Microhabitat conditions drive uncertainty of risk and shape neophobic responses in Trinidadian guppies, Poecilia reticulata.

In response to uncertain risks, prey may rely on neophobic phenotypes to reduce the costs associated with the lack of information regarding local conditions. Neophobia has been shown to be driven by information reliability, ambient risk and predator diversity, all of which shape uncertainty of risk. We similarly expect environmental conditions to shape uncertainty by interfering with information availability. In order to test how environmental variables might shape neophobic responses in Trinidadian guppies (Poecilia reticulata), we conducted an in situ field experiment of two high-predation risk guppy populations designed to determine how the 'average' and 'variance' of several environmental factors might influence the neophobic response to novel predator models and/or novel foraging patches. Our results suggest neophobia is shaped by water velocity, microhabitat complexity, pool width and depth, as well as substrate diversity and heterogeneity. Moreover, we found differential effects of the 'average' and 'variance' environmental variables on food- and predator-related neophobia. Our study highlights that assessment of neophobic drivers should consider predation risk, various microhabitat conditions and neophobia being tested. Neophobic phenotypes are expected to increase the probability of prey survival and reproductive success (i.e. fitness), and are therefore likely linked to population health and species survival. Understanding the drivers and consequences of uncertainty of risk is an increasingly pressing issue, as ecological uncertainty increases with the combined effects of climate change, anthropogenic disturbances and invasive species.

Assessing effects of predator density and diversity on neophobia in Trinidadian guppies.

Neophobic predator avoidance, where prey actively avoid novel stimuli, is thought to allow prey to cope with the inability to predict predation risk (i.e. uncertainty) while reducing the costs associated with learning. Recent studies suggest that neophobia is elicited as a response to unpredictable and elevated mean predation risk, and is linked to experience with diverse novel cues. However, no research has disentangled the effects of predator density and diversity on neophobia. We conditioned Trinidadian guppies (Poecilia reticulata) to high- or low-diversity predator model treatments paired with high, intermediate, or low concentrations of conspecific alarm cues as a proxy for predator density. We tested behavioural responses to a novel stimulus vs. a water control to determine differences in neophobia among treatments. We found that neophobic shoaling behaviour was shaped by mean risk (predator density). However both density and diversity shaped neophobic freezing, and to a weaker extent, neophobic area use. Our research suggests that predator diversity might elicit neophobic responses in guppies, but only when mean risk is high enough. The relationship between neophobia and components of predation risk is becoming increasingly relevant as ecological uncertainty becomes more prevalent with increasing climate change, anthropogenic impacts, and invasive species.

Exploratory decisions of Trinidadian guppies when uncertain about predation risk.

Animals can reduce their uncertainty of predation risk by gathering new information via exploration behaviour. However, a decision to explore may also be costly due to increased predator exposure. Here, we found contextual effects of predation risk on the exploratory activity of Trinidadian guppies Poecilia reticulata in a novel environment. First, guppies were exposed to a 3-day period of either high or low background predation risk in the form of repeated exposure to either injured conspecific cues (i.e. alarm cues) or control water, respectively. A day later, guppies were moved into a testing arena with limited visual information due to structural barriers and were then presented with an acute chemical stimulus, either alarm cues (a known and reliable indicator of risk), a novel odour (an ambiguous cue), or control water. In the presence of control water, guppies from high and low background risk showed a similar willingness to explore the arena. However, high-risk individuals significantly reduced their spatial evenness, although not their movement latency, in the presence of both the alarm and novel cues. When these high-risk individuals were a member of a shoal, they became willing to explore the environment more evenly in the presence of alarm cues while remaining cautious toward the novel cue, indicating an effect of the greater uncertainty associated with the novel cue. In contrast, low-risk guppies showed a willingness to explore the arena regardless of acute threat or social context. Such contextual effects of background risk and social context highlight the complexity of exploratory decisions when uncertain.

Sensory-based quantification of male colour patterns in Trinidadian guppies reveals no support for parallel phenotypic evolution in multivariate trait space.

