Table Of ContentThe Senses of Fish
Adaptations for the Reception of Natural Stimuli
The Senses of Fish
Adaptations for the Reception of
Natural Stimuli
Editors
Gerhard von der Emde
Joachim Mogdans
B G Kapoor
Springer-Science+Business Media, B. V.
A. C.I.P. catalogue record for the book is available from the Library of Congress
ISBN 978-94-010-3779-2 ISBN 978-94-007-1060-3 (eBook)
DOI 10.1007/978-94-007-1060-3
In India, Bangladesh, Nepal, Pakistan and Sri Lanka by Narosa Publishing House
22 Daryaganj, Delhi Medical Association Road, New Delhi 110 002, India
All Rights Reserved
Copyright © 2004 Springer Science+Business Media Dordrecht
Originally published by Kluwer Academic Publishers in 2004
Softcover reprint of the hardcover lst edition 2004
Ali rights reserved. No part of this publication may be reproduced,
stored in a retrieval system or transmitted in any form or by any means,
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without prior written permission of the publishers.
Foreword
FISHANDFOLK
V. Benno Meyer-Rochow
International University Bremen (IUB),
FacultyofEngineering & Science, Bremen,Germany
Ilovefishand when asked towritethis Foreword wasveryhappy tobegiventhe opportunityto
welcome this exciting tome on "The Senses of Fish: Adaptations for theReception of Natural
Stimuli", edited by Profs. Gerhard von der Emde, Joachim Mogdans, and B.G. Kapoor. My
enthusiasm was briefly damped when a graduate student of mine, whom I told of the task
allotted tome,remarked "Whostillreadsbooks these days?".Temporarilystunned, Ihastened
toreply"Smartpeople do,ofcourse!".
This volume contains such a wealth of information and presents such a wonderfully
balanced variety of contributions byexperts in their own fields, each and all expanding their
subject one or another, that I could have added "This book makes smart people smarter still
and that's whysmart peoplewillread it".The topicscovered fallneatly intosixcategories.The
first twochapters, byBarbara Evansand Arnold Sillman & David Dahlin, provide the reader
withexcitingnewdetailson fisheyeadaptationsand the reasonsbehindsuch adaptations. Eyes
and vision in fish are finely tuned to the photic environment and as a consequence of this
relationship aswellasthe widerange ofhabitats thatfishoccur in,avariety ofmodifications to
the eye'soptics,development, retinal organization, photopigments, absolute and spectral sensi
tivities have evolved. Without a thorough examination of these adaptations, we would be
unable tomake muchsenseofthe visualbehavior offish.
Recent yearshaveseenan upsurgeofinterestin the chemosensory abilitiesoffishand three
chapters, one each byAnne Hansen& KlausReutter,Tine Valentineie, and GabrielleNevitt&
Andrew Dittman, testifyto thisfact.Usingbehavioral responsesand a comparative approach,
Tine Valentineie showsthat predatory fishwith functional olfactoryand taste receptors do not
necessarilyusethese sensesduring foodprocurement.Visualhunters usethe taste systemsolely
during oral food evaluation. The situationfor the detectionofunderwatersmellsissomewhat
different as Hansen and Reutter demonstrate. However, that olfaction in migratory species
playsamaior rolehas been known foralongtime, but how,forinstance, imprintinginjuvenile
vi Foreword
salmon might work, in contrast to imprinting in mammalian species, isinvestigated byNevitt
and Dittman. The two authors provide evidence that odor memories may also be retained
peripherally and thatolfactory receptor neurons could be "selectively tuned" byresponding to
specificodors present"during ahormonallylinkedsensitive period". Thisisan exciting concept
and one can expect more fascinating discoveries in this fertile field of 'developmental neuro
etho-ecology'.
A fascinating overview of the sensory systemsand sensory brain areas in deep sea fish by
Hans Joachim Wagner allows the reader not only to appreciate the specializations that are
present in the denizens of deep water, but also to see the developmental parallels in fishes of
otherhabitats (cf.,forinstance,Meyer-Rochow &Coddington, 2003, In: FishAdaptations,eds.
ValA.L. & Kapoor B.G., Oxford and IBH Pub!. Mis Sci. Pub!., Enfied, New Hampshire, pp.
339-383). This chapter byWagner, placed in the centre of the book, thus connects the more
detailed treatments of selected senses and sensory adaptations, preceding and following
Wagner's chapter, with eachotherand, likethe fish'sbrain, has an integrativefunction.
