Dangerous love? Predation risk does not affect female mate choice in blue‐black grassquits

Predation risk may be an important factor affecting female mate choice. Hypothetically, females could choose extravagantly ornamented males that survive in high predation risk environments. However, this decision could be different if choosing a conspicuous male under high predation risk is costly for females or results in reduced offspring survival. In such contexts, females could become indifferent to male quality or prefer inconspicuous males. We tested this idea using captive blue‐black grassquits (Volatinia jacarina, Linnaeus, 1766), a species in which males perform conspicuous leap displays coupled with songs during the breeding season, which presumably subjects females and offspring to higher predation risk. Females were placed in an arena with speakers on opposite sides emitting male courtship songs. One speaker emitted songs at a high rate (proxy for a conspicuous male) while the other speaker broadcast songs at a low rate (proxy for a less conspicuous male). While the female evaluated the two male songs, a third speaker emitted vocalizations characterizing three levels of risk: adult predator, nest predator, and no‐risk control. Females showed no preference for either male stimuli across the predation risk treatments. This lack of preference relative to frequency of male vocal displays suggests that leap‐song frequency is not used by females during mate choice. We suggest that in addition to its role in courtship, male grassquit displays also signal status to other males when competing for territories. Thus, we propose that predation risk does not directly influence blue‐black grassquit intersexual selection and that females in this species may exercise indirect mate choice, choosing social mates based on male ability to establish and defend a territory, and relying secondarily upon other aspects of male display attributes, such as its visual components.     

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.     

Sex‐Specific Response of Pardosa milvina (Araneae: Lycosidae) to Experience with a Chemotactile Predation Cue

Predators frequently leave behind chemical information (i.e., semiochemicals such as pheromones or kairomones) that can be detected by their prey and used to avoid areas where predators are likely present. Prey that have interacted indirectly with predators via chemical information thus may gain insight into their risk of being consumed that naïve individuals lack. Pardosa milvina (Araneae: Lycosidae) is a chemosensitive wolf spider that shows adaptive responses to chemotactile cues deposited by the larger wolf spider Tigrosa helluo. We raised offspring from P. milvina to examine the effect of experience with a predation cue on activity, foraging, and antipredator behavior. Spiders differed in activity and foraging behavior across ontogeny and between sexes, but there was no effect of experience with a predation cue. However, a sex‐specific effect of experience was found in antipredator behavior. Male spiders, but not females, used experience with a predator cue to increase their survival in the presence of a live predator. Specifically, naïve males were attacked sooner than experienced males, indicating that prior exposure to predator cues can modify Pardosa antipredator behavior. Intersexual differences in how spiders respond to experience with a predation cue likely reflect the risk of predation faced by males and females in nature.     

A female's past experience with predators affects male courtship and the care her offspring will receive from their father

Differential allocation occurs when individuals adjust their reproductive investment based on their partner''s traits. However, it remains unknown whether animals differentially allocate based on their partner''s past experiences with predation risk. If animals can detect a potential mate''s experience with predators, this might inform them about the stress level of their potential mate, the likelihood of parental effects in offspring and/or the dangers present in the environment. Using threespined stickleback (Gasterosteus aculeatus), we examined whether a female''s previous experience with being chased by a model predator while yolking eggs affects male mating effort and offspring care. Males displayed fewer conspicuous courtship behaviours towards females that had experienced predation risk in the past compared with unexposed females. This differential allocation extended to how males cared for the resulting offspring of these matings: fathers provided less parental care to offspring of females that had experienced predation risk in the past. Our results show for the first time, to our knowledge, that variation among females in their predator encounters can contribute to behavioural variation among males in courtship and parental care, even when males themselves do not encounter a predator. These results, together with previous findings, suggest that maternal predator exposure can influence offspring development both directly and indirectly, through how it affects father care.     

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.     

