ro to b ran ch s, 58, 283 Pseudocalanus, 42, 94, 155 susceptibility to patchiness, 84 Pse.udomm.a, 183 Pseudoscopelus, 2 13 pteropods, 11, 78

THE BIOLOGY OF THE DEEP OCEAN

310

Pterotradiea, 108 pycnocline, 10, 76 Pyrosoma, 60 lum inous bacteria, 201 r- a n d K- selection, 220, 237 rabbitfishes, 110 radiolarians, 275 Raja, 146 R a p o p o rt’s Rule, 246 rarefaction curves, 242, 245 rattails. See m acrourids rays, 55, 146 recycling. See rem ineralization re d biolum inescence, 2 1 0 - 211 red-sensitive visual pigm ents, 173 reflecting superposition eyes, 179 reflectors, 169, 178, 182, 192-195, 204 o n specific organs, 194 spectral b a n d w id th , 192 refracting superposition eyes, 179, 182 regional species diversity, 250, 252 rem ineralization, 11, 34, 35, 43, 46, 61 effect o f viruses, 45 rem ote sensing o f ocean d ata, 12—15 reproductive cycles, 235, 237 reproductive life-history Gnathophausia, 223 reproductive o u tp u t, 218 reptiles, 293 re so n an t frequency (gas bubble), 125, 137 resource allocation, 217, 218, 234, 238 respiration , 11, 29, 30, 122, 237 c arb o n dioxide p ro d u ctio n , 11 p h ytoplankton, 29 respiration rates, 62 A ntarctic a n d C alifo rn ian fishes, 118, 119 A ntarctic pelagic fauna, 118 reduction w ith d ep th , 117 respiratory7 adap tatio n s in deep-sea fishes, 120 rele mirabile, 116 retina. See eyes retinula cells, 175 R eynolds num ber, 47, 49 relation to size, 48 rh a b d o m , 175, 178, 179, 182-184 Rhincalanus, 89 rhodopsins, 165, 173

ribosom al R N A d a ta o n Cyclothone, 252 Ridgeia, 66 Riftia, 63, 66, 67, 231 Rimicaris, 65, 185, 197. See also bresiliid shrim p R o o t effect, 115-116 rotifers, 241, 279 R O V s (remotely/ o p e rated vehicles), 12, 21, 22, 52, 53, 69 Sagitta, 84, 138 salinity, 8 -1 0 , 80. See also density o f seaw ater Salpa, 108 salps, 46 sam pling, 7, 15, 197. See also nets; acoustic techniques; optical techniques benthos, 52 corers, dredges a n d grabs, 52 fish larvae, 74 flashing organism s, 21 gelatinous anim als, 21 hyd ro th erm al vents, 53 large anim als, 2 3 -2 5 longlines, 23 m edium -sized organism s, 17-22 m ethods for patches, 83 n e t hauls for D V M , 90, 92 nu m b ers o f species, 242 p h o to g rap h ic a n d video surveys, 14, 21, 47, 52, 55, 57, 60, 63, 69, 236, 237 scales, 26, 73, 74, 86 squid beaks, 23 tagging systems, 23, 24, 151 three-dim ensional distribution, 21, 22 traps, 23 sm all organism s, 15-16, 26, 45 Sandalops, 177 Sargasso Sea, 81, 84 Sargassum w eed, 60 satellite d a ta , 7 2 -7 7 , 80 iron en rich m en t, 40 surface reflectance, 12, 13, 31 tem p eratu re, 81, 83, 251 tracking, 24, 146 S cap h o p o d a, 235, 282 scattered light. See light: scattering scavengers, 56, 62, 71, 131, 149, 282, 284, 287, 288, 290, 291 scavenging am phipods, 60, 70, 102

