Antipredator Responses Research Articles

A non-vocal alarm? Effects of wing trill playbacks on antipredator responses in the scaled dove

Animals have evolved a variety of mechanisms to detect and avoid predation. The non-vocal sounds produced by some bird species during takeoff flights have been considered to function as an alarm call, because they may convey information about predation risk. Here, we experimentally investigated the effects of the non-vocal sound (wing trills) produced by the scaled dove (Columbina squammata) on antipredation behaviours of conspecifics. We evaluated the individual response to playbacks of the wing trill stimulus and compared it to the response to other two control stimuli (vocalizations of the scaled dove and the southern house wren). We found that doves’ probability to become vigilant or to display freezing behaviour was higher after a wing trills stimulus in comparison to the other playback stimuli. These results suggest that wing trill production in scaled doves communicate potential risks and are considered by the individuals in the decision-making process, but we cannot rule out the possibility that any takeoff flight sound might also promote antipredator responses.

The disturbance leg-lift response (DLR): an undescribed behavior in bumble bees.

BackgroundBumble bees, primarily Bombus impatiens and B. terrestris, are becoming increasingly popular organisms in behavioral ecology and comparative psychology research. Despite growing use in foraging and appetitive conditioning experiments, little attention has been given to innate antipredator responses and their ability to be altered by experience. In this paper, we discuss a primarily undescribed behavior, the disturbance leg-lift response (DLR). When exposed to a presumably threatening stimulus, bumble bees often react by lifting one or multiple legs. We investigated DLR across two experiments.MethodsIn our first experiment, we investigated the function of DLR as a prerequisite to later conditioning research. We recorded the occurrence and sequence of DLR, biting and stinging in response to an approaching object that was either presented inside a small, clear apparatus containing a bee, or presented directly outside of the subject’s apparatus. In our second experiment, we investigated if DLR could be altered by learning and experience in a similar manner to many other well-known bee behaviors. We specifically investigated habituation learning by repeatedly presenting a mild visual stimulus to samples of captive and wild bees.ResultsThe results of our first experiment show that DLR and other defensive behaviors occur as a looming object approaches, and that the response is greater when proximity to the object is lower. More importantly, we found that DLR usually occurs first, rarely precedes biting, and often precedes stinging. This suggests that DLR may function as a warning signal that a sting will occur. In our second experiment, we found that DLR can be altered as a function of habituation learning in both captive and wild bees, though the captive sample initially responded more. This suggests that DLR may be a suitable response for many other conditioning experiments.

Coral degradation impairs learning of non‐predators by Whitetail damselfish

Abstract A prerequisite for effective antipredator responses is the ability of a prey to distinguish animals that pose a threat from those that do not. Prey often have efficient learning mechanisms to learn threats but learning to recognize nonpredators may be equally or more important. Moreover, the ability to generalize learned information is of key importance for prey animals. Prey take information they know about one species to make ‘educated guesses’ about the predatory/nonpredatory status of other unknown species. Here, we investigate the ability of Whitetail damselfish Pomacentrus chrysurus to learn the identity of non‐predators and then generalize their responses to other unknown animals. Our work is completed within the context of unprecedented habitat degradation in reef ecosystems. When corals die, the remaining skeleton is colonized by algae, cyanobacteria and sessile invertebrates. These opportunistic colonists change the physical and chemical landscape of the reef and hence the background odour in which predator and non‐predator recognition occurs. Our results indicated that Whitetail damselfish learn to classify Moonwrasse Thalasomma lunare as a non‐predator through the process of latent inhibition, whereby the prey are repeatedly exposed to Moonwrasse odour multiple times in the absence of negative reinforcement. These fish subsequently generalized their nonpredator recognition to other unknown wrasse, but not distantly related fish. Of key importance was our finding that the patterns and extent of non‐predator learning and generalization were dramatically altered in dead coral habitats. As predicted, prey that learned the Moonwrasse as a nonpredator in live coral environments did not subsequently respond to Moonwrasse when we tried to teach them Moonwrasse was a predator in live coral. However, this non‐predator recognition was reduced in dead coral environments. Moreover, generalization completely failed when we changed from live to dead coral environments. Juvenile damselfishes need to rapidly catalogue the identity of unknown animals when they arrive at a reef. Changing background odours, that occur with changing tides and currents, means that prey need to learn non‐predator identities separately in each water source. This cognitive challenge likely has significant survival consequence in a changing environment. A free Plain Language Summary can be found within the Supporting Information of this article.