Predators can influence the host‐parasite dynamics of their prey via nonconsumptive effects

Ecological communities are partly structured by indirect interactions, where one species can indirectly affect another by altering its interactions with a third species. In the absence of direct predation, nonconsumptive effects of predators on prey have important implications for subsequent community interactions. To better understand these interactions, we used a Daphnia‐parasite‐predator cue system to evaluate if predation risk affects Daphnia responses to a parasite. We investigated the effects of predator cues on two aspects of host–parasite interactions (susceptibility to infection and infection intensity), and whether or not these effects differed between sexes. Our results show that changes in response to predator cues caused an increase in the prevalence and intensity of parasite infections in female predator‐exposed Daphnia. Importantly, the magnitude of infection risk depended on how long Daphnia were exposed to the cues. Additionally, heavily infected Daphnia that were constantly exposed to cues produced relatively more offspring. While males were ~5× less likely to become infected compared to females, we were unable to detect effects of predator cues on male Daphnia–parasite interactions. In sum, predators, prey, and their parasites can form complex subnetworks in food webs, necessitating a nuanced understanding of how nonconsumptive effects may mediate these interactions.     

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.     

Uninformative polymorphisms bias genome scans for signatures of selection

Background

A female preference for intense sexual visual signals is widespread in animals. Although the preferences for a signal per se and for the intensity of the signal were often regarded to have the identical origin, no study has demonstrated if this is true. It was suggested that the female fiddler crabs prefer males with courtship structures because of direct benefit to escape predation. Here we tested if female preference for both components (i.e. presence and size) of the courtship structure in Uca lactea is from the sensory bias to escape predation. If both components have the identical origin, females should show the same response to different-sized courtship structures regardless of predation risk.

Results

First, we observed responses of mate-searching female U. lactea to courting males with full-sized, half-sized and no semidomes which were experimentally manipulated. Females had a directional preference for males with bigger semidomes within normal variation. Thereafter, we tested the effect of predation risk on the female bias in the non-courtship context. When threatened by an avian mock predator, females preferentially approached burrows with full-sized semidomes regardless of reproductive cycles (i.e. reproductive periods and non-reproductive periods). When the predator cue was absent, however, females preferred burrows with semidomes without discriminating structure size during reproductive periods but did not show any bias during non-reproductive periods.

Conclusions

Results indicate that selection for the size of courtship structures in U. lactea may have an origin in the function to reduce predation risk, but that the preference for males with structures may have evolved by female choice, independent of predation pressure.     

Elevating perceived predation risk modifies the relationship between parental effort and song complexity in the song sparrow Melospiza melodia

Adult‐directed predation risk elevates costs of parental care, and may modify relationships between sexually selected ornaments and parental effort by accentuating the tradeoff between survival and parental investment. We assessed multiple hypotheses regarding the relationship between maternal effort, paternal effort, and the sexually selected trait of male song complexity in the song sparrow Melospiza melodia. Further, we explored whether experimentally elevating perceived adult‐directed predation risk near nests affected these relationships. We quantified two dimensions of song complexity: song repertoire size and residual syllable number (the relative number of syllables for a given song repertoire size). Under elevated perceived predation risk, but not in the absence of the predator stimuli, females mated to males with higher residual syllable number displayed higher nestling provisioning rates and performed a greater proportion of nestling provisioning trips. In other words, elevating perceived predation risk induced a pattern of maternal investment consistent with differential allocation. In contrast, under elevated perceived predation risk, only, females performed a lesser proportion of provisioning trips when mated to males with large song repertoire sizes. Further, consistent with the good parent hypothesis, males with large song repertoire sizes displayed lower latencies to return to the nest, independent of the predator stimuli. Results suggest that residual syllable number may reflect some aspect of male genetic quality, such that females are more willing to maintain maternal effort while facing heightened predation risk. On the other hand, females may gain paternal benefits when mated to males with large song repertoires. Our study supports the hypothesis that increased costs of parental care associated with predation risk may induce relationships between sexually selected traits and parental behavior, which may increase the strength of sexual selection. Additionally, results suggest that different aspects of song complexity may fulfill non‐equivalent signaling roles.     

Are behavioural responses to predation cues linked across life cycle stages?

