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'False orgasm' in female brown trout: Trick or treat?
Abstract
No Abstract
... The increase in dopamine, oxytocin and prolactin concentration can, therefore, be considered as a signal of sexual arousal. All mammals have the physiological capacity for orgasm (Fox and Fox 1971) and numerous vertebrates are known to experience orgasm-like states such as primates i.e. bonobo, chimpanzee, gorilla, orangutan, proboscis monkey, macaques (Chevalier-Skolnikoff 1974;Allen and Lemon 1981;Troisi and Carosi 1998;Murai 2006;de Waal 2011;Grueter and Stoinski 2016), carnivores and rodents (Adler 1969;Heeb and Yahr 1996;Coolen et al. 1997;Kollack-Walker and Newman 1997;Tenk et al. 2009;Pavlicev and Wagner 2016), birds and reptiles (Cabanac 1971;Winterbottom et al. 1999;Ball and Balthazart 2011) and fishes (Petersson and Jarvi 2001). It has even been demonstrated that ejaculation provoked by the activation of Crz-expressing neurons is rewarding to male flies (Zer-Krispil et al. 2018). ...
... Females of teleost fishes can control the numbers of eggs laid (Alonzo et al. 2016). They also present a 'false orgasm', demonstrating all the patterns of the spawning behaviour, without laying in the nest where the male spills out his sperm (Ridgway et al. 1989;Petersson and Jarvi 2001). Such misleading behaviours reveal that orgasm can be a signal used to manipulate males. ...
Why the sexual climax, in humans, results in a pleasurable experience remains an important biological question. Analysis of evolutionary traits in numerous Vertebrates suggests that orgasm evolved through three phylogenetic stages during the transition from external to internal fertilization and viviparity. First, orgasm is directly dependent on ejaculation in males and the expulsion of fluids from the ovarian and urethral glands (Skene’s) in females. I propose that sexual orgasm could come from the primitive reflex of discharging gametes to ensure reproduction. Thus, the understanding of orgasm should not be reduced to a penis- or a clitoris-centred paradigm. Secondly, orgasm has evolved to stimulate sexual activity because the evolutionary transition from external fertilization to internal fertilization has been accompanied in numerous species with a lessening in reproductive rates. Because sexual activity encourages reproduction, it can be argued that orgasm has evolved to increase sexual activity, particularly in viviparous species with low reproductive rates. Third, internal fertilization in the genital tract of females weakens the visibility of the putative success of fertilization. Female sexual fluids and proteins can bias fertilization in favour of preferred males. Because orgasm could promote a better choice of partner, I argue that female orgasm may have evolved as a post-copulatory selection tactic by which females can increase their control of mates.
... There are, however, no studies supporting or refuting this hypothesis. It has been suggested that false spawning is a form of female choice by which females trick undesirable males; females mimic the spawning act to fool their mates into sperm release, and then, by delaying spawning, allow other, more desirable, mates the opportunity to participate (Petersson and Järvi 2001). It is also possible that false spawning increases the final number of males with which the female mates (Schroder 1981). ...
... This observation agrees with those of Schroder (1981), who states that females performing false spawning provide cues to males in the vicinity about imminent spawning. By increasing the number of mates, females can increase the genetic diversity of their offspring and/or the quality of the participating males (Petersson and Järvi 2001). ...
Data collected from underwater video recordings in the wild and in a semi-natural channel were used to study two examples
of relatively unknown behaviour in the Salmoninae subfamily—false spawning in females and digging in Oncorhynchus males. Observations suggest that false spawning should be regarded as an incomplete fixed behavioural pattern (FBP) and that
male digging represents two special types of FBP (displacement FBP) with threatening and courting functions as ultimate causes.
... In fact, two results suggest that the dynamics of spawning acts within a night might be influenced by social factors. First, the temporal proximity of acts performed by a given female in a given night in this study, and the high proportion of acts performed without oocyte expulsion reported by Langkau et al. (2016) are reminiscent of female trout's 'false orgasm' (Petersson & Järvi 2001) or female lamprey's 'sham mating' (Yamazaki & Koizumi 2017). For both of these species, it has been suggested that repeated spawning simulations enable the female to exert mate choice, by both exhausting the sperm stock of an unwanted courtier and signalling its mating activity to peripheral males. ...
During the reproductive season, animals have to manage both their energetic budget and gamete stock. In particular, for semelparous capital breeders with determinate fecundity and no parental care other than gametic investment, the depletion of energetic stock must match the depletion of gametic stock, so that individuals get exhausted just after their last egg is laid and fertilized. Although these budgets are managed continuously, monitoring the dynamics of mating acts and energy expenditure at a fine temporal scale in the wild is challenging. This study aimed to quantify the individual dynamics of spawning acts and the concomitant energy expenditure of female Allis shad (Alosa alosa) throughout their mating season. Using eight individual-borne accelerometers for one month, we collected tri-axial acceleration, temperature, and pressure data that we analysed to i) detect the timing of spawning acts, ii) estimate energy expenditure from tail beat frequency and water temperature, and iii) monitor changes in body roundness from the position of the dorsally-mounted tag relative to the vertical plane. Female shad had a higher probability to spawn during warmer nights, and their spawning acts were synchronized (both individually and inter-individually) within each active night. They experienced warmer temperature, remained deeper, swan more slowly and spent less energy during daytime than night time. Over one month of spawning, they performed on average 15.75 spawning acts, spent on average 6 277 kJ and died with a significant portion of residual oocytes. The acceleration-based indicator of body roundness was correlated to condition coefficient measured at capture, and globally decreased through the spawning season, although the indicator was noisy and was not correlated to changes in estimated energy expenditure. Despite significant individual variability, our results indicate that female shad exhausted their energetic stock faster than their egg stock. Water warming will increase the rate of energy expenditure, which might increase the risk that shad die with a large stock of unspent eggs. Although perfectible, the three complementary analyses of acceleration data are promising for in situ monitoring of energy expenditure related to specific behaviour.
