Antipredator Behavior Research Articles

Dynamic fine-tuning of anti-predator behaviour in snowshoe hares illustrates the context dependence of risk effects.

Research Highlight: Shiratsuru, S., & Pauli, J. N. (2024). Food-safety trade-offs drive dynamic behavioural antipredator responses among snowshoe hares. Journal of Animal Ecology, DOI: 10.1111/1365-2656.14183. Predation-risk effects are known to be context dependent, with impacts of perceived predation threat on individual antipredator responses, prey population demography, species interactions and community organization hinging on traits of the prey, the predator(s) and setting of the interaction. Yet, few empirical studies to date have simultaneously explored how these three drivers shape contingency in antipredator behaviour, the key first step in the process by which predation-risk effects play out, especially in free-living vertebrates. In a new study, Shiratsuru & Pauli (2024) address this knowledge deficit by showing that snowshoe hares (Lepus americanus) trade foraging for anti-predator vigilance dynamically as a function of winter food availability (a proxy for individual energetic state), the timing and intensity of predator activity, and environmental properties associated with elevated vulnerability to predator-induced mortality, notably including coat colour mismatch caused by variation in snow cover. These results offer new insight into the complexity of predation-risk effects and should serve as a guide for research aiming to better understand the expression of these effects under varying circumstances.

Neighbor Density and Post‐Contact Immobility Duration as Antipredator Behavior: Antlion Larvae Do Not Fit the Selfish Prey Hypothesis

ABSTRACTRemaining immobile for an unpredictable period after being touched by a potential predator (post‐contact immobility, PCI) may favor survival. However, the factors that determine variation in PCI duration are poorly understood. We tested whether PCI duration depends on the surrounding conspecific density (the selfish prey hypothesis) in the tropical antlion larvae Myrmeleon crudelis. These insects avoid predation by being immobile or burying themselves. The selfish prey hypothesis predicts a reduction in the PCI duration as conspecific density increases because this high density of conspecifics around can stimulate the redirection of the predator's interest in other nearby potential prey. In the field, we measured PCI and found that its duration was independent of the conspecific density. In the lab, we also measured the PCI of a subset of the same larvae in the absence of neighbors. Using a paired design, we found that PCI duration was lower in the lab in the absence of neighbors than in the field. Our results suggest that the antlion larvae did not follow the selfish prey hypothesis. We propose two alternative explanations. First, the larvae have a limited ability to detect neighbors in the field and keep up with the changing number of surrounding active pits. Second, burying may be more important than PCI as an antipredator strategy. In our lab experiment, larvae had a more accurate idea of the conspecific density around their pit because they explored the area. We propose that knowing the absence of conspecifics triggered a shorter PCI duration. Under a high predation risk (i.e., no other prey to which the predator would redirect its attention), the larvae select the unequivocal antipredator behavior of burying. This work illustrates the relevance of accurate information in deciding how to avoid predation, especially when prey can prioritize between alternative behaviors, with success varying between the contexts.

Landscape use by prey: Bottom‐up regulation prevails under reduced predation risk

AbstractResource specialist herbivores may suppress antipredator strategies to access scarcely available key resources, while proactive antipredator behaviors should be favored by generalists or when resources are abundant. We quantified the relative effects of predation‐ (top‐down) and resource‐driven (bottom‐up) constraints on spatiotemporal patterns of landscape use by a prey community in a dynamic system under low predator abundance, and investigated how prey manage the risk posed by predators with different hunting strategies. We fitted Royle–Nichols co‐abundance models to camera‐trapping data collected between 2017 and 2019 in Bicuar National Park (Angola), to assess spatial association/segregation across predator–prey dyads, while accounting for the effects of water and food availability during dry and wet seasons. We further estimated pairwise seasonal differences in diel activity overlap between predator and prey. We failed to detect spatiotemporal proactive antipredator responses either toward the cursorial or ambush predator. The community‐wide predator–prey association patterns we found support that predation pressure is insufficient to displace prey from their preferred habitats or to adjust their endogenous clock, and support predominantly bottom‐up regulated behaviors. We suggest that, in landscapes where predator density is low, limited perception of risk may prevent the employment of proactive antipredator behavior.

Public information use—are invasive demersal fish species more effective than natives?

