139,99 €
Mehr erfahren.
- Herausgeber: John Wiley & Sons
- Kategorie: Fachliteratur
- Sprache: Englisch
Advances in underwater exploration, in situ observation of fish populations, as well as the development of cutting-edge technologies, provide modern insights into behaviors and strategies of fish, whose cognitive abilities have long been underestimated and undervalued. Fish Behavior 2 presents current knowledge about fish biology, ecology and ethology. In light of the most recent scientific work, this book examines topics such as their reproductive behavior and the expression of their personalities. It also addresses issues associated with neurophysiological conditioning of behaviors, in relation to the structural and functional complexity of their brains. This book is intended for researchers, teachers, master s and doctoral students in biology and biogeography, engineers and technicians responsible for the development and protection of natural environments and public aquariums, in addition to aquaculturists, fishermen, environmentalists and ecologists.
Sie lesen das E-Book in den Legimi-Apps auf:
Seitenzahl: 431
Veröffentlichungsjahr: 2020
Ähnliche
Table of Contents
Cover
Prefece
Introduction
1 Reproductive Behavior: Spawners
1.1. The preparatory phase of pre-spawning: the preliminaries
1.2. The phase of realization: couplings and spawning
2 Reproductive Behavior: Parents
2.1. The post-spawning phase: the future of the offspring
2.2. Parental care
3 Remarkable Capabilities
3.1. Aces of ballistics
3.2. Possession of a black box
3.3. Using tools
3.4. Capacity to play
3.5. Artists
3.6. Counting
3.7. Having a personality
3.8. Disguise
3.9. Having a very precise biological clock
4 Neurological and Neuroendocrine Conditioning Requirements
4.1. Experience of stress and suffering
4.2. A question asked about their period of inactivity: are they able to sleep?
4.3. The complexity of their brains: their cognitive abilities
Conclusion
Glossary
Species Index
Summary of Volume 1
End User License Agreement
List of Illustrations
Chapter 1
Figure 1.1. The copulatory organ or gonopod of the male guppy Poecilia reticulat...
Figure 1.2. The caudal sword of the swordtail Xiphophorus sp
Figure 1.3. Adipose fin of a salmonid Salmo trutta fario
Figure 1.4. Opercular expansion imitating the form of an insect (ant) and intend...
Figure 1.5. Male of the priapus Phallostethus cuulong possessing a cephalic clam...
Figure 1.6. The two pterygopods of a shark (top); copulation of sharks (bottom):...
Chapter 2
Figure 2.1. Couple of salmonids (top), where the female “sweeps” the substrate o...
Figure 2.2. Lamprologue Lamprologus sp. carrying with his mouth a snail shell to...
Figure 2.3. Nest of the stickleback Gasterosteus aculeatus made of woven and pas...
Figure 2.4. Couple of wrasses Symphodus cinereus on their nest of algae (source:...
Figure 2.5. Male of the Siamese fighting fish Betta splendens expectorating mucu...
Figure 2.6. Nests of cichlid fish whose morphological characteristics (dimension...
Figure 2.7. Fry of cichlid fish who take refuge in the maternal mouth in case of...
Figure 2.8. Male of the Apogon sp. practicing buccal incubation of clutches (sou...
Figure 2.9. Ventral coupling of seahorses Hippocampus abdominalis: the female de...
Figure 2.10. Male hippocampus performing gestation of eggs in his marsupial pouc...
Figure 2.11. Larvae of the discus feeding on mucous secretions lactated from the...
Chapter 3
Figure 3.1. Archerfish Toxotes sp. projecting a water jet, like a blowgun, in th...
Figure 3.2. Otolith of eel Anguilla anguilla: different growth streaks tracing t...
Figure 3.3. Spawning nest of the Japanese fugu Takifugu rubripes forming a decor...
Figure 3.4. The blenny Aspidontus tæniatus (left), a predator, mimics the color ...
Figure 3.5. Grunions Leuresthes tenuis deposited on a Californian beach during h...
Chapter 4
Figure 4.1. Diagram of a “FishEthoBase” taking into account comparative data bet...
Figure 4.2. Tetras Astyanax mexicanus: hypogeal (top) and epigeal (bottom) form ...
Figure 4.3. Fish encephalon (roach Rutilus rutilus) in dorsal view
Figure 4.4. Larvae of zebrafish Danio rerio (top) and neuronal activity rendered...
Figure 4.5. Facial recognition test (top) in the spotted archerfish Toxotes sp. ...
Guide
Cover
Table of Contents
Begin Reading
Pages
v
iii
iv
ix
x
xi
xii
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
73
74
75
76
77
78
79
80
81
82
83
84
85
86
87
88
89
90
91
92
93
94
95
96
97
98
99
100
101
102
103
104
105
106
107
108
109
110
111
112
113
114
115
116
117
118
119
120
121
122
123
124
125
126
127
128
129
130
131
132
133
134
135
136
137
138
139
140
141
142
143
144
145
146
147
148
149
150
151
152
153
154
155
156
157
158
159
160
161
162
163
164
165
166
167
168
169
170
171
172
173
174
175
176
177
178
179
180
181
182
183
184
185
186
187
188
189
190
191
192
193
194
195
196
197
198
199
200
201
202
203
204
205
206
207
208
209
210
211
212
213
214
215
216
217
218
219
220
221
223
224
225
226
227
229
230
231
Fish Behavior 2
Ethophysiology
Jacques Bruslé
Jean-Pierre Quignard
First published 2020 in Great Britain and the United States by ISTE Ltd and John Wiley & Sons, Inc.
Apart from any fair dealing for the purposes of research or private study, or criticism or review, as permitted under the Copyright, Designs and Patents Act 1988, this publication may only be reproduced, stored or transmitted, in any form or by any means, with the prior permission in writing of the publishers, or in the case of reprographic reproduction in accordance with the terms and licenses issued by the CLA. Enquiries concerning reproduction outside these terms should be sent to the publishers at the undermentioned address:
ISTE Ltd27-37 St George’s RoadLondon SW19 4EUUK
www.iste.co.uk
John Wiley & Sons, Inc.111 River StreetHoboken, NJ 07030USA
www.wiley.com
© ISTE Ltd 2020
The rights of Jacques Bruslé and Jean-Pierre Quignard to be identified as the authors of this work have been asserted by them in accordance with the Copyright, Designs and Patents Act 1988.