Thermal dependence and individual variation in tonic immobility varies between sympatric amphibians

Tonic immobility (TI) is an important antipredator response employed by prey in the last stages of a predation sequence. Evolution by natural selection assumes consistent individual variation (repeatability) in this trait. In ectotherms, which experience variable body temperatures, TI should be repeatable over a thermal gradient to be targeted by natural selection; however, information on thermal repeatability of this trait is missing. We examined thermal repeatability of TI in juveniles of two sympatric amphibians, smooth (Lissotriton vulgaris) and alpine (Ichthyosaura alpestris) newts. Both species showed disparate TI responses to body temperature variation (13-28°C). While the proportion of TI response was repeatable in both taxa, it increased with body temperature in alpine newts but was temperature independent in smooth newts. Duration of TI decreased with body temperature in both taxa but was only repeatable in smooth newts. Our results suggest that a warming climate may affect population dynamics of sympatric ectotherms through asymmetry in thermal reaction norms for antipredator responses.

Convergence and divergence in anti-predator displays: a novel approach to quantitative behavioural comparison in snakes

AbstractAnimals in nature use many strategies to evade or deter their predators. Within venomous snake mimicry, stereotyped anti-predator behaviours are hypothesized to be effective warning signals under strong selection for independent convergence across species. However, no studies have systematically quantified snake anti-predator displays across taxonomically broad clades to examine how these behaviours evolve within a comparative methods framework. Here we describe a new high-throughput approach for collecting and quantifying anti-predator displays in snakes that demonstrates both low observer bias and infinite extension. Then, we show this method’s utility by comparing 20 species spanning six taxonomic families from Peru. We found that a simple experimental set-up varying simulated predator cues was successful in eliciting displays across species and that high-speed videography captured a great diversity of anti-predator responses. Although display components show complicated patterns of covariance, we found support for behavioural convergence in anti-predator displays among elapid coral snakes and their distantly related mimics. Our approach provides new analytical opportunities for both behaviour and kinematics, especially macroevolutionary analyses across clades with similar difficulty in observing or comparing trait diversity.

Impact of conspecific necromones on the oxygen uptake rates of a benthic elasmobranch

Given the vulnerability of early life stages to predation, many species elicit antipredator responses to predator-associated cues (e.g. alarm cues, necromones). However, the response used may vary between predatory stimuli. Antipredator responses, while ostensibly enhancing survival, are costly, either resulting in missed opportunities (e.g. foraging) through decreased activity and crypsis strategies (i.e. predator avoidance) or incurring high energetic costs through the use of generalized stress responses and increased activity (i.e. predator evasion). Juvenile Port Jackson sharks, Heterodontus portusjacksoni, were exposed to the scent of dead conspecifics (conspecific necromones) coupled with a simulated predator chase to determine the energetic effects of a predator ‘attack’. When exposed to necromone cues alone, juvenile sharks depressed their oxygen uptake rates for up to 3 h following exposure, indicating that they used crypsis to avoid detection by predators. However, when forced to swim and evade a predator, sharks increased their oxygen uptake rates, regardless of whether or not they were exposed to predatory cues. Juvenile sharks exposed to conspecific necromones may primarily rely on strategies that depress activity to avoid detection by predators; however, if forced to evade capture they use energetically costly escape strategies similar to typical ‘fight or flight’ responses.

Coyote (Canis latrans) diet and spatial co-occurrence with woodland caribou (Rangifer tarandus caribou)

The interplay of predator encounters and antipredator responses is an integral part of understanding predator–prey interactions and spatial co-occurrence and avoidance can elucidate these interactions. We conducted hard-part dietary analysis of coyotes (Canis latrans Say, 1823) and space use of coyotes and woodland caribou (Rangifer tarandus caribou (Gmelin, 1788)) to test two competing hypotheses about coyote and caribou predator–prey spatial dynamics using resource selection functions. The high encounter hypothesis predicts that coyotes would maximize encounters with caribou via high spatial co-occurrence, whereas the predator stealth hypothesis predicts that through low spatial co-occurrence with caribou, coyotes act as stealth predators by avoiding habitats that caribou typically select. Our dietary analysis revealed that ∼46% of sampled coyote diet is composed of caribou. We found that coyote share space with caribou in lichen-barren habitat in both summer and winter and that coyotes co-occur with caribou in forested habitat during summer, but not during winter. Our findings support predictions associated with the high encounter predator hypothesis whereby coyotes and caribou have high spatial co-occurrence promoting caribou in coyote diet.

