Localization Error and Search Costs during Mate Choice in Túngara Frogs,Physalaemus pustulosus

Search costs can have profound influences on female choice, causing females to become less choosy or sample less of the diversity of available mates. Predator foraging strategies, however, determine exactly how search time affects predator encounter rates. Ambush predators are more likely to be encountered by females traveling longer distances to evaluate males, but evaluation time is unlikely to influence encounter‐rate with this type of predator. Actively searching predators, however, may be more likely to be encountered by females employing longer travel times and evaluation times. In this study, we examine the effects of perceived search costs on both temporal and spatial aspects of the search behavior of female túngara frogs, Physalaemus pustulosus. Females were collected from natural choruses and presented with conspecific calls at a distance of 50, 115, or 180 cm from their release point. Assays were conducted in either darkness or simulated full moon light levels. Longer starting distances caused longer choice latencies, but choice latency was considerably lowered under higher light conditions. Females spent considerably less time moving under higher light conditions; however, light levels did not affect path length. Females were more likely to leave the release point with more accurate orientation to the sound source under higher light conditions. We demonstrate that females can respond to perceived search costs by altering spatial and temporal aspects of female search behavior. The overall emphasis of females on reducing time spent moving and increasing movement speed indicates that predation by actively searching predators represents a stronger cost to females than ambush predators.     

Sexual Differences in the Behavioral Response of Túngara Frogs, Physalaemus pustulosus, to Cues Associated with Increased Predation Risk

Engaging in mating behaviors usually increases exposure to predators for both males and females. Anti‐predator strategies during reproduction may have important fitness consequences for prey. Previous studies have shown that individuals of several species adjust their reproductive behavior according to their assessment of predation risk, but few studies have explored potential sexual differences in these strategies. In this study, we investigate whether the acoustic cues associated with predatory attacks or those associated with predators themselves affect the mating behavior of female and male túngara frogs, Physalaemus pustulosus. We compared the responses of females approaching a mate and those of calling males when exposed to mating calls associated with sounds representing increased hazard. When presented with mating calls that differed only in whether or not they were followed by a predation‐related sound, females preferentially approached the call without predation‐related sounds. In contrast to females, calling males showed greater vocal response to calls associated with increased risk than to a call by itself. We found significant differences in the responses of females and males to several sounds associated with increased hazard. Females behaved more cautiously than males, suggesting that the sexes balance the risk of predation and the cost of cautious mating strategies differently.     

Visual mate choice in poison frogs

We investigated female mate choice on the basis of visual cues in two populations of Dendrobates pumilio, the strawberry poison frog, from the Bocas del Toro Archipelago in Panama, Central America. Mate choice experiments were carried out by presenting subject females of each of two morphs of this species (orange and green) from two different island populations (Nancy Key and Pope Island) with object frogs (one of each morph) under glass at one end of a terrarium. Recorded calls were played simultaneously from behind both object frogs. The experiments were carried out under two light regimes: (i) white light, and (ii) relatively monochromatic filtered blue light. Subject females from each population displayed a significant preference for their own morph under white light, but not under blue light. These results indicate that female D. pumilio use visual cues in mate choice, and suggest that colour may be the visual cue they use.     

A preference for a sexual signal keeps females safe

Predation is generally thought to constrain sexual selection by female choice and limit the evolution of conspicuous sexual signals. Under high predation risk, females usually become less choosy, because they reduce their exposure to their predators by reducing the extent of their mate searching. However, predation need not weaken sexual selection if, under high predation risk, females exhibit stronger preferences for males that use conspicuous signals that help females avoid their predators. We tested this prediction in the fiddler crab Uca terpsichores by increasing females' perceived predation risk from crab-eating birds and measuring the attractiveness of a courtship signal that females use to find mates. The sexual signal is an arching mound of sand that males build at the openings of their burrows to which they attract females for mating. We found that the greater the risk, the more attractive were males with those structures. The benefits of mate preferences for sexual signals are usually thought to be linked to males' reproductive contributions to females or their young. Our study provides the first evidence that a female preference for a sexual signal can yield direct survival benefits by keeping females safe as they search for mates.     

