Influence of prey foraging posture on flight behavior and predation risk: predators take advantage of unwary prey

Foraging in animals is often associated with characteristicbody postures, such as the head-down posture. When foragingconflicts with the ability to detect predators or to flee, individualsmay incur a greater risk of mortality to predation than otherwise.Here we investigate the influence of different foraging postures(horizontal versus nose-down body posture) on the ability ofindividuals to respond to approaching predators and on the riskof mortality to predation in the guppy (Poecilia reticulata).Individuals engaged in nose-down foraging were assumed to beable to visually scan a smaller area for predators and to escapeless effectively due to their body posture, and thus are morevulnerable to stalking predators than horizontally foragingones. In a first experiment, we separately exposed nonforaging,horizontally foraging, and nose-down foraging guppies to anapproaching cichlid fish predator model. Nonforaging guppiesreacted sooner to and initiated flight further away from theapproaching model than did foraging fish collectively, and horizontallyforaging individuals responded sooner to the model than nose-downforaging ones. Comparing all test guppies, nose-down foragingindividuals were the most likely not to exhibit any responseto the predator model. When presented with a simultaneous choiceof two guppies behind a one-way mirror, individual blue acaracichlid (Aequidens pulcher), a natural predator of the guppy,preferred to attack foraging guppies over nonforaging ones andnose-down foraging guppies over horizontally foraging individuals.In a final experiment with free-swimming cichlids and guppies,we demonstrated that individual risk of predation for guppiesforaging nose down was greater than for guppies foraging horizontally,and both were at greater risk than nonforaging guppies. Thislatter result is consistent with the above differences in theguppy's responsiveness to approaching predators depending ontheir foraging behavior, and with the finding that cichlid predatorspreferred fish that were less likely to show any response tothem. Our results therefore indicate that the ability to respondto approaching predators and the risk of mortality to predationin the guppy is strongly influenced by their foraging activity,and in particular their foraging posture, and that cichlid predatorspreferentially select less wary and more vulnerable guppies.[BehavEcol 7: 264–271 (1996)]     

Ornamental evolution in Trinidadian guppies (Poecilia reticulata): insights from sensory processing‐based analyses of entire colour patterns

The evolution of exaggerated sexual ornamentation is classically thought to proceed as a compromise between opposing vectors of sexual and natural selection. In colour‐based ornamentation, as exhibited by guppies (Poecilia reticulata), heightened trait expression may be beneficial in promoting attractiveness, but costly in terms of predation. Opportunities to reconcile this compromise will exist if there are differences between conspecifics and predators in their sensory systems; in such situations guppies should evolve to exploit the ways in which their ornamentation would appear maximally conspicuous to conspecifics. In the present study, we addressed this hypothesis via a study of geographic variation employing the most sophisticated colour analysis yet attempted for Trinidadian guppies. We made two paired contrasts, one between two Aripo populations that vary in the presence of the potential predator Aequidens pulcher, and another between Quare and Marianne populations that vary in exposure to a predatory prawn, Macrobrachium crenulatum. We predicted that, if ornamentation is constrained by the presence of either predator, then guppy conspicuousness should change most markedly across each of the two paired populations as viewed by that predator. Although disparity analysis of entire colour patterns indicated significant differences in both contrasts, this prediction was most clearly supported for the Marianne/Quare contrast. Marianne fish, which co‐exist with prawns, exhibited larger black spots coupled with less extensive, less bright flank iridescence. The brightness reductions are notable because, as the only potential guppy predator with a dedicated ultraviolet (UV) photoreceptor, prawns may detect passing male guppies via their UV‐bright blues, violets and ‘UV/oranges’. We discuss our findings in light of the additional insights that might be obtained by combining spectral assessments and visual modeling with more traditional methods of colour pattern appraisal. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 734–747.     