Food level and light conditions affect the antipredator behavior in larvae of a stream-breeding amphibian

Understanding how long-term changes in environmental conditions influence the way that individuals cope with threats is essential in the context of behavioral adaptation to a rapidly changing world. However, little is known about the behavioral responses to predation risk for individuals that experienced different environmental conditions for extended periods of time, such as food levels and light conditions. In this experimental study, we tested whether previous long-term exposure to different food levels (low versus high) and light conditions (0-h light versus 8-h light) plays a significant role in shaping the antipredator response (i.e., the probability of emerging from the refuge and the distance moved) to stimuli from caged larval dragonflies, in larvae of the fire salamander (Salamandra salamandra). Specifically, we quantified behavioral differences in the response to predation risk in larval salamanders that were reared in the laboratory for 2 months under controlled food and light conditions. The results of this study showed that the interaction between food level and light conditions affected the antipredator behavior of the larvae. Fire salamander larvae maintained at low food levels and in 8-h light conditions emerged from the refuge with a higher probability (i.e., took more risk) than larvae maintained at high food levels and all other combinations of light conditions. Thus, our results highlight the complexity of antipredator responses, pointing attention to the fact that interactions among environmental factors are likely to determine the magnitude of antipredator response. Few studies have investigated the role of multiple environmental factors on the expression of predator-induced behavioral responses. Specifically, because no study has so far investigated the risk-taking behavior in individuals exposed to long-term, contrasting food levels, and light conditions, we investigated this in amphibian larvae. We showed that environmental conditions interactively determined antipredator behavior. This highlights the importance of considering long-term environmental conditions experienced by an organism and their interactions when experimentally studying behavioral variation to adequately understand its expression in natural conditions.

Genetic Variation in Parental Effects Contributes to the Evolutionary Potential of Prey Responses to Predation Risk.

AbstractDespite the ubiquity of parental effects and their potential effect on evolutionary dynamics, their contribution to the evolution of predator-prey interactions remains poorly understood. Using quantitative genetics, here we demonstrate that parental effects substantially contribute to the evolutionary potential of larval antipredator responses in a leaf beetle (Leptinotarsa decemlineata). Previous research showed that larger L. decemlineata larvae elicit stronger antipredator responses, and mothers perceiving predators improved offspring responses by increasing intraclutch cannibalism-an extreme form of offspring provisioning. We now report substantial additive genetic variation underlying maternal ability to induce intraclutch cannibalism, indicating the potential of this adaptive maternal effect to evolve by natural selection. We also show that paternal size, a heritable trait, affected larval responses to predation risk but that larval responses themselves had little additive genetic variation. Together, these results demonstrate how larval responses to predation risk can evolve via two types of parental effects, both of which provide indirect sources of genetic variation for offspring traits.

Who is crying wolf? Seasonal effect on antipredator response to age-specific alarm calls in common ravens, Corvus corax

Communication about threats including those posed by the presence of predators occurs mainly through acoustic signals called alarm calls. The comprehension of these calls by receivers and their rapid antipredator response are crucial in terms of survival. However, to avoid overreaction, individuals should evaluate whether or not an antipredator response is needed by paying attention to who is calling. For instance, we could expect adults to be more experienced with predator encounters than juveniles and thus elicit stronger antipredator responses in others when alarming. Similarly, we could expect a stronger response to alarm calls when more than one individual is calling. To test these assumptions, we applied a playback experiment to wild ravens, in which we manipulated the age class (adult or juvenile) and the number (one or two) of the callers. Our results revealed a seasonal effect of age class but no effect of number of callers. Specifically, the ravens responded with stronger antipredator behaviour (vigilance posture) towards alarm calls from adults as compared to juveniles in summer and autumn, but not in spring. We discuss alternative interpretations for this unexpected seasonal pattern and argue for more studies on call-based communication in birds to understand what type of information is relevant under which conditions.