Abstract Organisms determine environmental quality using their senses and personal experience (personal information) but can also use byproducts of other individuals’ activities (i.e. public information). The ability to use public information originating from both con- and heterospecifics gives an advantage over individuals relying only on personal information or conspecific cues. The role of public information in invasion ecology is of high concern, as any differences in this aspect between alien and native species may determine the success of the former. Here, we studied 2 pairs of sympatric invasive and native demersal fish species (racer goby Babka gymnotrachelus/European bullhead Cottus gobio; monkey goby Neogobius fluviatilis/gudgeon Gobio gobio) facing 2 types of public cues (associated with antipredatory and foraging behavior). We used them as a model to check if the invaders could use public information from more sources than the natives. Both invaders and the native gudgeon used cues from con- and heterospecifics, exhibiting antipredatory behavior, while the native bullhead failed to recognize such cues from heterospecifics. The monkey goby and both native species were attracted to foraging cues from donors less likely to exert competitive pressure on the observer (i.e. native species rather than potentially more aggressive invaders). On the other hand, the racer goby appeared unable to correctly recognize heterospecific foraging cues. Our results showed that public cues can enable invaders to read threat from a wide range of individuals and to find optimal food patches, which may contribute to their invasion success.

Effects of glyphosate based herbicide exposure in early developmental stages of Physalaemus gracilis

The impact of environmental pollutants has been a focus of investigation in recent years. Studies assessing the effects of these pollutants are essential for understanding the challenges faced by non-target species. Among the many substances used for agricultural purposes, the herbicide glyphosate is one of the most widely marketed in recent years. This broad-spectrum herbicide is commonly used to protect a variety of crops. In this study, we evaluated the effects of chronic glyphosate exposure on a native amphibian species, Physalaemus gracilis. Amphibians, which develop in aquatic environments, are highly sensitive to pesticides. Because of this, we investigated morphological, physiological, behavioral, and biochemical parameters in the early stages of development. The animals were exposed to environmentally relevant concentrations of a glyphosate-based herbicide (0, 100, 350, and 700 µg L⁻¹) during their first seven days of life. As a result, we observed impairments in anti-predatory behavior, reduced body mass index, and scaled mass index, malformations of the mouth and intestine, increased acetylcholinesterase activity, cardiotoxicity, and oxidative stress. These findings underscore the importance of studying native non-target species and highlight the need to evaluate the effects of environmentally relevant concentrations, as well as to review legislation regarding permissible levels of glyphosate in surface water and public water supplies.

Application of sparrow search swarm intelligence optimization algorithm in identifying the critical surface in slope-stability

The use of nature-inspired meta-heuristics to tackle complex optimization problems is steadily gaining popularity within a rapidly evolving world. Swarm intelligence (SI) optimization motivated by behavior of community-based organisms of flocks of birds, schools of fish, colonies of ants and bees performs the search through agents whose trajectories are primarily adjusted stochastically and sporadically deterministically, by golden rules drawn from Mother Nature. Each entity within the swarm is swayed by its individual ‘best’ and group’s ‘best’ position while moving randomly to converge to optimal through competition and cooperation. The sparrow search algorithm (SSA), developed by Xuea and Shen (Xue and Shen in Syst Sci Cont Eng 8:22–34, 2020) is a very recent SI approach that adopts the sparrow producer–scrounger model metaphorically for designing optimum searching strategies, inspired by the foraging, anti-predation behavior, and the overall group wisdom of sparrows. SSA has been experimented on some hard benchmark test functions to test its effectiveness and thereafter, applied in slope-stability problems in searching the critical failure surface. The objective function to be optimized is the factor of safety against failure given by Bishop's (Bishop in Geotechnique 5:7–17, 1955) simplified method. Results show SSA is a strong contender to bio-inspired methods like genetic algorithms, big-bang big-crunch, simulated annealing, and artificial bee colony algorithms. The study illustrates the flexibility, efficiency, and robustness of the methodology in function optimization.

