Mobbing calls signal predator category in a kin group-living bird species

Many prey species gather together to approach and harass their predators despite the associated risks. While mobbing, prey usually utter calls and previous experiments have demonstrated that mobbing calls can convey information about risk to conspecifics. However, the risk posed by predators also differs between predator categories. The ability to communicate predator category would be adaptive because it would allow other mobbers to adjust their risk taking. I tested this idea in Siberian jays Perisoreus infaustus, a group-living bird species, by exposing jay groups to mounts of three hawk and three owl species of varying risks. Groups immediately approached to mob the mount and uttered up to 14 different call types. Jays gave more calls when mobbing a more dangerous predator and when in the presence of kin. Five call types were predator-category-specific and jays uttered two hawk-specific and three owl-specific call types. Thus, this is one of the first studies to demonstrate that mobbing calls can simultaneously encode information about both predator category and the risk posed by a predator. Since antipredator calls of Siberian jays are known to specifically aim at reducing the risk to relatives, kin-based sociality could be an important factor in facilitating the evolution of predator-category-specific mobbing calls.     

Birds adjust acoustic directionality to beam their antipredator calls to predators and conspecifics

Animals in many vertebrate species vocalize in response to predators, but it is often unclear whether these antipredator calls function to communicate with predators, conspecifics or both. We evaluated the function of antipredator calls in 10 species of passerines by measuring the acoustic directionality of these calls in response to experimental presentations of a model predator. Acoustic directionality quantifies the radiation pattern of vocalizations and may provide evidence about the receiver of these calls. We predicted that antipredator calls would have a lower directionality if they function to communicate with surrounding conspecifics, and a higher directionality and aimed at the receiver if they function to communicate with the predator. Our results support both of these functions. Overall, the birds produce antipredator calls that have a relatively low directionality, suggesting that the calls radiate in many directions to alert conspecifics. However, birds in some species increase the directionality of their calls when facing the predator. They can even direct their calls towards the predator when facing lateral to it—effectively vocalizing sideways towards the predator. These results suggest that antipredator calls in some species are used to communicate both to conspecifics and to predators, and that birds adjust the directionality of their calls with remarkable sophistication according to the context in which they are used.     

A note on an interaction between Rhinopithecus bieti and a buzzard at Baima Snow Moutain

Predation avoidance relies primarily on behavioural mechanisms [van Schaik and van Hooff, 1983]. Primates alarm call at predators, including most birds and mammals [Cheney and Wrangham, 1987]. Alarm calls could be used to signal to the predator that it has been spotted [Zuberbühler et al., 1999], thereby probably decreasing the likelihood of an attack [Schultz, 2001], and they also inform prey of the presence of the predator, thereby increasing overall attention levels [Schülke, 2001]. Although eagles are reported to be one of the predators of Rhinopithecus bieti [Bai et al., 1987], few interactions between these monkeys and raptors have been documented to date. Here I document an interaction witnessed between R. bieti and a buzzard [Buteo sp., Yang X-J, pers. comm.].     

Linking Morphological and Behavioural Defences: Prey Fish Detect the Morphology of Conspecifics in the Odour Signature of their Predators

Predation is a strong selective force acting on both morphology and behaviour of prey animals. While morphological defences (e.g. crypsis, presence of armours or spines or specific body morphologies) and antipredator behaviours (e.g. change in foraging or reproductive effort, or hiding and fleeing behaviours) have been widely studied separately, few studies have considered the interplay between the two. The question raised in our study is whether antipredator behaviours of a prey fish to predator odours could be influenced by the morphology of prey conspecifics in the diet of the predator. We used goldfish (Carassius auratus) as our test species; goldfish exposed to predation risk significantly increase their body depth to length ratio, which gives them a survival advantage against gape‐limited predators. We exposed shallow‐bodied and deep‐bodied goldfish to the odour of pike (Esox lucius) fed either form of goldfish. Deep‐bodied goldfish displayed lower intensity antipredator responses than shallow‐bodied ones, consistent with the hypothesis that individuals with morphological defences should exhibit less behavioural modification than those lacking such defences. Moreover, both shallow‐ and deep‐bodied goldfish displayed their strongest antipredator responses when exposed to the odour of pike fed conspecifics of their own morphology, indicating that goldfish are able to differentiate the morphology of conspecifics through predator diet cues. For a given individual, predator threat increases as the prey become more like the individual eaten, revealing a surprising level of sophistication of chemosensory assessment by prey fish.     