Independent Mating Preferences for Male Body Size and Coloration in Female Trinidadian Guppies

Although females in numerous species generally prefer males with larger, brighter and more elaborate sexual traits, there is nonetheless considerable intra‐ and interpopulation variation in mating preferences amongst females that requires explanation. Such variation exists in the Trinidadian guppy, Poecilia reticulata, an important model organism for the study of sexual selection and mate choice. While female guppies tend to prefer more ornamented males as mates, particularly those with greater amounts of orange coloration, there remains variation both in male traits and female mating preferences within and between populations. Male body size is another trait that is sexually selected through female mate choice in some species, but has not been examined as extensively as body coloration in the guppy despite known intra‐ and interpopulation variation in this trait among adult males and its importance for survivorship in this species. In this study, we used a dichotomous‐choice test to quantify the mating preferences of female guppies, originating from a low‐predation population in Trinidad, for two male traits, body length and area of the body covered with orange and black pigmentation, independently of each other. We expected strong female mating preferences for both male body length and coloration in this population, given relaxation from predation and presumably relatively low cost of choice. Females indeed exhibited a strong preference for larger males as expected, but surprisingly a weaker (but nonetheless significant) preference for orange and black coloration. Interestingly, larger females demonstrated stronger preferences for larger males than did smaller females, which could potentially lead to size‐assortative mating in nature.     

Conspicuous male coloration impairs survival against avian predators in Aegean wall lizards,Podarcis erhardii

Animal coloration is strikingly diverse in nature. Within‐species color variation can arise through local adaptation for camouflage, sexual dimorphism and conspicuous sexual signals, which often have conflicting effects on survival. Here, we tested whether color variation between two island populations of Aegean wall lizards (Podarcis erhardii) is due to sexual dimorphism and differential survival of individuals varying in appearance. On both islands, we measured attack rates by wild avian predators on clay models matching the coloration of real male and female P. erhardii from each island population, modeled to avian predator vision. Avian predator attack rates differed among model treatments, although only on one island. Male‐colored models, which were more conspicuous against their experimental backgrounds to avian predators, were accordingly detected and attacked more frequently by birds than less conspicuous female‐colored models. This suggests that female coloration has evolved primarily under selection for camouflage, whereas sexually competing males exhibit costly conspicuous coloration. Unexpectedly, there was no difference in avian attack frequency between local and non‐local model types. This may have arisen if the models did not resemble lizard coloration with sufficient precision, or if real lizards behaviorally choose backgrounds that improve camouflage. Overall, these results show that sexually dimorphic coloration can affect the risk of predator attacks, indicating that color variation within a species can be caused by interactions between natural and sexual selection. However, more work is needed to determine how these findings depend on the island environment that each population inhabits.     

Another battle of the sexes: the consequences of sexual asymmetry in mating costs and predation risk in the guppy, Poecilia reticulata.

The risk of predation and cost or benefit of a mating attempt are rarely the same for both sexes. An excellent example is provided by the guppy. Poecilia reticulata, a species that has a promiscuous mating system in which female choice plays an important role. Male engage almost continuously in courtship behaviour but, as females are sexually receptive for short periods only, most male displays are ignored and sneaky mating attempts avoided. Experiments on guppies from wild Trinidad populations reveal that females appear to perceive themselves to be at a greater risk of predation and devote more time to antipredator behaviour, for example, schooling when threatened. Inspections of the predator are also mainly initiated and led by female guppies. Males exploit this behavioural switch by increasing their sneaky mating attempts. A game theoretical analysis is used to explore the sexual asymmetry in mating cost and predation risk. Together these approaches show that there is no intersexual cooperation during predator inspection behaviour in this species, and may explain the paradoxical increase in mating activity by male guppies under threat.     

Phenotypic variation in male guppies from natural inland populations: an additional test of Haskins' sexual selection/predation hypothesis