Multi-group sparrow search algorithm based on K-means clustering

In order to improve the defects of the Sparrow Search Algorithm (SSA) in single-species search, which causes redundancy in its speed of collection and easily ignores high-quality solutions and falls into local optimality, a K-means Multigroup Sparrow Search Algorithm (KSSA) based on K-means clustering was proposed. Firstly, the multi-population mechanism is introduced into SSA to weaken the collection ability of a single population and reduce the probability of falling into the local optimum. Secondly, the K-means algorithm is used to divide the sub-populations to increase the differences between the sub-populations, and at the same time, the individuals in the sub-populations focus on searching in a small range, thereby improving the efficiency of the initial search. Then, the weighted centroid communication strategy is used to improve the quality of communication between populations, reduce the interference of the own population, and reduce the risk of all sub-populations falling into the local optimum due to a sub-population falling into the local optimum. Finally, dynamic reverse learning is introduced into the vigilant to enhance its anti-predator behavior and improve the defects of slower collection speed and insufficient collection accuracy caused by the increase in the number of sub-populations. The test function simulation experiment shows that KSSA has better optimization performance than SSA and other algorithms.

Predator-prey space use and landscape features influence movement behaviors in a large-mammal community.

Predator hunting strategies, such as stalking versus coursing behaviors, are hypothesized to influence antipredator behaviors of prey and can describe the movement behaviors of predators themselves. Predators and prey may alter their movement in relation to predator hunting modes, yet few studies have evaluated how these strategies influence movement behaviors of free-ranging animals in a multiple-predator, multiple-prey system. We fit hidden Markov models (HMM) with movement data derived from >400 GPS-collared ungulates and large predators in eastern Washington, USA. We used these models to test our hypotheses that stalking (cougars [Puma concolor]) and coursing (gray wolves [Canis lupus]) predators would exhibit different broad-scale movement behaviors consistent with their respective hunting strategies in areas that increased the likelihood of encountering or capturing ungulate prey (e.g., habitats selected by deer [Odocoileus spp.]). Similarly, we expected that broadscale movement behaviors of prey would change in response to background levels of predation risk associated with each predator's hunting strategy. We found that predators and ungulate prey adjusted their broadscale movements in response to one another's long-term patterns of habitat selection but not based on differences in predator-hunting strategies. Predators changed their movement behaviors based on the type of prey, whereas ungulates generally reduced movement in areas associated with large predators, regardless of the predator's hunting strategy. Both predator and prey movements varied in response to landscape features but not necessarily based on habitat that would facilitate specific hunting behaviors. Our results suggest that predators and prey adjust their movements at broad temporal scales in relation to long-term patterns of risk and resource distributions, potentially influencing their encounter rates with one another at finer spatiotemporal scales. Habitat features further influenced changes in movement, resulting in a complex combination of movement behaviors in multiple-predator, multiple-prey systems.

Snake-like bird hisses induce anti-predator responses in a frog

Some snakes emit hissing calls which are imitated by birds to deter potential predators. However, the effect of these snake and bird hisses on anuran risk recognition is not yet explored. Here we hypothesize that these hisses may advertise dangers to frogs and evoke their anti-predator responses. We used little torrent frogs (Amolops torrentis) as subjects and conducted sound playbacks to test their anti-predator behaviors. We found that little torrent frogs changed their calling behaviors during sympatric snake hiss playbacks, but showed no response to white noise and allopatric snake hiss playbacks. They did not respond to sympatric avian hiss that has low acoustic similarity with snake sounds. However, they decreased calling activity in response to sympatric avian hiss that has high acoustic similarity with snakes. As compared to other treatments, more individuals ceased calling during the playbacks of the highly similar bird hiss. These results suggest that frogs may recognize risks from snake and snake-like hissing calls and perform anti-predator responses.

The Slithering Dead: Does locomotor performance affect post-capture death feigning in dice snakes (Natrix tessellata, Laurenti 1768)?