Library of Congress Control Number: 2019957600
British Library Cataloguing-in-Publication Data
A CIP record for this book is available from the British Library
ISBN 978-1-78630-537-4
Preface
Fish, our distant cousins, are able to perform a considerable number of daily tasks to survive, having conquered all aquatic environments, in all climates and at all latitudes and depths.
They are the vertebrates most widely used by humans: fisheries exploit stocks of wild fish populations and carry out intensive fish farming, making fish, in number and mass, the most consumed of all vertebrates. They also occupy an important place in aquariology and are used as experimental models in scientific research (second only to mice). However, the general public’s perception remains limited, particularly with regard to their sensitivity, “well-being” and cognitive abilities. Contemporary ichthyologists have a fairly high level of scientific information that can shed new light on the actual behavioral potential of fish.
Observations of animal behavior have long focused on species that are familiar to us and considered worthy of interest, such as birds (parrots, titmice, swallows or wild geese) and, in particular, mammals, especially those to whom we are most closely related (gorillas, chimpanzees, bonobos, etc.) or who live near us (horses) or in our homes (cats and dogs). The enthusiasm they inspire justifies the success of circuses and zoos. Fish, although they arouse a certain curiosity, especially among anglers and aquarists, rarely receive the attention they deserve, being reduced to the unflattering status of “inferior vertebrates”, beings who seem devoid of language, memory and apparent sensitivity. It is an unflattering and erroneous public perception, linked to the fact that we communicate little with them, separated as we are by such distinct natural environments.
Scientists, through observations and experiments published in credible international journals and from whom the authors of this book take their inspiration, bear witness to the surprising abilities of fish. Abilities that are not so far removed from those of other vertebrates, and even humans with similar characteristics because they are derived and inherited from these “fish ancestors”.
This book consists of two volumes that provide data of 630 species cited, originating from more than 1,500 bibliographical references. It provides new information on recent achievements in the field of ichthyology. These data reveal that our distant cousins are well endowed with cognitive abilities and a potential for memorization and innovation that explains their remarkable capacity to adapt to often difficult environments.
“Ordinary” fish are capable of doing extraordinary things. Some of them are not only great travelers able to orient themselves using the sun and navigate through terrestrial geomagnetism, but are also capable of adopting sophisticated behaviors. Some are subtle hunters or breeders who call upon collective strategies, clever architects and builders of complex nests designed to protect their eggs, courageous fighters willing to sacrifice their lives to defend their offspring and cooperative beings united with a shared goal or producing descendants. Some are even talented imitators anxious to perhaps deceive their partners or predators, Machiavellian strategists, clever courtiers, flamboyant seducers and great lovers. They also demonstrate memory and calculation skills, and the ability to play, use tools and even indulge in artistic creation. Finally, they can sometimes even be good models that can inspire advances in technology and human health.
Jacques BRUSLÉ
Jean-Pierre QUIGNARD
January 2020
Introduction
Those of you who are interested in the natural world and are curious to better understand animal behavior, in all its capacity to surprise and be misunderstood, will probably be satisfied to be able, thanks to this book, to learn what fish really are. They deserve much better than their current, hardly flattering, status as “inferior vertebrates”.
Advancing knowledge in the field of fish ethology requires abundant scientific literature consisting of numerous publications in international journals that constantly provide new data to contribute to enriching our view of the behavior of these “conquerors of the aquatic world”, who are rich in their biodiversity and never cease to amaze us.
The authors of this book, academics who have devoted their careers to icthyological studies, have made extensive use of the most recent data in order to present a broad overview of the knowledge acquired in the field of behavior related to fish feeding, protection, social interrelationships and reproduction. This is based on the most representative and original examples cited among the 30,000 species currently listed, but only a few of them have given rise to field observations and laboratory experiments. Recent technological advances in human penetration of the underwater world (submarines, bathyscaphes, etc.) and in situ observation of fish (video cameras, acoustic markers, satellite telemetry, etc.), as well as laboratory data (samples, video images, etc.), have led to the development of new technologies. Those acquired through the use of advanced technologies applied to fish (radioactive isotopes, magnetic resonance, genetic sequencing, etc.) have greatly contributed to providing a modern perspective on their remarkable strategies and surprising behaviors.
The considerable progress made in the field of neurophysiology, as regards their sensory perception, communication, memory, innovation and so on, suggests that they are so sensitive to stress and pain that they deserve to be treated with more care than they usually are. Their need for “well-being” is as important as ours or that of our cats and dogs.
Acknowledgments
The authors would like to express their sincere thanks to all those who helped them by generously providing the original photos and figures to illustrate this book.
1Reproductive Behavior: Spawners
Fish respond to their “reproductive duty” and their reproductive needs by adopting a large diversity of adaptive behaviors in relation to constraints exerted by environmental conditions. In fact, acts of reproduction are highly variable in time: in terms of duration and position in the annual cycle, they spread over a whole year in hot regions or thermally stable regions such as the abysses, reduce to a single season in temperate and cold regions, and are more often limited to a few months or sometimes even reduced to a few days. They also vary greatly in space: in the same area as their habitats or in more or less distant habitats, which require reproductive migration. These behaviors differ from one family to another and from one species to another. Fish have shown remarkable inventiveness in succeeding in what constitutes an essential part of their existence: to mate and produce quality offspring with an optimum survival.
It should be noted that, among the initial phases of fish reproduction, those of emission, control and management of gametes show a great diversity of original behaviors. Potential fertility rates are strongly variable: there are 300 million oocytes in the female of the ocean sunfishMola mola, while there are only 3,000–4,000 oocytes in the common gobyPomatoschistus microps. Knowing that their respective masses are 1 tonne and 2 g, the reproductive effort is thus 1,500–2,000 oocytes per unit of mass (gram) in the former and 2,000 oocytes/g in the latter. In comparison, males are generally very productive in gametes: 27 billion sperm per milliliter of semen in the pikeEsox lucius. Such gametic production is justified by the fact that the aquatic environment is a great “devourer” of sexual cells, and subsequently eggs, due to the rapid dilution of sexual cells which reduces their chances of being fertilized, their high mortality due to osmotic shock, in both fresh and salt water, as well as predation by various species of oophagous predators. As a result, very few of these gametes (approximately 0.001–0.01%) will give birth to a new generation.
