Cortisol does not increase risk of mortality to predation in juvenile bluegill sunfish: A manipulative experimental field study.

The hypothalamic-pituitary-interrenal (HPI) or stress axis in teleost fishes produces their primary glucocorticoid, cortisol. Although generally an adaptive response, prolonged HPI axis stimulation can impair organismal performance. Previous work has shown that stressed teleosts have higher mortality to predation than unstressed conspecifics, suggesting a role for HPI axis in modulating predator-prey interactions. Our current study investigated whether elevated cortisol levels altered the predation rate of a wild teleost fish, the bluegill sunfish (Lepomis macrochirus). Wild juvenile bluegill were given intraperitoneal implants of cocoa butter (i.e., sham), or cocoa butter containing cortisol or cortisol and the glucocorticoid receptor antagonist RU486. After 24 hr, fish were tethered along the bottom of the lake and their survival under natural predation was recorded following 24 hr. A subset of fish was used to validate the efficacy of cortisol implants in this setting. No treatment effect on survival was observed, suggesting that elevated cortisol has minimal involvement in mediating predator-prey interactions in this context. However, experimental fish may have demonstrated resiliency to physiological perturbations owing to the relatively acute duration of our experimental series, and negative effects might be manifested over a more chronic period.

Chronic Plasma Cortisol Elevation Does Not Promote Riskier Behavior in a Teleost Fish: A Test of the Behavioral Resiliency Hypothesis.

Stressed fish have been shown to have higher predator-induced mortality than unstressed conspecifics, suggesting a role for the hypothalamic-pituitary-interrenal axis in modifying risk-taking behaviors. Yet, there is also evidence of behavioral resiliency in the face of chronic stressors. Here, we tested the behavioral resiliency hypothesis, which posits that animals can maintain consistent behavioral phenotypes in the face of significant physiological challenges. We determined whether chronic plasma cortisol elevation promotes risk-taking behaviors in a model teleost fish, the pumpkinseed sunfish (Lepomis gibbosus). Experimental fish were implanted with cocoa butter either as a sham or with cortisol. At 48 h post-implantation, the behavior of individual focal fish was tested in an experimental arena comprising of a simulated physical refuge, an open zone containing a constrained conspecific shoal, and a compartment containing either a model of a northern pike (Esox lucius) paired with corresponding pike olfactory cues in lake water or no pike model (control) paired with sham lake water cues only. The fish were assayed individually for their refuge utilization, shoaling tendency, and general activity. Neither cortisol treatment nor predation-risk treatment influenced any of these behaviors. This suggests that sunfish, in the context of our experiment, were behaviorally resilient to the physiological effects of chronic plasma cortisol elevation and in the face of an apparent threat of predation. Our results thus provide support for the behavioral resiliency hypothesis in fish under both physiological and ecological stressors. We posit that behavioral resiliency is an evolutionary adaptation ensuring appropriate responses to environmental conditions.

Elevação Crônica do Cortisol Plasmático não Promove Comportamento Mais Arriscado em um Peixe Teleósteo: Um teste da Hipótese de Resiliência Comportamental (Chronic Plasma Cortisol Elevation Does Not Promote Riskier Behavior in a Teleost Fish: A Test of the Behavioral Resiliency Hypothesis) Foi demonstrado que peixes estressados têm maior mortalidade causada por predadores do que co-específicos não estressados, sugerindo um papel para o eixo hipotálamo­hipófise­interrenal na modificação de comportamentos de risco. No entanto, há também evidências de resiliência comportamental frente a estressores crônicos. Aqui testamos a hipótese de resiliência comportamental, que postula que os animais podem manter fenótipos comportamentais consistentes frente a desafios fisiológicos significativos. Determinamos se a elevação crônica do cortisol plasmático promove comportamentos de risco em um peixe teleósteo modelo, o perca-sol (Lepomis gibbosus). Peixes experimentais foram implantados com manteiga de cacau, tanto como um placebo ou com cortisol. Após 48 h da implantação, o comportamento de peixes individuais foi testado em uma arena experimental composta por um refúgio simulado, uma zona aberta contendo um cardume co-específico e um compartimento contendo um modelo de lúcio-do-norte (Esox lucius) pareado com as pistas olfativas correspondentes de lúcios em água fluvial ou sem modelo (controle) pareado apenas com iscas falsas. Os peixes foram analisados individualmente quanto à utilização de refúgio, tendência de formar cardumes, e atividade geral. Nem o tratamento com cortisol e nem o com risco de predação influenciaram qualquer um desses comportamentos. Isto sugere que os perca-sol, no contexto do nosso experimento, eram comportamentalmente resilientes aos efeitos fisiológicos da elevação crônica do cortisol plasmático e diante de uma aparente ameaça de predação. Nossos resultados fornecem apoio para a hipótese de resiliência comportamental em peixes sob estressores fisiológicos e ecológicos. Nós postulamos que a resiliência comportamental é uma adaptação evolutiva que garante respostas apropriadas às condições ambientais. translated to Portuguese by G. Sobral (gabisobral@gmail.com).