Parallel evolution, in which independent populations evolve along similar phenotypic trajectories, offers insights into the repeatability of adaptive evolution. Here, we revisit a classic example of parallelism, that of repeated evolution of brighter males in the Trinidadian guppy (Poecilia reticulata). In guppies, colonisation of low predation habitats is associated with emergence of 'more colourful' phenotypes since predator-induced viability selection for crypsis weakens while sexual selection by female preference for conspicuousness remains strong. Our study differs from previous investigations in three respects. First, we adopted a multivariate phenotyping approach to characterise parallelism in multitrait space. Second, we used ecologically-relevant colour traits defined by the visual systems of the two selective agents (i.e., guppy, predatory cichlid). Third, we estimated population genetic structure to test for adaptive (parallel) evolution against a model of neutral phenotypic divergence. We find strong phenotypic differentiation that is inconsistent with a neutral model but very limited support for the predicted pattern of greater conspicuousness at low predation. Effects of predation regime on each trait were in the expected direction, but weak, largely nonsignificant, and explained little among-population variation. In multitrait space, phenotypic trajectories of lineages colonising low from high predation regimes were not parallel. Our results are consistent with reduced predation risk facilitating adaptive differentiation, potentially by female choice, but suggest that this proceeds in independent directions of multitrait space across lineages. Pool-sequencing data also revealed SNPs showing greater differentiation than expected under neutrality, among which some are found in genes contributing to colour pattern variation, presenting opportunities for future genetic study.

Social partner cooperativeness influences brain oxytocin transcription in Trinidadian guppies (Poecilia reticulata).

For non-kin cooperation to be maintained, individuals need to respond adaptively to the cooperative behaviour of their social partners. Currently, however, little is known about the biological responses of individuals to experiencing cooperation. Here, we quantify the neuroregulatory response of Trinidadian guppies (Poecilia reticulata) experiencing cooperation or defection by examining the transcriptional response of the oxytocin gene (oxt; also known as isotocin), which has been implicated in cooperative decision-making. We exposed wild-caught females to social environments where partners either cooperated or defected during predator inspection, or to a control (non-predator inspection) context, and quantified the relative transcription of the oxt gene. We tested an experimental group, originating from a site where individuals are under high predation threat and have previous experience of large aquatic predators (HP), and a control group, where individuals are under low predation threat and naïve to large aquatic predators (LP). LP, but not HP, fish showed different behavioural responses to the behaviour of their social environment, cooperating with cooperative partners and defecting when paired with defecting ones. In HP, but not LP, fish brain mid-section oxt relative transcription varied depending on social partner behaviour. HP fish experiencing cooperation during predator inspection had lower oxt transcription than those experiencing defection. This effect was not present in the control population or in the control context, where the behaviour of social partners did not affect oxt transcription. Our findings provide insight into the neuromodulation underpinning behavioural responses to social experiences, and ultimately to the proximate mechanisms underlying social decision-making.

Numerical abundance and biomass reveal different temporal trends of functional diversity change in tropical fish assemblages.

Understanding how the biodiversity of freshwater fish assemblages changes over time is an important challenge. Until recently most emphasis has been on taxonomic diversity, but it is now clear that measures of functional diversity (FD) can shed new light on the mechanisms that underpin this temporal change. Fish biologists use different currencies, such as numerical abundance and biomass, to measure the abundance of fish species. Nonetheless, because they are not necessarily equivalent, these alternative currencies have the potential to reveal different insights into trends of FD in natural assemblages. In this study, the authors asked how conclusions about temporal trends in FD are influenced by the way in which the abundance of species has been quantified. To do this, the authors computed two informative metrics, for each currency, for 16 freshwater fish assemblages in Trinidad's Northern Range that had been surveyed repeatedly over 5 years. The authors found that numerical abundance and biomass uncover different directional trends in these assemblages for each facet of FD, and as such inform hypotheses about the ways in which these systems are being restructured. On the basis of these results, the authors concluded that a combined approach, in which both currencies are used, contributes to our understanding of the ecological processes that are involved in biodiversity change in freshwater fish assemblages.

Causal evidence for the adaptive benefits of social foraging in the wild.

Sociality is a fundamental organizing principle across taxa, thought to come with a suite of adaptive benefits. However, making causal inferences about these adaptive benefits requires experimental manipulation of the social environment, which is rarely feasible in the field. Here we manipulated the number of conspecifics in Trinidadian guppies (Poecilia reticulata) in the wild, and quantified how this affected a key benefit of sociality, social foraging, by investigating several components of foraging success. As adaptive benefits of social foraging may differ between sexes, we studied males and females separately, expecting females, the more social and risk-averse sex in guppies, to benefit more from conspecifics. Conducting over 1600 foraging trials, we found that in both sexes, increasing the number of conspecifics led to faster detection of novel food patches and a higher probability of feeding following detection of the patch, resulting in greater individual resource consumption. The extent of the latter relationship differed between the sexes, with males unexpectedly exhibiting a stronger social benefit. Our study provides rare causal evidence for the adaptive benefits of social foraging in the wild, and highlights that sex differences in sociality do not necessarily imply an unequal ability to profit from the presence of others.