Abstract Functional constraints between different types of antipredator behavior should be common, especially if they are on the opposite sides of the behavioral spectrum such as flight and post-capture immobility. We examined a potential compromise between post-capture immobility displays and sprint speed in dice snakes (Natrix tessellata), using a field-based approach. We sampled snakes (N = 238) from two populations: from a dense island population free of mammal predators, and from a less dense mainland population, preyed upon by both bird and mammal predators. We explored the effects of sexual maturity, temperature, body size, presence of palpable food in the gut, and injuries on the occurrence and duration of post-capture immobility as well as sprint speed. Our results confirm the existence of functional constraints between locomotor performance and post-capture immobility in dice snakes. Faster dice snakes start escaping promptly after release, while slower individuals utilize more passive antipredator behaviors such as death feigning. Local adaptations seem to have great influence on behavioral compromise, since the mammal-free island population exhibited a higher incidence of post-capture immobility and a significantly lower sprint speed, compared to the less dense mainland population. Additionally, immature individuals tended to avoid death feigning and their post-capture immobility lasted shorter compared to adult individuals. It remains to be seen how individuals adjust their behavior to accomodate locomotor constraints, and in which specific phases of the predator-prey interaction these adjustments occur.

Competition is the main factor, compared to non-lethal threat of predation, affecting life-history traits of Aedes aegypti (Diptera, Culicidae) mosquitoes.

Mosquito larvae coexist with different species of predators in small freshwater bodies. These environments can vary widely in terms of the amount of food and larval densities. Our objective was to understand the impacts of the non-lethal threat of predation, combined with competition effects on Aedes aegypti development and adult life cycle. We tested the effects of two types of non-lethal threat of predation, divided into nine combinations of larvae densities and resource availability on Ae. aegypti larvae. We measured their isolated and combined impacts on larval mortality rate, time to reach pupation, adult size, and lifespan. Real non-lethal threat of predation resulted in a higher larval mortality (71%), compromised the sizes of the individuals (-7%) and prolonged the lifespan (19%) compared to control. Simulated treatment, the anti-predation behaviors led to an increase in larval mortality (21%) compared to the control treatment. Accelerating the larva's development time (-14%) to escape from a dangerous environment severely compromised the size of the individuals (-23%) and increased adult life (10%). The scarcity of food resources, high levels of competition, and non-lethal threat of predation as well, are effective stressors for Ae. aegypti. We observed that resources (food and space) were more important than predation risk for the fitness of the survivors. However, these stressors, individually or combined, can result in high larvae mortality, altered larval development and pupation, affecting the emergence of the adults, with small sizes and altered lifespan, ultimately reducing the fitness of the individuals. © 2024 Society of Chemical Industry.

Kappa-opioid receptor blockade in the inferior colliculus of prey threatened by pit vipers decreases anxiety and panic-like behaviour.

The dorsal midbrain comprises dorsal columns of the periaqueductal grey matter and corpora quadrigemina. These structures are rich in beta-endorphinergic and leu-enkephalinergic neurons and receive GABAergic inputs from substantia nigra pars reticulata. Although the inferior colliculus (IC) is mainly involved in the acoustic pathways, the electrical and chemical stimulation of central and pericentral nuclei of the IC elicits a vigorous defensive behaviour. The defensive immobility and escape elicited by IC activation is commonly related to panic-like emotional states. To investigate the role of κ-opioid receptor of the IC in the antiaversive effects of endogenous opioid receptor blockade in a dangerous situation, male Wistar rats were pretreated in the IC with the κ-opioid receptor-selective antagonist nor-binaltorphimine at different concentrations and submitted to the non-enriched polygonal arena for a snake panic test in the presence of a rattlesnake and, after 24 h, prey were resubmitted to the experimental context. The snakes elicited in prey a set of antipredatory behaviours, such as the anxiety-like responses of defensive attention and risk assessment, and the panic-like reactions of defensive immobility and either escape or active avoidance during the elaboration of unconditioned and conditioned fear-related responses. Pretreatment of the IC with microinjections of nor-binaltorphimine at higher concentrations significantly decreased the frequency and duration of both anxiety- and panic-attack-like behaviours. These findings suggest that κ-opioid receptor blockade in the IC causes anxiolytic- and panicolytic-like responses in threatening conditions, and that kappa-opioid receptor-selective antagonists can be a putative coadjutant treatment for panic syndrome treatment.

Long-term anti-predator learning and memory differ across populations and sexes in an intertidal snail.

