Nest site attributes and temporal patterns of northern flicker nest loss: effects of predation and competition

To date, most studies of nest site selection have failed to take into account more than one source of nest loss (or have combined all sources in one analysis) when examining nest site characteristics, leaving us with an incomplete understanding of the potential trade-offs that individuals may face when selecting a nest site. Our objectives were to determine whether northern flickers (Colaptes auratus) may experience a trade-off in nest site selection in response to mammalian nest predation and nest loss to a cavity nest competitor (European starling, Sturnus vulgaris). We also document within-season temporal patterns of these two sources of nest loss with the hypothesis that flickers may also be constrained in the timing of reproduction under both predatory and competitive influence. Mammalian predators frequently depredated flicker nests that were: lower to the ground, less concealed by vegetation around the cavity entrance and at the base of the nest tree, closer to coniferous forest edges and in forest clumps with a high percentage of conifer content. Proximity to coniferous edges or coniferous trees increased the probability of nest predation, but nests near conifers were less likely to be lost to starlings. Flickers may thus face a trade-off in nest site selection with respect to safety from predators or competitors. Models suggested that peaks of nest predation and nest loss to eviction occurred at the same time, although a competing model suggested that the peak of nest loss to starlings occurred 5 days earlier than the peak of mammalian predation. Differences in peaks of mammalian predation and loss to starlings may constrain any adjustment in clutch initiation date by flickers to avoid one source of nest loss.     

Innate predator recognition in giant pandas

Innate predator recognition confers a survival advantage to prey animals. We investigate whether giant pandas exhibit innate predator recognition. We analyzed behavioral responses of 56 naive adult captive giant pandas (Ailuropoda melanoleuca), to urine from predators and non-predators and water control. Giant pandas performed more chemosensory investigation and displayed flehmen behaviors more frequently in response to predator urine compared to both non-predator urine and water control. Subjects also displayed certain defensive behaviors, as indicated by vigilance, and in certain cases, fleeing behaviors. Our results suggest that there is an innate component to predator recognition in captive giant pandas, although such recognition was only slight to moderate. These results have implications that may be applicable to the conservation and reintroduction of this endangered species.     

Innate and Learned Predator Recognition Mediated by Chemical Signals in Eurycea nana

Effective and efficient predator recognition and avoidance are essential for the persistence of prey populations, especially in habitats where non-native predators have been introduced. Predator recognition studies are commonly couched within a learned or innate dichotomous framework; however, characteristics of some systems or species could favor innate recognition combined with the ability to alter avoidance responses based on experience with predators. Eurycea nana is a fully aquatic salamander inhabiting a system with a diverse, yet temporally stable, community of native and non-native opportunistically foraging fish predators. To examine predator recognition, we examined avoidance responses (decreased activity) of predator-naïve (first-generation, captive-reared) and predator-experienced (recently collected) E. nana to the chemical cues of a native predator, a non-native predator, a non-predator, and a blank control. Both predator-naïve and predator-experienced E. nana significantly lowered activity in response to the native fish predator when compared with a blank control. Interestingly, predator-naïve E. nana decreased activity in response to the non-native fish predator while predator-experienced E. nana did not. These results indicate that while there is an innate component to predator recognition in E. nana , experience and risk assessment may also be important.     

Antipredator Behavior of American Bullfrogs (Lithobates catesbeianus) in a Novel Environment