Experience buffers extrinsic mortality in a group‐living bird species

Extrinsic mortality has a strong impact on the evolution of life‐histories, prey morphology and behavioural adaptations, but for many animals the causes of mortality are poorly understood. Predation is an important driver of extrinsic mortality and mobile animals form groups in response to increased predation risk. Furthermore, in many species juveniles suffer higher mortality than older individuals, which may reflect a lower phenotypic quality, lower competitiveness, or a lack of antipredator or foraging skills. Here we assessed the causes of mortality for 371 radio tagged Siberian jays. This sedentary bird species lives in family groups that contain a breeding pair as well as related and unrelated non‐breeders. Ninety‐five percent of death were due to predation (n = 59 out of 62 individuals) and most individuals were killed by Accipiter hawks. Multivariate Cox proportional hazards models showed that non‐breeders had a lower survival than breeders, but only in territories in managed forest with little visual cover. Examining breeders, only sex influenced survival with males having a lower survival than females. For non‐breeders, juveniles had lower survival than older non‐breeders, and those on managed territories had lower survival than those on unmanaged territories. Additionally, a low feather quality reduced the survival probability of non‐breeders only. Thus, living on managed territories and having a low feature quality affected only non‐breeders, particularly juveniles. These findings add to previous research demonstrating that juvenile Siberian jays acquire critical antipredator skills from experienced group members. Thus, experience can buffer extrinsic mortality, highlighting that group living not only provides safety in numbers, but also provide social opportunities to learn critical life‐skills.     

Avoiding Predators: Expectations and Evidence in Primate Antipredator Behavior

Predation and antipredator behavior are important but poorly studied influences on the evolution of primate societies. I review recent evidence of predation and antipredator strategies among primates. I describe patterns of antipredator behavior and attempt to explain the variation among primate taxa and among antipredator strategies. I use predation by chimpanzees on red colobus and antipredator strategies by the colobus as a case study of how a primate prey species may respond to the threat of predation.     

An enemy of your enemy is your friend: Impact of predators on aggregation behavior of gammarids

Predation pressure may affect many aspects of prey behavior, including forming groups and changes in social interactions. We studied the aggregation behavior of competing gammarids Dikerogammarus villosus and Pontogammarus robustoides (Amphipoda, Crustacea) to check whether they modify their preferences for conspecifics or heterospecifics in response to predator (the racer goby Babka gymnotrachelus) kairomones in the presence or absence of stone shelters (alternative protection source). Both species exhibited preferences toward shelters occupied by conspecifics over empty shelters and conspecifics apart from shelters, suggesting that their aggregation depends not only on habitat heterogeneity, but also on their social interactions. Moreover, gammarids in the presence of shelters (safer conditions) preferred conspecifics over heterospecifics, but predator kairomones made them form aggregations irrespective of species. In the predator presence, P. robustoides increased its aggregation level only in the sheltered conditions, whereas D. villosus exhibited this response only in the absence of shelters, suggesting that this behavior can protect it against predators. Therefore, we tested the antipredator effectiveness of D. villosus aggregations by exposing them to fish predation. Gobies foraged most effectively on immobile single gammarids compared to moving and aggregated individuals. Fish also avoided aggregated prey, confirming the protective character of aggregations. We have demonstrated that the predator presence increases aggregation level of prey gammarids and affects their social behavior by reducing antagonistic interactions and avoidance between competing species. This is likely to affect their distribution and functioning in the wild, where predator pressure is a standard situation.     