Aspects of sound production and hearing in fish are dealt with in another fascinating
section of this book. Far from being silent creatures, Friedrich Ladich introduces us to the
'noisy' underwater world and describes how and why fish produce sounds. Little known and
poorlystudies isthe abilityofsome speciesoffishto detectsounds ashigh as 180kHz.Adapta
tions responsible for this remarkable feat, in particular within the Clupeiformes, and possible
ecological consequencesofultrasound detectionare being reviewed byDennis Higgs.But how
the acousticsignalsin the end are 'heard'and processedbythe fish'snervoussystemisthe topic
ofZhongminLu'schapter.Concentratingon what has beendiscovered on the goldfish'ssound
detecting pathways, Lu alsoexamines acoustic communication and directional hearing in the
mormyrid Pollimyrus adspersus, the midshipman Porichthys notatus, and other species. Hong
YoungYanthensummarizesthe currentstateofknowledge with regard to hearinginfishesand
emphatically draws attention to the fact that despite considerable progress, many aspects of
sound perception in fishare still poorly understood.
A very comprehensive treatment byJohn Janssen is given to the role of the lateral line,
especially in species that inhabit dark environments or turbid waters. Yet,how the different
species of fish integrate the signals coming from the lateral line with those being received
through channels of the other senses is still largely unknown. Joachim Mogdans, Sophia
Krother, &Jacob Engelmannin theirchaptertouch upon this problem, butdeal primarilywith
recentfindingson the lateral linebrainstem's responses to avariety ofstimuli.Twosubsystems,
consisting of superficial neuromasts whose function is impaired in running water, and canal
neuromasts, whose function remains unaffected in runningwater,were discovered and led the
researchers to conclude the presence of a clear form-function relationship for the lateral line.
Finally,the enigmaticelectricsenseofsomefish:Thattopicformsthe subjectofchaptersby
LonWilkens, Tim Tricas&JosephSisneros,Clifford Keller, and MaryHagedorn. Wilkens intro
duces us to the paddlefish, a fish that rarely features as an experimental subject. However, as
Wilkens ever so ablydemonstrated with his remarkable research, the paddlefish usesrostrally
located electroreceptors to detect plankton and to investigate its environment. A form of
Foreword vii
"passive electroreception", and what exactly this term entails, is revealed in the chapter by
Tricas and Sisneros. The two researchers have chosen skates as their experimental subjects,
marine species in other words, which, unlike the weakly electricfish (dealtwith in the chapter
by Keller), are not at all famous for communicating electrically. Keller leads us into an alien
world of senses, into a world in which signals familiar to us humans have become largely
replacedbyelectricalstimuli.Aimed primarily at conspecifics,suchsignals,likeMary Hagedorn
explains, can also be apowerful incentive to those adventurous humanbeings, wishing to work
with fish in remote junglesettings.
Although the contributors to this book hail from several different countries and presum
ably were not brought up in the same cultural environments, their fascination for fish unites
them all. As someone who wasborn under the sign ofPisces, Itoo, have a"softspot" forfishof
allkinds: Ilike themfried, cooked, and smoked, and Iregularlyenjoyed 'gefilte fish' asa boy in
my grandmother's home. But I am equally fond of them when I find them cut open in the
dissection dish, under the microscope, or placed in some apparatus designed to reveal their
physiological secrets.Ilove watching themdartaround in myaquariumathomeand havegone
diving to see them in their natural habitats. Ieven have a collection ofcoins that feature fish
and Iknowpeople, who possessthousands offishstampsfrom allover the world. Obviously,as
the enthusiasm has shown, with which this book's contributors have written their chapters,
there are manydifferent waysto express one's adorationforfish.
What makes fish so attractive to humans? Where does this age-old fascination for the
slippery creature of the aquatic domain come from? Isit because we all pass through fish-like
stages in our embryological development? Is it because the class Pisces outnumbers all other
vertebrate classes with regard to the number of species (at least 25,000 species have been
described to date)?Orisit,becausefishare seenasinhabitantsand messengersofaworld alien,
and maybe even threatening, to humans? Iguess there isn't a single reason why humans since
ancient times have found fishcaptivating, butfact isthat the humblefish, as asymbol, has had
averylong historyand occursin cultures and religions throughout the world.So fond must the
earlyEnglish havebeenoffish (orwere theysimplybad observers?) thattheyevenlentthis term
to animals, which have little to do with real fish (witness shellfish, starfish, crawfish, jellyfish,
cuttlefish, crayfish, and silverfish).