Invasive species capable of recognizing potential predators may have increased establishment rates in novel environments. Individuals may retain historical predator recognition and invoke innate responses in the presence of taxonomically or ecologically similar predators, generalize antipredator responses, or learn to avoid risky species in novel environments. Invasive amphibians in aquatic environments often use chemical cues to assess predation risk and learn to avoid novel predators via direct experience and/or associated chemical cues. Ontogeny may also influence recognition; experience with predators may need to occur at certain developmental stages for individuals to respond correctly. We tested predator recognition in invasive American bullfrog ( Lithobates catesbeianus) tadpoles that varied in experience with fish predators at the population and individual scale. We found that bullfrog tadpoles responded to a historical predator, largemouth bass ( Micropterus salmoides), only if the population was locally sympatric with largemouth bass. Individuals from a population that did not co‐occur with largemouth bass did not increase refuge use in response to either largemouth bass chemical cues alone or chemical cues with diet cues (largemouth bass fed bullfrog tadpoles). To test whether this behavioral response was generalized across fish predators, we exposed tadpoles to rainbow trout ( Oncorhynchus mykiss) and found that tadpoles could not recognize this novel predator regardless of co‐occurrence with other fish species. These results suggest that environment may be more important for predator recognition than evolutionary history for this invasive species, and individuals do not retain predator recognition or generalize across fish predators.     

Experimental evidence for innate predator recognition in the Seychelles warbler.

Nest predation is a major determinant of fitness in birds and costly nest defence behaviours have evolved in order to reduce nest predation. Some avian studies have suggested that predator recognition is innate whereas others have stressed the importance of learning. However, none of these studies controlled for the genetic origin of the populations investigated and the effect of unfamiliarity with the predator. Here we determined whether experience with a nest predator is a prerequisite for nest defence by comparing predator recognition responses between two isolated but genetically similar Seychelles warbler (Acrocephalus sechellensis) populations, only one of which had experience of the egg predating Seychelles fody (Foudia sechellarum). Individuals in the predator-free population significantly reduced nest guarding compared to individuals in the population with the predator, which indicates that this behaviour was adjusted to the presence of nest predators. However, recognition responses (measured as both alarm call and attack rates) towards a mounted model of the fody were equally strong in both populations and significantly higher than the responses towards either a mounted familiar non-predator and a mounted, novel, non-predator bird species. Responses did not differ with a warbler's age and experience with the egg predator, indicating that predator recognition is innate.     

Predation Risk Avoidance by Terrestrial Amphibians: The Role of Prey Experience and Vulnerability to Native and Exotic Predators

We studied avoidance, by four amphibian prey species (Rana luteiventris, Ambystoma macrodactylum, Pseudacris regilla, Tarichia granulosa), of chemical cues associated with native garter snake (Thamnophis elegans) or exotic bullfrog (R. catesbeiana) predators. We predicted that avoidance of native predators would be most pronounced, and that prey species would differ in the intensity of their avoidance based on relative levels of vulnerability to predators in the wild. Adult R. luteiventris (presumably high vulnerability to predation) showed significant avoidance of chemical cues from both predators, A. macrodactylum (intermediate vulnerability to predation) avoided T. elegans only, while P. regilla (intermediate vulnerability to predation) and T. granulosa (low vulnerability to predation) showed no avoidance of either predator. We assessed if predator avoidance was innate and/or learned by testing responses of prey having disparate levels of prior exposure to predators. Wild‐caught (presumably predator‐exposed) post‐metamorphic juvenile R. luteiventris and P. regilla avoided T. elegans cues, while laboratory‐reared (predator‐naive) conspecifics did not; prior exposure to R. catesbeiana was not related to behavioural avoidance among adult or post‐metamorphic juvenile wild‐reared A. macrodactylum and P. regilla. These results imply that (i) some but not all species of amphibian prey avoid perceived risk from garter snake and bullfrog predators, (ii) the magnitude of this response probably differs according to prey vulnerability to predation in the wild, and (iii) avoidance tends to be largely learned rather than innate. Yet, the limited prevalence and intensity of amphibian responses to predation risk observed herein may be indicative of either a relatively weak predator–prey relationship and/or the limited importance of predator chemical cues in this particular system.     