Searching for the Audience of the Weeping Lizard's Distress Call

The evolution and functions of avian and mammalian antipredator calls are well understood, which contrasts with a lack of progress in reptiles. Here, we present the first investigation of the functions of a distress call in a lizard. We studied Liolaemus chiliensis, which emits a short and complex high‐pitched scream when it is subdued. We determined the behavioral responses of two potential targets to these calls, conspecifics, and a snake predator. Additionally, we tested whether the chemical environment (presence of chemical scents from conspecifics) modulates the lizards' responses to calls. Both the conspecifics and the predator responded to the distress calls, which triggered a longer period of immobility in the lizards and a reduction in exploratory behavior in the snake, as compared to a white noise. In addition, the lizards in the arena with scents of conspecifics responded to distress calls and noise with more movements and escape attempts. These results suggest that distress calls may enhance the survival of L. chiliensis individuals.     

Anthropogenic influences on primate antipredator behavior and implications for research and conservation

Predation risk affects prey species' behavior, even in the absence of a direct threat, but human-induced environmental change may disturb ecologically significant predator–prey interactions. Here, we propose various ways in which knowledge of antipredator tactics, behavioral risk effects, and primate–predator interactions could assist in identifying human-caused disruption to natural systems. Using behavior to evaluate primate responses to the ongoing environmental change should be a potentially effective way to make species conservation more predictive by identifying issues before a more dramatic population declines. A key challenge here is that studies of predation on primates often use data collected via direct observations of habituated animals and human presence can deter carnivores and influence subjects' perception of risk. Hence, we also review various indirect data collection methods to evaluate their effectiveness in identifying where environmental change threatens wild species, while also minimizing observer bias.     

Phenotypic integration between antipredator behavior and camouflage pattern in juvenile sticklebacks

Predation is a strong selective force that promotes the evolution of antipredator behaviors and camouflage in prey animals. However, the independent evolution of single traits cannot explain how observed phenotypic variations of these traits are maintained within populations. We studied genetic and phenotypic correlations between antipredator behaviors (shoaling and risk‐taking) and morphology traits (pigmentation and size) in juvenile three‐spined sticklebacks by using pedigree‐based quantitative genetic analysis to test phenotypic integration (or complex phenotype) as an evolutionary response to predation risk. Individuals with strongly melanized (i.e., camouflaged) phenotype and genotype were less sociable to conspecifics, but bolder during foraging under predation risk. Individuals with faster growing phenotype and genotype were bolder, and those with lager eyes were more fearful. These phenotypic integrations were not confounded with correlated plastic responses to predation risk because the phenotypes were measured in naïve fish born in the laboratory, but originated from a natural population with predation pressure. Consistent selection for particular combinations of traits under predation pressure or pleiotropic genes might influence the maintenance of the genetic (co)variations and polymorphism in melanin color, growth trajectory, and behavior patterns.     

Predator‐Naïve Brown Trout (Salmo trutta) Show Antipredator Behaviours to Scent from an Introduced Piscivorous Mammalian Predator Fed Conspecifics

Introduced mammalian predators may pose a high risk for native and naïve prey populations, but little is known about how native fish species may recognize and respond to scents from introduced mammalian predators. We investigated the role of diet‐released chemical cues in facilitating predator recognition, hypothesizing that native brown trout (Salmo trutta) would exhibit antipredator behaviours to faeces scents from the introduced American mink (Neovision vison) fed conspecifics, but not to non‐trout diets. In treatments‐control and replicate stream tank experiments, brown trout showed significant antipredator responses to faeces scent from mink fed conspecifics, but not to faeces scent from mink fed a non‐trout diet (chicken), or the non‐predator food control, Eurasian beaver (Castor fiber). We conclude that native and naïve brown trout show relevant antipredator behaviours to an introduced mammalian predator, presumably based on diet‐released conspecific alarm cues and thereby estimate the predation risk.     