Two major strategies of bisexual reproduction are often seen: one is based on a “numbers effect” and anonymity of spawners, which is at the mercy of chance for the meeting of gametes and the survival of clutches, and the other is a “quality effect” and personalization of gametes based on sexual selection, which is supposed to operate for the benefit of the “best”, in order to ensure optimal reproductive success.
It is the “populational” strategy based on the vagaries of the encounter of gametes within an anonymous “spermato–oocyte cloud” that is practiced by the sardineSardina pilchardus and the Atlantic bluefin tunaThunnus thynnus, among which the concept of “filiation” does not apply (fish born to an unknown father and mother). However, despite the fact that this “spawning in open water” results in a considerable waste of gametes, and then of eggs, it shows itself to be rather successful if we are to judge by the number of the species concerned and the density of the schools of pelagic fish (“blue fish”) that successfully practice this.
In contrast, the strategy of forming couples tends to aim at a certain “personalization” of spawners who “select” each other based on their own supposed qualities of “best partners” who are able to offer “the best genes”, conditions for the best perspectives for reproductive success. However, such a “safe” management of gametes, although ideal in principle, is subject to various vagaries linked to the intervention of sneakers* who practice “parasite fertilization” (Volume 2, section 1.2.1), to the cases of coercive couplings (Volume 2, sections 1.2.3 and 1.2.4) or to the errors of judgment by partners whose couplings are harmful at the level of genetics and/or immune systems (consanguineous matings and hybridizations which are considered to be “genetic pollution” (Volume 2, section 1.1.5)).
Original variants of sexuality involve hermaphroditic species* (Volume 2, section 1.2.9): either synchronous hermaphrodism as in the painted comber Serranus scriba or successive hermaphrodism, protandrous* as in the gilthead bream Sparus aurata, protogynous* as in the Nassau grouperEpinephelus striatus, and species whose sex change is reversible as in the dwarf hawkfishCirrhiticthys falco (Volume 2, section 1.2.10) and species which practice parthenogenesis* (Volume 2, section 1.2.12), gynogenesis* as in the Prussian carpCarassius gibelio (Volume 2, section 1.2.12) and exceptionally androgenesis* as in the spiny dogfishSqualius acanthias (Volume 2, section 1.2.12). All these, often very subtle, variations of gametic production and fertilization reveal a certain “inventiveness”, which is not only anatomical but also physiological and behavioral.
One form of “progress” for reducing gametic waste concerns the tactics of oocyte immobilization: for females, this consists of setting their oocytes on a rocky substrate rather than dispersing them in open water (such as the ruffeGymnocephalus cernuus), burying them in a sandy and gravelly mineral substrate (such as the brown troutSalmo trutta) and fastening them onto vegetal supports (such as the big-scale sand smeltAtherina boyeri). For the males of these different species, this consists of “spreading at random” their semen in the immediate vicinity of clutches, where the waste of sperm is less costly in energy than oocyte production. In all these cases, the spawners abandon their eggs and then their larvae.
An additional step in securing gametes and then eggs and larvae consists of the building of nests by males (Volume 2, section 2.1.1), which leads to a cavitary containment of gametes and the provision of parental care by both partners of the couple or by the males only (Volume 2, section 2.2.1). The “ultimate” search for gametic and embryonic protection is reached with incubation in the mouth such as that practiced by the cardinal fishApogon sp. (Volume 2, section 2.1.2) and especially with gestation in incubator pouches, as in male seahorsesHippocampus sp. (Volume 2, section 2.1.4) and in the genital tracts of females, as among elasmobranchs and various teleosts (Volume 2, section 2.1.4). Hydroclimatic vagaries and threats of predation are reduced to the extent that parental investment is increased. If females are more invested in these “conservational” concerns and if “maternal effects” are often considered significant (Volume 2, section 2.2.1), males are often effectively involved in the achievement of optimal conditions of survival of gametes, eggs and subsequently larvae, and “paternal effects” are far from negligible (Volume 2, section 2.2.1).
Thus, if many species adopt populational strategies, reproductive strategies of fish may also reach a high level of “personalization” associated with a common concern for reducing gametic waste and sometimes larvae (viviparity), which reflects the fact that nature has explored, at all times and in all places, the various “pathways” which have been available to ensure the diverse reproductive successes of fish.
Bibliography: Acad.Sci.Lett.Montpellier, 2018, 49: 12 pp, J.Fish Biol., 2006, 69: 1-27.
This “mating” period includes a number of successive steps under neuroendocrine control that are correlated with environmental factors: the lunar cycle, the solar cycle, water levels, tidal movements, thermal and haline variations.
The reproductive act may be unique in the life of the fish (semelparity*1), as in short-lived fish such as the sand gobyPomatoschistus minutus, and also among long-lived species such as the eels Anguilla anguilla and A. rostrata. In contrast, among long-lived species such as the carpCyprinus carpio, the act of egg-laying may be repeated several times during the course of their life (iteroparity*), such as for most species, whether they are freshwater or marine.
The reproductive scenario can be broadly divided into four major phases:
1) an anticipatory phase during which, in reproductive migration, the population of mature age moves from its feeding habitat to spawning grounds. These zones are hydrologically favorable: in terms of temperature, salinity, quality of substrates, quantity of potential food. Other factors may also intervene, so the list is indefinite: for example, the protection and development of clutches, and then of larvae, to ensure greater reproductive success. In contrast, some particularly far-sighted species build spawning nests to host their offspring before even going in search of mating partners;
2) a preparatory or
pre-spawning
phase which features the end of gonadal maturation and selection of sexual partners, appealing to seduction and/or force;
3) a phase of realization or
spawning
and fertilization during a more or less intimate encounter of the two sexes and which gives rise to a coupling, with or without copulation, and a mixture of their respective gametes, followed by fertilization with the ejaculation of males and ovulation of females. Fertilization may be extracorporeal in open water or intracorporeal in the genital tract of the female (oviparity*, viviparity) or in the marsupium* of the male (paraviviparity);
4) a terminal or
postspawning
phase which relates to the fate of fertilized oocytes, then the eggs and then the larvae that may develop in open water, in the genital tracts of females and in other body cavities (mouth, gill chamber, marsupium of male syngnathids, etc.), or in nests that are sometimes subject to parental care intended to promote the survival of the offspring. They may also entrust custody to other animals (mollusks, crustaceans, ascidians, etc.). Most spawners abandon their offspring and return to their feeding habitats, and sometimes even die. Others remain at the spawning site and provide parental care to their offspring.