... Usually, males show a longer period of spermiation, which encompasses the spawning season of females by a few months, and they can fertilize eggs of several females in the wild. In addition, a female may spawn with more than one male, either by spawning with many males on one occasion or by spawning with different males on successive occasions (Petersson and Järvi, 2001). These male and female behaviors secure the reproductive success of an individual and favor the maintenance of genetic variability within a wild population. ...
... This agrees withSchroder (1981) stating that by performing false spawnings females provide cues to males in the vicinity about immediate spawning. By increasing the number of mates females increase either the genetic diversity of their offspring or the quality of the participating males(Petersson & Järvi, 2001 for brown trout). ...
Summary
Long-term data from underwater video recordings in the wild and in semi-natural channels
are used to describe and compare the reproductive behaviour of fishes in the Salmoninae
subfamily. The thesis is divided into five chapters. In the first, a new division of male
alternative strategies and tactics based on relative age at maturation (strategy) and on
behaviour in the spawning grounds (tactic) is proposed. A variation to the evolutionarily
stable strategies (ESS) model based on a growth velocity-dependent maturation threshold is
suggested.
In the second chapter, methods of video recording and analyzing behaviour during spawning
are introduced. The reproductive behaviour in the Salmoninae is described dividing it into
different phases related to female nest selection, construction, and completion.
In the third chapter, the role of instincts during spawning, as well as the mechanisms by
which they are released, are explained based on internal motivation and external stimuli.
Data are used to propose
false spawnings
in females should be regarded as
low intensity
behaviour and
that
male digging
represents
two different types of displacement reaction with
threatening and courting functions as ultimate causes.
In the fourth chapter, observations on different species are used to open a theoretical
discussion about the role of female choice in salmonines. Particularly, the importance of
Zahavi’s principle among the different breeding patterns is contrasted with Fisherian runaway
selection. A combination of both mechanisms is suggested. Special attention is given to
male’
quivering
behaviour. Different hypotheses are proposed to explain its origin and
function.
Chapter 5 uses data from underwater video recordings to construct the phylogeny of
Oncorhynchus
and
Salvelinus
based only on behavioural traits during spawning. A maximum
parsimony analysis using
Thymallus
,
Hucho
and
Salmo
as outgroups is conducted (PAUP*
4.0 b10). The results agree with some minor differences our current understanding of these
two genera based on morphological and molecular data. The possible evolution of several
characters is discussed in detail.
Throughout the manuscript still underwater video frames are used to illustrate the
explanations
... Our data allowed extrapolation from the few tens of centimeters around the nest and the few tens of minutes around the oviposition usually scrutinized when studying brown trout spawning behavior (e.g. Petersson 2001;Tentelier et al. 2011). At the scale of the whole network, the higher variability in the duration of male-female encounters on days when spawning occurred indicated that some male-female pairs predominated at the approach of the spawning act. ...
Individual interactions are crucial to many ecological processes but are difficult to quantify for long periods in aquatic animals. In this study, we applied a digital proximity logging device recently developed for terrestrial animals to a freshwater fish, the brown trout (Salmo trutta L.). After preliminary calibration and quantification of detection errors, we recorded the interactions occurring between five male and four female brown trout in an artificial channel during one week of the spawning season. The 55,637 logs recorded allowed us to describe the encounter network and its fine scale evolution. In particular, the time spent with females varied a lot across males, from two to 24 h in a five-day period, and the males, which spent the most time with females tended to mate more. At the individual level, the temporal distribution of encounters reflected shifts in dominance status, with males sequentially taking over exclusive proximity with females before spawning. Beyond sexual encounters, the method presented here could be applied to many processes interesting to fish ecologists, such as predator-prey interactions, intra and interspecific competition or disease transmission.
... All rights reserved. and the ability and cost to assess and monopolize mates (Allouche & Gaudin, 2001;Labonne et al., 2009;Petersson & Järvi, 2001). ...
Assortative mating is thought to play a key role in reproductive isolation. However, most experimental studies of assortative mating do not take place in multiple natural environments and, hence, they ignore its potential context dependence. We implemented an experiment in which two populations of brown trout (Salmo trutta) with different natural flow regimes were placed into semi-natural stream channels under two different artificial flow regimes. Natural reproduction was allowed and reproductive isolation was measured by means of parentage assignment to compare within-population versus between-population male-female mating and relative offspring production. For both metrics, reproductive isolation was highly context dependent: no isolation was evident under one flow regime but strong isolation was evident under the other flow regime. These patterns were fully driven by variance in the mating success of males from one of the two populations. Our results highlight how reproductive isolation through assortative mating can be strongly context dependent, which could have dramatic consequences for patterns of gene flow and speciation under environmental change. This article is protected by copyright. All rights reserved.