INDEX

311

schooling, 83, 132, 136, 213 sciaenid fishes, 136 Scina, 205 scom broid fishes, 104 scopelarchid fishes, 76 Scopdarchus, 167, 173 Scopelosaurus, 173 screening pigm ent, 178, 183, 184 Scypholanceola, 182 S cyphozoa, 277 sea birds, 23, 24, 98, 154, 294 sea cows. See Sirenia sea cucum bers. See holothurians sea lilies. See crinoids sea snails. See L iparidae sea snakes, 293 sea spiders, 55 sea stars. See asteroids sea urchins. See echinoids seafloor currents, 51, 52, 57, 71, 88 seagrasses, 60 seals, 2 3 -2 5 , 294 m ec h an o recep tio n , 133 seam ounts, 8, 51, 146, 249 Searsia, 128 seasonality, 5, 12, 31, 33, 39, 60, 71, 72, 80, 93, 96, 161, 221, 230, 2 3 5 -2 3 7 , 246, 250, m igrations, 89, 146, 294 m ovem ents o f fronts, 76 p hyto d etritu s sinking, 159, 2 3 5 -2 3 6 upwelling, 37, 87 secondary p ro d u ctio n , 42, 49, 154 defined, 41 sedim ents, 86 b ackground, 197 c arb o n ate, 11, 62 cores, 53, 55, 71, 78, 81, 83, 242, 243, 244, 245, 280 d isturbance, 247 feeders, 71 fluidization, 51 load, 51 oxygen levels, 53 respiration, 62 resuspension, 56 rew orking, 61 scouring, 51, 249 slum ps, 69 traps, 48, 61, 236

Selenoteuthis, 194 sem icircular canals, 133 sensors on anim als, 12, 25 o n buoys o r vehicles, 12 o n nets, 18, 22 sensory systems, 123, 148, 164 Sepia, 141 Sergestes, 208, 224 Sergia, 215, 224 settlem ent cues, 159 sex, 217, 2 3 1 -2 3 3 , 237 sex a n d size, 231 sexual b e h av io u r a n d m echan o recep tio n , 139 sexual biom ass differences, 231 sexual d im orphism , 210 d ru m m in g system , 136 ph o tophores, 2 1 4 -2 1 5 size in fishes, 232 sexual e n co u n te r probability, 158 sexual pherom ones, 154, 158, 160, 232, 234 sexual signals, 232 acoustic, 136, 137, 143 biolum inescent, 207, 210, 2 1 4 -2 1 6 chem ical, 149. See also sexual ph ero m o n es sharks, 146. See also squaloid sharks Shewanella, 199 Shinkailepas, 66 shortw ave visual pigm ents, 186 Sicyonis, 57 silicate, 10, 32, 39, 40 silvering, 192-196 silversides, 132 single c o n ce n tra tin g effect, 115, 116 sinking o f w'ater masses, 8, 10, 75, 88 sinking o f particles a n d organism s, 4. 29. 33, 39, 45, 48, 60. See also phytodetritus; export flux buoyancy, 39, 104, 111 chem oreception, 153, 155 density' 7 faecal pellets, 11, 61, 76, 96 m arin e snow', 46 sinking rates particle size, 35, 103, 106 siphonophores, 21, 22, 111, 277 acoustic reflection, 14

THE BIOLOG Y OF THE DEEP OCEAN

312

siphonophores (conl.) benthic, 59, 277 sipunculids, 56, 241, 243, 284 Sirenia, 294 Siriella, 183 size, 190 acoustic sorting o f particles, 83 benthic fauna, 52, 53, 55 biolum inescent display, 205 cy anobacteria, 35 discrim ination from w hale song, 144 m eso- a n d bathypelagic fishes, 230 o f organism s for sam pling, 15 o f prey, 100, 101 p lankton, 16 value o f food particle to grazer, 39, 85 skates, 55 slickheads. See alepocephalid fishes Snell’s \vi ndow, 162 snipc-eels, 128, 293 sound a tten u atio n , 5, 125, 126 com m unication, 124, 142, 143, 147 direction sensitivity, 135-136 frequency, 14, 15, 124 126, 130, 134, 137, 138, 141 -1 4 4 particle velocity. See particle displacem ent pressure waves, 123 prod u ctio n , 1 3 6 -1 3 8 ,1 4 2 -1 4 5 speed in water, 4, 136 S o u th e rn O c ea n , 38, 40, 154, 202 circulation, 80 copcpod a n d euphausiid herbivores, 46 copepod dorm ancy, 89 iron enrichm ent, 40 Spadella, 138 spatial distribution trophic guilds at hyd ro th erm al vents, 65 spatial heterogeneity, 7 0 -7 1 , 74, 83, 246, 249, 284. See also patchiness spatial sep aratio n betw een adults and larvae, 89 speciation, 75, 250, 253 species n u m b ers dem ersal fishes, 245 nem atodes, 246 pelagic groups, 250 phy-toplankton, 250 tropical insects, 242