Hearing is not necessarily believing in nocturnal anurans

The recent discovery of the use of visual cues for mate choice by nocturnal acoustic species raises the important, and to date unaddressed, question of how these signals affect the outcome of mate choice predicted by female preference for male calls. In order to address this question, we presented female Hyla arborea tree frogs with a series of choices between combinations of acoustic and visual cues of varying quality in nocturnal conditions. While females exhibited the expected preference for a combination of attractive values for visual and acoustic signals over combinations of unattractive values for both signals, when presented with conflicting acoustic and visual cues, they equally adopted one of two strategies, preferring either attractive calls or intense vocal sac coloration. This constitutes novel evidence that the outcome of mate choice, as predicted on the basis of male calling quality, can be drastically different when additional communication modalities—in this case vision—are taken into account. These results also highlight the possible existence of individual variation in female rules for cue prioritization. The implications of these results for the study of mate choice in nocturnal acoustic species are discussed.     

Predator experience overrides learned aversion to heterospecifics in stickleback species pairs

Predation risk can alter female mating decisions because the costs of mate searching and selecting attractive mates increase when predators are present. In response to predators, females have been found to plastically adjust mate preference within species, but little is known about how predators alter sexual isolation and hybridization among species. We tested the effects of predator exposure on sexual isolation between benthic and limnetic threespine sticklebacks (Gasterosteus spp.). Female discrimination against heterospecific mates was measured before and after females experienced a simulated attack by a trout predator or a control exposure to a harmless object. In the absence of predators, females showed increased aversion to heterospecifics over time. We found that predator exposure made females less discriminating and precluded this learned aversion to heterospecifics. Benthic and limnetic males differ in coloration, and predator exposure also affected sexual isolation by weakening female preferences for colourful males. Predator effects on sexual selection were also tested but predators had few effects on female choosiness among conspecific mates. Our results suggest that predation risk may disrupt the cognitive processes associated with mate choice and lead to fluctuations in the strength of sexual isolation between species.     

Effect of alarm calling by male Red‐winged Blackbirds on nestling begging and female provisioning behavior

ABSTRACT Nestling begging and parental provisioning can attract nest predators and reduce reproductive success, so parents and their offspring might be expected to respond adaptively by minimizing predator‐attracting cues when predators threaten nests. Male Red‐winged Blackbirds (Agelaius phoeniceus) are well known for their antipredator alarm calls that contain information about the approach of potential nest predators. We examined the begging behavior of nestlings and the provisioning behavior of females in response to antipredator alarm calls of males to test the adaptive response hypothesis. Playback experiments provided no evidence that alarm calls function to switch off vocal begging; nestlings were equally likely to beg vocally during playback and control periods. Video recordings showed that male alarm calling had no significant effect on inappropriate vocal begging (in the absence of an adult), but significantly reduced the incidence of spontaneous calling (in the absence of begging). Adult females responded to male antipredator alarm calls by delaying their provisioning visits. In addition, although having no significant effect on use of nest‐arriving calls by females, male alarm calling significantly reduced their use of nest‐leaving calls. We conclude that nestling and female Red‐winged Blackbirds respond to male alarm calls in ways that might reduce the risk of predation, but nestlings beg vocally when females arrive to feed them, regardless of male alarm calling, perhaps to avoid a competitive disadvantage with broodmates.     

Elevated stress hormone diminishes the strength of female preferences for acoustic signals in the green treefrog

Mate selection can be stressful; time spent searching for mates can increase predation risk and/or decrease food consumption, resulting in elevated stress hormone levels. Both high predation risk and low food availability are often associated with increased variation in mate choice by females, but it is not clear whether stress hormone levels contribute to such variation in female behavior. We examined how the stress hormone corticosterone (CORT) affects female preferences for acoustic signals in the green treefrog, Hyla cinerea. Specifically, we assessed whether CORT administration affects female preferences for call rate — an acoustic feature that is typically under directional selection via mate choice by females in most anurans and other species that communicate using acoustic signals. Using a dual speaker playback paradigm, we show that females that were administered higher doses of CORT were less likely to choose male advertisement calls broadcast at high rates. Neither CORT dose nor level was related to the latency of female phonotactic responses, suggesting that elevated CORT does not influence the motivation to mate. Results were also not related to circulating sex steroids (i.e., progesterone, androgens or estradiol) that have traditionally been the focus of studies examining the hormonal basis for variation in female mate choice. Our results thus indicate that elevated CORT levels decrease the strength of female preferences for acoustic signals.     