Anti-predator behaviours in response to predator cues can be innate, or they can be learned through prior experience and remembered over time. The duration and strength of continued anti-predator behaviour after predator cues are no longer present, and the potential for an enhanced response when re-exposed to predator cues later is less known but could account for the observed variation in anti-predator responses. We measured the carryover effects of past predation exposure and the potential for anti-predator learning and memory in the marine snail Nucella canaliculata from six populations distributed over 1000 km of coastline. We exposed lab-reared snails to cues associated with a common crab predator or seawater control in two serial experiments separated by over seven months. Responses were population- and sex-dependent, with some populations retaining anti-predator behaviours while others showed a capacity for learning and memory. Male snails showed a strong carryover of risk aversion, while females were able to return to normal feeding rates and grow more quickly. These behavioural differences culminated in strong impacts on feeding and growth rates, demonstrating that this variation has implications for the strength of trait-mediated indirect interactions, which can impact entire ecosystems.

Developmental Social Experience Changes Behavior in a Threatening Environment in Corydoras Catfish

ABSTRACTCoordinated responses to threats are important for predator evasion in many species. This study examines the effect of developmental social experience on antipredator behavior and group cohesion in a highly gregarious catfish that communicates via tactile interaction, Corydoras aeneus. We reared fish either in a mixed‐age group of age‐matched peers and adult C. aeneus (mixed‐age condition, or MAC), or with age‐matched peers only (same‐age condition, or SAC). A startle test was conducted with small groups of subadults from either social rearing condition. Prior to any startle events, SAC subadults had increased tactile communication compared to MAC subadults, but SAC individuals were overall less active. SAC fish exhibited a stronger antipredator response to startles, and were more likely to freeze or take refuge in cover in response to a startle than MAC fish. MAC fish tended to respond to startle events by maintaining or decreasing their cohesion, whereas SAC fish tended to maintain or increase their cohesion. These behavioral differences are attributed to MAC fish developing with group protection as a result of shoaling with adults, resulting in reduced antipredator responses when reared with adults. This study underscores how social context during development can be critical in shaping how individuals perceive and respond to potential threats in their environment.

Elevated vitamin D levels in diurnally-active female fruit bats

Animal species have evolved to enhance their survival by focusing their temporal activity on specific parts of the diurnal-nocturnal cycle. Various factors, including inter-specific competition and anti-predator behavior, as well as anthropogenic effects like light pollution, have prompted some species to expand or shift their temporal niches. Our study focuses on the temporal niche shift of the Egyptian fruit bat (Rousettus aegyptiacus) to diurnal activity in Israel.Through an extensive citizen-science study, we assessed the distribution of these bats’ diurnal activity across Israel. We also documented the sex and age of bats from a colony known for its diurnal activity and collected blood samples from them for metabolic analysis.Our findings indicate that the shift toward daytime activity predominantly takes place in urban settings and is mostly exhibited by females. We found a significant physiological effect of this temporal shift, namely: diurnal bats’ vitamin D levels were significantly higher, and their parathyroid hormone (PTH) levels were significantly lower than those of nocturnal bats.We suggest that the reproductive metabolic demands of female bats might be a key factor driving this shift to diurnal activity. We hypothesize that the increase in vitamin D, derived from sunlight hours, might play a crucial role in regulating calcium homeostasis, thus contributing to the bats’ physiological needs during the reproduction season.

Oxygen loss compromises growth and cognition of cuttlefish newborns.

Ocean deoxygenation and standing levels of hypoxia are shrinking fundamental niches, particularly in coastal areas, yet documented repercussions on species development and behaviour are limited. Here, we tackled the impacts of deoxygenation (7 mg O2 l-1), mild hypoxia (nocturnal 5 mg O2 l-1) and severe hypoxia (nocturnal 2 mg O2 l-1) on cuttlefish (Sepia officinalis) development (hatching success, development time, mantle length), cognition (ability to learn individually and socially) and behaviour (ability to camouflage and to explore its surroundings spatially). We found that hypoxia yielded lower survival rates, smaller body sizes and inhibited predatory (increased latency to attack the prey) and anti-predator (camouflage) behaviours. Acute and chronic exposure to low oxygen produced similar effects on cognition (inability to socially learn, increased open-field activity levels, no changes in thigmotaxis). It is thus expected that, although cuttlefish can withstand oxygen limitation to a certain degree, expanding hypoxic zones will diminish current habitat suitability.