La Elevación Crónica de Cortisol en el Plasma no Promueve un Comportamiento más Riesgoso en un Pez Teleósteo: Una Prueba de la Hipótesis de Resistencia de Comportamiento (Chronic Plasma Cortisol Elevation Does Not Promote Riskier Behavior in a Teleost Fish: A Test of the Behavioral Resiliency Hypothesis) Se ha demostrado que los peces estresados tienen una mayor mortalidad inducida por depredadores que los conespecíficos no estresados, lo que sugiere un papel para el eje hipotálamo­pituitario­interrenal en la modificación de los compartamientos de riesgo. Sin embargo, también hay evidencia de resistencia del comportamiento frente a los factores estresantes crónicos. Aquí, probamos la hipótesis de resistencia del comportamiento, que postula que los animales pueden mantener fenotipos de comportamiento consistentes ante desafíos fisiológicos significativos. Determinamos si la elevación crónica de cortisol en plasma promueve comportamientos de riesgo en un pez modelo teleósteo, el pez sol de semillas de calabaza (Lepomis gibbosus). Los peces experimentales se implantaron con manteca de cacao como una farsa o con cortisol. A las 48 h posteriores a la implantación, se evaluó el comportamiento de los peces focales individuales en un campo experimental que comprende un refugio físico simulado, una zona abierta que contiene un banco de peces conspecificos constreñidos, y un compartimento que contiene un modelo de lucio norteño (Esox lucius) emparejado con señales olfativas de lucio correspondientes en el agua del lago o sin modelo de lucio (control) emparejado solo con señales de agua del lago simulado. Los peces fueron analizados individualmente por su utilización de refugio, tendencia al cardumen y actividad general. Ninguno de estos comportamientos fuero influidos por el tratamiento con cortisol o el tratamiento de riesgo de depredación. Esto sugiere que los peces sol, en el contexto de nuestro experimento, eran resistentes al comportamiento frente a los efectos fisiológicos de la elevación crónica de cortisol en el plasma y ante una amenaza aparente de depredación. Por lo tanto, nuestros resultados brindan apoyo para la hipótesis de resistencia de comportamiento en peces bajo factores de estrés fisiológicos y ecológicos. Postulamos que la resiliencia conductual es una adaptación evolutiva que garantiza respuestas adecuadas a las condiciones ambientales. translated to Spanish by Y. E. Jimenez (yordano_jimenez@brown.edu).

Does experimental cortisol elevation mediate risk-taking and antipredator behaviour in a wild teleost fish?