The search for sexual partners, the success of couplings, the production of eggs and larvae and subsequently their protection thus constitute the major tasks. These tasks depend on the development of behaviors, often elaborate and generally complex, intended to enable the greatest reproductive success, both qualitative and quantitative.
Reproductive migrations (Volume 1, section 2.2) involve movements of spawners of varied magnitude and variable duration according to the species. They are particularly large among amphihaline* fish such as the Atlantic salmon of the genus Salmo and the Pacific salmon of the genus Oncorhynchus, the brown troutSalmo trutta, the lamprey of the genus Petromyzon, the sturgeonAcipenser sp., the shadAlosa sp. and the eelsAnguilla sp. whose populational movements, precise in time and determined in space, have not ceased to impress observers. They also concern marine species such as tuna, sharks, etc. whose holobiotic* movements, although apparently less spectacular, are no less important. After spawning, the migration of spawners on an outbound journey is followed or not by return migration.
The foresighted behaviors of spawners concerned with the survival of their offspring have led some species, especially freshwater species such as sticklebacksGasterosteus sp. as well as marine species such as the wrasses, to build laying nests (Volume 1, section 2.2.2.1) before even mating and proceeding to the act. Such nests are often a determining factor in the behavior of females who are led to choose a partner (Volume 1, section 3.7; Volume 2, section 1.1.1).
1.1. The preparatory phase of pre-spawning: the preliminaries
1.1.1. Selection of sexual partners
The behaviors conditioned by the exchanges of communication signals (visual, olfactory, auditory, tasting and/or electric) have been discussed in Chapter 3 of Volume 1.
1.1.2. Seducers
1.1.2.1. The requirements of sexual selection
The choice of sexual partners by females, in the framework of strict sexual selection (Volume 1, section 3.7), forces males to adopt forms, display colors and practice behaviors which are as ostentatious and spectacular as possible in order to attract their attention and earn their favors. They must often “make themselves beautiful” for a chance to please the females. Thus, these males adopt colorful patterns, which is considered as secondary sexual characteristics controlled by the androgenic hormone 11-KT, in contrast to females who, in general, only display drab grayish or brownish color patterns which make them less detectable by predators. Various ornamentations are thus exhibited by males under the gaze of females whose visual acuity is such that they are able to recognize the best among them.
Bibliography: J.Fish Biol., 2006, 68: 1636-1661, Mar.Ecol.Prog.Ser., 2014, 514: 207-215 & DOI:10.3354./meps11032
1.1.2.2. A wide range of colorful patterns
During reproductive periods, the vivid and even flamboyant colors of males are an ornamentation with the value of a sexual signal of recognition. They reflect a quality that is required by females who tend to choose the more colorful of their suitors judged to be, a priori, the best bearers of good genes which their descendants will inherit.
Teleosts have several types of pigment cells: chromatophores* (melanophores*, erythrophores, xanthophores, cyanophores, leucophores, iridophores, etc.) present in their skin (epidermis, dermis) and containing a variety of colored pigments (melanin, carotenoids* such as astaxanthin, canthaxanthin, zeaxanthine and β-carotene), pteridines (pterins or flavins) or reflective crystals of purine. The carotenoid pigments* involved in red, orange and yellow colorations, pigments which are not synthesized de novo but derived from their algal diet, possess antioxidant and immunostimulatory properties which play a protective role in cells and tissues. The other pigments – the melanins responsible for black, brown and gray colorations, and pterins inducing red, orange and yellow colorations – also have antioxidant functions and contribute to the fish’s immune defenses.
Carotenoids* and melanins are the most commonly found pigments in the coloration of fish, the former acting as indicators of the physical condition of their owner in direct relation to its feeding activity, while the latter has an indicator value for the dominant–subordinate social status. These chromatophores* have the ability to alter the concentration or the spread of their intracellular colored pigments in cells possessing contractile dendrites*, in order to modify the intensity of certain colors under hormonal control: adreno-adrenocorticotropic hormone (ACTH) and α-melanocyte-stimulating hormone (α-MSH).
Bibliography: Anim.Behav., 2005, 69: 757-764 & OI:10.1016/j.anbehav.2004.06.022
1.1.2.2.1. Red
The males of the minnowPhoxinus phoxinus present vivid and spectacular abdominal red colors, corresponding to a concentration of carotenoid pigments* which constitute honest signals of high quality: best fitness*, greater vigor and better swimming performance. Reproductive success is achieved by the most strongly colorful individuals that are free of parasitic infestations by the nematod Philometra ovata, which cause fading of the color pattern due to a decrease in the level of carotenoids*. It is also achieved by those who are bearers of reproductive tubercles which diffuse encouraging olfactory cues for females who have previously acquired a certain olfactory experience.
The males of the threespine sticklebackGasterosteus aculeatus also exhibit, under the gaze of the females, a nuptial color pattern in the form of flamboyant red colors linked to carotenoid pigments* (astaxanthin, β-carotene) originating in their food (gammarids). β-Carotene accumulates in the skin of the chin and the sides during the spring, in order to reach its maximum concentration at the beginning of the reproductive period, in April–May. This is precisely the time where the retinas of females, the opsin of their retinal* cones*, are the most sensitive to red radiation, which enables them to select the most richly colored males. A phenotypic plasticity in the expression of retinal opsin* enables a remarkable visual adaptation to different conditions of brightness: the clear or colored waters of lakes constitute a visual background. These males, which are rich in carotenoids* with antioxidant properties, have strong capabilities for fertilizing oocytes and thus show high rates of reproduction. This color shows seasonal variations, which is highest at the beginning of the breeding season (spring–summer) and then reduces quickly as soon as the mating ends when males become guardians of nests (Volume 2, section 2.2.1) and are no longer concerned with pleasing. In Alaska, guardianship of nests and protection of clutches against groups of cannibals have such a high energy cost that the intensity of coloration decreases over time. It should be noted that these males may “fade” if they are parasitized by the cestode Schistocephalus solidus, with the color of their eyes then becoming the object for determining the choice of females.