... These artistic displays take an immense amount of time, and yet females tend to mate with only those males with the most elaborate and well-decorated bowers. Another fascinating behavior is seen in female brown trout (Salmo trutta), who have false orgasms to incite males to prematurely ejaculate in an effort to either increase her offspring's genetic diversity by multiply mating or increase the quality of males with whom she spawns (Petersson and Järvi, 2001). Animals do the most fascinating things to increase their survival and reproduction. ...
... These events occurred while the other males, either the guarding or the sneaker males, were occupied with intra-sexual interactions that resulted in a delayed presence at the spawning site and no milt release. Premature male milt release may result from misinterpretation of female signals (Petersson & Järvi, 2001) or, alternatively, from differences in risk assessment between sneaker and guarding males. That is, sneaker males may take greater risks than guarding males and may experience to release milt without females releasing eggs. ...
A mismatch in timing between the release of male and female gametes in external fertilizers may lead to failed fertilization or, under sperm competition, reduced paternity. To quantify the actual synchrony of gamete release and the level of sperm competition we placed video cameras on two spawning grounds of a naturally spawning population of Arctic charr (Salvelinus alpinus). Females release eggs in response to courting (quivering) in less than 1% of the cases, yet to both dominant and sneaker males. That is, females initiated spawning with dominant males in 73.3% of the recorded spawning events. Although the actual spawning seems to be largely under female control, 55.6% of spawning events occur under sperm competition. The average time delay between dominant and sneaker males milt release under sperm competition is 0.68 s. Thus, female reproductive decisions seem to be strongly influenced by male-male competition and this may have set the stage for the evolution and maintenance of the observed plasticity in ejaculate characteristics of male charr.
... Usually, males show a longer period of spermiation, which encompasses the spawning season of females by a few months, and they can fertilize eggs of several females in the wild. In addition, a female may spawn with more than one male, either by spawning with many males on one occasion or by spawning with different males on successive occasions (Petersson and Järvi, 2001). These male and female behaviors secure the reproductive success of an individual and favor the maintenance of genetic variability within a wild population. ...
The Sparidae is a cosmopolitan family, and sparid fishes can be found and reproduced in both temperate and tropical seas around the world. Most of the members of this family are sequential hermaphrodites—either protogynous, such as the red porgy (Pagrus pagrus), or protandrous, such as the gilthead sea bream (Sparus aurata)– but gonochoristic species also exist, such as the common dentex (Dentex dentex). Fish in this family have a long spawning season, ranging between 60 and 150 days, and spawn daily or in a highly cyclical fashion. Fecundity is very high ranging between 0.4 and 3.2×106 eggs kg−1 of female body weight. The eggs are pelagic and transparent and have a diameter between 800 and 1,000 µm. Hormonal therapies have been developed to address the reproductive dysfunctions that exist in the early days of establishing captive wild or hatchery-produced broodstocks. At present, most Sparidae that are cultured commercially reproduce spontaneously in captivity and hatchery produced broodstocks have been developed and in some cases selected for traits of commercial importance.
... Finally, seconds before spawning, the female will start vibrating her body while probing and gaping. At this moment, females may sometimes perform a false spawning (Figures 23 and 24; Jones and Ball, 1954; Petersson and Ja¨rvi, 2001; Esteve, 2005). During false spawning, the female imitates a real spawning (probing, gaping and vibrating), but does not expel eggs. ...
Long-term data from underwater video recordings in the wild and semi-natural channels are compared to the current literature
to review the reproductive behaviour of fishes in the subfamily Salmoninae. Male alternative strategies and tactics are discussed.
Reproductive behaviour in Salmoninae is divided into different phases related to female nest selection, construction, and
completion. Still underwater video frames are used to support conclusions drawn on spawning behaviour.
... Research on pretending orgasm has been minimal, and almost all available studies are about women's pretending (even an article we found on ''false orgasms'' by brown trout was about false orgasms by female brown trout; Petersson & Järvi, 2001). We found only one study-an unpublished dissertation-that included men's pretending orgasm (Steiner, 1981). ...
Research shows that many women pretend or "fake" orgasm, but little is known about whether men pretend orgasm. The purpose of this study was to investigate (a) whether, how, and why men pretend orgasm and (b) what men's and women's reports of pretending orgasm reveal about their sexual scripts and the functions of orgasms within these scripts. Participants were 180 male and 101 female college students; 85% of the men and 68% of the women had experienced penile-vaginal intercourse (PVI). Participants completed a qualitative questionnaire anonymously. Both men (25%) and women (50%) reported pretending orgasm (28% and 67%, respectively, for PVI-experienced participants). Most pretended during PVI, but some pretended during oral sex, manual stimulation, and phone sex. Frequently reported reasons were that orgasm was unlikely, they wanted sex to end, and they wanted to avoid negative consequences (e.g., hurting their partner's feelings) and to obtain positive consequences (e.g., pleasing their partner). Results suggest a sexual script in which women should orgasm before men, and men are responsible for women's orgasms.
... Usually, males show a longer period of spermiation, which encompasses the spawning season of females by a few months, and they can fertilize eggs of several females in the wild. In addition, a female may spawn with more than one male, either by spawning with many males on one occasion or by spawning with different males on successive occasions (Petersson and Järvi, 2001). These male and female behaviors secure the reproductive success of an individual and favor the maintenance of genetic variability within a wild population. ...