Female response to predation risk alters conspecific male behaviour during pre‐copulatory mate guarding

Mating behaviour often increases predation risk, but the vulnerability within mating pairs differs between the sexes. Such a sex difference is expected to lead to differences in responses to predation risk between the sexes. In the two‐spotted spider mite Tetranychus urticae, males engage in pre‐copulatory mate guarding because only the first mating results in fertilisation. We investigated (i) whether pre‐copulatory pairs are more conspicuous to the predatory mite Phytoseiulus persimilis than solitary females, (ii) whether the vulnerability to the predator differs between sexes within the pre‐copulatory pair, (iii) whether each sex of T. urticae responds to predation risk during pre‐copulatory mate guarding and (iv) whether T. urticae's response to predation risk affects predator behaviour. Because T. urticae females are immobile during pre‐copulatory mate guarding, we observed male behaviour to evaluate effects of predation risk. We found that the predators detect more pre‐copulatory pairs than solitary females and that more females than males of the pre‐copulatory pairs are preyed upon by the predators. The preference of spider mite males for pre‐copulatory pairs versus solitary females was affected by whether or not the female had been exposed to predators during development. Male T. urticae exposed to predation risk did not alter their behaviour. These results suggest that only the most vulnerable sex, that is the female, responds to predation risk, which modifies male behaviour. Regardless of T. urticae females’ experience, however, P. persimilis detected more T. urticae pre‐copulatory pairs than solitary females, suggesting that pre‐copulatory mate guarding itself is dangerous for T. urticae females when these predators are present. We discuss our results in the context of sex‐dependent differences in predation risk.     

Adult frogs are sensitive to the predation risks of olfactory communication

Olfaction is a common sensory mode of communication in much of the Vertebrata, although its use by adult frogs remains poorly studied. Being part of an open signalling system, odour cues can be exploited by 'eavesdropping' predators that hunt by smell, making association with odour a high-risk behaviour for prey. Here, we show that adult great barred frogs (Mixophes fasciolatus) are highly attracted to odour cues of conspecifics and those of sympatric striped marsh frogs (Limnodynastes peronii). This attraction decreased significantly with the addition of odours of a scent-hunting predator, the red-bellied black snake (Pseudechis porphyriacus), indicating that frogs perceived predation risks from associating with frog odours. Male frogs, however, maintained some attraction to unfamiliar conspecific scents even with predator odours present, suggesting that they perceived benefits of odour communication despite the risk. Our results indicate that adult frogs can identify species and individuals from their odours and assess the associated predation risk, revealing a complexity in olfactory communication previously unknown in adult anurans.     

Phenotypic Plasticity in the Reproductive Behavior of Female Sand Tilefish, Malacanthus plumieri

Female sand tilefish (Malacanthus plumieri) inhabiting a deep channel in the fringing reef at Glover's Atoll, Belize (channel females) spawned planktonic eggs more frequently than those occupying the shallow sand‐rubble slopes adjacent to patch coral reefs inside the atoll lagoon (reef‐slope females). We tested five non‐exclusive hypotheses to explain habitat differences in female spawning frequency. We found no evidence that spawning frequency variation was a consequence of differences in food availability, variation in male fertility, or the intensity of predation on spawned eggs. On reef slopes, barracuda stalked tilefish near their benthic burrows, whereas these piscivores attacked channel tilefish by diving suddenly from higher in the water column. Differences in the hunting behavior of barracuda suggested that the behavior of tilefish females might be influenced by temporal variation in predation risk (risk allocation hypothesis). Consistent with this hypothesis, reef‐slope females had a much higher frequency of retreats to burrows in response to barracuda, spent more time burrowing and ventured less far from these refugia in response to a simulated predatory threat. As predicted by the risk allocation hypothesis, reef‐slope females also had lower and more variable frequencies of foraging bites, and shorter and more variable travel distances to forage than channel females. Estimated mortality from predation was over nine times higher in channel tilefish. Consistent with the hypothesis that investment in current vs. future reproduction is influenced by rates of adult mortality (mortality risk hypothesis), channel females invested more supplemental energy in egg production whereas reef‐slope females invested more in growth. Our results indicate that behavioral and life‐history traits of female tilefish show phenotypic plasticity depending upon the nature and intensity of localized predation risk.     