1. Prey organisms can perceive cues to predation hazard and adopt low‐risk behaviours to increase survival. Animals with complex life cycles, such as insects, can exhibit such anti‐predatory behaviours in multiple life stages. 2. Cues to predation risk may induce ovipositing females to choose habitats with low predation risk. Cues to predation risk may also induce larvae to adopt facultative behaviours that reduce risk of predation. 3. One hypothesis postulates that anti‐predation behaviours across adult and larval stages may be negatively associated because selection for effective anti‐predator behaviour in one stage leads to reduced selection for avoidance of predators in other stages. An alternative hypothesis suggests that selection by predation favours multi‐component defences, with both avoidance of oviposition and facultative adoption of low‐risk behaviours by larvae. 4. Laboratory and field experiments were used to determine whether defensive responses of adult and larval mosquitoes are positively or negatively associated. The study tested effects of waterborne cues from predatory Toxorhynchites theobaldi on oviposition choices and larval behaviours of three of its common prey: Culex mollis, Limatus durhamii and Aedes albopictus. 5. Culex mollis shows strong anti‐predator responses in both life stages, consistent with the hypothesis of a multi‐component behavioural defence. The other two species showed no detectable responses to waterborne predator cues in either adult or larval stages. Larvae of these unresponsive species were significantly more vulnerable to this predator than was C. mollis. 6. For these mosquitoes, species appear either to have been selected for multi‐component defences against predation or to act in ways that could be called predator‐naïve.     

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.     

Hamsters Use Predator Odors as Indirect Cues of Predation Risk

Golden hamsters (Mesocricetus auratus) use olfactory cues to assess traits of conspecifics such as kinship, individual identity, and reproductive status. The environment, however, is full of a wide variety of other olfactory information such as signals emitted by some of the hamster’s primary predators. Given this, we hypothesized that hamsters use odors from predators as an indirect sign of increased predation risk in the environment. In addition, based on data that show that wild hamsters are diurnal while laboratory hamsters are nocturnal, we hypothesized that if golden hamsters did respond to the predator odors, perceived predator risk might influence daily activity patterns in hamsters. We tested male and female hamsters over 5 d with scent gland secretion from domestic ferrets (Mustela putorius furo) and compared their behavior to that observed when they were exposed to a clean arena. In response to the predator odor, subjects significantly decreased the amount of time active outside of their burrow, returned to their burrow more quickly, and spent less time near the predator odor than the clean control stimulus. These results strongly support our hypothesis that hamsters, like other species of small mammals, avoid predator odors. The results did not, however, support our second hypothesis that exposure to predator odors during the dark phase of the light cycle would elicit a switch to a more diurnal pattern of activity. More work is needed to understand how environmental cues and internal mechanisms interact to shape activity patterns.     

Firefly Courtship: Behavioral and Morphological Predictors of Male Mating Success in Photinus greeni

Differences in male mating success can generate selection on male morphological traits and courtship behaviors involved in male–male competition or female mate choice. In Photinus fireflies (Coleoptera: Lampyridae), courtship is based on bioluminescent flash signals produced by both sexes. We conducted field observations of Photinus greeni fireflies engaged in competitive courtships, in which females are able to simultaneously assess several males, to identify male morphological traits and courtship behaviors that might predict male mating success. Male morphological traits did not differ between males that successfully mated compared with unsuccessful males (dialoging males that did not mate). However, courtship behavioral interactions differed: successful males tended to have higher flash pattern rates (number of flash patterns per minute), and their courtship flashes were more likely to be answered by females. We also examined how the risk of predation by Photuris fireflies altered courtship behavior of their Photinus prey. When predatory Photuris fireflies were present, P. greeni females were less likely to mate, and showed decreased flash responses to most males. However, P. greeni males that did successfully mate in spite of Photuris presence were males that maintained high flash pattern rates that elicited female responses. These results suggest that both female mate choice and Photuris predation exert strong selective pressures on the evolution of courtship signals in Photinus fireflies.     