species ranges, 78 species richness, 240 regional differences, 246 species succession, 31, 37 spectral b an d w id th light at d ep th , 30, 161 reflectors, 193 satellite data, 12 scattering a n d abso rp tio n , 8 sunlight, 161 visual pigm ents, 169-170 spectral filters eyes, 173, 186 p hotophores, 204, 208, 209, 211 sperm w hales, 23, 24, 294 density adju stm en t a n d buoy'ancy, 110 spherical a b erra tio n , 183 spiny-eels, 59 diet, 59 Spirula, 112- 113, 142 sponges, 55, 64, 67, 241, 276 sprat, 129- 130 spring bloom . See p h ytoplankton bloom s squaloid sharks, 59, 60, 109-110, 292 squat lobsters, 66 squid. See also cephalopods buoyancy, 107 feeding in nets, 19 hearing, 142 stability o f the w ater colum n, 10, 33, 34, 71, 87, 160, 223, 246, 254 stalked eves, 17 7 standing stock, 29, 38, 39, 49, 80 statocysts, 141 142 relation to cep h alo p o d lifestyle, 141 statoliths, 123, 125, 142 stealth m ode o f feeding, 99, 101 Stemoptyx, 102, 158, 170, 213 stom atopod eyes, 186 stom iatoid fishes, 158, 210, 226, 227, 232, 292 S trait o f G ibraltar, 87 S trait o f M essina, 87 stratification, 33, 87, 93, 95. See also m ixed layer: stability Slylephorus, 167, 173 Slylocheiron, 176, 183 sublittoral zone, 50 subm ersibles, 14, 21, 22, 52, 53, 62, 63, 64, 66, 180, 196, 277, 288

INDEX

313

nam es o f vent anim als, 66 sulphate in seawater, 64, 108 sulphide, 27, 29, 64, 65, 67 superposition eyes, 179, 182, 184 -187 reflecting, 184 refracting, 182-184 surface p ro d u ctio n , 76, 246, 248 - 250 correlation w ith m eg afau n a, 56 surface reflectance, 13 suspension feeders, 51, 56, 58, 84, 99, 281, 290 sw im bladder, 59, 104, 105, 110- 117, 120, 122, 125, coupling to in n er ear, 134 -135 drum m ing, 136, 137 lipid, 114 m ain ten a n ce o f gas volum e, 113 rele length, 117 Symbion, 279 sy n a p h o b ran c h id eels, 59, 60 Synechococcus, 35 Systellaspis, 91, 92, 186, 196, 206, 210, 224 tanaidaceans, 56 Taonius, 17 7 tap e tu m , 169, 173, 174, 176, 177, 180, 183 185, 193, 292 tardigrades, 58, 241, 285 taxonom ic kingdom s, 239 teleost fishes. See also bony fishes; fishes buoyancy, 110 fecundity, 229 Temora, 153, 155 tem p erate regions, 38, 41, 60, 88, 201, 220, 235, 237, 248, 291 seasonal cycle, 3 2 -3 4 tem p eratu re, 5, 8, 9, 10, 25, 39, 64, 80 anom alies, 63 bacterial action, 62 effect o n density, 2 fluid viscosity, 4, 120 profile, 3 relation to m etabolic rates, 118 terrestrial biodiversity, 2 4 0 -2 4 3 , 246 terrestrial biolum inescence, 198 terrestrial cam ouflage, 188 terrestrial countershading, 207 terrestrial ecosystem c o m parison w ith oceanic ecosystem , 1, 2, 5- 7, 26, 27, 29, 38, 73, 79, 148, 250