Exploring the threat-sensitive predator avoidance hypothesis on mate competition in two wild populations of Trinidadian guppies.

The intensity of mate competition is often influenced by predation pressure. The threat-sensitive predator avoidance hypothesis predicts that prey should precisely adjust their fitness-related activities to the level of perceived acute predation risk and this effect should be stronger under high background risk. Individuals should compensate during periods of moderate risk for lost opportunities during high risk. Our study examined the interaction between acute and background predation risk on mate competition. Under laboratory conditions, we explored the effects of acute risk (low vs. high) using chemical alarm cue (AC; control (results presented in Chuard et al. (2016)) The effects of adult sex ratio on mating competition in male and female guppies (Poecilia reticulata) in two wild populations. Behav Process 129:1-10), 25 % concentration, and 100 % concentration), and population of origin (low vs. high background risk) on mate competition in guppies (Poecilia reticulata). Surprisingly, males favored courtship over forced mating under acute predation risk irrespective of background risk, potentially benefiting from a female preference for bold males. We discuss our results in the context of chemical threat-sensitivity and resource differences in defendability (e.g. mates vs. food).

The propensity for re-triggered predation fear in a prey fish.

Variation in predation risk can drive variation in fear intensity, the length of fear retention, and whether fear returns after waning. Using Trinidadian guppies, we assessed whether a low-level predation threat could easily re-trigger fear after waning. First, we show that background risk induced neophobia after either multiple exposures to a low-level threat or a single exposure to a high-level threat. However, a single exposure to the low-level threat had no such effect. The individuals that received multiple background exposures to the low-level threat retained their neophobic phenotype over an 8-day post-risk period, and this response was intensified by a single re-exposure to the low-level threat on day 7. In contrast, the neophobia following the single high-level threat waned over the 8-day period, but the single re-exposure to the low-level threat on day 7 re-triggered the neophobic phenotype. Thus, despite the single low-level exposure being insufficient to induce neophobia, it significantly elevated existing fear and re-triggered fear that had waned. We highlight how such patterns of fear acquisition, retention, and rapid re-triggering play an important role in animal ecology and evolution and outline parallels between the neophobic phenotype in fishes and dimensions of post-traumatic stress in humans.

An evaluation of the public's Knowledge, Attitudes and Practices (KAP) in Trinidad and Tobago regarding sharks and shark consumption.

There is a global lack of data concerning shark consumption trends, consumer attitudes, and public knowledge regarding sharks. This is the case in Trinidad and Tobago, where shark is a popular culinary delicacy. A Knowledge, Attitudes, and Practices (KAP) survey was conducted in Trinidad and Tobago. Six hundred and seven questionnaires were administered. Univariate and stepwise multivariate logistic regressions were performed to test the association between KAP and demographic categories. The response rate was 93.4% with 567 questionnaires returned (473 from Trinidad and 94 from Tobago). Two hundred and seventeen (38.3%) participants were knowledgeable, 422 (74.4%) displayed attitudes in favour of shark conservation and sustainable use, and 270 (47.6%) displayed practices promoting shark conservation and sustainable use. Island (AOR = 2.81, CI = 1.78, 4.46) and tertiary education (AOR = 2.31, CI = 1.20, 4.46) significantly influenced knowledge level. Gender (AOR = 1.50, CI = 1.02, 2.20) and island (AOR = 0.56, CI = 0.35, 0.90) significantly influenced attitude. Gender (COR = 1.59, CI = 1.14, 2.22) was significantly associated with practices. Over 70% of respondents ate shark, and 54.7% ate shark infrequently enough to avoid risks from heavy metal toxicity. Our results may be useful to develop public awareness and practice improvement initiatives in order to improve KAP regarding shark meat consumption.

A Matador-like Predator Diversion Strategy Driven by Conspicuous Coloration in Guppies.

Understanding the adaptive function of conspicuous coloration has been a major focus of evolutionary biology for much of the last century. Although considerable progress has been made in explaining how conspicuous coloration can be used in functions as diverse as sexual and social signaling, startling predators, and advertising toxicity [1], there remain a multitude of species that display conspicuous coloration that cannot be explained by existing theory. Here we detail a new "matador-like" divertive antipredator strategy based on conspicuous coloration in Trinidadian guppies (Poecilia reticulata). Guppies encountering predatory fish rapidly enhance the conspicuousness of their eyes by blackening their irises. By pitting biomimetic robotic guppies against real predatory fish, we show this conspicuous eye coloration diverts attacks away from the guppies' center of mass to their head. To determine the function of this seemingly counterintuitive behavior, we developed a method for simulating escape probabilities when live prey interact with ballistic attacking predators, and find this diversion effect significantly benefits black-eyed guppies because they evade capture by rapidly pivoting away from the predator once it has committed to its attack. Remarkably, this antipredator strategy reverses the commonly observed negative scaling relationship between prey size and evasive ability, with larger fish benefiting most from diverting predators. Taken together, our results introduce a new antipredator divertive strategy that may be widely used by conspicuously colored prey that rely on agility to escape their predators.