Choosing a mate in a high predation environment: Female preference in the fiddler crab Uca terpsichores

The interplay between a receiver's sensory system and a sender's courtship signals is fundamental to the operation of sexual selection. Male courtship signals that match a female receiver's preexisting perceptual biases can be favored yet the message they communicate is not always clear. Do they simply beacon the male's location or also indicate his quality? We explored this question in a species of fiddler crab Uca terpsichores that courts under elevated predation risk and that mates and breeds underground in the safety of males' burrows. Sexually receptive females leave their own burrows and are thereby exposed to avian predators as they sequentially approach several courting males before they choose one. Males court by waving their single greatly enlarge claw and sometimes by building a sand hood next to their burrow entrance. Hoods are attractive because they elicit a risk‐reducing orientation behavior in females, and it has been suggested that claw waving may also serve primarily to orient the female to the male. If the wave communicates male quality, then females should discriminate mates on the basis of variation in elements of the wave, as has been shown for other fiddler crabs. Alternatively, variation in elements of the claw waving display may have little effect on the display's utility as a beacon of the location of the male and his burrow. We filmed courting males and females under natural conditions as females responded to claw waving and chose mates. Analysis of the fine‐scale courtship elements between the males that females rejected and those they chose revealed no differences. When predation risk during courtship is high, males' courtship displays may serve primarily to guide females to safe mating and breeding sites and not as indicators of male quality apart from their roles as beacons.     

Behavioral responses of a sex-role reversed pipefish to a gradient of perceived predation risk

Conspicuous behaviors such as courtship and mating often makeanimals susceptible to predation. When perceiving themselvesat an elevated level of risk, animals frequently reduce conspicuousbehaviors in tradeoff for a decrease in probability of beingpreyed upon. In the present study, we used two experiments toexamine the effect of perceived predation risk from cod (Gadusmorhud) on nonreproductive and reproductive behaviors in thesex-role reversed pipefish (Syngnathus typhle). In the firstexperiment, no differences due to predation risk were detectedin the nonreproductive behaviors of either males or females.In the second experiment, predation risk had significant effectson reproductive behaviors. Pipefish were allowed to court andcopulate at four different predation levels. We created predationlevels differing in perceived predation risk by controllingthe number of sensory modes through which pipefish could detectthe presence of a cod. As predation risk increased, pipefishcopulated and courted less frequently, swam alone (displayedand searched for conspecifics) less often, and waited longerbefore commencing courtship. These changes in behavior minimizedthe amount of time spent above the eelgrass and presumably reducedconspicuousness to visual predators. Pipefish also copulatedafter a smaller amount of courtship as predation risk increased,indicating that they may trade information concerning mate qualityfor a reduction in predation risk. No differences were foundin any response variable between males and females. The roleof operational sex ratios and intersexual competition in determiningwhich sex assumes greater costs in mate acquisition is questioned.     

The Consequences of Predation Risk on the Male Territorial Behavior in a Solitary Bee

Territorial males may adopt a mating tactic that yields greater reproductive success but that at the same time increases the risk of predation. Plasticity in reproductive behavior can reflect a balance between sexual selection and natural selection. In this study, we sought to verify the effect of predation risk on territorial behavior of males of the solitary bee Ptilothrix fructifera (Apidae). Males of the species employ alternative mating tactics and can be territorial in defense of larval food sources. By manipulating predator models in the field, we tested whether (1) males avoid perch flowers containing predator models; (2) males alternate between mating tactics when their territory is associated with a predation risk; and (3) female foraging on flowers in a territory is altered in the presence of a predator model. We measured the responses of males and females in flowers containing and not containing a model of a spider or a stuffed bird. The results show that territorial males of P. fructifera alter their territorial behavior when faced with a high risk of predation. They do not abandon their territory or change to a non‐territorial mating tactic, but instead change the use of their territory, avoiding flowers containing predator models or perching on other flowers when the previous flower presented a potential predation risk. Female P. fructifera decreases the frequency of their visits to flowers and the length of time spent there in the presence of a spider model. In short, in the face of predation risk, females and males alter their behaviors at the cost of less efficient foraging and searching for partners, respectively.     

