Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait

Although conspicuous visual sexual signals, such as bright colors,in males serve to attract females in numerous species, theymay also attract the attention of potential predators and thusmay be costly in terms of increasing individual risk of mortalityto predation. Most models of the evolution of extravagant malesexual traits and female preferences for them assume that thesexually preferred male trait is costly to produce and maintain.However, there is surprisingly little empirical evidence fordirect fitness costs associated with sexually selected visualtraits that enhance male mating success. In the present study,we report a direct fitness cost for sexually selected, brightbody-color patterns in males in the form of an associated greaterrisk of mortality to predation. By using the guppy (Poeciliareticulata) and the blue acara cichlid fish (Aequidens pulcher)as a model prey–predator system, we demonstrate experimentallythat individual cichlids preferentially and consistently approached,attacked, and captured the more brightly colored of two size-matchedmale guppies presented simultaneously in staged encounters.This resulted in the brightly colored male incurring, on average,a significantly higher risk of mortality given an encounterwith the predator than with the drabber male in matched pairs.Our results constitute strong behavioral evidence for a directviability cost associated with bright coloration in male guppies,and they corroborate the generally accepted paradigm that directionalpredation by visual fish predators against brightly colored,adult male guppies underlies the evolution of the known divergentcolor patterns in natural guppy populations that experiencedifferent intensities of predation. The viability cost associatedwith bright conspicuous coloration in male guppies potentiallyreinforces for females the reliability of this sexually selectedtrait as an indicator trait of male quality.     

Predator inspection,shoaling and foraging under predation hazard in the Trinidadian guppy,Poecilia reticulata

Synopsis Guppies,Poecilia reticulata, living in stream pools in Trinidad, West Indies, approached a potential fish predator (a cichlid fish model) in a tentative, saltatory manner, mainly as singletons or in pairs. Such behavior is referred to as predator inspection behavior. Inspectors approached the trunk and tail of the predator model more frequently, more closely and in larger groups than they approached the predator's head, which is presumably the most dangerous area around the predator. However, guppies were not observed in significantly larger shoals in the stream when the predator model was present. In a stream enclosure, guppies inspected the predator model more frequently when it was stationary compared to when it was moving, and made closer inspections to the posterior regions of the predator than to its head. Therefore, the guppies apparently regarded the predator model as a potential threat and modified their behavior accordingly when inspecting it. Guppies exhibited a lower feeding rate in the presence of the predator, suggesting a trade-off between foraging gains and safety against predation. Our results further suggest that predator inspection behavior may account for some of this reduction in foraging. These findings are discussed in the context of the benefits and costs of predator inspection behavior.     

Population Differences in the Schooling Behaviour of Newborn Guppies,Poecilia reticulata

Population differences in the schooling behaviour of adult guppies (Poecilia reticulata) from Trinidad have previously been well documented. This paper demonstrates that variation in schooling behaviour is also present in newborn fish. Guppies from the Aripo River of Trinidad display well-developed schooling behaviour from birth. In addition to forming cohesive and polarized groups, these newborn fish also exhibit predator inspection behaviour. Newborn guppies from the Paria River perform inspections but, unlike the Aripo fish, are poor schoolers. Population variation in behaviour at birth does not necessarily reflect the pattern observed in the adult fish. As adults, guppies from the Upper section of the Aripo River have a much lower schooling tendency and are less wary during inspection than the downstream Lower Aripo guppies. At birth, however, the schooling behaviour and inspection behaviour in the two populations is identical. These results suggest that different selective pressures operate on adult and newborn guppies in Trinidad.     