Persistence of Alarm-Call Behaviour in the Absence of Predators: A Comparison Between Wild and Captive-Born Meerkats (Suricata Suricatta)

Performing correct anti‐predator behaviour is crucial for prey to survive. But, are such abilities lost in species or populations living in predator‐free environments? How individuals respond to the loss of predators has been shown to depend on factors such as the degree to which anti‐predator behaviour relies on experience, the type of cues evoking the behaviour, the cost of expressing the behaviour and the number of generations under which relaxed selection has taken place. Here we investigated whether captive‐born populations of meerkats (Suricata suricatta) used the same repertoire of alarm calls previously documented in wild populations and whether captive animals, as wild ones, could recognize potential predators through olfactory cues. We found that all alarm calls that have been documented in the wild also occurred in captivity and were given in broadly similar contexts. Furthermore, without prior experience of odours from predators, captive meerkats seemed to distinguish between faeces of potential predators (carnivores) and non‐predators (herbivores). Despite slight structural differences, the alarm calls given in response to the faeces largely resembled those recorded in similar contexts in the wild. These results from captive populations suggest that direct, physical interaction with predators is not necessary for meerkats to perform correct anti‐predator behaviour in terms of alarm‐call usage and olfactory predator recognition. Such behaviour may have been retained in captivity because relatively little experience seems necessary for correct performance in the wild and/or because of the recency of relaxed selection on these populations.     

Prey naivety in the behavioural responses of juvenile Chinook salmon (Oncorhynchus tshawytscha) to an invasive predator

1. Non‐native predators might inflict proportionally higher mortality on prey that have no previous experience of them, compared to species that have coexisted with the predator for some time. 2. We tested whether juvenile Chinook salmon (Oncorhynchus tshawytscha) were less able to recognise a non‐native than a native predator, by investigating behavioural responses to the chemical cues of the invasive smallmouth bass (Micropterus dolomieu) and the native northern pikeminnow (Ptychocheilus oregonensis) in both laboratory and field experiments. 3. Laboratory results demonstrated strong innate antipredator responses of individual juvenile Chinook salmon to northern pikeminnow; fish spent 70% of time motionless and exhibited 100% greater panic response than in controls. By contrast, antipredator responses to the chemical cues of smallmouth bass did not differ from controls. 4. These results were supported by similar differences in recognition of these predator odours by groups of juvenile Chinook salmon in fully natural conditions, though responses reflected a greater range of antipredator behaviours by individuals. In field trials, responses to northern pikeminnow odour resulted in increased flight or absence, reductions in swimming and foraging, and increased time spent near the substratum, compared to smallmouth bass odour. 5. Given that survival of juvenile fish is facilitated by predator recognition, our results support the hypothesis that naivety may be an important factor determining the effect of non‐native predators on prey populations. Efforts to manage the effect of native and non‐native predators may benefit by considering complex behavioural interactions, such as these at the individual and group levels.     

Generalization of learned predator recognition: an experimental test and framework for future studies

While some prey species possess an innate recognition of their predators, others require learning to recognize their predators. The specific characteristics of the predators that prey learn and whether prey can generalize this learning to similar predatory threats have been virtually ignored. Here, we investigated whether fathead minnows that learned to chemically recognize a specific predator species as a threat has the ability to generalize their recognition to closely related predators. We found that minnows trained to recognize the odour of a lake trout as a threat (the reference predator) generalized their responses to brook trout (same genus as lake trout) and rainbow trout (same family), but did not generalize to a distantly related predatory pike or non-predatory suckers. We also found that the intensity of antipredator responses to the other species was correlated with the phylogenetic distance to the reference predator; minnows responded with a higher intensity response to brook trout than rainbow trout. This is the first study showing that prey have the ability to exhibit generalization of predator odour recognition. We discuss these results and provide a theoretical framework for future studies of generalization of predator recognition.     