Control of reproductive function in captivity is essential for the sustainability of commercial aquaculture production, and in many fishes it can be achieved by manipulating photoperiod, water temperature or spawning substrate. The fish reproductive cycle is separated in the growth (gametogenesis) and maturation phase (oocyte maturation and spermiation), both controlled by the reproductive hormones of the brain, pituitary and gonad. Although the growth phase of reproductive development is concluded in captivity in most fishes-the major exemption being the freshwater eel (Anguilla spp.), oocyte maturation (OM) and ovulation in females, and spermiation in males may require exogenous hormonal therapies. In some fishes, these hormonal manipulations are used only as a management tool to enhance the efficiency of egg production and facilitate hatchery operations, but in others exogenous hormones are the only way to produce fertilized eggs reliably. Hormonal manipulations of reproductive function in cultured fishes have focused on the use of either exogenous luteinizing hormone (LH) preparations that act directly at the level of the gonad, or synthetic agonists of gonadotropin-releasing hormone (GnRHa) that act at the level of the pituitary to induce release of the endogenous LH stores, which, in turn act at the level of the gonad to induce steroidogenesis and the process of OM and spermiation. After hormonal induction of maturation, broodstock should spawn spontaneously in their rearing enclosures, however, the natural breeding behavior followed by spontaneous spawning may be lost in aquaculture conditions. Therefore, for many species it is also necessary to employ artificial gamete collection and fertilization. Finally, a common question in regards to hormonal therapies is their effect on gamete quality, compared to naturally maturing or spawning broodfish. The main factors that may have significant consequences on gamete quality-mainly on eggs-and should be considered when choosing a spawning induction procedure include (a) the developmental stage of the gonads at the time the hormonal therapy is applied, (b) the type of hormonal therapy, (c) the possible stress induced by the manipulation necessary for the hormone administration and (d) in the case of artificial insemination, the latency period between hormonal stimulation and stripping for in vitro fertilization.
Besides egg fertilization, females of many taxa obtain direct fitness benefits from male mates, such as food, protection or paternal care. But males often increase their own fitness by mating with several females, among which they distribute sperm along with the above-mentioned benefits, reducing the benefits to individual females. These diverging interests lead to a conflict in which each female may try to ensure male fidelity and get exclusive access to male-provided benefits. Here, we use a theoretical model to show how a female of an externally fertilizing species may achieve mate fidelity by soliciting copulations at such a rate that the male has insufficient sperm left to increase his fitness with additional females. We show that three alternative condition-dependent evolutionarily stable mating relationships emerge in this scenario, based on whether one mate’s preference for mating rate dominates, or the conflict is resolved by what amounts to negotiation. We demonstrate how these outcomes depend on some features of physiology, ecology, and behavior. In particular, a greater reproductive benefit to a female from exclusive access to a male partner—or the occasional tendency of females to withhold eggs during mating—can increase male fidelity; and continuous sperm regeneration rather than an initially-set stock of sperm allows for multiple within-pair mating across all three mating patterns.
Se realizó un estudio para evaluar la calidad espermática de machos adultos de robalo chucumite (Centropomus parallelus) implantados con GnRH-a. Los peces se colectaron en las costas de los municipios de Paraíso y Centla, Tabasco, México con redes de luz de malla de 3 pulgadas. se hizo un muestreo de semen previo a la aplicación hormonal y posteriormente después de observado el evento reproductivo (desoves) en 29 organismos. Se evaluó la cualidad de fluidez del semen, motilidad en segundos, tipos de movimiento, porcentaje de células activas y el número de espermatozoides por volumen. Los resultados indican que no existen efectos significativos del factor dosis en el número de esperamatozoides/mL. Sin embargo, el mayor número de espermatozoides/mL en promedio fue producido por los peces que se trataron con 100 μg/pez. En el caso de la motilidad en segundos no existen diferencias estadísticas significativas entre los tratamientos. Los resultados de cualidad espermática, porcentaje de células activas (móviles) y el tipo de movimiento se registraron en los rangos reportados como viables para otras especies.
As a component of natural selection, sexual selection produces variation in reproductive success throughout the reproductive period, and therefore impacts genes transmission between generations. During this PhD, the effect of variation in hydraulic environment on sexual selection in brown trout was investigated at both within and between populations scales. New approaches to improve estimation of reproductive investment, as well as models to decompose the effect of traits on individual fitness at each stage of sexual selection, were developed. Experiments in natural and semi-natural environments indicate that environmental variation does not impact reproduction habitat choice by females, but it can modify reproductive investment in some populations, as well as it can control gene flow between genetically distinct populations. These results help to understand the evolution of sexual selection in the broad context of increasing stochastic variations of river systems hydrology as predicted by climate change models in temperate areas.
A bstract
During the reproductive season, animals have to manage both their energetic budget and gamete stock. In particular, for semelparous capital breeders with determinate fecundity and no parental care other than gametic investment, the depletion of energetic stock must match the depletion of gametic stock, so that individuals get exhausted just after their last egg is laid and fertilized. Although these budgets are managed continuously, monitoring the dynamics of mating acts and energy expenditure at a fine temporal scale in the wild is challenging.
This study aimed to quantify the individual dynamics of spawning acts and the concomitant energy expenditure of female Allis shad ( Alosa alosa ) throughout their mating season.