Disturbance cues as a source of risk assessment information under natural conditions

1. Disturbance cues are released by stressed or disturbed prey prior to a predator attack and convey useful risk assessment information regarding local threats. While studies have shown that disturbance cues may be important early on within the predation sequence (prior to an attack), their role in predator–prey interactions remains relatively overlooked by ecologists. Critically, experimental studies examining disturbance cues, especially among prey fishes, have been conducted primarily under laboratory or semi-natural conditions.
2. Here, we tested the prediction that disturbance cues function as sources of risk assessment information in situ. We exposed Trinidadian guppies, in two natural populations differing in predation risk, to a model predator paired with stream water or the disturbance cue collected from guppies from either a high- or low-predation risk population.
3. We found that the predator inspection response of guppies to disturbance cues depends on the level of risk of both the focal and the cue source population. Guppies from both populations exhibited increased latencies to inspect, lower inspection rates and reduced inspecting group sizes towards the model paired with conspecific disturbance cues versus a stream water control. Interestingly, guppies of both populations showed evidence of higher perceived predation risk towards the disturbance cues collected from high-predation risk donors compared to low-predation risk donors.
4. Our results support the hypothesis that disturbance cues function as a source of information used by prey fish in the assessment of predation risk and provide the first evidence of disturbance cue function under fully natural conditions.

     

Schooling preferences for familiar fish vary with group size in a wild guppy population

The ability of fish to recognize and preferentially associate with familiar conspecifics has been well documented in a series of laboratory experiments. In this paper we investigate the schooling preferences of wild female guppies, Poecilia reticulata, in the Upper Tunapuna River in Trinidad and confirm that they do indeed prefer to associate with familiar individuals. The guppies in this river occur in a series of pools that become isolated during the dry season. These fish interact solely with other individuals in their pool for periods of several months at a time and thus have ample opportunity to become accustomed to one another. Our study also reveals that the tendency of female guppies to school with familiar fish declines as the group size in which they naturally live increases. Preferences are strong when there are small numbers of females in a pool, but diminish thereafter. This indicates that the expression of familiarity is constrained by group size. The basis of recognition and the consequences of schooling preferences for familiar individuals are discussed.     

Do competing males cooperate? Familiarity and its effect on cooperation during predator inspection in male three‐spined sticklebacks (Gasterosteus aculeatus)

We investigated the trade‐off between conflict and cooperation, using predator inspection behaviour in sticklebacks as a model system. Male three‐spined sticklebacks ( Gasterosteus aculeatus ) compete for territories during the breeding season and it has been demonstrated that the level of aggression between territorial neighbours declines with time, a phenomenon known as the dear enemy effect. In this experiment we examine whether this increase in familiarity between territorial neighbours can facilitate an increase in cooperation during predator inspection events. This was analyzed using male sticklebacks from four pond populations, two with and two without predatory rainbow trout ( Oncorhyncus mykiss ). Males were each exposed to five different treatments: (1) the presentation of a live rainbow trout when alone; (2) with a newly revealed territorial neighbour; (3) with this neighbour after two days of familiarization; (4) with another unfamiliar neighbour (termed a 'floater'); and (5) a second solitary trial (to provide controls at the start and end of the experiment). As predicted, fish from predator‐sympatric populations showed higher levels of predator inspection and lower rates of misdirected territorial aggression towards the predator throughout. However, familiarity between neighbouring males did not facilitate an increase in predator inspection behaviour. Instead, predator inspection behaviour decreased throughout treatments involving the presence of any sort of neighbouring male. Familiarity between neighbours did not influence their ability to cooperatively inspect, but only the nature of any aggressive territorial behaviours, all of which detracted equally from individual inspection effort.     

Interpopulational differences in the use of the Tit-For-Tat strategy during predator inspection in the guppy,Poecilia reticulata

Summary Prior work (Dugatkin, 1991a) has argued that guppies, originating from an area of high predation pressure, employ the Tit-For-Tat strategy during predator inspection visits. Guppies from the high predation site show all three characteristics associated with Tit-For-Tat; nice, retaliatory and forgiving behaviour. Since predation is the major selective force favouring Tit-For-Tat during predator inspection, we predicted fish from an area of low predation would not display the Tit-For-Tat strategy. Our results confirm this prediction; males display retaliatory, but not nice and forgiving behaviour, while females display none of the three characteristics. Thus as predation pressure changes, so too does the conditional nature of the cooperative strategy used during predator inspection.     