Predator density and the functional responses of coral reef fish

Predation is a key process driving coral reef fish population dynamics, with higher per capita prey mortality rates on reefs with more predators. Reef predators often forage together, and at high densities, they may either cooperate or antagonize one another, thereby causing prey mortality rates to be substantially higher or lower than one would expect if predators did not interact. However, we have a limited mechanistic understanding of how prey mortality rates change with predator densities. We re-analyzed a previously published observational dataset to investigate how the foraging response of the coney grouper (Cephalopholis fulva) feeding on the bluehead wrasse (Thalassoma bifasciatum) changed with shifts in predator and prey densities. Using a model-selection approach, we found that per-predator feeding rates were most consistent with a functional response that declines as predator density increases, suggesting either antagonistic interactions among predators or a shared antipredator behavioral response by the prey. Our findings suggest that variation in predator density (natural or anthropogenic) may have substantial consequences for coral reef fish population dynamics.     

Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study

Antipredator behaviour is an important fitness component in most animals. A co-evolutionary history between predator and prey is important for prey to respond adaptively to predation threats. When non-native predator species invade new areas, native prey may not recognise them or may lack effective antipredator defences. However, responses to novel predators can be facilitated by chemical cues from the predators’ diet. The red swamp crayfish Procambarus clarkii is a widespread invasive predator in the Southwest of the Iberian Peninsula, where it preys upon native anuran tadpoles. In a laboratory experiment we studied behavioural antipredator defences (alterations in activity level and spatial avoidance of predator) of nine anurans in response to P. clarkii chemical cues, and compared them with the defences towards a native predator, the larval dragonfly Aeshna sp. To investigate how chemical cues from consumed conspecifics shape the responses, we raised tadpoles with either a tadpole-fed or starved crayfish, or dragonfly larva, or in the absence of a predator. Five species significantly altered their behaviour in the presence of crayfish, and this was largely mediated by chemical cues from consumed conspecifics. In the presence of dragonflies, most species exhibited behavioural defences and often these did not require the presence of cues from predation events. Responding to cues from consumed conspecifics seems to be a critical factor in facilitating certain behavioural responses to novel exotic predators. This finding can be useful for predicting antipredator responses to invasive predators and help directing conservation efforts to the species at highest risk.     

Tadpoles of the bronze frog (Rana temporalis) assess predation risk before evoking antipredator defense behavior

Predation threat-associated behavioral response was studied in Rana temporalis tadpoles to discover the importance of predators’ visual and chemical cues (kairomones and diet-derived metabolites of consumed prey) in evoking antipredator behavior. The caged predators (dragonfly larvae) fed on prey tadpoles or insects (Notonecta spp.) and water conditioned with the predators provided the threat stimuli to the tadpole prey. The predators’ visual cues were ineffective in evoking antipredator behaviors in the tadpole prey. However, exposure to caged tadpole-fed predators or water conditioned with tadpole-fed predators elicited predator avoidance behavior in the tadpoles; they stayed away from the predators, significantly reduced swimming activity (swimming time and distance traveled), and increased burst speed. Interestingly, exposure to water conditioned with starved predators did not elicit any antipredator behavior in the prey. Further, the antipredator responses of predator-experienced tadpoles were significantly greater than those exhibited by predator-na?ve tadpoles. The study shows that R. temporalis tadpoles assess predation threat based exclusively on chemical cues emanating from the predators’ dietary metabolites and that the inclusion of conspecific prey items in the diet of the predators is perceived as a threat. The study also shows that antipredator behavior in these tadpoles is innate and is enhanced during subsequent encounters with the predators.     

Use of prey hotspots by an avian predator: purposeful unpredictability?