The hypothalamic-pituitary-interrenal (HPI) axis is centrally implicated in stressor mitigation in teleost fishes. Sustained HPI axis activation can be detrimental to the physiological functioning of an organism and can result in fitness-related trade-offs. Predator-induced mortality is known to be higher in stressed fish than in unstressed conspecifics, suggesting a role for the HPI axis in mediating fish behaviour. However, the underlying specific mechanism(s) for this phenomenon is(are) unknown. The purpose of the current study was to address how the HPI axis influences risk-taking, and antipredator behaviours in a wild teleost, the pumpkinseed sunfish (Lepomis gibbosus). Here, individual juvenile pumpkinseed were implanted either with cocoa butter as a sham control or with a biologically-relevant concentration of cortisol. Forty-eight hours post-implantation, fish were assessed for behavioural metrics associated with boldness and risk taking in three sequential behavioural tests: (i) a predation-risk test, (ii) an exploration tendency test, and (iii) a shoaling tendency test, with test order randomized among different trials. Cortisol treatment had no influence on antipredator, exploratory, or shoaling behaviours. However, post-attack swimming duration (in predation-risk test) and exploratory activity (in Z-maze exploration test) were significantly affected by body mass. Collectively, our results indicate that cortisol may not have a role in mediating sociability, boldness, and risk-taking behaviours in pumpkinseed sunfish, at least under the current laboratory conditions. However, cortisol may nonetheless play a role in mediating predator-prey interactions in fishes in more natural environmental settings that were not considered here.

Do Males Form Social Associations Based on Sexual Attractiveness in a Fission-Fusion Fish Society?

Recent theory predicts that males should choose social environments that maximize their relative attractiveness to females by preferentially associating with less attractive rivals, so as to enhance their mating success. Using the Trinidadian guppy (Poecilia reticulata), a highly social species, we tested for non-random social associations among males in mixed-sex groups based on two phenotypic traits (body length and coloration) that predict relative sexual attractiveness to females and sexual (sperm) competitiveness. Based on a well-replicated laboratory dichotomous-choice test of social group preference, we could not reject the null hypothesis that focal males chose randomly between a mixed-sex group that comprised a female and a rival male that was less sexually attractive than themselves and another mixed-sex group containing a sexually more attractive male. The same conclusion was reached when females were absent from the two groups. As might be expected from these laboratory findings, free-ranging males in the field were not assorted by either body length or colour in mixed-sex shoals. The apparent lack of an evolved and expressed preference in wild male guppies from our study population to form social associations with other males based on their relative sexual attractiveness and competitiveness might be due to the fission-fusion dynamics of guppy shoals in nature. Such social dynamics likely places constraints on the formation of stable phenotype-based social associations among males. This possibility is supported by a simulation model which assumes group departure rules based on relative body size and coloration in males.

Towards a synthesis of frameworks in nutritional ecology: interacting effects of protein, carbohydrate and phosphorus on field cricket fitness.

Phosphorus has been identified as an important determinant of nutrition-related biological variation. The macronutrients protein (P) and carbohydrates (C), both alone and interactively, are known to affect animal performance. No study, however, has investigated the importance of phosphorus relative to dietary protein or carbohydrates, or the interactive effects of phosphorus with these macronutrients, on fitness-related traits in animals. We used a nutritional geometry framework to address this question in adult field crickets (Gryllus veletis). Our results showed that lifespan, weight gain, acoustic mate signalling and egg production were maximized on diets with different P : C ratios, that phosphorus did not positively affect any of these fitness traits, and that males and females had different optimal macronutrient intake ratios for reproductive performance. When given a choice, crickets selected diets that maximized both lifespan and reproductive performance by preferentially eating diets with low P : C ratios, and females selected diets with a higher P : C ratio than males. Conversely, phosphorus intake was not regulated. Overall, our findings highlight the importance of disentangling the influences of different nutrients, and of quantifying both their individual and interactive effects, on animal fitness traits, so as to gain a more integrative understanding of their nutritional ecology.

Spatial separation from family in the mobile young of a biparental fish: risks and dynamics of returning home.

In species with extended parental care, mobile dependent young are potentially more vulnerable to predators when they stray and become separated from their parents. We would expect that the likelihood of, and latency time for, a separated young to safely return to its 'family unit' (i.e. parents and brood mates) to be, respectively, inversely and positively related to the initial distance of separation and potentially mediated by its age or body size. Using the biparental convict cichlid fish (Amatitlania siquia), we tested these predictions by capturing individual young and displacing them at varying distances from their family unit in both the field and laboratory. As expected, displaced fish were less likely, and took longer, to return to their family with increasing separation distance from the family unit. The body length of displaced young mediated these relationships and their antipredator behaviour; larger young refuged more than smaller ones and were also less likely to be eaten by predators. These results suggest that selection should favour strong affiliative behaviour in mobile young animals towards their brood mates and protective parents because straying from the family unit leads to increased exposure to predation and a reduced likelihood of returning home with increasing separation distance.