Female Size Influences Mate Preferences of Male Guppies

Guppies (Poecilia reticulata) have a promiscuous mating system in which female choice for brightly coloured males plays an important role. Consequently, much research on guppies has examined how mate choice by females has lead to the evolution of male colour patterns. Much less attention has been devoted to mate choice by males in this species. In this study, we show that male guppies are choosy when selecting a female to associate with, significantly preferring the larger female when presented with two females that differed by ≥2 mm in standard length (SL). The strength of their preference for each female increased with absolute female size. The relative sizes of the females, however, also influenced male mating preferences: males showed stronger preferences for the larger female as the difference in SL between the two females increased. Such a preference for larger females is not unexpected as fecundity generally increases with body size in female fish. Thus, males choosing to mate with the larger female should have higher reproductive success. An apparent, but non‐significant anomaly, whereby males appear to prefer the smaller of the two females when the difference between female SL was <4 mm, deserves further investigation.     

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)]     

Who dares, learns: chemical inspection behaviour and acquired predator recognition in a characin fish

Individuals that dare approach predators (predator inspection behaviour) may benefit by acquiring information regarding the potential threat of predation. Although information acquisition based on visual cues has been demonstrated for fish, it is unknown whether fish will inspect predators on the basis of chemical cues or whether such inspection behaviour results in information acquisition. Here, we first ascertained whether predator inspection behaviour can be mediated by chemical cues from predators by exposing groups of predator-naive glowlight tetras (Hemigrammus erythrozonus) to the chemical cues of a potential fish predator (convict cichlid Cichlasoma nigrofasciatum) that had been fed either tetras (which possess an alarm pheromone) or swordtails (Xiphophorus helleri, which lack Ostariophysan alarm pheromones). Tetras showed a significant increase in antipredator behaviour when exposed to the tetra-diet cue, but not when exposed to the swordtail-diet cue. Chemically mediated predator inspection behaviour was also affected. Both the latency to inspect and the minimum approach distance to the predator significantly increased, and the mean number of inspectors per predator inspection visit significantly decreased when tetras were exposed to the tetra-diet versus the swordtail-diet chemical cues. We then examined a potential benefit associated with chemically mediated predator inspection behaviour. Only tetras that were initially exposed to the tetra-diet cue and that had inspected the predator acquired the visual recognition of a convict cichlid as a predation threat. Our results thus demonstrate that (1) predator inspection behaviour in the glowlight tetra can be initiated by chemical cues, (2) chemically mediated inspection behaviour is affected by the presence of alarm pheromone, and (3) inspectors benefit by acquiring the recognition of novel predators. Copyright 1999 The Association for the Study of Animal Behaviour.     

Population divergence of private and non-private signals in wild guppies

Private signalling, where conspecifics use mating signals that are difficult to detect by predators, can reduce the compromise between opposing natural and sexual selection. We investigated whether guppies, Poecilia reticulata, use an hypothesized private signal. In some areas, guppies, who can detect ultraviolet (UV) light, coexist with dangerous predators, but at least some of these cannot detect UV. In these populations of guppies, UV might be used as a private signal. We tested this hypothesis by quantifying the UV and non-UV colouration of male guppies from paired high- and low-predation sites in five rivers. We found evidence in support of the use of UV as a private signal: male guppies living with the predator generally had greater UV reflectance than male guppies living without the predator. Closer inspection revealed differences in this trend among rivers and thus suggested the influence of modifying factors. We also found that the non-UV colour of male guppies does not differ consistently between high- and low-predation environments. This result suggests that a number of factors in addition to predation act on male colour in guppies.     