The males of the guppyPoecilia reticulata use the same type of color signals to temporarily display themselves before the eyes of females. The orange-red color is the most common feature used by the males of a large number of species, associated with black areas of melanin and iridescent reflections. Present in most of the world populations of this small poeciliid, it has been judged universal. Such carotenoid pigments* (β-carotene) find their origin in microalgae such as Dunaliella sp., in which they represent more than 10% of dry mass and are consumed by these males. Those who have the largest feeding activity show the most intense color patterns. These pigments that have antioxidant properties that are capable of reducing oxidative stress by neutralizing free radicals* confer on these spawners a health value which is very much appreciated by females. The latter thus give to the world a progeny made of a greater number of males than females (85♂ vs. 45♀); these dominant males are therefore as beautiful and as seductive as their fathers.
Red ornamentation, by far the most widespread, not only provides males with chances of success in love, but also increases their risk of predation, because predators do not fail to recognize the sign of a good meal in the good health of these males. Hence, when predators are present in their habitat, these males reduce the intensity of their coloring.
Females of the guppy are more sensitive to the size of the orange-colored area than to the intensity of the color itself. Male guppies who possess a large colored spot produce abundant and high quality sperm (in terms of swim speed and longevity), indicating a fine progeny. The quality of the sperm is determined by the richness of the food in polyunsaturated fatty acids (PUFAs) and carotenoids*. Some male guppies experience high reproductive success that can be measured by the number of genetically identifiable descendants. Various characteristics other than color and size, for example, explain the multiple paternities of these beautiful males. The colors of male guppies can give rise to a wide polychromatism ranging from drab color patterns comparable to those of females to brilliant red, blue, yellow, etc., often accompanied by transverse black bands which accentuate the contrasts and mark out shapes of original colors among Poecilia immaculata and P. parae in Guiana. These colors, which play an important role in sexual selection, enable increases in the biodiversity of various progenies. More common colors are less valued and new chromatic combinations resulting from mutations and crossings provide greater reproductive success. Various predation pressures exerted by sympatric* predators select survivors who are likely to be all the rarer, the more strongly colored, and therefore optically identifiable, they are. Thus guppies, originating in Trinidad in Central America and widely introduced to natural waters around the world, have given rise to diversified populations, characterized by a large polymorphism of colors in males: red, orange and yellow color patterns due to carotenoids*, with black spots of melanin and reflections which are more or less iridescent under UV light, which explains their considerable success in aquaria.
The red nuptial color pattern of male bitterlingsRhodeus amarus is a signal of quality for the benefit of females, since the intensity of this coloration relates to large testes and the production of a large number of sperm. Such spermatic potential is an important criterion which is very useful for females who fear seeing their oocytes poorly fertilized by a partner subject to a limitation of sperm or, worse, possible infertility. A fertile male is a strong guarantee of greater reproductive success for a female who is always anxious to produce beautiful descendants. The male of the dwarf gouramiTrichogaster lalius (formerly Colisa lalia), an osphronemid, is distinguished by an ornamentation of bright red color based on a diet rich in astaxanthin, a synthetic carotenoid* pigment used in aquaria.
Note that the color red is considered to be sexually very attractive in very many animal species as well as among the human species (see The Woman in Red, Gene Wilder, 1984).
Bibliography: Anim.Behav., 2008, 75: 1041-1051 & DOI:10.1016/j.anbehav.2007.08.014, 2009, 77: 1187-1194 & DOI:10.1016/j.anbehav.2008.12.032, Behav., 2007, 144: 101-113, 2011, 148: 909-925 & DOI:10.1163/000579511X584104, Biol.Lett., 2007, 3: 353-356 & DOI:10.1098/rsbl.2007.0072, 2010, 6: 191-193 & DOI:10.1098/rsbl.2009.0815, Ecol.Freshwat.Fish, 2008, 17: 292-302 & DOI:10.1111/j.16000-0633.2007.00279.x, Env.Biol.Fish, 2014, 97: 209-215, Ethol., 2010, 116: 895-903 & DOI:10.1111/j.1439-0210.2010.01802.x, 2013, 119: 605-613 & DOI:10.1111/eth.12102, Evol.Ecol., 2007, 21: 601-611 & DOI:10.1007/s10682-006-9138-4, J.Compilation Eur.Soc.Evol.Biol., 2006, 19: 1595-1602 & DOI:10.1111/j.1420-9101.2006.01117.x, J.Exp.Biol., 2013, 216: 656-667 & DOI:10.1042/jeb.078840, J.Fish Biol., 2007, 70: 165-177 & DOI:10.1111/j.1095-8649.2006.01292.x, 2015, 86: 1638-1642 & DOI:10.1111/jfb.12661, Zool.Sci., 2007, 24: 571-576 & DOI:10.2108/zsj.24.571
1.1.2.2.2. Blue
During the 1980s in Japan, as a result of mutations, males of the guppyPoecilia reticulata with blue coloring were discovered. The evolution of this original color affects the size, shape and intensity of the areas colored in blue to which females are visually very sensitive, to the point of having made a decisive criterion of choice of sexual partners. Blue has become attractive to the detriment of the red and orange colors of all the other populations in the world. Females are attracted by the bluest individuals, who also find great success with aquarium keepers. These blue frequencies of short wavelengths are easily transmitted in clear and transparent waters, enabling these guppies to colonize new waters and not be limited to turbid aquatic environments which favor the transmission of red radiation with longer wavelengths. It is necessary that females of these populations show new preferences for this color pattern for it to establish itself as the reference color for their romances and become, thanks to generalized natural selection, the single color of natural populations.
The males of the ornate rainbow fish or Australian dwarf perchRhadinocentrus ornatus, a freshwater melanotaeniid, display two color patterns: one is blue, which is shown by the majority (more than 80% of the population), and the other is red, which is rarer (18%). A female preference for mating with males of blue phenotype* should lead to the gradual disappearance of those of red phenotype* and the establishment of generalized monochromatism*. This has not occurred, and non-rigorous sexual selection enables females to not comply with the preference model, thus ensuring the persistence of a dichromatism* that affects one-fifth of the population.