Interacting effects of short-term and long-term noise exposure on antipredator behaviour in sand gobies

In today's marine habitats, anthropogenic noise is widespread in space and time, affecting aquatic animal communities. Short-term exposure to noise is known to affect vital behaviours, such as the ability to evade predators. However, long-term noise pollution may lead to differences in short-term responses between naïve and experienced animals. We investigated the interaction between short-term and long-term sound exposure on the antipredator response of free-ranging sand gobies, Pomatoschistus minutus. We tested the effects of short-term boat noise playback on the response to a simulated predator strike in areas across a range of low to high long-term noise disturbance levels. Exposure to boat noise did not affect the startle response, time frozen or response latency of gobies to a predator stimulus. However, individuals exposed to short-term boat noise playback were absent from the experimental area for shorter periods after the predator strike than gobies exposed to the silent control. Moreover, gobies in long-term noisy habitats also stopped avoiding the area after the predator strike under silent control conditions. These changes point to a decreased magnitude in antipredator response, as a function of interacting short- and longer-term levels of disturbance. Thus, prey species alter their antipredator behaviour in ways that can potentially lead to higher mortality for individual prey. This could ultimately have implications at the level of the food web.

Comparison between two tritrophic food chain models with multiple delays and anti-predation effect

Exploring the predator–prey linkage in food chain system is the most familiar research work in population biology. Recently, some research experiments show that predator–prey interaction not only governed by direct hunting but also influenced by some indirect effect such as fear effect (felt by prey) that may change the physiological behavior of prey. Based upon this fact, we consider a tritrophic food chain model incorporating with anti-predation response (fear effect) and multiple time delays for biomass conversion from prey to middle predator and middle to top predator. We analyze the resulting delay differential equations and explore how the anti-predation response level affects the population dynamics. We also investigate the effect of delay parameters, for which the model system switches its stability through Hopf-bifurcation. We compare all of our results between two different food chain models consisting of two different functional responses. Some numerical simulations are performed to validate the effectiveness of the derived theoretical results.

Behavioural responses of females of the eriophyoid mite, Aculops allotrichus, to the presence of injured conspecifics

ABSTRACT In many animal taxa, the presence of injured conspecifics triggers escape or freezing behaviour. We examined these anti-predatory responses in the eriophyoid mite Aculops allotrichus from Robinia pseudoacacia. The mite was tested on leaflets in cages with two leaf chambers connected by a tunnel, on compound leaves, on which only two opposite leaflets remained, and on leaf discs placed on glass. We released females onto a site with freshly pierced individuals and allowed them to move to a “safe” place. Females did not escape from dangerous patches in any of our tests. They did not refrain from oviposition or become motionless in the presence of damaged conspecifics, either. On the contrary, in the test with old leaf discs, females prolonged their stay on “risky” patches. Additionally, after five hours the proportion of females in chambers with pierced conspecifics was significantly higher than in the control, and only after 24 hours were there no differences between the two combinations. It indicates that the presence of injured conspecifics is not a cue of predation risk for A. allotrichus. In contrast, the eriophyoid can be arrested on “dangerous” leaves, and possible factors underlying this phenomenon are discussed.

Courting danger: socially dominant fish adjust their escape behavior and compensate for increased conspicuousness to avian predators

Males of many species display conspicuous colors to attract mates and deter rivals, although this benefit can incur an increased predation risk. In the African cichlid fish, Astatotilapia burtoni, males can change both their social status (dominant, DOM, or subordinate, SUB) and primary body color (yellow or blue). We hypothesized that these phenotypes vary in conspicuousness to predators and conspecifics, thus establishing a trade-off between intraspecific signaling and predation. We quantified the spectral reflectance of yellow and blue DOM and SUB males. We then constructed avian and conspecific visual receiver models to determine the relative conspicuousness of each phenotype. We show that there are significant differences in conspicuousness to predators and conspecifics, with the flanks of the yellow DOM males exhibiting more spectral contrast to both avian predators and conspecifics than the flanks of blue DOM males. Our measurements of escape behavior revealed that each morph exhibits distinct anti-predatory responses, with SUB males shoaling for protection, and the more conspicuous yellow DOM males executing more escape responses, potentially compensating for their increased conspicuousness. Our results suggest a novel mechanism for the maintenance of alternative male phenotypes in this species, where dynamically enhanced conspicuousness is offset by plastic changes in behavior.