Can convict Cichlids (Amatitlania siquia) socially learn the degree of predation risk associated with novel visual cues in their environment?

For many animals, the ability to distinguish cues indicative of predation risk from cues unrelated to predation risk is not entirely innate, but rather is learned and improved with experience. Two pathways to such learning are possible. First, an animal could initially express antipredator behaviour toward a wide range of cues and subsequently learn which of those cues are non-threatening. Alternatively, it could initially express no antipredator behaviour toward a wide range of cues and subsequently learn which of them are threatening. While the learned recognition of threatening cues may occur either through personal interaction with a cue (asocial learning) or through observation of the behaviour of social companions toward a cue (social learning), the learned recognition of non-threatening cues seems to occur exclusively through habituation, a form of asocial learning. Here, we tested whether convict cichlid fish (Amatitlaniasiquia) can socially learn to recognize visual cues in their environment as either threatening or non-threatening. We exposed juvenile convict cichlids simultaneously to a novel visual cue and one of three (visual) social cues: a social cue indicative of non-risk (the sight of conspecifics that had previously been habituated to the novel cue), a social cue indicative of predation risk (the sight of conspecifics trained to fear the novel cue), or a control treatment with no social cue. The subsequent response of focal fish, when presented with the novel cue alone, was not influenced by the social cue that they had previously witnessed. We therefore did not find evidence that convict cichlids in our study could use social learning to recognize novel visual cues as either threatening or non-threatening. We consider alternative explanations for our findings.

Disruptive camouflage impairs object recognition.

Whether hiding from predators, or avoiding battlefield casualties, camouflage is widely employed to prevent detection. Disruptive coloration is a seemingly well-known camouflage mechanism proposed to function by breaking up an object's salient features (for example their characteristic outline), rendering objects more difficult to recognize. However, while a wide range of animals are thought to evade detection using disruptive patterns, there is no direct experimental evidence that disruptive coloration impairs recognition. Using humans searching for computer-generated moth targets, we demonstrate that the number of edge-intersecting patches on a target reduces the likelihood of it being detected, even at the expense of reduced background matching. Crucially, eye-tracking data show that targets with more edge-intersecting patches were looked at for longer periods prior to attack, and passed-over more frequently during search tasks. We therefore show directly that edge patches enhance survivorship by impairing recognition, confirming that disruptive coloration is a distinct camouflage strategy, not simply an artefact of background matching.

Covariation and repeatability of male mating effort and mating preferences in a promiscuous fish.

Although mate choice by males does occur in nature, our understanding of its importance in driving evolutionary change remains limited compared with that for female mate choice. Recent theoretical models have shown that the evolution of male mate choice is more likely when individual variation in male mating effort and mating preferences exist and positively covary within populations. However, relatively little is known about the nature of such variation and its maintenance within natural populations. Here, using the Trinidadian guppy (Poecilia reticulata) as a model study system, we report that mating effort and mating preferences in males, based on female body length (a strong correlate of fecundity), positively covary and are significantly variable among subjects. Individual males are thus consistent, but not unanimous, in their mate choice. Both individual mating effort (including courtship effort) and mating preference were significantly repeatable. These novel findings support the assumptions and predictions of recent evolutionary models of male mate choice, and are consistent with the presence of additive genetic variation for male mate choice based on female size in our study population and thus with the opportunity for selection and further evolution of large female body size through male mate choice.

Are fast explorers slow reactors? Linking personality type and anti-predator behaviour.

Response delays to predator attack may be adaptive, suggesting that latency to respond does not always reflect predator detection time, but can be a decision based on starvation-predation risk trade-offs. In birds, some anti-predator behaviours have been shown to be correlated with personality traits such as activity level and exploration. Here, we tested for a correlation between exploration behaviour and response latency time to a simulated fish predator attack in a fish species, juvenile convict cichlids (Amatitlania nigrofasciata). Individual focal fish were subjected to a standardized attack by a robotic fish predator while foraging, and separately given two repeated trials of exploration of a novel environment. We found a strong positive correlation between exploration and time taken to respond to the predator model. Fish that were fast to explore the novel environment were slower to respond to the predator. Our study therefore provides some of the first experimental evidence for a link between exploration behaviour and predator-escape behaviour. We suggest that different behavioural types may differ in how they partition their attention between foraging and anti-predator vigilance.