Using eight individual-borne accelerometers for one month, we collected tri-axial acceleration, temperature, and pressure data that we analysed to i) detect the timing of spawning acts, ii) estimate energy expenditure from tail beat frequency and water temperature, and iii) monitor changes in body roundness from the position of the dorsally-mounted tag relative to the vertical plane.
Female shad had a higher probability to spawn during warmer nights, and their spawning acts were synchronized (both individually and inter-individually) within each active night. They experienced warmer temperature, remained deeper, swan more slowly and spent less energy during daytime than night time. Over one month of spawning, they performed on average 15.75 spawning acts, spent on average 6 277 kJ and died with a significant portion of residual oocytes. The acceleration-based indicator of body roundness was correlated to condition coefficient measured at capture, and globally decreased through the spawning season, although the indicator was noisy and was not correlated to changes in estimated energy expenditure.
Despite significant individual variability, our results indicate that female shad exhausted their energetic stock faster than their egg stock. Water warming will increase the rate of energy expenditure, which might increase the risk that shad die with a large stock of unspent eggs. Although perfectible, the three complementary analyses of acceleration data are promising for in situ monitoring of energy expenditure related to specific behaviour.
Rainbow trout has been considered for many years as a model of glucose intolerant species. The different hypothesis raised by many researchers to explain such phenomenon has been tested thoroughly in recent years without arriving at a clear explanation. One of the processes that could be involved in its inability to deal with increased levels of glucose could be the absence of glucosensing mechanisms similar to those found in mammals. However, several recent studies in rainbow trout have demonstrated the existence of glucosensor systems in hypothalamus, hindbrain and Brockmann bodies. The fact that this system has been characterized in a species whose natural diet contains less than 1% carbohydrate intake makes rainbow trout an attractive model for glucosensing studies, as so far it is the only vertebrate carnivorous species in which this system has been explored.The glucosensing system has been shown to be activated when glucose levels increase at the same time that food intake decreases while conversely, when glucose levels decrease, glucosensors are inactivated and food intake increases. The mechanisms through which these glucosensor systems operate are similar to those described in mammalian brain regions, though quite different in pancreatic cells. Information has also been reported regarding the molecular characterization of these systems, their specific location in the brain and their endocrine regulation.The present review will provide a general overview of the research carried out in this area in recent years and provide perspectives for future research in this field.
Reproduction in salmonids is characterized by intense sexual selection, where intrasexual competition is fierce, leading to a high variance in reproductive success. Females are known to build a redd, a form of parental care, whereas males apparently do not provide paternal care. In brown trout (Salmo trutta), one of the most semelparous salmonids, the intrasexual competition is direct for males, and body size generally predicts the outcome, whereas it is mostly indirect for females. While the relationship between mating success and phenotype, such as body size or color patterns has been investigated, there are far less data available on intersexual preference in salmonids. It is generally supposed to be aimed at indirect benefits, such as good genes or compatible genes. But the brown trout presents an intriguing case, where selective pressures on freshly laid eggs can be strong and are directly correlated to intrasexual competition. Indeed, dramatic cannibalism events can be observed before the female can cover the redd with gravels, especially when operational sex ratio is high (number of males on number of females). As a countermeasure, some males exhibit post-fertilization aggressive behaviour that reduce the opportunity for cannibalism. This opens an interesting perspective in salmonids: female preference for males could be directed at both indirect and direct benefits (here egg protection). Because the selective pressure controlling for egg survival is driven by environment (density and phenotypes of males for instance), the potential for evolution is also therefore dependent on environmental change: habitat modification, connectivity, temperature and water discharge dynamics. These parameters affect the population density, the distribution of phenotypes and the fitness of eggs depending on redd location. In this chapter, we describe recently acquired knowledge on the evolution of the brown trout reproductive system with emphasis on the interaction between sexual and natural selection. We then propose possible paths in order to make decisive advances in this area, and explain how environmental change may shape the stage for the outcome of mating system evolution in brown trout.
Abstract (sammanfattning på engelska),3 Inledning,4 Bakgrund: genetiska konsekvenser,4 Definition på vild och odlad öring i Dalälven,5 Bakgrund: genetiska skillnader och likheter mellan vild och odlad
At what age do Atlantic salmon and brown trout become sexually mature, and which factors and mechanisms determine the seasonal
timing of maturation and spawning? How are resources allocated to the development of sexual characters and reproduction, and
how do they maximize their reproductive output? This chapter reflects on these issues.
The reproductive ecology of Atlantic salmon involves the allocation of substantial amounts of resources, which need to be garnered throughout life, to the successful production of offspring. This investment of resources is devoted not only to the production of gametes, but also to breeding migration, competition for breeding resources and mates, courtship and mate choice, and the elaborate traits that underpin these behaviours. In this chapter, we explore the patterns and traits that comprise the reproductive ecology of Atlantic salmon, and their influences on the growth and survival of early life-stage juveniles. Both males and females invest approximately 60% of their total energy during reproduction, with females investing heavily in egg production and males in behavioural activity (e.g. mate competition). Intense male competition for access to mating opportunities has led to the evolution of elaborate secondary sexual characters (e.g. hooked snouts and gaudy breeding colouration) and alternative reproductive phenotypes, where some males mature in fresh water as parr at less than a hundredth the weight of their anadromous male counterparts. Rather than fight for access to spawning females, these mature parr attempt to ‘sneak’ fertilisations. In contrast to males, females direct much of their behaviour during reproduction towards
activities that ensure oviposition success and offspring survival. There can be tight, direct links between maternal traits, such as egg size, spawning time and spawning location, and offspring success. Egg size largely determines the offspring’s resources until exogenous feeding several months after fertilisation, and spawning time and location the environmental conditions the offspring experiences prior to, and following emergence from the gravel nest.