Friend or foe? Development of odour detection, differentiation and antipredator response in an embryonic elasmobranch

Young animals, especially those developing within eggs, are extremely vulnerable to predation risk given their immobility, small size and limited functionality of developing sensory systems. Embryos from a range of taxa can detect predator cues and use antipredator responses to reduce risk; however, little is known about this capacity in elasmobranchs, especially regarding olfactory detection. Embryonic Port Jackson sharks (Heterodontus portusjacksoni) were exposed to elasmobranch and teleost odours across key developmental stages to investigate their capacity to detect and discern between cues. Oxygen uptake rates were measured as a proxy for antipredator response and to estimate their energetic costs. Earlier developmental stages exhibited limited responses, regardless of the odour, likely associated with an undeveloped sensory system. However, older shark embryos depressed oxygen uptake rates (i.e. crypsis responses) when exposed to teleost cues, but showed little response to elasmobranch cues. In contrast, hatchlings exhibited minimal responses to teleost cues but a significant increase in oxygen uptake rates when exposed to elasmobranch odours, indicative of a general stress response in preparation for escape. Collectively, our data suggest that embryonic sharks can differentiate between odour cues and elicit various responses, but this ability is limited by their developing sensory capacity.

Not so naïve: endangered mammal responds to olfactory cues of an introduced predator after less than 150 years of coexistence

Inability to recognise and/or express effective anti-predator behaviour against novel predators as a result of ontogenetic and/or evolutionary isolation is known as ‘prey naivete’. Natural selection favours prey species that are able to successfully detect, identify and appropriately respond to predators prior to their attack, increasing their probability of escape and/or avoidance of a predator. However, for many prey species, learning and experience are necessary to develop and perform appropriate anti-predator behaviours. Here, we investigate how a remnant population of bilbies (Macrotis lagotis) in south-west Queensland responded to the scents of two predators, native dingoes (Canis familiaris) and introduced feral cats (Felis catus); a procedural control (rabbits; Oryctolagus cuniculus); and an experimental control (no scent). Bilbies in Queensland have shared more than 8000 years of co-evolutionary history with dingoes and less than 140 years with feral cats and less than 130 years with rabbits. Bilbies spent the greatest proportion of time investigating and the least amount of time digging when cat and dingo/dog faeces were present. Our results show that wild-living bilbies displayed anti-predator responses towards the olfactory cues of both a long-term predator (dingoes) and an evolutionary novel predator (cats). Our findings suggest that native species can develop anti-predator responses towards introduced predators, providing support for the idea that predator naivete can be overcome through learning and natural selection as a result of exposure to introduced predators. Not so naive—As a result of lifetime and/or evolutionary isolation from predators, some prey species appear to be naive towards introduced predators. This is particularly the case in Australia, where native mammalian species appear to be naive towards recently introduced predators such as the feral cat and European red fox. In a study of wild-living bilbies, we found that 150 years of co-evolutionary experience is enough to develop predator recognition.

Impact of fear effect on plankton-fish system dynamics incorporating zooplankton refuge

In this paper, we analyze the impact of anti-predator behavior due to fear effect (K) and zooplankton refuge (r1) on a 3-D plankton-fish dynamical system involving phytoplankton, zooplankton, and fish species. We assume that zooplankton species have developed defense mechanisms against fish predation. The fear of fish predation altered anti-predator defenses, which affects the growth of the fish population. On the other hand, zooplankton refuge reduces fish induced mortality of zooplankton and plays a significant role in controlling phytoplankton growth. The density of fish species is suppressed in the presence of high refuge and the anti-predator response of zooplankton. It is determined that K and r1 can influence not only plankton-fish demography but also induce some mechanism to terminate planktonic blooms. Our mathematical study reveals that the low level of fear can stabilize the system dynamics in the presence of high rate of zooplankton refuge. Moreover, the low rate of zooplankton refuge can exclude complexity from the plankton-fish ecosystem in the presence of strong anti-predator responses of zooplankton. We have established the existence of all feasible biological equilibria and derived the conditional local and global stability of the given system around it. The Hopf-bifurcation analysis is carried out by considering K and r1 as bifurcation parameters. The direction of bifurcating solutions is also determined using the centre manifold arguments. Numerical simulation is carried out to substantiate our analytical findings.