Sender and receiver experience alters the response of fish to disturbance cues.

Predation is a pervasive selection pressure, shaping morphological, physiological, and behavioral phenotypes of prey species. Recent studies have begun to examine how the effects of individual experience with predation risk shapes the use of publicly available risk assessment cues. Here, we investigated the effects of prior predation risk experience on disturbance cue production and use by Trinidadian guppies Poecilia reticulata under laboratory conditions. In our first experiment, we demonstrate that the response of guppies from a high predation population (Lopinot River) was dependent upon the source of disturbance cue senders (high vs. low predation populations). However, guppies collected from a low predation site (Upper Aripo River) exhibited similar responses to disturbance cues, regardless of the sender population. In our second experiment, we used laboratory strain guppies exposed to high versus low background risk conditions. Our results show an analogous response patterns as shown for our first experiment. Guppies exposed to high background risk conditions exhibited stronger responses to the disturbance cues collected from senders exposed to high (vs. low) risk conditions and guppies exposed to low risk conditions were not influenced by sender experience. Combined, our results suggest that experience with background predation risk significantly impacts both the production of and response to disturbance cues in guppies.

High-risk environments promote chemical disturbance signalling among socially familiar Trinidadian guppies.

Under predation threat, many species produce cues that can serve as crucial sources of information for social companions. For instance, chemical cues released when experiencing a disturbing event (i.e. 'disturbance cues'), such as a predator chase, can lead to antipredator avoidance and increased survival for nearby individuals. These chemicals also have potential to be produced as a voluntary signal for communicating threat to others. We found evidence for this hypothesis by manipulating the shoal familiarity of guppies from populations differing in background predation risk and then presenting their disturbance cues to unfamiliar conspecifics from the same populations. Receivers from low-risk sites increased shoal cohesion and decreased area use regardless of whether the disturbance cues were produced in donor groups where members were familiar or unfamiliar with each other. However, receivers from high-risk sites showed strong antipredator reactions towards disturbance chemicals produced in familiar groups and no response towards those produced in unfamiliar groups, suggesting that donors from high-risk sites may alter the quality or quantity of their disturbance cues to influence familiar individuals to enact predator defences. Because high-risk environments strengthen guppy social networks, these environments may facilitate reliance on chemical disturbance signalling to coordinate group defences with familiar individuals.

Females facilitate male food patch discovery in a wild fish population.

Responding to the information provided by others is an important foraging strategy in many species. Through social foraging, individuals can more efficiently find unpredictable resources and thereby increase their foraging success. When individuals are more socially responsive to particular phenotypes than others, however, the advantage they obtain from foraging socially is likely to depend on the phenotype composition of the social environment. We tested this hypothesis by performing experimental manipulations of guppy, Poecilia reticulata, sex compositions in the wild. Males found fewer novel food patches in the absence of females than in mixed-sex compositions, while female patch discovery did not differ regardless of the presence or absence of males. We argue that these results were driven by sex-dependent mechanisms of social association: Markov chain-based fission-fusion modelling revealed that less social individuals found fewer patches and that males reduced sociality when females were absent. In contrast, females were similarly social with or without males. Our findings highlight the relevance of considering how individual- and population-level traits interact in shaping the advantages of social foraging in the wild.

Evolution of non-kin cooperation: social assortment by cooperative phenotype in guppies.

Cooperation among non-kin constitutes a conundrum for evolutionary biology. Theory suggests that non-kin cooperation can evolve if individuals differ consistently in their cooperative phenotypes and assort socially by these, such that cooperative individuals interact predominantly with one another. However, our knowledge of the role of cooperative phenotypes in the social structuring of real-world animal populations is minimal. In this study, we investigated cooperative phenotypes and their link to social structure in wild Trinidadian guppies (Poecilia reticulata). We first investigated whether wild guppies are repeatable in their individual levels of cooperativeness (i.e. have cooperative phenotypes) and found evidence for this in seven out of eight populations, a result which was mostly driven by females. We then examined the social network structure of one of these populations where the expected fitness impact of cooperative contexts is relatively high, and found assortment by cooperativeness, but not by genetic relatedness. By contrast, and in accordance with our expectations, we did not find assortment by cooperativeness in a population where the expected fitness impact of cooperative contexts is lower. Our results provide empirical support for current theory and suggest that assortment by cooperativeness is important for the evolution and persistence of non-kin cooperation in real-world populations.