Bibliography: Proc.Roy.Soc.B, 2018, 285 & DOI.org/10.1098/rspb.1335, Anim.Behav., 2010, 80: 845-851 & DOI:10.1016/j.anbehav.2010.08.004
1.1.2.2.3. Black
The black nuptial coloration of melanin in the males of the brook sticklebackCulaea inconstans in North America apparently plays no role in sexual selection, although it exercises a function of strengthening contrasts in the tea-colored waters which it often encounters in this geographical area. The synthesis of this pigment, melanin, is under genetic control. It does not reflect a physiological state as expressed by the carotenoid pigments*, but has the indicator value of social status, constituting a signal of expression of behavioral dominance. It is also a signal of aggression, especially when these males guard their nests (Volume 2, section 2.2.1).
Bibliography: Anim.Behav., 2006, 71: 749-763 & DOI:10.1016/j.anbehav.2005.07.016, Behav., 2006, 143: 483-510, Funct.Ecol., 2010, DOI:10.1111/j.1365.2010.01781.x
1.1.2.2.4. Blue-green
The male of the blue-throated wrasseNotolabrus tetricus displays a brilliant blue-green coloration of the most beautiful effect due to the presence of biliverdin, a pigment derived from the degradation of bile pigments. In fact, it has inherited this metabolic pigment originally accumulated by the female at its sex change. This species is protogynous* (Volume 2, section 1.2.9) and the female is brown in color.
Bibliography: J.Fish Biol., 2006, 68: 1879-1882 & DOI:10.1111/j.1095-8649.2006.01033.x
1.1.2.2.5. Iridescence
The cheeks of the males of the bluegillLepomis macrochirus and sticklebackGasterosteus aculeatus strongly influence their attractiveness, determining the choice of females measured by the number of females who visit their nests, the number of eggs laid and the time they spend in the nest.
Bibliography: Ethol., 2010, 116: 416-428 & DOI:10.1111/j.1439-0310.2010.01755.x, J.Exp.Biol., 2013, 216: 2806-2812 & DOI:10.1242/jeb.0874889
1.1.2.3. …and also seductresses
The red color of seduction is not a nuptial exclusivity of males. Females of the pink-belly wrasseHalichoeres margaritaceus also show nuptial color in the form of a red belly which, associated with body-swaying behavior, is intended to alert males to their availability for spawning. The largest, with the largest colored spots, benefit from the greatest reproductive success.
Among the Arctic charSalvelinus alpinus, the two sexes are bearers of a red abdominal color pattern rich in carotenoids*, which is more intensely colorful and more brilliant in males than in females. The females invest their pigment potential for the benefit of their eggs, which are thus assured of a better quality of survival and hatching, related to a greater antioxidative potential. They thus gift their carotenoids* to their offspring, while males prefer to selfishly allocate them to their personal adornment. Studies of human ethology have shown that red color has the value of a sexual signal for women, who use this color to increase their attractiveness. In this respect, they copy the females of primates, whose red genitals play a comparable role.
A yellow spot on the belly of the females of the Adriatic dwarf gobyKnipowitschia panizzae constitutes a signal that is very attractive to males, regardless of the size of the female, but especially if it is large in size.
A reversal of roles (Volume 2, section 1.1.4) is seen among syngnathids, among whom there are females who make a charm offensive to seduce the males. Among the Gulf pipefishSyngnathus scovelli, sexual selection takes place among settled populations within marine coastal eelgrass beds, in which males, generally less numerous than females, observe the seductive behaviors of potential partners who, equipped with attractive colorful patterns, move by swimming above the seagrass beds. These “dancers of the sea” seek to attract the attention of males in order to choose among them the most beautiful and also the strongest, a priori the best spawners. Therefore, these secondary sexual and behavioral characteristics assume, among these pipefish as well as among seahorses who are their near relatives, a greater energy investment by females, while the males save their energy to better cope with their subsequent constraints, which consist of ensuring the internal brooding of eggs in their incubation pouch; such an effort is equivalent to actual gestation (Volume 2, section 2.1.4).
Bibliography: Behav., 2015, 152: 705-725 & DOI:10.1163/1568539X-00003250, Behav.Ecol.Sociobiol, 2008, 62: 521-528 & DOI:10.1007/s00265-007-0476-1, Ecol.Freshxat.Fish, 2008, 17: 328-339 & DOI:10.1111/j.1600-0633.2007.00286.x, Ethol., 2013, 119: 692-701 & DOI:10.1111/eth.12110
1.1.2.4. Seasonal sexual dichromatism
The adoption of nuptial colors described in the previous examples is only seen among one gender: either the male or the female. In contrast, among the kelp* bassParalabrax clathratus, both males and females who are monochromatic* for a large part of the year change their colors during the breeding season (from April to October); they adopt colors which are distinct from their adult color pattern during sexually dormant times and which differ from one another. Males acquire black color patterns with white dots and a bright orange snout, while females acquire black color patterns without white dots, which facilitates intersexual recognition during courting and spawning behaviors, at sunset (6–10 p.m.), in low-light conditions and in groups of 3–20 individuals.
Bibliography: Bull.South.Calif.Acad.Sci, 2005, 104: 45-62, J.Fish Biol., 2006, 68: 157-184 & DOI:10.1111/j.1095-8649.2005.00886.x
1.1.2.5. Instant seductive power
Most nuptial color patterns require long metabolic preparation over several months to reach their maximum expression at the time of the mating season and to be maintained during the entire period of reproduction that lasts from several days to several weeks and/or several months. However, certain chromatic modifications are much more ephemeral, which are only expressed during intersexual meetings, with a one-time role of attraction during the few minutes or hours of courtship behavior, as in the zebrafishDanio rerio among whom the dark transverse bars appear briefly, then disappear by fading, in relation to the behavioral variations of males. Rapid changes of color also occur in response to changes in the color of habitats in order to escape the gaze of predators, becoming more or less light and/or dark based on the environmental color, as well as when forming schools in order to avoid attracting attention by adopting the same color as all its species-mates to dilute the risk of predation (Volume 2, section 2.3), as in the guppyPoecilia reticulata. Regardless of the energy cost of this change in color, it is always advantageous, for these “chameleon fish”, to adopt inconspicuous behavior.