Heart rate variability in Konik and purebred Arabian horses in response to different predator vocalisations

The current predation threat of domestic horses is generally low, and horses do not know predators' frightening cues. We studied whether horses still recognise predation threats. The aim of the study was to analyse the emotional response of purebred Arabian horses (Arabian) and Polish Konik horses (Konik) to an Arabian panther (Panthera pardus nimr) (panther) growl and a grey wolf (Canis lupus) (wolf) howl. Panther vocalisation was known to Arabian ancestors, whereas ancestors of Konik knew wolf vocalisation. The response to the howls of golden jackals (Canis aureus) (jackal), which did not prey on equids, was also studied comparatively. Two groups of 10 adult horses of each breed were subject to predator sounds of one predator daily for 5 min during a turn out on pasture. The test was performed for 18 days in total. The sound of each predator was interchangeably featured from one loudspeaker for 3 days followed by four loudspeakers simultaneously to imitate a group of predators for 3 days. The horses' emotional agitation in response to the sounds was measured based on the parameters of heart rate variability (HRV) using telemetric devices. The results showed that the predators' sounds were identified by horses as stressful or neutral. Horses generally retained their anti-predator responses even in the current habitat, which typically lacks predation cues. The results are not always coherent and may demonstrate that the response is somewhat attenuated. The wolf howl elicited a stronger response in Koniks. The panther growl more strongly influenced Arabians, whereas the jackal howl minimally elicited an agitation in the horses. The differentiated response of the two horse breeds to the three predator species suggests that the response is an innate adaptation to the predation risk in the habitat of the breed ancestors. This response occurs regardless of the emotional arousal specific to a breed, and the frightening cue is not the sound per se but the possible attack of predators. Horses display a type of understanding of the sound meaning. Their HRV response seems to be adequate for the threat signalised by the sound.

Cautious clams? Energetic state modifies risk assessment in giant clams

AbstractA fundamental trade‐off exists between the essential activities of acquiring energy and avoiding predators, thus animals are expected to make decisions that optimize foraging and avoid predation. These assessments are often state‐dependent with hungrier animals taking greater risks when foraging. Previous studies have explored state‐dependent risk assessment in a variety of taxa, yet no studies have focused on giant clams, genus Tridacna. These organisms provide a unique system to test foraging‐risk trade‐offs because they have two main energy sources: photosynthesizing symbiotic algae and siphoning nutrients from the water column. These activities can only occur when the clams’ shells are open and the mantle is vulnerable to predation. Here, we tested whether risk assessment in giant clams was state‐dependent. We designed three experiments of different shading durations (within‐day and multiday) to block photosynthesis while allowing limited water flow for siphoning. We measured the latency of the clams to reopen after a simulated predator touch to determine whether different duration of shading modified their antipredator response. Our single‐day experiment did not show a change in the hiding times across the three treatments. However, clams increased their hiding time as the treatments increased food deprivation (no restrictions on flow or photosynthesis, restriction on flow, restriction on flow and photosynthesis) when exposed to treatments for multiple days. Overall, we found that clams that were more energy‐deprived had a longer hiding time. This contrasts with findings from previous state‐dependent risk assessment literature and suggests that clams are more cautious when energy deprived, a result that may be generalizable to other sessile invertebrates.

Diagnosing nest predators and anti-predator response of red wattled lapwing, Vanellus indicus (Boddaert, 1783)

Identification of nest predators and anti-predator behavior of Vanellus indicus (red wattled lapwings) were studied during two constitutive breeding periods (March-August) of 2018 and 2019. The study was performed along the river Ganges, Raebareli (Uttar Pradesh), India. The number of nesting pairs was counted by the line transect method and anti-predator responses were recorded by the focal sampling method. The nesting pairs varied significantly within and between study sites and years. A variety of predators (avian, mammalian and reptilian) were identified while some predators were designated in the unknown category. Sitting tight response was significantly different during the incubation period. The mobbing response, flying away and running away responses were significantly different during the post-incubation period. Circle noisily over the nests and alarm call were not significant between the two reproductive stages. We conclude that red wattled lapwings can differentiate among diverse predator species and adopt various anti-predator responses against them at different stages of their breeding cycle.