Predator-induced life history changes in amphibians: egg predation induces hatching

The timing of transitions between life history stages should be affected by factors that influence survival and growth of organisms in adjacent life history stages. In a series of laboratory experiments, we examined the influence of predation risk as a cue to trigger a life history switch in amphibians. In the Oregon Cascade Mountains, some populations of Pacific treefrogs ( Hyla regilla ) and Cascades frogs ( Rana cascadae ) are under intense egg predation by predatory leeches (families Glossiphonidae and Erpobdellidae). We document that both treefrogs and Cascades frogs show plasticity in hatching characteristics in response to the threat of egg predation. Pacific treefrogs hatch sooner and at an earlier developmental stage when either predatory leeches or non-predatory earthworms are allowed direct contact with the developing egg mass. The same response is elicited even without direct contact. Chemical cues of predatory leeches and chemicals released from injured eggs appear to elicit the same early hatching response in treefrogs. For Cascades frogs, cues of leeches, but not those of injured eggs, elicit an early hatching response. Hatching early in response to egg predators may reduce predation. Plasticity of hatching characteristics has rarely been examined. However, we suspect that it may be common, particularly in populations or species that experience high variability in predation pressure between years.     

Past and Present Risk: Exposure to Predator Chemical Cues Before and after Metamorphosis Influences Juvenile Wood Frog Behavior

Animals are exposed to different predators over their lifespan. This raises the question of whether exposure to predation risk in an early life stage affects the response to predators in subsequent life stages. In this study, we used wood frogs (Rana sylvatica) to test whether exposure to cues indicating predation risk from dragonfly larvae during the wood frog larval stage affected post‐metamorphic activity level and avoidance of garter snake chemical cues. Dragonfly larvae prey upon wood frogs only during the larval stage, whereas garter snakes prey upon wood frogs during both the larval stage and the post‐metamorphic stage. Exposure to predation risk from dragonflies during the larval stage caused post‐metamorphic wood frog juveniles to have greater terrestrial activity than juvenile wood frogs that were not exposed to larval‐stage predation risk from dragonflies. However, exposure to predation risk as larvae did not affect juvenile wood frog responses to chemical cues from garter snakes. Wood frogs exposed as larvae to predation risk from dragonfly larvae avoided garter snake chemical cues to the same extent as wood frog larvae not exposed to predation risk from dragonfly larvae. Our results demonstrate that while some general behaviors exhibit carry‐over effects from earlier life stages, behavioral responses to predators may remain independent of conditions experienced in earlier life stages.     

Hatching responses of subsocial spitting spiders to predation risk

The carrying of eggs often renders parents vulnerable to predators due to increased conspicuousness or decreased mobility. Nonetheless, egg-carrying parents can escape from the predators to which they are vulnerable. Previous studies have demonstrated heavy predation by spider-eating jumping spiders (Portia labiata) on egg-carrying spitting spider (Scytodes pallida) females, but little predation on eggless females. If the timing of hatching is phenotypically plastic, then both S. pallida females and their eggs could reduce the risk of predation by hatching early. Hence, this study examines the hatching responses of S. pallida to chemical cues from P. labiata, both in the laboratory and in the field, and addresses the following questions. (i) Do cues from predatory P. labiata influence the hatching traits of S. pallida? (ii) Are the olfactory cues from predators sufficient for predator detection by S. pallida ? (iii) Are hatching responses to predatory P. labiata controlled by egg-carrying S. pallida females, or directly by their embryos? The study provides evidence of hatching as a life-history switch point, which shows an adaptive plasticity in response to predation risk in egg-carrying S. pallida. Egg-carrying S. pallida females, but not unattended eggs, adjust egg-hatching time (the interval between oviposition and hatching) in response to the threat of predation on both the female and her eggs by P. labiata. In the presence of P. labiata, eggs that are carried by females hatch sooner; the hatchlings of these eggs are therefore smaller than hatchlings born in the absence of P. labiata. Chemical cues that are released from the draglines of P. labiata are sufficient to elicit changes in the egg-hatching traits of S. pallida. Hatching early in response to this predator may benefit both females and their offspring. To my knowledge, this is the first direct experimental study to demonstrate predator-induced hatching plasticity in spiders and, in particular, in animals with parental care.     