Individual- and population-level drivers of consistent foraging success across environments.

Individual foraging is under strong natural selection. Yet, whether individuals differ consistently in their foraging success across environments, and which individual- and population-level traits might drive such differences, is largely unknown. We addressed this question in a field experiment, conducting over 1,100 foraging trials with subpopulations of guppies, Poecilia reticulata, translocated across environments in the wild. We show that individuals consistently differed in reaching and acquiring food resources, but not control 'resources', across environments. Social individuals reached and acquired more food resources than less-social ones and males reached more food resources than females. Yet, overall, individuals were more likely to join females at resources than males, which might explain why individuals in subpopulations with relatively more females reached and acquired, on average, more food resources. Our results provide rare evidence for individual differences in foraging success across environments, driven by individual- and population-level (sex ratio) traits.

Dynamic eye colour as an honest signal of aggression.

Animal eyes are some of the most widely recognisable structures in nature. Due to their salience to predators and prey, most research has focused on how animals hide or camouflage their eyes [1]. However, across all vertebrate Classes, many species actually express brightly coloured or conspicuous eyes, suggesting they may have also evolved a signalling function. Nevertheless, perhaps due to the difficulty with experimentally manipulating eye appearance, very few species beyond humans [2] have been experimentally shown to use eyes as signals [3]. Using staged behavioural trials we show that Trinidadian guppies (Poecilia reticulata), which can rapidly change their iris colour, predominantly express conspicuous eye colouration when performing aggressive behaviours towards smaller conspecifics. Furthermore, using a novel, visually realistic robotic system to create a mismatch between signal and relative competitive ability, we show that eye colour is used to honestly signal aggressive motivation. Specifically, robotic 'cheats' (that is, smaller, less-competitive robotic fish that display aggressive eye colouration when defending a food patch) attracted greater food competition from larger real fish. Our study suggests that eye colour may be an under-appreciated aspect of signalling in animals, shows the utility of our biomimetic robotic system for investigating animal behaviour, and provides experimental evidence that socially mediated costs towards low-quality individuals may maintain the honesty of dynamic colour signals.

Divergent biodiversity change within ecosystems.

The Earth's ecosystems are under unprecedented pressure, yet the nature of contemporary biodiversity change is not well understood. Growing evidence that community size is regulated highlights the need for improved understanding of community dynamics. As stability in community size could be underpinned by marked temporal turnover, a key question is the extent to which changes in both biodiversity dimensions (temporal α- and temporal ß-diversity) covary within and among the assemblages that comprise natural communities. Here, we draw on a multiassemblage dataset (encompassing vertebrates, invertebrates, and unicellular plants) from a tropical freshwater ecosystem and employ a cyclic shift randomization to assess whether any directional change in temporal α-diversity and temporal ß-diversity exceeds baseline levels. In the majority of cases, α-diversity remains stable over the 5-y time frame of our analysis, with little evidence for systematic change at the community level. In contrast, temporal ß-diversity changes are more prevalent, and the two diversity dimensions are decoupled at both the within- and among-assemblage level. Consequently, a pressing research challenge is to establish how turnover supports regulation and when elevated temporal ß-diversity jeopardizes community integrity.

Individual variation in reproductive behaviour is linked to temporal heterogeneity in predation risk.

Variation in predation risk is a major driver of ecological and evolutionary change, and, in turn, of geographical variation in behaviour. While predation risk is rarely constant in natural populations, the extent to which variation in predation risk shapes individual behaviour in wild populations remains unclear. Here, we investigated individual differences in reproductive behaviour in 16 Trinidadian guppy populations and related it to the observed variation in predator biomass each population experienced. Our results show that high heterogeneity in predator biomass is linked to individual behavioural diversification. Increased within-population heterogeneity in predator biomass is also associated with behavioural polymorphism. Some individuals adjust the frequency of consensual mating behaviour in response to differences in sex ratio context, while others display constantly at elevated frequencies. This pattern is analogous to a 'live fast, die young' pace-of-life syndrome. Notably, both high and low mean differences in predator biomass led to a homogenization of individual frequency of consensual mating displays. Overall, our results demonstrate that individual behavioural variation is associated with heterogeneity in predator biomass, but not necessarily with changes in mean values of predator biomass. We suggest that heterogeneity in predator biomass is an informative predictor of adaptive responses to changes in biotic conditions.