Inspection behaviour and inter-individual cooperation in juvenile qingbo: the effects of prior predator exposure and food deprivation

The predation pressure and food availability to which individuals are exposed during their life histories shape inspection behaviour in animals. In this study, we aimed to test whether such behaviours varied with prior experience (predation, starvation or both treatments) or measurement condition (with or without the presence of a predator; here, the snakehead fish, Channa argus) in the fish species Spinibarbus sinensis, known as qingbo. Unexpectedly, prior predator experience showed no significant effect on inspection behaviour as demonstrated by either the frequency or the duration of each activity outside shelter or on cooperation as demonstrated by the inter-individual distance or synchronization of speed. This may have been due to the different adjustments in behaviour among individuals (more shelter use vs. more inspection), the predator treatment used in the present study (exposure to caged predator rather than direct predation) and/or a species-specific strategy in the qingbo. The starved fish displayed shorter inspection latency, increased inspection behaviour and greater cooperation when measured without the predator; however, when measured in the presence of the predator, the starved fish showed increased inspection frequency but shorter inspection duration, possibly due to the compromise between energy needs and predation risk. Similar to those of the predation group, the fish from the double-treated group showed no difference in inspection behaviour compared to the control group under the predator-absent condition, while the high-frequency, short-duration inspection behaviours remained the same as in the starved group. These findings suggested that the adjustment of inspection behaviour and related cooperation are rather complicated according to either predator experience or food deprivation, partially due to the inter-individual differences in behavioural adjustment and/or different environmental conditions.     

Change in male coloration associated with artificial selection on foraging colour preference

Sensory drive proposes that natural selection on nonmating behaviours (e.g. foraging preferences) alters sensory system properties and results in a correlated effect on mating preferences and subsequently sexual traits. In colour‐based systems, we can test this by selecting on nonmating colour preferences and testing for responses in colour‐based female preferences and male sexual coloration. In guppies (Poecilia reticulata), individual functional links of sensory drive have been demonstrated providing an opportunity to test the process over more than one link. We measured male coloration and female preferences in populations previously artificially selected for colour‐based foraging behaviour towards two colours, red and blue. We found associated changes in male coloration in the expected direction as well as weak changes in female preferences. Our results can be explained by a correlated response in female preferences due to artificial selection on foraging preferences that are mediated by a shared sensory system or by other mechanisms such as colour avoidance, pleiotropy or social experiences. This is the first experimental evidence that selection on a nonmating behaviour can affect male coloration and, more weakly, female preferences.     

Predation pressure shapes brain anatomy in the wild

There is remarkable diversity in brain anatomy among vertebrates and evidence is accumulating that predatory interactions are crucially important for this diversity. To test this hypothesis, we collected female guppies (Poecilia reticulata) from 16 wild populations and related their brain anatomy to several aspects of predation pressure in this ecosystem, such as the biomass of the four major predators of guppies (one prawn and three fish species), and predator diversity (number of predatory fish species in each site). We found that populations from localities with higher prawn biomass had relatively larger telencephalon size as well as larger brains. Optic tectum size was positively associated with one of the fish predator’s biomass and with overall predator diversity. However, both olfactory bulb and hypothalamus size were negatively associated with the biomass of another of the fish predators. Hence, while fish predator occurrence is associated with variation in brain anatomy, prawn occurrence is associated with variation in brain size. Our results suggest that cognitive challenges posed by local differences in predator communities may lead to changes in prey brain anatomy in the wild.     

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.     

Caudal eyespots on fish predators influence the inspection behaviour of Trinidadian guppies, Poecilia reticulata

The effect of the false caudal eyespots (ocelli) of fish predators on guppy inspection behaviour was tested by use of predator ( Crenicichla ) models with and without a caudal ocellus. When a false eyespot was present, inspecting guppies spent significantly less time near the tail compared to a control model without a tail eyespot.     