Can Wall Lizards Combine Chemical and Visual Cues to Discriminate Predatory from Non‐Predatory Snakes Inside Refuges?

The ability to use multiple cues in assessing predation risk is especially important to prey animals exposed to multiple predators. Wall lizards, Podarcis muralis, respond to predatory attacks from birds in the open by hiding inside rock crevices, where they may encounter saurophagous ambush smooth snakes. Lizards should avoid refuges with these snakes, but in refuges lizards can also find non‐saurophagous viperine snakes, which lizards do not need to avoid. We investigated in the laboratory whether wall lizards used different predator cues to detect and discriminate between snake species within refuges. We simulated predatory attacks in the open to lizards, and compared their refuge use, and the variation in the responses after a repeated attack, between predator‐free refuges and refuges containing visual, chemical, or visual and chemical cues of saurophagous or non‐saurophagous snakes. Time to enter a refuge was not influenced by potential risk inside the refuge. In contrast, in a successive second attack, lizards sought cover faster and tended to increase time spent hidden in the refuge. This suggests a case of predator facilitation because persistent predators in the open may force lizards to hide faster and for longer in hazardous refuges. However, after hiding, lizards spent less time in refuges with both chemical and visual cues of snakes, or with chemical cues alone, than in predator‐free refuges or in refuges with snake visual cues alone, but there were no differences in response to the two snake species. Therefore, lizards could be overestimating predation risk inside refuges. We discuss which selection pressures might explain this lack of discrimination of predatory from similar non‐predatory snakes.     

An indirect cue of predation risk counteracts female preference for conspecifics in a naturally hybridizing fish Xiphophorus birchmanni

Mate choice is context dependent, but the importance of current context to interspecific mating and hybridization is largely unexplored. An important influence on mate choice is predation risk. We investigated how variation in an indirect cue of predation risk, distance to shelter, influences mate choice in the swordtail Xiphophorus birchmanni, a species which sometimes hybridizes with X. malinche in the wild. We conducted mate choice experiments to determine whether females attend to the distance to shelter and whether this cue of predation risk can counteract female preference for conspecifics. Females were sensitive to shelter distance independent of male presence. When conspecific and heterospecific X. malinche males were in equally risky habitats (i.e., equally distant from shelter), females associated primarily with conspecifics, suggesting an innate preference for conspecifics. However, when heterospecific males were in less risky habitat (i.e., closer to shelter) than conspecific males, females no longer exhibited a preference, suggesting that females calibrate their mate choices in response to predation risk. Our findings illustrate the potential for hybridization to arise, not necessarily through reproductive "mistakes", but as one of many potential outcomes of a context-dependent mate choice strategy.     

Predation Risk Reduces a Female Preference for Heterospecific Males in the Green Swordtail

The presence of a predator can result in the alteration, loss or reversal of a mating preference. Under predation risk, females often change their initial preference for conspicuous males, favouring less flashy males to reduce the risk of being detected by predators. Previous studies on predator‐induced plasticity in mate preferences have given females a choice between more and less conspicuous conspecific males. However, in species that naturally hybridize, it is also possible that females might choose an inconspicuous heterospecific male over a conspicuous conspecific male under predation risk. Our study addresses this question using the green swordtail (Xiphophorus helleri) and the southern platyfish (Xiphophorus maculatus), which are sympatric in the wild. We hypothesized that X. helleri females would prefer the sworded conspecific males in the absence of a predator but favour the less conspicuous, swordless, heterospecific males in the presence of a predator. Contrary to our expectation, females associated more with the heterospecific male than the conspecific male in the control (no predator) treatment, and they were non‐choosy in the predator treatment. This might reflect that females were attracted to the novel male phenotype when there was no risk of predation but became more neophobic after predator exposure. Regardless of the underlying mechanism, our results suggest that predation pressure may affect female preferences for conspecific versus heterospecific males. We also found striking within‐population, between‐individual variation in behavioural plasticity: females differed in the strength and direction of their preferences, as well as in the extent to which they altered their preferences in response to changes in perceived predation risk. Such variation in female preferences for heterospecific males could potentially lead to temporal and spatial variation in hybridization rates in the wild.     