Do female fruit flies (Drosophila serrata) copy the mate choice of others?

Female mate-choice copying is a social learning phenomenon whereby a female's observation of a successful sexual interaction between a male and another female increases her likelihood of subsequently preferring that male. Although mate-choice copying has been documented in several vertebrate species, to our knowledge it has not yet been investigated in insects. Here, we investigated whether female mate-choice copying occurs in the fruit fly Drosophila serrata, a model system for the study of mate preferences and the sexual selection they generate. We used two complementary experiments in which focal females were given a choice between two males that differed in either their apparent (as determined visually by the focal female) or actual recent mating success. Mate-choice copying was evaluated by testing whether focal females mated more frequently with the 'preferred' male as opposed to the other male. In both experiments, however, we found no evidence for mate-choice copying. We discuss possible reasons for the apparent absence of mate-choice copying in this species.

Behaviourally mediated crypsis in two nocturnal moths with contrasting appearance.

The natural resting orientations of several species of nocturnal moth on tree trunks were recorded over a three-month period in eastern Ontario, Canada. Moths from certain genera exhibited resting orientation distributions that differed significantly from random, whereas others did not. In particular, Catocala spp. collectively tended to orient vertically, whereas subfamily Larentiinae representatives showed a variety of orientations that did not differ significantly from random. To understand why different moth species adopted different orientations, we presented human subjects with a computer-based detection task of finding and 'attacking' Catocala cerogama and Euphyia intermediata target images at different orientations when superimposed on images of sugar maple (Acer saccharum) trees. For both C. cerogama and E. intermediata, orientation had a significant effect on survivorship, although the effect was more pronounced in C. cerogama. When the tree background images were flipped horizontally the optimal orientation changed accordingly, indicating that the detection rates were dependent on the interaction between certain directional appearance features of the moth and its background. Collectively, our results suggest that the contrasting wing patterns of the moths are involved in background matching, and that the moths are able to improve their crypsis through appropriate behavioural orientation.

Association patterns and shoal fidelity in the three-spined stickleback.

We investigated pairwise association patterns and shoal fidelity in free-ranging, individual three-spine sticklebacks (Gasterosteus aculeatus) by capturing entire shoals of sticklebacks and tagging each shoal member with a unique individual mark before releasing the shoal at the point of capture. We recaptured tagged fishes in the study area on five subsequent days, noting their identity, their location and the individuals with which they were associated. Stable partner associations between fishes were observed which might provide the basis for shoal fidelity via social networks. These results suggest the potential for the kinds of inter-individual association patterns assumed by models of predator inspection and 'tit-for-tat' behaviours in free-ranging fishes.

Body length variation within multi-species fish shoals: the effects of shoal size and number of species.

Theory predicts that selection should favour phenotypic homogeneity in fish shoals, and field studies have indeed confirmed that variation in body length within fish shoals is significantly lower than expected from a random distribution of fish among shoals. We investigated the extent to which variation in fish body length within shoals is determined by the shoal mean of body length, the number of species in a shoal, and the overall shoal size. We collected 34 fish shoals, ranging in size from 6 to 776 individuals, from the littoral zone of a Canadian lake. Shoals consisted of up to four different species, with multi-species shoals being larger and more frequent than single-species ones. The strongest determinant of body length variation within shoals was the shoal mean of body length, followed by the number of fish species in a shoal; i.e. multi-species shoals were less size-assorted than single-species ones. A more detailed analysis showed that the higher body length variation observed in multi-species shoals was due to increased body length variation both within and between component species. Shoal size had no significant effect on body length variation within shoals. Potential explanations of the positive relationship between body length variation and the number of species in a shoal are suggested. The implications of the above results for the evolution of multi-species shoals are discussed.