Bibliography: Anim.Behav., 2005, 70: 1063-1066 & DOI:10.1016/j.anbehav.2005.02.005, Ethol., 2012, 118: 1208-1218 & DOI:10.1111/eth.12027/pdf, Fish Fish., 2010, 11:159-193 & DOI:10.1111/j.1467-2979.2009.00346.x
1.1.2.6. Other sexual ornamentation
1.1.2.6.1. Eye color
Females of the sticklebackGasterosteus aculeatus are sensitive to the color patterns (red-colored throats) of males and are also strongly attracted by their eyes, which become blue and iridescent at the time of reproduction, which constitutes an important signal in courtship behavior; the red color of their throat reinforces the contrast of their eyes. The diameter of the iris, of red coloration in male bitterlingsRhodeus amarus, the development of which is among their greatest criteria of dominance, plays an attractive role in females and participates in sexual selection.
Bibliography: Anim.Behav., 2006, 71: 307-313, J.Exp.Biol., 2013, 216: 2806-2812 & DOI:10.1242/jeb.084889
1.1.2.6.2. The size of the gonopod
Among other characteristics attractive to females of the guppyPoecilia reticulata are the size of the gonopod, the organ of mating and the intromission of semen, in the form of spermatozeugmas*, into the genital tract of females. Its length of about one third of that of the body is a selective trait that explains a large part of reproductive success, as shown in a study of the progeny of males.
Figure 1.1.The copulatory organ or gonopod of the male guppy Poecilia reticulate. For a color version of the figures in this book, see www.iste.co.uk/bruslé/fish2.zip
Bibliography: Biol.Lett., 2013, 9 & DOI:10.1016/rsbl.2013.0267
1.1.2.6.3. A sword
Male swordtails of the genus Xiphophorus, such as X. helleri, possess a “sword” resulting from the association or grouping of the lower rays of their caudal fin. This constitutes a signal of good physical condition and masculine aptitudes, as well as a criterion of deterrence in inter-male rivalry and of selection by females who attentively choose a mating partner with the longest sword. This characteristic, associated with a vivid red color in a localized band on its flanks, constitutes for them a sign of virility. A rapid change, in less than 2 min, of color (from black to red) of this colored strip shows the status of the dominant male, which is quite distinct from that of subordinates* who are males with a black band.
Figure 1.2.The caudal sword of the swordtail Xiphophorus sp
In addition, this signal of dominance towards rivals offers the advantage of imposing submission on the latter, thus avoiding energy-costing conflicts such as physical assaults. This secondary sexual characteristic, if it provides advantages in terms of reproductive success, also presents a cost, in the form of a handicap to locomotion. It decreases the swimming speed because of an unfavorable hydrodynamic drag, which increases the risk of predation. Thus, laboratory analysis of the swimming performance of X. montezumae shows that if the sword is excised, the propulsion speed increases by 21%. However, other research on the supposed handicap on the swimming behavior of swordtails tends to show that this exaggerated adornment has only a minor impact on the fish’s swimming system, and does not impose a locomotive penalty as previously assumed. The removal of the organ induces a change in the amplitude of beats of the tail, but not their frequency, and physiological mechanisms are presumed to compensate for the possession of this cumbersome structure.
Surprisingly, the natural preference of females for males carrying long swords can be manipulated by the social environment, which shows its lability. In fact, females of X. helleri who are exposed from their youth only to the presence of males with short swords retain an attraction for this phenotype* and mate with them without problem Only experienced females, having a certain familiarity with males with long swords, are able to make the right choices. Sexual requirements relating to male ornamentation are not confined to the size of their sword. The selection of partners is more complicated when attractiveness is based on multiple visually detectable components, as the presence of three colored bands on the sword of X. helleri, which is shiny and contrasting – two black bands and one band of green or orange –, serves as amplifiers of visual signals and strengthens their attractiveness. The loss of a black band renders the male inferior.
The color patterns of the males of the delicate swordtailX. cortezi serve as a signal of attractiveness for females, particularly the presence of dark bands which are symmetrical or asymmetrical according to the individual as a result of a lateralization phenomenon. The oldest females show a clear preference for males showing asymmetric bands, while young females are less discriminating. These males show off this characteristic during their courtship behavior by performing a figure-eight swim, in order to be better appreciated. A preference for this type of male means that this genetic characteristic is selected for in the population, so that the number of asymmetric males therein becomes increasingly large. Young females of X. malinche can also be distinguished by their preference for symmetric males (6 bars to the right and 6 bars to the left), while large females choose asymmetric ones (6 right and 8 left). Virgin females, regardless of their age, are indifferent to the size of the swords of males. This results in an advantage for them, that of being able to mate with all the types of males present. The preferences of older females do not manifest until later, with a certain degree of experience.
The development of the sword among the swordtails is genetically determined, under the control of several genes, principally MSX, which is common to all poeciliids and associated with the secretion of the androgenic hormone testosterone. In fact, juveniles do not possess swords; the expression of the gene is under-regulated during this juvenile phase by a deficit in the androgenic hormone. If most male swordtails are distinguished by their caudal sword, a Mexican species, X. continens, presents the originality of not possessing such an organ, due to a relaxation of sexual selection. Females are neither attracted by the size of males nor by the designs on their color patterns, while in turn these males give up on courtship and refuse to attack other male rivals, with no competition taking place.