The Influence of Chemical Stimuli from Predators on Precopulatory Pairing by the Amphipod,Gammarus pseudolimnaeus

Many amphipod crustaceans exhibit precopulatory mate guarding. Field samples of the amphipod Gammarus pseudolimnaeus indicated that pairs were positively size assortative. Receptive individuals readily formed pairs in the laboratory and the latency to formation of precopulatory pairs was decreased under threat of predation. In addition, females and, under conditions of extreme danger, males that formed pairs were significantly smaller when under the threat of predation. Amphipods distinguished between chemical stimuli (aquarium water) from predatory and nonpredatory fishes and between chemical cues from fish predators (trout) that had recently eaten conspecific amphipods vs. those fed a control diet of pelleted commercial fish food. These data indicate that chemical stimuli associated with predators can influence reproductive behavior of amphipods. The results also suggest the hypotheses that: 1. search time may be costly in terms of probability of predation; and 2. small pairs may be safer from predation than larger pairs.     

Introduced mammalian predators induce behavioural changes in parental care in an endemic New Zealand bird

The introduction of predatory mammals to oceanic islands has led to the extinction of many endemic birds. Although introduced predators should favour changes that reduce predation risk in surviving bird species, the ability of island birds to respond to such novel changes remains unstudied. We tested whether novel predation risk imposed by introduced mammalian predators has altered the parental behaviour of the endemic New Zealand bellbird (Anthornis melanura). We examined parental behaviour of bellbirds at three woodland sites in New Zealand that differed in predation risk: 1) a mainland site with exotic predators present (high predation risk), 2) a mainland site with exotic predators experimentally removed (low risk recently) and, 3) an off-shore island where exotic predators were never introduced (low risk always). We also compared parental behaviour of bellbirds with two closely related Tasmanian honeyeaters (Phylidonyris spp.) that evolved with native nest predators (high risk always). Increased nest predation risk has been postulated to favour reduced parental activity, and we tested whether island bellbirds responded to variation in predation risk. We found that females spent more time on the nest per incubating bout with increased risk of predation, a strategy that minimised activity at the nest during incubation. Parental activity during the nestling period, measured as number of feeding visits/hr, also decreased with increasing nest predation risk across sites, and was lowest among the honeyeaters in Tasmania that evolved with native predators. These results demonstrate that some island birds are able to respond to increased risk of predation by novel predators in ways that appear adaptive. We suggest that conservation efforts may be more effective if they take advantage of the ability of island birds to respond to novel predators, especially when the elimination of exotic predators is not possible.     

Sire coloration influences offspring survival under predation risk in the moorfrog

When breeding, male moor frogs Rana arvalis develop a bright blue dorsal coloration which varies in intensity between males. We tested whether this colour acts as a potential signal of a male's genetic quality to female moor frogs by artificially crossing pairs of males differing in the extent of the blue coloration to the same female. Maternal half-sibships provide a powerful means to detect paternal genetic effects on offspring as they control for other potentially confounding variables. We assayed the ability of offspring to survive an ecologically realistic test of fitness by exposing them to predation by the larvae of the predatory water beetle Dytiscus marginalis. Although sire's coloration did not influence tadpole body size, it did affect their ability to survive the predation trial. Offspring of bright blue males had higher survival than those of dull males when exposed to large predators, which were more voracious predators than smaller ones. Our results indicate that paternal secondary sexual traits provide information about genetic effects on offspring fitness in this species, but suggest that these effects may be context-dependent. Variable selection caused by contextual dependence may have important consequences for the evolution of female choice rules, and for the maintenance of genetic variation for both male trait and female preference.