Cues by which suspended-leaf nests of Euryattus (Araneae: Salticidae) females are recognized by conspecific males and by an aggressive-mimic salticid, Portia fimbriata

Females of Euryattus sp. indet, a salticid from Queensland, suspend rolled-up leaves for nests. Euryattus males respond to conspecific females in nests with vibratory courtship. Portia fimbriata , a sympatric salticid that preys on Euryattus , responds to Euryattus females' nests by mimicking the courtship of Euryattus males. In the laboratory, cues by which potential mates (conspecific males) and potential predators ( P. fimbriata females) recognize the nests of Euryattus females are investigated experimentally. Both the position of the leaf in relation to the substratum and the number of threads between the leaf and the substratum appear to be important cues by which both the Euryattus males and P. fimbriata females find nests. In addition, chemical cues from Euryattus females influence conspecific males, but there is no evidence that chemical cues are important to the predator.     

Increased predation risk while mate guarding as a cost of reproduction for male broad-headed skinks (Eumeces laticeps)

We investigated antipredatory costs associated with mate guarding as potential costs of reproduction for male broad-headed skinks. Mate guarding by male lizards may increase fitness by preventing loss of fertilizations of the guarded female's eggs to other males, but it may have several costs. In addition to lost opportunities to search for additional females, risk of injury while fighting other males, and energetic expenditures while following females and fighting, guarding males might suffer increased risk of predation and reduction of opportunities to forage. We studied potential antipredatory costs of mate guarding by simulating predators searching for and approaching pairs of lizards in the field. Among pairs of lizards in close proximity to each other, males were detected before females 10 times more frequently than females were detected before males, and females fled before males much more frequently than males fled before females when pairs were approached, leaving the males exposed to the predator. After one or both lizards fled, males frequently followed females by scanning visually and scent trailing, exposing themselves to the predator while the female hid. Females never followed males. The implications of these findings for antipredatory costs of mate guarding are discussed. Electronic Publication     

Predator faunas past and present: quantifying the influence of waterborne cues in divergent ecotypes of the isopod Asellus aquaticus

Waterborne chemical cues are an important source of information for many aquatic organisms, in particular when assessing the current risk of predation. The ability to use chemical cues to detect and respond to potential predators before an actual encounter can improve prey chances of survival. We investigated predator recognition and the impact of chemical cues on predator avoidance in the freshwater isopod Asellus aquaticus. This isopod has recently colonised a novel habitat and diverged into two distinct ecotypes, which encounter different predator communities. Using laboratory-based choice experiments, we have quantified behavioural responses to chemical cues from predators typical of the two predator communities (larval dragonflies in the ancestral habitat, perch in the newly colonised habitat) in wild-caught and lab-reared Asellus of the two ecotypes. Individuals with prior experience of predators showed strong predator avoidance to cues from both predator types. Both ecotypes showed similar antipredator responses, but sexes differed in terms of threat-sensitive responses with males avoiding areas containing predator cues to a larger extent than females. Overall, chemical cues from fish elicited stronger predator avoidance than cues from larval dragonflies. Our results indicate that in these isopods, prior exposure to predators is needed to develop antipredator behaviour based on waterborne cues. Furthermore, the results emphasise the need to analyse predator avoidance in relation to waterborne cues in a sex-specific context, because of potential differences between males and females in terms of vulnerability and life history strategies.     

Sublethal pesticide exposure disrupts courtship in the striped lynx spider,Oxyopes salticus (Araneae: Oxyopidae)

The striped lynx spider, Oxyopes salticus, is a dominant predator of pests in agricultural crops where pesticides are readily applied. While past research shows pesticides directly affect the mortality of agricultural pest predators, recent research has found that pesticide exposure may cause sublethal effects in these organisms. This study examined how residues of three common pesticides (active ingredients: bifenthrin, carbaryl, malathion) impact courtship behaviour of O. salticus. Males provided with cues left by females readily performed courting behaviours. However, when females left cues on a substrate containing bifenthrin and carbaryl, males were less likely to perform courtship behaviours and did so for less time. While males on the malathion treatment showed a trend for reduced courting, this was not significantly different from the treatment without pesticides. The cue produced by females is unknown in this species. However, our study found males reduced their courting over time, suggesting that the cue is ephemeral and not long lived. This study adds important insight into the growing evidence that pesticides greatly impact the ecology of agricultural pest predators and other non‐target organisms by altering their behaviour.