Synopsis In Venezuela, guppies,Poecilia reticulata, are found in a diversity of aquatic ecosystems fringing the western slope of the eastern Andes. These inland drainages are associated with large between-site variation in both physical and biotic environments. Numbers of potential guppy predators vary greatly between low diversity piedmont streams and high diversity llanos swamps. We analyze geographic variation in several phenotypic traits associated with conspicuousness of male guppies as an independent test of Haskins' (Haskins et al. 1961) hypothesis of natural balance between sexual selection (driving male conspicuousness) and predation (driving crypsis). Four sites were compared: a diverse llanos swamp (high predation), two Andean piedmont streams (intermediate and low predation), and a spring pool located south of Venezuela's Paría Peninsula (no aquatic predators). Because tropical wet and dry seasons are associated with varying degrees of environmental change at these sites, within-site seasonal samples provided an additional test of the role of selective predation on Male phenotypes. Phenotypic traits associated with both size and coloration supported the sexual selection/predation hypothesis. male guppies from the spring were generally more colorful than male guppies from inland drainages. Males from the diverse swamp site were smaller and less colorful than guppies from other sites. Males from the swamp population were smallest and least colorful during the early dry season, when diurnal aquatic piscivores were more diverse and abundant. Dominant spot pigments at each site were generally those that provided greatest contrast with the predominant environmental background color, lending further evidence that coloration patterns in male guppies enhance conspicuousness.     

Phenotypic correlates of spermatozoon quality in the guppy, Poecilia reticulata

The phenotype-linked fertility hypothesis suggests that a femalecan benefit directly from mate choice when the cues she usesindicate the quantity and/or quality of his spermatozoa. Wetested the link between sperm quality and male body size andcoloration in the resource-free mating system of the guppy,a tropical fish characterized by strong female choice. Largermales possessed larger testes and are therefore predicted toproduce larger numbers of spermatozoa than smaller males. Largermale guppies also produced longer spermatozoa than smaller males.Degree of carotenoid coloration did not predict either the quantityor the quality of a male's spermatozoa. These results are consistentwith a previous study that showed that female guppies in thestudy population prefer larger males to brightly colored males.The male-size directed increase in spermatozoon size may bethe result of interplay between sperm competition and the coevolutionof spermatozoon traits with the female reproductive tract.     

Discriminating between Hungry and Satiated Predators: The Response of Guppies (Poecilia reticulata) from High and Low Predation Sites1

Fixed anti-predator activities are costly because they limit the ability of the prey to take advantage of short term temporal patchiness in predation pressure. The ability to discriminate between hungry and satiated predators and a flexible response to the differential threat can help to lower the costs of anti-predator behavior. In this study Trinidadian guppies (Poecilia reticulata) were found to distinguish between hungry and satiated predators. In Trinidad, populations of guppies experience different levels of predation from piscivorous fish. Individuals taken from populations with chronically high predation pressure responded stronger to the hungry predator than those from low predation sites.     

A further cost for the sicker sex? Evidence for male‐biased parasite‐induced vulnerability to predation

Males are typically the sicker sex. Data from multiple taxa indicate that they are more likely to be infected with parasites, and are less “tolerant,” or less able to mitigate the fitness costs of a given infection, than females. One cost of infection for many animals is an increased probability of being captured by a predator. A clear, hitherto untested, prediction is therefore that this parasite‐induced vulnerability to predation is more pronounced among males than females. We tested this prediction in the sexually size dimorphic guppy, Poecilia reticulata, in which females are typically larger than males. We either sham or experimentally infected guppies with Gyrodactylus turnbulli, elicited their escape response using an established protocol and measured the distance they covered during 60 ms. To discriminate between the effects of body size and those of other inherent sex differences, we size‐matched fish across treatment groups. Infection with G. turnbulli reduced the distance covered during the escape response of small adults by 20.1%, whereas that of large fish was unaffected. This result implies that parasite‐induced vulnerability to predation is male‐biased in the wild: although there was no difference in escape response between our experimentally size‐matched groups of males and females, males are significantly smaller across natural guppy populations. These results are consistent with Bateman's principle for immunity: Natural selection for larger body sizes and longevity in females seems to have resulted in the evolution of increased infection tolerance. We discuss the potential implications of sex‐ and size‐biased parasite‐induced vulnerability to predation for the evolutionary ecology of this host–parasite interaction in natural communities.     

Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata)

In the guppy (Poecilia reticulata), males have two alternative mating tactics. Individual males may either display to a receptive female prior to attempting to copulate with her or attempt to quickly sneakcopulate with a female without first displaying to her or without a prior receptive response from her. In this study, I experimentally investigated the effects of simulated local increases in the risk of predation (in the form of a cichlid fish predator model in situ) on the mating tactics used by free-ranging male guppies in two typical macrohabitats (riffle and pool) of a Trinidadian river. Focal male guppies displayed to females significantly less often on average, and conversely attempted sneak copulations more often, in the presence of the predator model than in its absence; this pattern was similar for both habitats. These fish therefore performed a lower proportion of sigmoid displays and increased their sneaky mating attempts when the apparent risk of predation had increased locally. This predator-mediated response is consistent with a trade-off between mating success and risk of mortality due to predation. The results are the first to confirm risk-sensitive mating behaviour in free-ranging male guppies within a population, and demonstrate the potential importance of predators in influencing the relative use of alternative mating tactics in this species on a microgeographical scale in the wild.     

Metabolic stoichiometry and the ecology of fear in Trinidadian guppies: consequences for life histories and stream ecosystems

Consumer-driven nutrient recycling, the release of chemicals as byproducts and excesses of consumer physiology, can alter ecosystems by changing the availability of limiting nutrients at the base of the food web. The mere presence of predators can alter consumer physiology by restricting food intake and inducing stress. Predation risk, then, can influence ecosystem function by modifying the role of prey as nutrient recyclers, yet there are few empirical tests of how predation risk alters nutrient recycling by prey. Here, we present the results of a test for the effects of predation risk on the C and N budgets of Trinidadian guppies (Poecilia reticulata). We reared female guppies for 7 weeks on diets of varying quality, and we compared control individuals to those exposed continuously to chemical cues emitted by a guppy predator, Crenicichla alta. We measured food consumption, growth rate, tissue elemental stoichiometry and N excretion by guppies on all treatments. Guppies strongly reduced food intake in the presence of predator cues; however, cue-exposed guppies assimilated nutrients more efficiently than controls. Specifically, cue-exposed guppies strongly increased N retention efficiency while only moderately increasing C efficiency. Consequently, guppies reared with predator cues excreted 39 % less N than control guppies. We suggest that reduced foraging, enhanced nutrient efficiency, and decreased N excretion are adaptive responses to the extrinsic mortality threat posed by guppy predators. The resulting substantial reduction in N excretion by guppies may influence ecosystem function in natural streams by reducing the supply of a limiting nutrient.     

Relationship between algal-foraging ability and expression of sexually selected traits in male guppies

In the guppy Poecilia reticulata, males exhibit orange spots on their body and tail, and the orange spot patterns are often criteria for female mate choice. The orange spot coloration of males is determined by the intake of algae, a natural source of carotenoids. Therefore, males exhibiting conspicuous orange coloration are considered to possess high algal-foraging ability. In the present study, we examined the influence of algal-foraging ability, measured by algal-searching ability and algal-foraging frequency, on the expression of orange spot patterns and on other sexually selected traits in male guppies. Males exhibiting better performance in terms of both algal-searching ability and algal-foraging frequency grew larger. The size of the orange spots on males also increased with algal-foraging ability. However, neither algal-searching ability nor algal-foraging frequency influenced the coloration of the orange spots. In this experiment, a limited supply of carotenoids possibly prevented the males from completely developing their spots to the intrinsic size. The results of this study suggest that in male guppies under a carotenoid-limited situation, the allocation of carotenoids is directed toward enlargement of the size of the orange spots rather than enhancement of their coloration. Since both the body size and orange spot patterns of males contribute to their sexual attractiveness to females, high algal-foraging ability may enhance their mating success.     