Constitutive exposure to the volatile methyl salicylate reduces per‐capita foraging efficiency of a generalist predator to learned prey associations

Understanding the factors that influence the ability of predators to find and kill herbivores is central to enhancing their impact on prey populations, but few studies have tested the impact of these factors on predation rates in realistic foraging environments. Using the tri‐trophic system consisting of tomato, Solanum lycopersicum L. (Solanaceae), hornworm caterpillars, Manduca sexta L. (Lepidoptera: Sphingidae), and the predaceous stink bug Podisus maculiventris (Say) (Hemiptera: Pentatomidae), we measured the effects of associative learning and plant volatile camouflage on predator behavior and foraging efficiency in field enclosures. To do so, we compared experienced vs. naive individuals under varying environmental contexts. Experienced predators were those with prior exposure to induced volatiles from the tomato–caterpillar association, whereas naive predators had not experienced tomato, only prey (caterpillars). We varied their environmental foraging matrix using either (1) tomato surrounded by basil (Ocimum basilicum L.; Lamiaceae) or (2) tomato exposed to the synthetic volatile, methyl salicylate (MeSA). We found that (1) experienced predators were more efficient than naive predators, capturing 28% more prey; (2) the tomato–basil combination did not affect predator–prey interactions; and (3) constitutive emission of synthetic MeSA caused a 22% reduction in P. maculiventris predation rate. These differences corresponded with distinct shifts in predator foraging; for example, experienced individuals were less stationary and exhibited unique behaviors such as stylet extension. Taken together, these results suggest that it is possible to improve the function of generalist predators in suppressing prey by coupling odors with food. However, constitutive emission of volatiles to attract natural enemies may ultimately camouflage neighboring plants, reducing the benefits of orientation to learned stimuli such as induced volatiles.     

Predator experience homogenizes consistent individual differences in predator avoidance

In the presence of predators, many prey species exhibit immediate behavioral responses like the avoidance of risky areas, which imposes opportunity costs, for instance, in the form of reduced foraging. Thus, prey species should be able to discriminate between different predator types and adjust their response to the imminent predation risk. In our current study, we evaluated the relative importance of innate versus learned components of predator recognition and avoidance in the guppy (Poecilia reticulata). We used a feral guppy population occurring in Germany and compared avoidance reactions of each focal individual towards both coevolved piscine predators from their original distribution range and novel, presently co-occurring predator species. Wild-caught, predator-experienced as well as laboratory-reared, predator-naïve individuals showed strong avoidance responses towards all predator animations. Avoidance was stronger in small-bodied than in large-bodied individuals in both cohorts; however, this effect was significant only in predator-naïve fish. Moreover, wild-caught individuals showed a significantly higher within-individual variance (across the six predator species) along with a lower among-individual variance in predator avoidance, which resulted in a lower behavioral repeatability in this cohort. Our results suggest that consistent individual differences in risk-taking behavior (also referred to as the personality trait ‘boldness’) are modified by predator exposure and learning about predators.     

Damage released prey alarm substances or predator odours? Risk assessment by an aquatic oligochaete

Although the abilities of prey to detect and respond to chemical substances associated with a predator have been widely reported, the factors promoting the evolution of responses to prey alarm cues vs. predator odours are still vague. In this article, we combined field research with laboratory experiments to explore which chemical substance associated with predator activity (predator odour, conspecific or heterospecific alarm substances) induces defence responses in the aquatic oligochaete Stylaria lacustris, which is vulnerable to common littoral predators. The field results indicated that predators injure the oligochaetes and a great proportion, up to 45% of individuals in the population, were found to be damaged. The results of the laboratory experiments revealed that chemical odours from damselfly larvae feeding on S. lacustris did not induce the defence response in the oligochaetes. On the contrary, oligochaetes detected and responded to alarm substances from damaged conspecifics alone and substances from damaged cladoceran Daphnia magna. We discussed conditions favouring the responses to damage released prey alarm cues instead of predator odours in Stylaria lacustris. Our data suggest that the selection of responses to alarm cues from damaged prey vs. predator odours may be dependent on three factors: (1) non-species-specific predation, (2) divergence of food niche of the different stages of the predator and (3) complex food web with multiple predators. Handling editor: S. Declerk     

The role of tactile interactions in flight responses in the Bronze Cory catfish (Corydoras aeneus)