Seeing orange: prawns tap into a pre-existing sensory bias of the Trinidadian guppy

Sensory bias, a predisposition towards certain signals, has been implicated in the origin of mate preferences in some species. A risk associated with these biases is that they can be co-opted by predators as sensory lures. Here we propose that the orange spots on the brown pincers of a diurnal, predatory species of prawn function as lures for Trinidadian guppies, which have a sensory bias for orange. We exposed female guppies to (i) a life-like model of this Trinidadian prawn with orange, green or no spots on the pincers or (ii) a live, novel (non-Trinidadian) crustacean (crayfish), also with spotted pincers. First, we provide evidence that guppies sympatric with the prawn recognized our model as a potential predator. Next, we found that guppies spent more time in the dangerous head region of the model prawn with orange-spotted pincers compared with unspotted pincers. Finally, we show that allopatric, but not sympatric, guppies spent more time in the vicinity of the head of a live crayfish when orange spots were added to its pincers than when brown spots were added. Our results suggest that the orange spots on prawn pincers can act as a sensory lure.     

Recent social history alters male courtship preferences

Phenotypically plastic mating behavior may allow males to modify their reproductive behavior to suit the prevailing social conditions, but we do not know if males only react to immediate social stimuli or change their inherent mate preferences according to their social history. Here we examine the effect of social experiences on the subsequent reproductive behavior of male guppies under standard conditions, allowing us to distinguish the effect of past and immediate social conditions. Males experienced experimental conditioning periods during which they interacted with three females, either of variable size or of similar size. Females arrived either simultaneously or consecutively. In subsequent standard assays, only males that had experienced females of variable size preferentially courted large females. Further, males exposed to sequential female arrival courted subsequent females more vigorously than males that had experienced simultaneous female arrival. In contrast, males did not alter their coercive mating attempts in relation to their recent social history. These results demonstrate that males use past experiences to modify their subsequent reproductive behavior rather than reacting only to immediate stimuli, and reveal the sophisticated ways in which males alter their reproductive tactics to suit the social environment and maximize fitness across changing selective landscapes.     

Predator-induced plasticity in guppy (<Emphasis Type="Italic">Poecilia reticulata</Emphasis>) life history traits

A number of invertebrates show predator-induced plasticity in life-history and morphological traits that are considered adaptive. Evidence is accumulating that vertebrates may also adjust their life-history traits in response to predators; however, some of the patterns of plasticity, which appear to be an adaptive response specifically to the risk of size-selective predation, may instead result from reduced foraging in response to predator presence. Here, we describe a study of predator-induced plasticity in guppies (Poecilia reticulata). We have predicted that the plastic response to cues from a small, gape-limited, natural predator of guppies, the killlifish (Rivulus hartii), would be the opposite of that caused by reduced food intake. We have found that male guppies increased their size at maturity, both length and mass, in response to the non-lethal presence of this predator. This pattern of plasticity is the opposite of that observed in response to reduced food intake, where male guppies reduce size at maturity. The increase in size at maturity that we observed would likely reduce predation on adult male guppies by this native predator because it is gape-limited and can only eat juvenile and small adult guppies. This size advantage would be important especially because male guppies grow very little after maturity. Therefore, the pattern of plasticity that we observed is likely adaptive. In contrast, female guppies showed no significant response in size at first parturition to the experimental manipulation; however, we did find evidence suggesting that females may produce more, smaller offspring in response to cues from this predator.     

Tendency to inspect predators predicts mortality risk in the guppy (Poecilia reticulata)

Although predator inspection behavior in fishes has become amodel system for examining game theoretical strategies suchas Tit for Tat, the direct costs of inspection behavior havenot been quantified. To begin quantifying such costs, I conductedan experiment that examined mortality due to predation as afunction of predator inspection in the guppy (Poecilia reticulata).Before being subjected to a "survivorship" experiment, guppieswere assayed for their tendency to inspect a predator. Groupswere then composed of six guppies that differed in their tendencyto inspect. These groups were placed into a pool containinga predator, and survivorship of guppies with different inspectiontendencies was noted 36 and 60 h later. Results indicate thatindividuals that display high degrees of inspection behaviorsuffer greater mortality than their noninspecting shoalmates.