A remote monitoring system was developed to provide information on the behaviour of mature and immature Atlantic salmon Salmo salar parr at nests during the spawning season. An octagonal passive integrated transponder (PIT) detector (0·865 m maximum diameter) designed to surround nests of Atlantic salmon was used to identify individual salmon parr present at 38 spawning events in three circular spawning channels. The range of the detector for PIT tags presented in the optimum orientation was 2·4 cm (range between tags 1·7–3·0 cm). Using a sub-sample of 20 spawnings, the mean efficiency of the detector (number of fish passes registered relative to number of passes observed on video) was 70·5% (range 32-100%). There were no significant effects of time from spawning, total number of registrations, body size or maturity status (mature or immature) on efficiency. However, fish were more likely to be detected entering nests than leaving, as departures were more rapid and higher in the water column. The PIT detector did not affect the numbers of parr at spawnings or between spawning intervals of females, and allowed for the individual identification of 65 of the 72 parr observed in nests during spawning. In all cases where certain identifications were not possible and the video was of satisfactory quality, this was due to obstruction of the camera view by anadromous fish. The remote monitoring system was thus effective in identifying behavioural differences, and only one of 20 immature parr was ever detected during the period encompassing 10 min before and after spawning compared with 30 or 40 mature parr.
Using a novel methodology, natural ejaculate volumes of 14 male rainbow trout Oncorhynchus mykiss were compared when males were housed with one female (absence of a rival male) or with another male and one female (rival male present). Contrary to theoretical predictions, male ejaculate expenditure was not influenced by the presence of a rival male. Male gape duration was positively correlated with the volume of sperm ejaculated. Release of sperm by the male always preceded release of eggs by the female. Analysis of the timing and duration of ejaculation suggests that males may rely on the timing and proximity of gamete release to enhance fertilization success. These results are discussed in the context of sperm competition theory.
The telmatherinid fishes of the Malili Lakes, Sulawesi, Indonesia provide a new and promising system for studying the processes
maintaining diversity in nature, and especially for testing the generality of the influential findings emerging from studies
of other fish systems. Here we develop the telmatherinid system by providing the first detailed descriptions of mating behaviour
for seven species representing both of the major Malili lakes and all three genera. The mating behaviour of all seven species
can be generalized, suggesting that particular behaviours are conserved within the group. For example, male–male competition
in the form of lateral fin displays and physical fighting is evident in all seven species. Males also perform a circling behaviour
alongside females that they are paired with, although the size of the circle varies across species. In some species egg cannibalism
and/or sneaking behaviour are also prevalent. Interspecific comparisons of mating behaviour show that habitat may play an
important role in driving behavioural differences between species. Parallel intraspecific variation in use of habitat and
mating behaviours is also noted for two species. This study will facilitate future behavioural and evolutionary ecology research
with this system.
Anadromous salmonid females exhibit indicators of mate choice based on male size. Direct benefits to females of mating with larger males have not been identified for semelparous Pacific salmon, Oncorhynchus spp. We tested the null hypothesis that females forced to spawn naturally in a stream channel and artificially (gametes removed manually) with males about half their body mass would experience egg fertilization rates similar to that of females forced to spawn with males of about equal mass. Fertilization rates did not differ significantly between large- and small-male pairs. The fertilization rates were also very similar for eggs deposited naturally and those that we fertilized artificially. Therefore, fertilization success does not appear to be the mechanism responsible for female mate choice based on male size. Benefits of females mating with larger males probably have only indirect (i.e., genetic) benefits to a females offspring, as suggested by previous authors.
Underwater observations on the courtship and spawning behavior of small-mouth bass (Micropterus dolomieui) were recorded at three sites in Ontario. The courtship sequence can be divided into two phases: an initial phase away from the nest site and a final phase at the nest site. The courtship behaviors of the male and female are described for each of these phases.
1.1. Trunk muscular EMG in both sexes of spawning chum salmon were recorded simultaneously with the aid of a telemetry system in order to determine the sex which initiates spawning.2.2. The trunk muscular activities for spawning in both sexes consisted of two stages i.e. an initial weak and a final strong burst. During the final stage, oviposition and sperm ejaculation occurred.3.3. The initial stage in the female began prior to that in the male, while the final stage in the male occurred before the female's.4.4. The possible significance of the amplitude change in the spawning convulsion as a signal for synchronizing the spawning of both sexes, was discussed.
Male pink salmon cluster in groups of up to 10 or more around a female as she prepares the substrate for spawning. The largest male in the group (in length and dorsal hump development) stays closest to the female; the others maintain a size-related hierarchy behind the pair. Position in the group is determined by frequent aggressive interactions among the members. Often a relatively small "outlier" male holds position near the central pair, to one side of the nest. These males are "female-like" in colour and size, and the dorsal hump is small. When the primary male settles into the nest bottom and quivers beside the female, males in the associated group, including the small outlier, dash into the nest. When the female and primary male spawn, some or all of the group males release sperm. Nest-digging females are territorial; they attack other females and small males. Their primary males are aggressive towards other males, but not towards females. They frequently attack the males closest to them in their group, but also attack nongroup males, including other large males who try, usually unsuccessfully, to replace them as the primary male. The phenomena of many males at a single nest, great variability in dorsal hump development, and outlier vs. fighting behaviour are all associated with male competition for access to spawning females.