life history theory, 220 terrestrial p la n t debris, 60 tertiary p ro duction, 42 Teuthowenia, 17 7 Tevnia, 67 Thalassiosira, 34, 154 Thalia, 108, 222 therm ocline, 10, 11, 30, 33, 39, 86 th erm o h alin e circulation, 8 -1 0 , 81 th in layers o f pliyto- a n d zooplankton, 20, 99 T h o rs o n ’s Rule, 2 3 5 -2 3 6 three-dim ensional distributions, 86 Thysanoessa, 85 7 hysanopoda, 183, 230 tim e scales in the ocean, 5 tintinnids, 275 Todarodes, 141 top dow;n control, 39, 41 Torpedo, 146 touch a n d sound, 123-147 trace elem ents, 11 tracks, 52, 246 on sedim ent, 5 2 -5 4 trail-following, 152, 155-156, 158, 159 transparency, 19 0 -1 9 1 , 216 destructive interference, 190 gelatinous anim als, 190 p olarizatio n , 191 refractive index, 190 th in tissues, 191 traw ls, 22, 24, 52, 53, 55, 69, 114, 231, 245, 253 b o tto m , 19 Engels, 20 M O C N E S S , 18 R ectan g u lar M id w a ter T raw l, 18 T ucker traw l, 18 trenches, 2, 50, 6 9 -7 0 , 249, 290, 292 Trichodesmium, 35 trim ethylam ine buoyancy a n d pressure stabilization, 109 trip o d fishes, 55, 133 trophic interactions. See food webs trophic levels, 42, 43, 45 tu b ero u s organs, 145 tubew orm s. See vestim entiferans tu b u la r eyes, 1 6 6-167, 170, 173, 177, 181, 186, 207, 293 tu n a, 17, 23

THE BIOLOG Y OF THE DEEP OCEAN

314

tu n a (cont.) visual acuity, 171 turbidites a n d diversity, 248 turbidity' currents, 52, 71 turbulence, 19, 37, 86, 96, 124, 133, 155 buoyancy, 103 feeding, 85 tu rb u le n t m ixing, 5, 33, 36, 37 turtles, 24, 293 m agnetic navigation, 146 u ltraso u n d sensitivity, 138 U n ira m ia, 286, 288 upw elling regions, 3 6 -3 7 , 39, 42, 43, 84, 85, 87, 89, 98 U ro c h o rd ata , 290, 291 Urolophus, 146 Valdiviella, 228 Valenciennellus, 158, 167 Vargula, 202, 215, 216 Velella, 111, 189 vent chimney's, 6 4 -6 6 Ventsia, 66 vertical dim ension, 1-2, 72, 76, 86 vertical distributions, 8 6 -8 8 changes a n d tim e scales, 87 light intensity, 94 vertical m igrations, 96 diel. &«?DVM ontogenetic, 89 seasonal, 89 vertical m ixing, 84, 88 vestibular organs, 133 vestim entiferans, 6 3 -6 8 , 288 vibration receptors fishes, 126-136 invertebrates, 138—142 vibrations, 123-124, 147 along a fish, 126 direction o f the source, 132 far field, 124, 125, 126 in w ater, 124 n e a r field, 124, 126, 138 shrim p a n te n n ae , 140 Vibrio, 199 Vinciguerria, 226 viperfish. See Chauliodus viruses, 15, 45

viscosity, 36, 103 blood, 120 feeding currents, 47 o f air a n d water, 4 vision, 1 6 1-187, 189. See also eyes surrogate senses, 174 visual acuity a n d sensitivity' 171, 177, 180, 183, 185 visual pigm ents, 165, 168, 169, 175, 184, 186, 211 ontogenetic changes, 17 3 visual p re d atio n in u p p e r w aters, 119 visual qu it zone, 174 Viireledonella, 177 viviparity, 228, 230, 232, 293 Watasenia, 175 w ater masses, 12, 51, 7 4 -7 7 , 79, 87, 275 as indicators o f ocean processes, 81 wavelengths. See also spectral b andw idth; biolum inescence colour sound in w ater, 4, 13 w eather lan d a n d ocean, 5 w hale sharks, 99 whales, 15, 23, 24, 68, 142, 143, 293. See also sperm w hale w ind m ixing, 32, 88, 96, 154 Winteria, 167, 200, 293 xenophyophores, 55, 57, 275 yellow lenses, 173, 177 zeid fishes, 136 zoarcid fishes, 55, 227 zooplankton aggregations, 86 at low' R eynolds num bers, 48 biom ass, 3 dispersal, 84 excretion, 35, 39 feeding a n d p h ytoplankton specificity, 85 g razer com ponent, 46, 47 optical a n d acoustic im aging, 14 populations, 13, 14, 45, 80 size categories, 16 th in layers, 87 vertical variability, 86

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