The use of space by predators in relation to their prey is a poorly understood aspect of predator-prey interactions. Classic theory suggests that predators should focus their efforts on areas of abundant prey, that is, prey hotspots, whereas game-theoretical models of predator and prey movement suggest that the distribution of predators should match that of their prey's resources. If, however, prey are spatially anchored to one location and these prey have particularly strong antipredator responses that make them difficult to capture with frequent attacks, then predators may be forced to adopt alternative movement strategies to hunt behaviorally responsive prey. We examined the movement patterns of bird-eating sharp-shinned hawks (Accipiter striatus) in an attempt to shed light on hotspot use by predators. Our results suggest that these hawks do not focus on prey hotspots such as bird feeders but instead maintain much spatial and temporal unpredictability in their movements. Hawks seldom revisited the same area, and the few frequently used areas were revisited in a manner consistent with unpredictable returns, giving prey little additional information about risk.     

Prey behavior, age-dependent vulnerability, and predation rates

Variation in the temporal pattern of vulnerability can provide important insights into predator-prey relationships and the evolution of antipredator behavior. We illustrate these points with a system that has coyotes (Canis latrans) as a predator and two species of congeneric deer (Odocoileus spp.) as prey. The deer employ different antipredator tactics (aggressive defense vs. flight) that result in contrasting patterns of age-dependent vulnerability in their probability of being captured when encountered by coyotes. We use long-term survival data and a simple mathematical model to show that (1) species differences in age-dependent vulnerability are reflected in seasonal predation rates and (2) seasonal variation in prey vulnerability and predator hunt activity, which can be associated with the availability of alternative prey, interact to shape seasonal and annual predation rates for each prey species. Shifting hunt activity from summer to winter, or vice versa, alleviated annual mortality on one species and focused it on the other. Our results indicate that seasonal variation in prey vulnerability and hunt activity interact to influence the impact that a predator has on any particular type of prey. Furthermore, these results indicate that seasonal variation in predation pressure is an important selection pressure shaping prey defenses.     

Intraguild predation drives evolutionary niche shift in threespine stickleback

Intraguild predation--competition and predation by the same antagonist--is widespread, but its evolutionary consequences are unknown. Intraguild prey may evolve antipredator defenses, superior competitive ability on shared resources, or the ability to use an alternative resource, any of which may alter the structure of the food web. We tested for evolutionary responses by threespine stickleback to a benthic intraguild predator, prickly sculpin. We used a comparative morphometric analysis to show that stickleback sympatric with sculpin are more armored and have more limnetic-like body shapes than allopatric stickleback. To test the ecological implications of this shift, we conducted a mesocosm experiment that varied sculpin presence and stickleback population of origin (from one sympatric and one allopatric lake). Predation by sculpin greatly increased the mortality of allopatric stickleback. In contrast, sculpin presence did not affect the mortality of sympatric stickleback, although they did have lower growth rates suggesting increased nonpredatory effects of sculpin. Consistent with their morphology, sympatric stickleback included more pelagic prey in their diets, leading to depletion of zooplankton in the mesocosms. These findings suggest that intraguild prey evolution has altered food web structure by reducing both predation by the intraguild predator and diet overlap between species.     

Biogeographic variation in behavioral and morphological responses to predation risk

