Table Of ContentRhythms in Fishes
NATO ASI Series
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Volume 23S—Rhythms in Fishes
edited by M. A. Ali
Series A: Life Sciences
Rhythm s in Fishe s
Edited by
M.A.Al i
University of Montreal
Montreal, Quebec, Canada
Springer Science+Busines sMedia, LLC
Proceedings of a NATO Advanced Study Institute
on Rhythms in Fishes,
heid August 4-17,1991,
in Montreal, Quebec, Canada
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Rhythms 1n fishe s / edite d by M.A. All .
p. cm. — (NATO ASI series . Serie s A, Lif e science s ; vol.
236)
"Proceeding s of a NATO Advanced Stud y Institut e on Rhythms i n
Fishes , hel d August 4-17 , 1991, i n Montreal , Quebec, Canada"—T.p.
verso.
"Publishe d 1n cooperatio n wit h NATO Scientifi c Affair s Division. "
Include s bibliographica l reference s and Index .
ISBN 978-1-4613-6326-2 ISBN 978-1-4615-3042-8 (eBook)
DOI 10.1007/978-1-4615-3042-8
1. Fishes—Physiology—Congresses . 2. Fishes—Behavior -
-Congresses . 3. Biologica l rhythms—Congresses. I . Ali ,M . A.
(Mohamed Ather) , 1932- . II . NATO Advanced Stud y Institut e on
Rhythms 1n Fishe s (199 1 : Montreal , Ouebec) III . Nort h Atlanti c
Treat y Organization . Scientifi c Affair s Division . IV . Series : NATO
.ASI series . Serie s A, Lif e science s ; v. 236.
QL639.1.R53 1992
597' . 01882—dc20 92-3286 3
CIP
ISBN 978-1-4613-6326-2
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PREFACE
Tush, my good lord, this superficial tale
Is but a preface of her worthy praise;
King Henry the Sixth: Part I, Act V, Sc. 5
This volume is the direct result of a NATO. Advanced Study Institute (ASI) of the same
title, held at Bishop's University, Lennoxville, Quebec, Canada in August 1991. All the
major presentations had been commissioned, so to speak, during the organisational phase.
This was done with the view of not only having a structured ASI, whIch is expected to be a
high-level tutorial activity, but also the ensuing volume. As will be indicated in the general
introduction, there have been a couple of meetings and publications dealing with rhythms in
fishes in the past twenty years. However, as in other disciplines, there has been substantial
progress in this field also. Further, I wished to cover almost all aspects and come out with a
volme which will be as complete as possible. Of course, this failed to materialise. In spite
of starting the arrangements two years before the event, several lecturers were not able to
attend due to a number of reasons. Some could be replaced while others could not
Taking into account their individual specialties, I asked about twenty active workers in
the field to provide provoking overviews, not simply reviews of their own work. Also, this
being a NATO. ASI, lecturers and authors had to be selected, as much as possible, from as
many different countries of the alliance as possible. Their speaking and writing ability as
well as personal compatibilities had to be taken into account. I am grateful to those who
accepted the challenge and honoured their commitment. It was an enriching experience for me
and a pleasure dealing with them. As director of the ASI, I listened to every one of the
presentations and as editor of the volume read as carefully as possible each chapter. I found
this to be enjoyable and fruitful and hope that the reader will fmd the effort worthwhile. Each
of the chapters was looked at by two referees, mostly anonymous, and I am grateful to them
for having advised me and the authors on improvements. In :>ome cases the referees's
comments imposed significant changes and two chapters were withdrawn.
Rhythmicity in fishes is of interest to two groups. Those interested in fishes and those
studying rhythms in general. This volume is aimed more at the former and I hope that it
satisfies their needs to some extent . Interest in the biology of fishes is increasing at a rapid
rate. This is due mainly to three reasons. First, the increase in human population and the
dwindling of food resources have exacerbated the need to exploit the oceans, in particular
fishes. This has led also to an increase in the aquaculture industry. Second, increase in
environmental pollution has prompted the study of ways to protect species, including fishes.
v
This was well exemplified in the pollution of the Rhine river in the not too distant past.
Third, due to diversity in their habitat, morphology and physiology, fishes offer excellent
models for the study of various biological phenomena. In all these aspects analysis of their
rhythms is bound to bring a better understanding of their natural history and I hope that this
volume will be of some use in that respect too.
I am grateful to Dr. Luis da Cunha, Director of the ASI programme at the NATO
Scientific Affairs Division (SAD) for his encouragement and understanding. The NATO
SAD, FCAR, Qu~bec and my University provided financial support for the organisation of
the AS!. I thank Monsieur J.-L. Gregoire, Vice-Principal and Mlle Marcia Boisvert, Director
of Conferences at Bishop's University, for all that they did to help me organise and run the
AS!. I appreciated the help provided by my colleages Simone Knijff, Andy Zachmann and
V al~rie Bolliet during the ASI in various aspects of its functioning. I am especially thankful to
Simone Knijff for the help she provided with the literature research.