Christiansrevere thefishasasymbolofChristand inJewish lore thefish,beingcustomarily
consumed on the Sabbath, symbolizes prosperity. Pre-Christian Germanic tribes ate fish in
honorofthe greatmothergoddess Freya,ahabitthataccordingtosome scholarspersists to this
day in the traditionofmanya Europeanto have ameal offishonFridays.In India areincarna
tionofthe goddess Durga, knownasMeenakshi, wasrespectfullycalled'thebeautiful fish-eyed
one'and the firstIndiancoinageof600-300BC has manyexamplesoffishmotifs. Severalother
non-IndiandeitieslikeIsis,Apollo,and Poseidon (theGodoftheSea) were alsoassociatedwith
fish.Amongstthe Maya oftheNew World differentspecies offishhelddifferentmeanings: hags
were seenasspies and destroyers, catfish represented cleaners and renewers, and otherspecies
were invoked in local systems ofcounting. InJapan, on the day known as 'kodomo no hi' (May
5th each year), even today tall bamboo poles with carp kites and streamers are erected in the
viii Foreword
gardens ofmanyahome,fortotheJapanese the carpembodiesstrengthand determination.On
the otherhand,fearand panic have nowadays,unfortunately, become almost synonymouswith
sharks around the world. However, actual shark-worshippers stillinhabit some remote islands
likeMalaita ofthe Solomons in the WestPacific.
Clearly,fish have accompanied humanity and human culture from their beginnings, and
this has alsofound numerous reflections in the arts. Poemsin praiseoffishhave been written
and set to music (ESchubert's composition "Die Forelle"comes to mind), fishpaintings (e.g.,
PaulKlee's"GoldenFish"),fishsculptures (the OlympicfishofBarcelonabeatingthemallwith
its gigantic size), and nowadays even fish movies, fishing competitions, and fish games exist.
Stories, fairy tales, and fables involving fish, often rooted in antiquity (who would not have
heard ofAesop's 'Fishermanand the Little Fish'?) have along history,butthey are stillpopular
today and they are being told in virtually allparts ofthe world.
This book, although anything else but a collection of mere fishystories and fables, does
follow that long tradition of human fascination with fish and there is not doubt that the
scientific research, reported in this volume, represents the fruits of years of patient and dedi
catedstudy.Theauthors, editors, and publishersmustfeelprivilegedtoshare in the production
ofsoworthy a text asIdo to have been called to welcome it on its appearance. As wegather
moreand moredataon the wondrous waysthe fishes'function',weslowlystarttograspwhy,for
at least400millionyears,these animalshave managed toflourishand beenable tolivethrough
gee-historic crises and environmental changes too profound for us to comprehend. We are
reminded of the fact that almost three quarter of the Earth's surface are the domain of our
friends, the fish.Andwearerealizingthatweareinthe processofunderstanding, what kindsof
adaptationshave allowedthemtosucceed inoccupyingeveryconceivablenicheoftheirwatery
realm and what roles their sensory capacities have played to guarantee their survival through
the ages.
Much ofwhat weknow today about the sensesoffish,represents abilities and adaptations
almost unimaginable to us'mere humans'onlyafewyearsago.This isafact and there isnoth
ing'fishyabout that. However, none of the exciting discoveries can diminish the deep respect
wehold forour 'scientific quarry'. Onthe contrary, the discoveries have served toenhanceour
appreciation of this formidable creature ofNature and sometimes mayeven cause usto take a
deep breath and reflect on our own imperfections.
BeforeIend this Forewordwith a translationofthat fitting and famous poem "Die Forelle/
TheTrout" byChristianSchubart, Ishould liketo emphatically state: This book cannot failto
givegreat pleasure to allthose people smart enough to pick it upand read it thoroughly!
Foreword ix
The Trout
Beneaththe limpid water
Isawajollytrout
As swiftas arrow darting
And flashing in and out.
Istood upon the margin,
All in the morning cool,
And watch'd the fishdisporting
Downin the crystal pool.
Nearbythere stood an angler,
With rod and line and hook,
And saw the trout a-swimming
Downin the crystal brook.
Withshine upon the water
Unbroken,so Ithought,
In vainwillbe his angling,
The fishwillnot be caught.
Atlast the thievish angler
Impatientgrew.Withguile
The waterclear he ruffled,
Andin a little while
He jerk'd hisrod in triumph.