Bibliography: Anim.Behav., 2005, 69: 1415-1424 & DOI:10.1016/j.anbehav.2004.08.013, 2006, 71: 129-134 & DOI:10.1016/j.anbehav.2005.05.004, 135-140 & DOI:10.1016/j.anbehav.2005.04.007, 2008, 75: 1981-1987 & DOI:10.1016/j.anbehav.2007.12.008, 76: 271-276 & DOI:10.1016/j.anbehav.2008.03.008, 2014, 87: 39-44 & DOI:10.1016/j.anbehav.2013.10.001, Behav. 2005, 142: 283-303, 2009, 146: 727-740 & DOI:10.1163/156853909X446172, Biol.Lett., 2006, 2: 8-11 & DOI:10.1098/rsbl.2005.0387, 2007, 3:144-146 & DOI:10.1098/rsbl.2006.0608, Ethol., 2009, 115: 812-822 & DOI:10.1111/j.1439-0310.2009.01676.x, Evol.Dev., 2003, 5: 466-477, Funct.Ecol., 2014, 28: 924-932 & DOI:10.1111/1365-2435.12222, J.Fish Biol., 2007, 70: 1161-1170 & DOI:10.1111/j.1095-8649.2007.01379.x, 2012, 80: 722-727 & DOI:10.1111.1095-8649.2011.03212.x
1.1.2.6.4. Lower jaw and adipose fin
Male salmonids have these sexual characteristics which express their dominant status in social interactions: a hooked lower jaw or hooknose* and a developed adipose fin, such as among the Arctic charSalvelinus alpinus. These characteristics feature at the same time in inter-male competition and in the sexual selection made by females.
Figure 1.3.Adipose fin of a salmonid Salmo trutta fario
Bibliography: J.Fish Biol., 2011, 79: 107 & DOI:10.1111/j.1095-8649.2011.0387.x
1.1.2.6.5. A badge
Males of all species are constantly trying to please females during the mating period, and seek all means to attract their attention so as to positively guide the females’ choice towards them, among all the contenders. Males of the long ear sunfishLepomis megalotis are equipped with an opercular expansion which they wave, like a flag, in front of females who, being curious and interested, show interest in this ornament. Males whose flags are the largest thus enjoy the greatest reproductive success. The swordtail characinCorynopoma riisei also uses an opercular expansion, imitating a terrestrial insect, that he displays to the gaze of females and which operates as a lure. Hungry females are attracted and become victims of this subterfuge (Volume 2, section 3.9).
Figure 1.4.Opercular expansion imitating the form of an insect (ant) and intended to attract females who consume this prey in the male of the swordtail characin Corynopoma risei
Bibliography: Curr.Biol., 2012, 22: 1440-1443 & DOI:10.1016/j.cub.2012.05.050, Env.Biol.Fish, 2011, 92: 159-166 & DOI:10.1007/s.10641-011-9825-z, Ethol.Ecol.Evol., 1997, 9: 223-231 & DOI:10.1080/08927014.1887.9522882, J.Evol.Biol., 2010, 22: 1907-1918 & DOI:10.1111/j.1420-9101.2010.02055.x, J.Fish Biol., 2013, 83: 343-354 & DOI:10.1111/jfb.12175
1.1.2.6.6. Other characteristics
A large caudal fin in the guppyPoecilia reticulata, a large dorsal fin in the Yucatan mollyPoecilia velifera, the Amur gobyRhinogobius brunneus or again the swordtailXiphophorus helleri, cephalic ridges among blenniesBlennius ocellaris, Salaria pavo, etc. constitute sexual characteristics which are generally attractive, although they are costly in energy and generally handicap their owners whose movements are limited. Females, seduced by male guppies with long tails, experience high reproductive success, superior to that from their matings with short-tailed males. Males of the Pacific blue-eyePseudomugil signifer are more attractive to females due to their highly developed dorsal fin that testifies to their high swimming capacity. In contrast, the possession of long filiform expansions of the fins by males of the threadfin rainbow fishIriatherina werneri constitutes a quite extravagant sexual ornament. Such an exaggerated desire to please results in a serious handicap to locomotion and an inordinate cost of energy expenditure in swimming.
The possession of long and symmetrical ventral spines by the males of the threespine sticklebackGasterosteus aculeatus contributes to their reproductive success. The presence of skin growths or reproductive tubercles on the head and fins of male cyprinids has a positive effect on the choices made by females, as evidenced by their reproductive success.
Bibliography: Anim.Behav., 2005, 70:1339-1348, 2009, 77: 823-829 & DOI:101016/j.anbehav.2008.12.006, Behav., 2005, 142: 191-202, 2006, 143: 183-195, 2008, 145: 897-913, Ethol., 2006, 112: 678-690 & DOI:10.1111/j.1439-0310.2006.01213.x, 1050-1055 & DOI:10.1111/j.1439-0310.2006.01261.x, 2007, 113: 802-812 & DOI:10.1111/j.1439-0310.2007.01388.x, Funct.Ecol., 2013, 27: 1034-1041 & DOI:10.1111/1365-2435.12097, J.Fish Biol., 2002, 60 & DOI:10.1006/jfbi.2002.2096, 61: 899-914, 2007, 71: 77-89, Zool.Sci., 2006, 23: 255-260 & DOI:10.2108/zsj.23.255
1.1.2.7. Dual function of certain visual signals
These multiple ornamentations in the form of cumulative multi-signals presented by males generally play a dual role and are intended, as in the minnowPhoxinus phoxinus, not only to trigger an attractive response on the part of interested females practicing sexual selection, but also to indicate to other males, who are potential rivals, their good health and aggressive potential. Males of the sheepshead swordtailXiphophorus birchmanni court females by straightening their dorsal fin. This behavior not only ensures success in mating, but also has the complementary effect of scaring their rivals.
Bibliography: Biol.Lett., 2007, 3: 5-7 & DOI:10.1098/rsbl.2006.0556
1.1.2.8. Permanent sexual dichromatism
In other species, the two sexes can be distinguished by their color patterns during all seasons, for example the male of the yellowfin grouperMycteroperca venenosa, in the Gulf of Mexico, has yellow spots on the two sides of its lower jaw and the female has red jaws. The male of the tiger grouperM. tigris is characterized by black pectoral fins, while the females have bright orange pectoral fins. These colors are particularly well visible as far as −35 m of depth where matings take place and are very useful for sexual partners to recognize each other in the areas of mating, with each male finding a female among the crowds of spawners grouped around the tropical spawning grounds (Volume 2, section 2.1.1).
Bibliography: J.Fish Biol., 2006, 69: 1744-1755 & DOI:10.1111/j.1095-8649.2006.01241.x
1.1.2.9. Female signals
Females of the guppyPoecilia reticulata and the mosquitofishGambusia sp. sometimes exhibit original sexual characteristics, such as a black-pigmented gravidity spot in close proximity to their cloacal sexual orifice.