Dr. Kristina Rascher was a great help not only during the ASI but also subsequently
with the copy editing of most manuscripts. She also provided extensive notes taken during
the presentations and discussion. I wish to express my profound gratitude to her. My
colleague Pierre Legendre helped with the setting-up of the printing format of the chapters. I
am grateful to Philippe Casgrain for the valuable help he provided with his mastery of
computers in the fmal preparation and printing of the camera ready manuscript of this volume
as well as the indices.
M.A.Ali
vi
CONTENTS
IN1RODUCfION ................................................................................... 1
M. A. Ali
m
TERMINOLOOY BIOLOGICAL RHY1lIMS .............................................. 7
M.A. Ali, Thierry Boujard and Menno P. Gerkemo.
INTRODUCTION TO THE ANALYSIS OF PERIODIC PHENOMENA ................ 11
Pierre Legendre and Pierre Dutilleul
BIOLOGICAL RHYTHMS: MECHANISMS AND ADAPTIVE V ALUES. ............. 27
Menno P. Gerkema
BEHAVIOUR AND RHYTHMS IN FISHES ..................................................3 9
David L.G. Noakes
m
ULTRADIAN RHYTHMS FISHES .........................................................5 1
Robert C. Peters and Robert J. Veeneklaas
TIDALLY-SYNCHRONISED BEHAVIOUR IN MARINE FISHES .......................6 3
R.N. Gibson
LUNAR AND SEMI-LUNAR RHYTHMS IN FISHES ......................................8 3
John F. Leatherland, Karen J. Farbridge and Thierry Boujard
CIRCADIAN BASIS FOR NEUROENDOCRmE REGULATION ....................... 109
A. H. Meier
SLEEP, INACTIVITY AND CIRCADIAN RHYTHMS IN FISH ........................ 127
Stephan Reebs
FEEDING-ENTRAINED CIRCADIAN RHYTHMS IN FISHES ......................... 137
Richard E. Spieler
MELATONm AND ITS EFFECTS IN FISHES: AN OVERVIEW. ..................... 149
Andreas Zachmann, M. Ather Ali, and Jacky Falcon
REGULATION OF THE RHYTHMIC MELATONIN SECRETION BY FISH
PINEAL PHOTORECEPTOR CELLS ........................•............................ 167
Jacky Falcon, Christelle Thibault, Valerie Begay, Andreas Zachmann and
Jean-Pierre Collin
vii
THE RAINBOW TROUT PINEAL ORGAN: AN ENDOCRINE PHOTOMETER ... 199
William A. Gem, Shelley S. Greenhouse, Jeanne M. Nervina,
and Paul J. Gasser
MELATONIN SYNlHESIS BY THE TELEOST PINEAL: AN OVERVIEW .......... 219
WilliamA. Gem, Jacky Falcon, Hilmar Meissl, M. A. Ali
PHOTORECEPTOR ORGANS AND CIRCADIAN LOCOMOTOR ACTIVITY IN
FISHES ......................................................................................... 223
Mitsuo Tabata
PHOTORECEPTIVE FUNCTIONS OF THE TELEOST PINEAL ORGAN AND
THEIR IMPLICATIONS IN BIOLOGICAL RHYTHMS ............................... 235
Hilmar Meissl and Roland Brand.Ytiitter
LIGHT DEPENDENT AND ENDOGENOUS CIRCADIAN CONTROL OF
ADAPTATION IN TELEOST RETINAE .................................................. 255
H.-J. Wagner, M. Kirsch and R.H. Douglas
RETINOHYPO'IHALAMlC PROJECTIONS AND THE SUPRACHIASMATIC
NUCLEUS OF THE TELEOST BRAIN ................................................... 293
Bo 1. Holmqvist, Thomas Ostholm and Peter Ekstrom
GENERAL DISCUSSION AND PERSPECTIVES ......................................... 319
M. A. Ali, R. N. Gibson, J. F. Leatherland, E. Morgan, and R. C. Peters
AUTlIOR INDEX ................................................................................ 325
SYSTEMATIC INDEX .......................................................................... 337
SUBJECT INDEX ............................................................................... 341
viii
INTRODUCTION
M. A. Ali
~partement de biologie
Universi~ de Montreal
CP 6128, Succ. A, Montreal, Qu6bec
H3C 3J7 Canada
The country cocks do crow, the clocks do toll,
And the third hour of drowsy morning name.