Mate-choice copying under predation risk in the Trinigadian guppy (Poecilia reticulata)

Although females of numerous species possess genetically-basedpreferences for certain male trails and male preferentiallywith males possessing these traits, recent theoretical and experimentalevidence indicates that they may also copy (imitate) the matechoices of other females under certain circumstances. Such mate-choicecopying is expected to be most prevalent when females have theopportunity to observe the mate choices of others and when matechoice is costly to females. One potential direct fitness costof mate choice is increased individual risk of mortality dueto predation. Here, we investigate for the first time the effectof increasing the apparent risk of predation on the tendencyof females to copy the experimentally staged mate choice ofanother female. Using adult female guppies (Poecilia reticulata)originating from a Trinidadian population that experiences arelatively high fish predation pressure, we first establishthat they possess a preference for the more brighdy coloredof two simultaneously presented males in the absence of bothmate-copying opportunity and an immediate threat of predation.However, most females reversed their initial mate preferencewhen given an opportunity to copy the mate preference of anotherfemale in the absence of predation threat The proportion offemales reversing their preference when given the opportunityto do so was not affected by increasing the apparent risk of(fish) predation. This result may be owing either to femaleguppies tending to copy the mate choice of others whenever theopportunity arises because the benefits of doing so accrue irrespectiveof the ambient risk of predation or to females choosing randomlybetween males with respect to their color pattern in the presenceof the predator irrespective of mate-copying opportunity. Thesetwo explanations for the apparent lack of an effect of predationrisk on mate-choice copying per se are both plausible but unfortunatelycould not be easily distinguished here. It may thus be possible,and interesting, that individual female guppies chose randomlybetween the available males in the presence of the predatorbut otherwise copied the choice of others when given the opportunityto do so.     

Crickets with extravagant mating songs compensate for predation risk with extra caution

Modern models for the evolution of conspicuous male mating displays assume that males with conspicuous displays must bear the cost of enhanced predation risk. However, if males can compensate behaviourally for their increased conspicuousness by acting more cautiously towards predators, they may be able to lower this cost. In the field cricket Gryllus integer, males call to attract females, and differ in their durations of uninterrupted trilling (calling-bout lengths). Differences among males in calling-bout lengths are heritable, and females prefer males with longer calling bouts. In this study, males with longer, more conspicuous songs behaved more cautiously than males with shorter songs on two different tests of predator avoidance. They took longer to emerge from a safe shelter within a novel, potentially dangerous environment, and they ceased calling for a longer time when their calls were interrupted by a predator cue. Thus, these males appear to compensate behaviourally for their more conspicuous mating displays. Additionally, latencies to emerge from a shelter in the novel environment were consistent over time for both individual males from the field and males that had been reared in the laboratory, indicating that the differences in latency among males may be heritable.     

Do bright colors at nests incur a cost due to predation?

Summary Birds show much interspecific variation in the coloration and brightness of their plumage. I examine the hypothesis that selection due to predation on incubating birds and their nest contents can explain part of this diversity. First, I argue that rather than using absolute rates of nest predation to make predictions about the costs of conspicuous colours, we should measure experimentally whether increases in plumage conspicuousness elevate rates of nest predation. Second, I present experimental data investigating the cost of red and brown colour at ground and tree nests. These data provide the first evidence that bright colours do attract predators to nests and that, in addition, this cost varies according to the nesting site. Natural selection seems to most strongly oppose the evolution of conspicuous colours in ground-nesting birds.     

The fitness consequences of the autotomous blue tail in lizards: an empirical test of predator response using clay models

Numerous vertebrates employ one or more autotomous body parts as an anti-predation mechanism. Many lizards possess an autotomous tail that is brightly colored blue, which has been suggested to either serve as a decoy mechanism to divert predator attention to the autotomous body part, as an interspecific signal, or as an aposematic signal to predators that it is distasteful or dangerous. While theoretical studies suggest that a conspicuous autotomous body part that increases the probability of escape while not increasing the rate of detection will be favorable over a completely cryptic form, there is little empirical evidence supporting the adaptive benefit of an autotomous blue tail. We used in situ clay models of a scincid lizard to test the fitness consequences of blue coloration. Lizard models with a dark base color and blue decoy coloration experienced no measurable difference in avian predation relative to an all-dark model, which suggests that blue coloration neither serves as an aposematic signal nor increases the conspicuousness of the lizard model. Despite statistically similar attack rates, avian attacks on models with blue coloration were indeed focused on body sections that were colored blue. Our results suggest that the blue tail in lizards serves as an effective decoy, and that avian predation has possibly played a role in the evolution of the blue tail.     