Reproductive behaviour and factors associated with male and female mating success were studied in sea trout (Salmo trutta) in a stream water aquarium, during three successive years. We compared a sea-ranched and a wild-produced strain, both of the same genetic origin. In general, dominant males courted females more often, spent more time on the spawnable areas, and had higher mating success than lower ranked males. Body mass explained about 18% of the males' position in the dominance hierarchy. Sea-ranched males, however, achieved on average fewer matings than wild ones. Wild males courted the nest-preparing females and chased away other males more frequently than did the sea-ranched males. Females were observed to be aggressive towards males, especially when the females were preparing a nest. The males that were more frequently the target of female aggression had smaller adipose fins and were more often aggressive towards females. In general the females spawned just once in each nest. Sea-ranched females defended and tested their redd less frequently than the wild females did. Digging activity by wild females diminished closer to spawning time, but not that of the sea-ranched females. To what extent the observed differences were due to the environmental conditions or to genetic differences is not known at present. However, the results of previous studies have revealed that behavioural and morphological differences exist between the strains, despite being reared under the same conditions. Thus, the behavioural changes noted in the sea-ranched sea-trout might have a genetic element.
In some salmonid species, the females have been assumed to choose their mates on the size of the male's adipose fin. This hypothesis was tested in a stream water aquarium, in which 19 brown trout, Salmo trutta, females were allowed to choose between two males of the same body size but with different adipose fin sizes. The two males were separated from each other in cages. After the female had started to prepare her nest close to one of them, the males were released and allowed to fight each other for the opportunity to spawn. Out of 19 females, 14 prepared a nest closest to the male with the larger adipose fin. However, only six of the 14 females spawned with this male. Males that spawned were more dominant (i.e. were more likely to win fights). When the female spawned with the male she chose, he was less aggressive towards her than when she spawned with the other male. There were no significant differences in the plasma levels of testosterone (T) and 11-ketotestosterone (11-KT) between the chosen males and those not chosen. However, the dominant males had significantly higher plasma levels of T and 11-KT both before and after the experiment. The results support the view that female brown trout exhibit mate choice, but their choice is overruled by male-male competition. Copyright 1999 The Association for the Study of Animal Behaviour.
Many salmon species include males which mature as much as 50% younger and as small as 30% of the adult body size of other males in the population1–8. In the semelparous Pacific salmon Oncorhynchus spp., these small males are known as ‘jacks’, and they compete with larger late-maturing ‘hooknose’ males for opportunity to spawn on the breeding grounds. The existence of jacks is problematical as it is believed that salmon populations should have a single optimal age or size at maturity9–11. I now show, however, that these two alternative life histories are evolutionarily favoured by frequency-dependent disruptive12 selection on the breeding grounds. In coho salmon (Oncorhynchus kisutch), small and large males gain access to females by sneaking and fighting respectively. By contrast, intermediate-sized males are at a competitive disadvantage. Jacks, which are specialized at sneaking, and hooknose males, which are specialized at fighting, have negatively frequency-dependent fitnesses from these alternative breeding tactics. Calculations suggest that the lifetime fitness of jacks is similar to that of hooknose males. Thus, age of maturity in salmon has probably not evolved as a single optimum, but rather as a ‘mixed evolutionarily stable strategy13,14 in which precocious maturity is an evolutionarily viable alternative life history strategy.
Induced breeding of Heteropneustes fossilis (Bloch.) was studied in laboratory aquaria. Quantitative and qualitative data on pre-mating, mating, and post-mating behaviour and related parameters were recorded. Among the pairs examined, 83% spawned successfully. Mating behaviour started between 6 and 15 h after administration of pituitary hormones. The number of enfoldings varied from 25 to 350. Over 93% of the released eggs hatched within 21–24 h at temperature 24–31°C.
Summary1.By using specially constructed tanks it has been possible to observe in detail and take cine films of thirteen spawnings of brown trout, and over eighty spawnings of the salmon. Despite the artificial conditions in which these fish spawned we believe that their spawning behaviour, as observed, was normal.2.A detailed description is given of the behaviour of the fish throughout the spawning act.3.The spawning behaviour is analysed and the possible significance of the various activities is discussed. It is shown that the orgasm can be regarded as a short reaction chain.4.An experiment was made to demonstrate the currents in the bottom of a bed in which a female had spawned Several redds were examined.