One of the primary functions of animal aggregations is defence against predators. Many social animals enjoy reduced predation risk as a result of grouping, and individuals within groups can benefit from information transferred by their group‐mates about a potential predator. We present evidence that a tactile interaction behaviour we term “nudging” substantially modified group responses to a potential threat in a highly social catfish, Corydoras aeneus. These catfish deployed nudges during flight responses, and these nudges were associated with a greater likelihood of group cohesion following a threat event. Increased nudging behaviour also resulted in longer flight responses, a potentially costly outcome in natural contexts. In addition, individuals that perceived the threat first were more likely to initiate nudges, implying that nudges could be used to alert group‐mates to the presence of a threat. Taken together, our results suggest that tactile communication plays an important role in mediating anti‐predator benefits from sociality in these fish.     

Antipredator Responses by Native Mosquitofish to Non-Native Cichlids: An Examination of the Role of Prey Naiveté

The strong impact of non‐native predators in aquatic systems is thought to relate to the evolutionary naiveté of prey. Due to isolation and limited dispersal, this naiveté may be relatively high in freshwater systems. In this study, we tested this notion by examining the antipredator response of native mosquitofish, Gambusia holbrooki, to two non‐native predators found in the Everglades, the African jewelfish, Hemichromis letourneuxi, and the Mayan cichlid, Cichlasoma urophthalmus. We manipulated prey naiveté by using two mosquitofish populations that varied in their experience with the recent invader, the African jewelfish, but had similar levels of experience with the longer‐established Mayan cichlid. Specifically, we tested these predictions: (1) predator hunting modes differed between the two predators, (2) predation rates would be higher by the novel jewelfish predator, (3) particularly on the naive population living where jewelfish have not invaded yet, (4) antipredator responses would be stronger to Mayan cichlids due to greater experience and weaker and/or ineffective to jewelfish, and (5) especially weakest by the naive population. We assayed prey and predator behavior, and prey mortality in lab aquaria where both predators and prey were free‐ranging. Predator hunting modes and habitat domains differed, with jewelfish being more active search predators that used slightly higher parts of the water column and less of the habitat structure relative to Mayan cichlids. In disagreement with our predictions, predation rates were similar between the two predators, antipredator responses were stronger to African jewelfish (except for predator inspections), and there was no difference in response between jewelfish‐savvy and jewelfish‐naive populations. These results suggest that despite the novelty of introduced predators, prey may be able to respond appropriately if non‐native predator archetypes are similar enough to those of native predators, if prey rely on general antipredator responses or predation cues, and/or show neophobic responses.     

Introduced predator elicits deficient brood defence behaviour in a crater lake fish

Introduced species represent one of the most serious global threats to biodiversity. In this field-based study, we assessed behavioural responses of brood tending cichlid fish to an invasive predator of their offspring. This was achieved by comparing parental defence responses of the endangered arrow cichlid (Amphilophus zaliosus), a fish species endemic to the crater lake Apoyo in Nicaragua, towards the bigmouth sleeper (Gobiomorus dormitor), a formidable predator of cichlid fry, and all other potential fish predators of offspring. The bigmouth sleeper was recently introduced into Apoyo but naturally co-exists with cichlids in a few other Nicaraguan lakes. Arrow cichlid parents allowed bigmouth sleepers to advance much closer to their fry than other predators before initiating aggressive brood defence behaviours. Interestingly, parents of a very closely related species, A. sagittae, which has coevolved with bigmouth sleepers in crater lake Xiloá, reacted to approaching bigmouth sleepers at comparable distances as to other predators of cichlid fry. These results provide a novel demonstration of the specific mechanism (i.e. naive parental behaviour) by which invasive predators may negatively affect species that lack the adequate behavioural repertoire.     