Male mating strategies under predation risk: do females call the shots?

Many authors have reported that, under elevated risk of predation,male guppies (Poecilia reticulata) alter their behavior fromcourtship to forced copulation (gonopodial thrusts not precededby sigmoid displays). This shift is presumed to benefit thebrightly colored male, whose intense courting activity mightotherwise increase his risk of detection and attack by predators.However, there is some evidence that females engaged in reproductiveactivity with males may be even more vulnerable to predatorsthan the males themselves, which suggests an alternative hypothesis:females in high-risk situations are less receptive to male courtship,and this leads males to change their behavior. We tested thishypothesis by providing either males and females separately,or both sexes concurrently, with information about elevatedpredation risk from a cichlid (Crenicichla sp.). We found thatwhen only females were provided with information about increased risk,males performed fewer courtship displays and fewer thrusts.They did not perform more forced copulations in any treatmentgroup. Nonetheless, our results suggest that the female's perceptionof predation risk can be at least as important as the male'sin changing male mating behavior.     

Predator exposure alters female mate choice in the green swordtail

Female green swordtails, Xiphophorus helleri, show a matingpreference for males with brightly colored, elongated swords.This preference is thought to be due to a preexisting receiverbias favoring longer sworded males. In this study, we examinedvariation in the expression of this sword bias in females. Specifically,we tested the hypothesis that an increase in perceived predationrisk will decrease female response to males with longer swords.We used a video playback experiment to evaluate female choicebetween two recordings of a displaying male that differed onlyin sword length. We scored responses of females to these recordingsimmediately before and after they had been exposed to a videorecording of a predation event between a cichlid and a malepossessing a long sword. We found that prior to exposure tothis predation event, females preferred the male with the longersword. However, after exposure to the predator, females alteredtheir mating response, preferring the male with the sword removed.Exposure to the predator also caused an increase in the frequencywith which females moved from potential mating positions toa neutral zone. The results presented here suggest that thefemale preference for males with longer swords can be modulatedbased on the perceived risk of predation.     

Variation in female guppy preference for male olfactory and visual traits

Animals often use different sensory systems to assess different sexually selected signals from potential mates. However, the relative importance of different signals on mate choice is not well understood in many animal species. In this study, we examined the relative importance of male olfactory and visual cues on female preference in the guppy Poecilia reticulata. We used digitally modified male images to standardize visual stimuli. We found that, regardless of whether females were presented without male visual stimuli or with identical male visual stimuli, they preferred stimuli with the odor of males to those without. However, when females were allowed to choose between dull male visual stimuli with male odor, and brightly colored male visual stimuli without male odor, there was no clear preference for either. Some females preferred the dull male visual stimuli with male odor, whereas some other females preferred the brightly colored male visual stimuli without male odor. These results indicate that the relative importance of olfactory and visual cues in female mate preference varied between individuals.     

Honest signaling and the uses of prey coloration

Abstract Although signal reliability is of fundamental importance to the understanding of animal communication, the extent of signal honesty in relation to antipredator warning signals has received relatively little attention. A recent theoretical model that assumed a physiological linkage between pigmentation and toxicity suggested that (aposematic) warning signals may often be reliable, in the sense that brightness and toxicity are positively correlated within prey populations. Two shortcomings of the model were (1) the requirement among predators for an innate aversion to brightly colored prey and (2) the assumption that prey can generate only bright coloration and not cryptic coloration. We evaluated the generality of predictions of reliable signaling when these shortcomings were removed. Without innate avoidance of bright prey, we found a positive brightness-toxin correlation when conspicuous prey coloration provided an additional fitness benefit unrelated to predation. Initially, this correlation could evolve for reasons unrelated to prey signaling; hence, aposematism might represent a striking example of exaptation. Given a choice between using pigmentation for bright or for cryptic coloration, crypsis was favored only in conditions of very low or very high resource levels. In the latter case, toxicity correlated positively with degree of cryptic coloration. Predictions of toxin-signal correlation appear robust, but we can identify interesting conditions in which signal reliability is not predicted.