And struggle, struggle asit may,
The poor outwittedvictim
Upon the greensward lay.
From:GarranR.R. 1946(reprinted1971) "SchubertandSchumann".MelbourneUniversity Press
Preface
Animals have to be able to perceive external sensory stimuli and generate appropriate
behavioral responses in order to live successfullyin their environments. On an ontogenetic
scale,behavioral responses to sensorystimuli are eitherinnate or learned. Learning enables an
animal torespond tochangingstimuli throughexperiences madeduring life.Onaphylogenetic
scale, organisms also 'learn' to adapt to changed signals in their environment. Evolutionary
learning works in a different time frame, however, that is from generation to generation. Its
motor is selection, and its result is an adaptation of the sensory apparatus and the nervous
system.During this adaptation process,'communication' with the environment ismaintained,
enabling the animal to gather important signalscoming either from the surroundings or from
otheranimals, likeprey, predators, or conspecifics.
In this book we use fishas model systemsto demonstrate how evolutionary learning has
shaped various sensorysystems.Why fish? There are three main reasons for this: First, 'fishs'
comprise a huge and diversegroup ofanimals.There are about 25000 extant fishspecies that
live in such diverse environments like the deep sea or shallow freshwater puddles in the
Himalayas.Closelyrelated taxa mayliveindifferent habitats and thus undercompletely differ,
ent environmental conditions. They have adapted to these diverse environmental conditions
not onlyin their externalbodyfeatures, but alsobymodifyingtheir sensoryapparatus. Second,
fish possessmore senses they many other animals. They are equipped with the well known
senses that humans have, but in addition they possessat least three more senses. Third, fish
stand at the basisofvertebrateevolution.While shaping the sensesoffish,evolutionworkedon
the very 'blueprint' of vertebrate organisation, which forms the basisof all other vertebrates,
including humans. Fish thus can serve as model systemsfor vertebrate evolution in general,
including the evolutionofsensorysystemsand their adaptations to environmental conditions.
Webrought together scientific experts fromdifferent areas, who report about the sensory
systemsof fish and unravel their physiologicaland ecological evolutionary adaptations. The
first two chapters deal with vision,one of the most important sensesofvertebrates. However,
vision in different aquatic habitats has to cope with quite diverse photic conditions and thus
requires fundamental adaptations of the eyes and their sensory receptors. Chemoreception,
dealt with in chapters three to five,maybeone ofthe "oldest"sensesofvertebrates. Yetagain,
xii Preface
environmental conditions differ in the various habitats fish live in, and this requires
adaptations ofthe olfactoryand taste systemsofthe different groups.Aninterestingcasestudy
ofolfactoryspecializationisolfactoryimprinting,whichcanbefound inseveral groupsoffishes.
The best-known example may be olfactory imprinting in the service of homing in salmons as
described inchapterfive.Chaptersixdoesnotdealwithaparticularsensorysystem,but takesa
lookat several groupsoffishlivingin an extreme environment:the deep sea.Here, the chemi
calsenses,vision,and the laterallinesystemareespeciallydevelopedand adapted to the differ
ent niches in this ultimate environment. Thatfishare not deafiswellknownsince the daysof
Karl von Frisch, and chapters seven to ten discuss several aspects of underwater hearing.
Related tohearing, sound productionbyfish(chapter 10),mainlyin the service ofintra-specific
communication, isan important evolutionary factor shaping fish hearing organs. The lateral
line systemoffishcompromises two main sub-systems: the mechanosensory lateral line, dealt
with in chapters 11and 12,and the electrosensory lateral line (chapters 13 to 16).The latter
canbe divided stillfurther, dependingon the typeofstimuli that are perceived:lowfrequency
electric signalsfor'passive' electrolocationthroughampullary electroreceptororgans (chapters
13 and 14), and high frequency signals, actively produced and thus involved in 'active'
electrolocation (chapter 15).Finally, chapter 16stressesan important'human' point:scienceis
made bypeople,sometimes underextremeconditions.Especiallywhen studying environmental
adaptations ofanimals, it isnecessaryto gooutinto the fieldand get informationdirectly from
the source. This canbedangerous at timesand mayrequire personal sacrificesbythe scientists
that are often forgotten and not mentioned in scientific reports, thus making scientific results
look simple and 'easy' to obtain. That this is often not the case is highlighted by our final
essay-chapter.
Gerhard von der Emde
Joacbdm ~ogdans
B G Kapoor