King Henry the Fifth, Act IV, Prologue
That fishes have rhythms was known to the oldest of human civilisations. There is
mention of this in the Egyptian, Chinese and Indian legends. A "scientific" mention of this
was made by Aristotle. Fishermen, fish farmers and gardeners who had ponds with fishes in
them, knew about the cyclic nature of various aspects of the fishes' life histories. I thought
that it will be suitable to give a brief historical account of some of the pioneering studies (up
to the late 1930s) in this field, as we know it
The first study of the "modern" type that I have come across was the one by Szymanski
(1914) showing something that many investigations since then have confirmed over and over
again with regard to several aspects of the biology of the goldfish (Carassius auratus). He
demonstrated for the frrst time that the goldf1Sh is a very rhythmic animal, more rhythmic than
the other f1Shes that he investigated in a less profound manner, and that the rhythm persists
even in constant conditions. Szymanski studied the rate of activity using apparatus that he had
assembled. His observations with the goldf1Sh were confirmed a quarter of a century later by
Spencer (1939a) using an actograph that he called an "ichthyometer". Szymanski was a
versatile investigator who studied not only insects and amphibians, in addition to flShes, but
also coined the terms "monophasic" and "polyphasic" to denote animals with one type of
activity during a 24 hr period and those with more than one type of activity. Incidentally,
Szymanski's actograph is still very valid. Five years later Thompson (1919) showed that the
California grunion, Leuresthes tenuis, is a lunar spawner. It takes advantage of unusually
high spring tides associated with new and full moon, to deposit eggs in the sand above the
normal surf zone. This was confirmed by Clark six years later (1925). He studied the same
fish, in the same region, showed the same things and published in the same series! His paper
Rhythms in Fishes, Edited by M.A. Ali
Plenum Press, New York, 1992 1
was longer. Also in 1919, Turner showed that there was a close correlation between the
reproductive cycles of the perch, Perca jlavescens, and the annual seasonal changes. This
was particularly well shown for spermatogenesis. Barney & Anson (1921) found that in the
pot minnow, Gambusia afjinis, from Louisiana there was a relation of water temperature to
the liberation of young and fecundity. About 80% of the annual production of young
occurred before any considerable decline in the water temperature was recorded. Egg
production in this fish was found to be a cyclical phenomenon with the number being
governed by the size and metabolic potentialities of the female for that season and not by
temperature alone. They did not follow light intensities or photoperiods. It was Rowan
(1926) who demonstrated the role of photoperiods in the timing of reproductive functions in
fishes and birds. His pioneering experimental studies were elegant and have retained their
significance to this day.
Ten years after he described the ichthyometer (1929a) and the rhythmic nature of the
goldfish (1929b), Spencer (1939) published the results of a comparative study of eight North
American freshwater species. He concluded that the pumpkinseed sunfish, Eupomotis
(=Lepomis) gibbosus, was diurnal in habit while the mud minnow, Umbra lima, was usually
nocturnal. Young carp, Cyprinus carpio, were nocturnal but became arhythmic as they grew
older, possibly because the pressure of predation is less on larger individuals. He found that
the majority of the species studied i.e. the bluegill, Lepomis pallidus, (=macrochirus), the
rockbass, Ambloplites rupestris, the perch, Perca jlavescens, the largemouth bass, Huro
(=Micropterus) salmoides and the black bullhead, Ameiurus (=lctalurus) melas were
arhythmic. According to Cloudsley-Thompson (1961) this is probably related to the fact that
the physical changes from day to night are far less marked in the aquatic environment than on
land and therefore there is probably less selection pressure in favour of rhythmic activity. In
the light of many recent findings which are being reviewed in this volume, this is a valid but
debatable point.
A Canadian, Helen Battle (1930), the professor of my professor W. S. Hoar, studied
semi-lunar spawning periodiCities and mortality rates in the fourbeard rockling, Enchelyopus
cimbrius, from Passamaquaddy Bay and found that the greatest number of eggs were
collected at the times of new and full moon. A year later (1931), MuZinic published his
observations that herring have two main feeding periods; one from the afternoon until
nightfall, and the other early in the morning. He also noted that they did not feed during
hours of bright daylight. One of the first observations made showing that the coregonids,
which are closely related to the salmonids, are arhythmic was made by Hart (1931), another
Canadian. He followed their movements in the field over prolonged periods and noted that
their active periods are at different times of day or night. The first physiological study that I
am aware of was by Schuett (1934) measuring oxygen consumption of goldfish, under
different conditions of aggregation: single, in small or large numbers. There was no
periodically changing pattern in their oxygen consumption. The well known J. Z. Young
published (1935) the first detailed report on the function of the photoreceptors in the pineal
complex in fishes. This work dealt with the lamprey and showed that there was a very
pronounced daily rhythm of colour change. This rhythm persisted when the lampreys were
kept in constant darkness but in continuous light there was no rhythm in colour change. The
fishes just became very dark and remained that way. Young also showed that this colour
change was not under nervous control but pinealectomy resulted in an interruption of the
rhythm and a constant maximal darkening. On the other hand, hypophysectomy produced a
maximal paling. Thus, this was the frrst defmitive evidence that the endocrine system plays
an important role in the maintenance of a daily rhythm in vertebrates.
2