Sexual behaviors of the salmon are composed of a stimulus-reaction chain, which ensures synchronous spawning between the sexes and successful fertilization. To characterize the signals involved in such a stimulusreaction chain, the body vibration and electromyographic activity of the trunk muscles during spawning were simultaneously recorded from freely behaving male and female pairs of him salmon (landlocked red salmon,Oncorhynchus nerkd) and were analyzed in combination with a videographic analysis of behavior sequences. The results showed that the him salmon have an elaborate communication system in which characteristic vibrational signals are exchanged. These are produced by body vibration due to trunk muscle activity related to spawning and are transmitted between the sexes with an accurate timing through the stimulus-reaction chain. They act as timing cues to synchronize gamete release and are thought to be shared among a wide variety of fishes. It was hypothesized that the lateral line sense is involved in the detection of these vibrational signals. Furthermore, based on the sequence matrix analysis as well as on information theory, intersexual behavioral sequences during spawning were analyzed statistically. The results showed that statistically significant interactions occur between the sexes and statistically significant amounts of information are transmitted through the interactions, supporting the results from recording experiments mentioned above. Characters of the signalling system and possible origins of the vibrational signals are also discussed.
We describe the spawning behaviour of Japanese charr,Salvelinus leucomaenis, which have begun to change their life history style from fluvial to lacustrine-fluvial after the construction of an artificial lake by damming. There was a discrete size distribution between mature lake run individuals (larger body size) and mature stream resident fish (smaller body size). Lake run males use pairing tactics, while stream resident males use satellite or pairing tactics depending on the presence of lake run males. Sneaking success of stream resident males is low relative to pairing success of lake run males. Pair formation is strongly assortative by body size and consequently by type. We suggest that both male-male competition and female choice of similar sized males, play an important role in pair formation. We hypothesize that the number of stream resident type relative to lake run type, especially stream resident females, will decrease in future years.
Dominance hierarchies are widely described in nature. Commonly, an individual's ordinal rank is used as a measure of its position in the hierarchy, and, therefore its priority of access to resources. This use of ordinal ranks has several related drawbacks: (1) it is difficult to assess the magnitude or the significance of the difference in degree of dominance between two individuals; (2) it is difficult to evaluate the significance of differences between dominance matrices based on different behaviours or on the same behaviour at different times, and (3) it is difficult to use parametric statistical techniques to relate dominance rank to other quantities of interest.In this paper we describe a method for assigning cardinal dominance indices that does not suffer from these drawbacks. This technique is based on the Bradley-Terry model from the method of paired comparisons. We show how this model can be reinterpreted in terms of dominance interactions. and we describe a simple iterative technique for computing cardinal ranks. We then describe how to evaluate (1) whether the rank differences between individuals are significant, and (2) whether differences in the cardinal hierarchies based on different behaviours or the same behaviour at different times are significant. We then show how to generalize the method to deal with behaviours that sometimes have ambiguous outcomes, or behaviours for which the rank difference between a pair of individuals affects the rate of interaction between them.
The paper, which has an informal discussion at the end, provides a game theoretical analysis of the asymmetric “war of attrition” with incomplete information. This is a contest where animals adopt different roles like “owner” and “intruder” in a territorial conflict, and where the winner is the individual prepared to persist longer. The term incomplete information refers to mistakes in the identification of roles. The idea by Parker & Rubenstein (1981) is mathematically worked out and confirmed that there exists only a single evolutionarily stable strategy (ESS) for the model with a continuum of possible levels of persistence and no discontinuities in the increase of cost during attrition. The ESS prescribes to settle the conflict according to “who has more to gain or less to pay for persistence”. The only evolutionarily stable convention is thus to give the player access to the resource who has the role which is favoured with respect to payoffs. By contrast, it was shown earlier (Hammerstein, 1981) for various asymmetric versions of the “Hawks-Doves” model that an ESS can exist which appears paradoxical with respect to payoffs. The nature of this contrast is further analyzed by introducing elements of discreteness in the asymmetric war of attrition. It turns out that some conditions must be satisfied in order to have the possibility of an alternative ESS which is not of the above simple commonsense type. First, a decision to persist (or escalate) further in a contest must typically commit a contestant to go on fighting for a full “round”, before he can give up without danger. Second, such a “discontinuity” must occur at a level of persistence where the contest is still cheap, and, finally, errors in the identification of roles must be rare.
Biological evolution is a fact--but the many conflicting theories of evolution remain controversial even today. In 1966, simple Darwinism, which holds that evolution functions primarily at the level of the individual organism, was threatened by opposing concepts such as group selection, a popular idea stating that evolution acts to select entire species rather than individuals. George Williams's famous argument in favor of the Darwinists struck a powerful blow to those in opposing camps. His Adaptation and Natural Selection, now a classic of science literature, is a thorough and convincing essay in defense of Darwinism; its suggestions for developing effective principles for dealing with the evolution debate and its relevance to many fields outside biology ensure the timelessness of this critical work.
Not all members of a sex behave in the same way. Frequency- and statusdependent selection have given rise to many alternative reproductive phenotypes within the sexes. The evolution and proximate control of these alternatives are only beginning to be understood. Although game theory has provided a theoretical framework, the concept of the mixed strategy has not been realized in nature, and alternative strategies are very rare. Recent findings suggest that almost all alternative reproductive phenotypes within the sexes are due to alternative tactics within a conditional strategy, and, as such, while the average fitnesses of the alternative phenotypes are unequal, the strategy is favoured in evolution. Proximate mechanisms that underlie alternative phenotypes may have many similarities with those operating between the sexes.
Reproductive behaviour, mating success, and differences between wild and sea-ranched sea trout (Salmo trutta)
- Petersson
Petersson, E. & Jä, T. 1997. Reproductive behaviour, mating success, and differences between wild and sea-ranched sea trout (Salmo trutta). Behaviour, 133, 1–22.