The expression of prey antipredator defenses is often related to ambient consumer pressure, and prey express greater defenses under intense consumer pressure. Predation is generally greater at lower latitudes, and antipredator defenses often display a biogeographic pattern. Predation pressure may also vary significantly between habitats within latitudes, making biogeographic patterns difficult to distinguish. Furthermore, invasive predators may also influence the expression of prey defenses in ecological time. The purpose of this study was to determine how these factors influence the strength of antipredator responses. To assess patterns in prey antipredator defenses based upon geographic range (north vs. south), habitat type (wave-protected vs. wave-exposed shores), and invasive predators, we examined how native rock (Cancer irroratus) and invasive green (Carcinus maenas) crab predators influence the behavioral and morphological defenses of dogwhelk (Nucella lapillus) prey from habitats that differ in wave exposure across an ~230 km range within the Gulf of Maine. The expression of behavioral and morphological antipredatory responses varied according to wave exposure, geographic location, and predator species. Dogwhelks from areas with an established history with green crabs exhibited the largest behavioral and morphological antipredator responses to green crabs. Dogwhelk behavioral responses to rock crabs did not vary between habitats or geographic regions, although morphological responses were greater further south where predation pressure was greatest. These findings suggest that dogwhelk responses to invasive and native predators vary according to geographic location and habitat, and are strongly affected by ambient predation pressure due to the invasion history of an exotic predator.     

Predator density and competition modify the benefits of group formation in a shoaling reef fish

Synthesis Predation risk experienced by individuals living in groups depends on the balance between predator dilution, competition for refuges, and predator interference or synergy. These interactions operate between prey species as well: the benefits of group living decline in the presence of an alternative prey species. We apply a novel model‐fitting approach to data from field experiments to distinguish among competing hypotheses about shifts in predator foraging behavior across a range of predator and prey densities. Our study provides novel analytical tools for analyzing predator foraging behavior and offers insight into the processes driving the dynamics of coral reef fish. Studies of predator foraging behavior typically focus on single prey species and fixed predator densities, ignoring the potential importance of complexities such as predator dilution; predator‐mediated effects of alternative prey; heterospecific competition; or predator–predator interactions. Neglecting the effects of prey density is particularly problematic for prey species that live in mixed species groups, where the beneficial effects of predator dilution may swamp the negative effects of heterospecific competition. Here we use field experiments to investigate how the mortality rates of a shoaling coral reef fish (a wrasse: Thalassoma amblycephalum), change as a result of variation in: 1) conspecific density, 2) density of a predator (a hawkfish: Paracirrhites arcatus), and 3) presence of an alternative prey species that competes for space (a damselfish: Pomacentrus pavo). We quantify changes in prey mortality rates from the predator's perspective, examining the effects of added predators or a second prey species on the predator's functional response. Our analysis highlights a model‐fitting approach that discriminates amongst multiple hypotheses about predator foraging in a community context. Wrasse mortality decreased with increasing conspecific density (i.e. mortality was inversely density‐dependent). The addition of a second predator doubled prey mortality rates, without significantly changing attack rate or handling time – i.e. there was no evidence for predator interference. The presence of a second prey species increased wrasse mortality by 95%; we attribute this increase either to short‐term apparent competition (predator aggregation) or to a decrease in handling time of the predator (e.g. through decreased wrasse vigilance). In this system, 1) prey benefit from intraspecific group living though a reduced predation risk, and 2) the benefit of group living is reduced in the presence of an alternative prey species.     

Recognition and Response to Native and Novel Predators in the Largespring mosquitofish,Gambusia geiseri

The introduction of predator species into new habitats is an increasingly common consequence of human activities, and the persistence of native prey species depends upon their response to these novel predators. In this study, we examined whether the Largespring mosquitofish, Gambusia geiseri exhibited antipredator behavior and/or an elevation of circulating stress hormones (cortisol) to visual and chemical cues from a native predator, a novel predator, or a non‐predatory control fish. Prey showed the most pronounced antipredator response to the native predator treatment, by moving away from the stimulus, while the prey showed no significant changes in their vertical or horizontal position in response to the novel or non‐predator treatments. We also found no significant difference in water‐borne cortisol release rates following any of the treatments. Our results suggest the prey did not recognize and exhibit antipredator behavior to the novel predator, and we infer that this predator species could be detrimental if it expands into the range of this prey species. Further, our study demonstrates prey may not respond to an invasive predator that is phylogenetically, behaviorally, and morphologically dissimilar from the prey species' native predators.