Individual consistency of hissing displays across night and day in a free-living female songbird

Birds have evolved a variety of antipredator strategies, which have been extensively studied during day-time. Yet, how diurnal birds directly respond to nocturnal predation threats remains largely elusive, despite that predation risk can be high during both night- and day-time. One form of antipredator behaviour found in several tit species when confronted with a predator at the nest is the hissing display. As for many forms of antipredator behaviour, studies on hissing displays have so far focussed on the day-time. Here, we exposed cavity-nesting free-living female great tits (Parus major) to simulated predator intrusions inside their nest box during both night- and day-time. We showed that 28 % of females uttered at least one hissing call during night-time, while the occurrence of hissing calls was higher during day-time (84 %). Hissing females at night, compared to non-hissing females, produced more hissing calls during day-time, providing evidence for individual cross-context consistency. Night-time hissing behaviour did not predict lay date, clutch size, breeding or nest success, indicating the absence of consequences in terms of current reproduction. Together, we reveal the hitherto undescribed occurrence of hissing displays at night in a cavity-nesting bird, while simultaneously strengthening the evidence for the existence of hissing behavioural types.

Site-specific fears: Negev gerbils from same points of origin share anti-predator behavior when translocated to new environments

Site-specific fears: Negev gerbils from same points of origin share anti-predator behavior when translocated to new environments

Naivety dies with the calf: calf loss to human hunters imposes behavioral change in a long-lived but heavily harvested ungulate

BackgroundIn prey, patterns of individual habitat selection and movement can be a consequence of an individuals’ anti-predator behavior. Adjustments of anti-predator behavior are important for prey to increase their survival. Hunters may alter the anti-predator behavior of prey. In long-lived animals, experience may cause behavioral changes during individuals’ lifetime, which may result in altered habitat selection and movement. Our knowledge of which specific events related to hunting activity induce behavioral changes in solitary living species is still limited.MethodsWe used offspring loss in a solitary and long-lived ungulate species, moose (Alces alces), as our model system. We investigated whether offspring loss to hunters induces behavioral changes in a species subjected to heavy human harvest but free from natural predation. To test for behavioral change in relation to two proxies for experience (calf fate and age), we combined movement data from 51 adult female moose with data on their offspring survival and female age. We tested for adjustments in females’ habitat selection and movement following calf harvest using Hidden Markov Models and integrated Step Selection Analysis to obtain behavioral state specific habitat selection coefficients.ResultsWe found that females with a harvested calf modified habitat selection and movement during the following hunting season. Female moose selected for shorter distance to roads during the night, selected for shorter distance to forests and greater distance to human settlements following calf harvest than females who had not lost a calf. The survival of twins in a given hunting season was related to female age. Older females we more likely to have twins survive the hunting season.ConclusionsOur findings suggest that losing offspring to human harvest imposes behavioral changes in a long-lived ungulate species, leading to adjustments in females' habitat selection and movement behavior, which may lower the risk of encountering hunters. In our study, female moose that experienced calf loss selected for lower distance to forest and selected for greater distance to human settlements during periods of high hunting pressure compared to females without the experience of calf loss during the previous hunting season. We interpret this as potential learning effects.

Differential Effects of Ephemeral and Stable Predator Chemical Cues on Spider Antipredator Behaviour

Semiochemicals left by predators in their foraging area can be utilised by prey to avoid predation. The range of predators’ chemical cues with contrasting degradation rates might provide information of different quality, potentially allowing prey to differentiate between the immediate and the longer-term presence of predators in a location. So far, knowledge about the roles of volatile versus stable chemical cues in informing predation risk is limited. We here seek to disentangle the role of ephemeral trail pheromones compared to persistent cuticular hydrocarbons of ants (predators) on the antipredator behaviour of juvenile spiders (prey), with the expectation that volatile semiochemicals induce avoidance behaviour in spiders at a higher rate compared to stable cues. We allowed the spiders to choose between sites with and without ant cues separately for volatile trail pheromones and stable hydrocarbons. Unexpectedly, spiders avoided the presence of persistent cuticular hydrocarbons more clearly than the highly volatile trail pheromone. This underscores the widespread impact of these stable cues on the avoidance behaviour of potential intraguild prey. The response to trail pheromones was unclear, possibly because spiders always encounter these cues simultaneously with visual and vibratory cues from ants; hence, trail pheromones may not contain any additional information, hindering the evolution of the ability to detect them.