Functional mechanisms of an inducible defence in tadpoles: morphology and behaviour influence mortality risk from predation

In many amphibian larvae a suite of morphological and behavioural characters varies together in an induced defence against predators, but it remains unclear which features are functionally related to defence. We independently manipulated behaviour and morphology in tadpoles of Hyla versicolor and assessed their consequences for swimming performance and predator escape. Data on burst swimming showed that tadpoles which accelerated rapidly were elongate, with shallow bodies and tails. Predator escape was measured by exposing tadpoles to predators (larval Anax dragonflies or larval Ambystoma salamanders) and recording time until death. Tadpoles were first reared for 30 days in ponds containing either caged Anax or no predators; individuals responded to predators by developing large brightly coloured tails and short bodies. We placed tadpoles of both morphological phenotypes into plastic tubs, and manipulated their behaviour using food and chemical cues from predators. Mortality risk experienced by the predator‐induced phenotype was about half that of the no‐predator phenotype, and risk increased with time spent swimming. An interaction between morphology and behaviour arose because increasing activity caused higher risk for tadpoles with deep tail fins but not shallow tail fins.     

The temporal selfish herd: predation risk while aggregations form

The hypothesis of the selfish herd has been highly influential to our understanding of animal aggregation. Various movement strategies have been proposed by which individuals might aggregate to form a selfish herd as a defence against predation, but although the spatial benefits of these strategies have been extensively studied, little attention has been paid to the importance of predator attacks that occur while the aggregation is forming. We investigate the success of mutant aggregation strategies invading populations of individuals using alternative strategies and find that the invasion dynamics depend critically on the time scale of movement. If predation occurs early in the movement sequence, simpler strategies are likely to prevail. If predators attack later, more complex strategies invade. If there is variation in the timing of predator attacks (through variation within or between individual predators), we hypothesize that groups will consist of a mixture of strategies, dependent upon the distribution of predator attack times. Thus, behavioural diversity can evolve and be maintained in populations of animals experiencing a diverse range of predators differing solely in their attack behaviour. This has implications for our understanding of predator–prey dynamics, as the timing of predator attacks will exert selection pressure on prey behavioural responses, to which predators must respond.     

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.     

Stone banging by wild capuchin monkeys: an unusual auditory display

Primates often react to possible predators by using intimidation displays, although the occurrence of these displays is dependent on the risk of predation. Functional explanations for these kinds of displays range from sexual selection to predator deterrence. The ability to respond to different predators can be socially acquired, and social traditions could explain population differences in response to the same potential predator. Here I report wild groups of Cebus apella libidinosus banging stones to produce sound in a remarkable aggressive display. I observed this display in 6 wild groups and I suggest its primary function is a predator-deterrent behaviour. Although banging objects is an innate behaviour in capuchin monkeys, in all wild groups observed so far it has been observed only in a foraging context. Stone banging is a novel behavioural variant that is most likely learned socially. The absence of this display in other populations of capuchins, which have access to stones, suggests that stone banging could be a social tradition in the population studied.     

Anti‐predatory behaviour of wild‐caught vs captive‐bred freshwater angelfish,Pterophyllum scalare

Environments and experiences encountered in early life stages of animals shape their adult behaviour. When environments are maintained for several generations, differential selection forces act upon individuals to select those most fit to the particular conditions. As such, differences in the behaviour of captive bred and wild caught individuals have been observed recurrently. In fish, hatchery raised individuals tend to seek refuge less, making them more vulnerable to predators. We tested the hypothesis that captive breeding induces non‐adaptive changes in behaviour of freshwater angelfish, Pterophyllum scalare. Wild‐caught and captive‐bred fish were exposed to a natural predator and measured for their anti‐predator behaviours; no differences were found in behaviour under control conditions. When exposed to a natural predator, wild‐caught fish exhibited significantly shorter freezing durations than captive‐bred fish, and took significantly shorter time to resume normal behaviour. No differences in the time taken to initiate investigations of the predator were detected. The results demonstrate that captive‐bred fish respond differently than their wild counterparts when exposed to a natural predator, and that this domestication has implications for captive rearing programmes.