Identifying the most effective behavioural assays and predator cues for quantifying anti-predator responses in mammals: a systematic review protocol

Background Mammals, globally, are facing population declines. Strategies increasingly employed to recover threatened mammal populations include protecting populations inside predator-free havens, and translocating animals from one site to another, or from a captive breeding program. These approaches can expose predator-naïve animals to predators they have never encountered and as a result, many conservation projects have failed due to the predation of individuals that lacked appropriate anti-predator responses. Hence robust ways to measure anti-predator responses are urgently needed to help identify naïve populations at risk, to select appropriate animals for translocation, and to monitor managed populations for trait change. Here, we outline a protocol for a systematic review that collates existing behavioural assays developed for the purpose of quantifying anti-predator responses, and identifies assay types and predator cues that provoke the greatest behavioural responses. Methods We will retrieve articles from academic bibliographic databases and grey literature sources (such as government and conservation management reports), using a Boolean search string. Each article will be screened for the satisfaction of eligibility criteria determined using the PICO (Population—Intervention—Comparator—Outcome) framework, to yield the final article pool. Using metadata extracted from each article, we will map all known behavioural assays for quantifying anti-predator responses in mammals and will then examine the context in which each assay has been implemented (e.g. species tested, predator cue characteristics). Finally, with mixed effects modelling, we will determine which of these assays and predator cue types elicit the greatest behavioural responses (standardised difference in response between treatment and control groups). The final review will highlight the most robust methodology, will reveal promising techniques on which to focus future assay development, and will collate relevant information for conservation managers.

Effects of parasitism on antipredatory responses and defensive behaviors in the subterranean rodent Ctenomys talarum.

Predation represents an important evolutionary force shaping specific adaptations. Prey organisms present behavioral adaptations that allow them to recognize, avoid and defend themselves from their predators. In addition to predation, there is a growing consensus about the role of parasitism in the structuring of biological communities. In vertebrates, the effects on hosts include changes in daily activity, feeding, mate selection, reproduction, and modifications in responses to environmental stimuli. These behavioral variations can benefit the parasite (parasitic manipulation), benefit the host, or appear as a side effect of the infection. We evaluated the influence of parasitism on the behavioral and physiological response of Ctenomys talarum (Thomas 1898) to predator cues. We found that individuals exposed to cat odors and immobilization entered less often and stayed less time in the transparent arms of elevated maze, exhibiting a preference for protected areas (anxiogenic response). Additionally, we evaluated if the presence of parasites affected antipredatory behaviors in tuco-tucos (naturally parasitized, deparasitized or inoculated with Eimeria sp.). We did not find differences among the groups as regards responses to predator cues. Therefore, while exposure to predator cues triggered a stress response, the manipulation of parasite loads did not modify homeostasis under these experimental conditions.

Long-Tailed Pygmy Rice Rats Modify Their Behavioural Response and Faecal Corticosterone Metabolites in Response to Culpeo Fox but Not to Lesser Grison

Even though behavioural and physiological reactions to predation risk exhibited by prey species have received considerable attention in scientific journals, there are still many questions still unsolved. Our aim was to broaden the knowledge on one specific question: do long-tailed pygmy rice rats adapt their behavioural and physiological antipredator strategies depending on the predator species? For this question, we live-trapped in a temperate forest in Southern Chile long-tailed pygmy rice rats (Oligoryzomys longicaudatus), which were exposed to three predator odour phases (Phase 0: preliminary, no predator cues; Phase 1: one plot with culpeo fox faeces (Lycalopex culpaeus), one plot with lesser grison (Galictis cuja) faeces and one plot acting as a control with no odour; Phase 2: post treatment, no predator cues). We measured the behavioural response by the capture ratio. To assess the physiological stress response, we collected fresh faecal samples to quantify faecal corticosterone metabolites (FCM). Our results showed that O. longicaudatus increased both the capture ratio and FCM levels in the presence of culpeo cues. Culpeo foxes have higher densities in the study area than G. cuja and exhibit a higher activity pattern overlap with O. longicaudatus. Moreover, it has been also been reported in other regions that L. culpaeus consumption of O. longicaudatus is more frequent compared to G. cuja diet. The increase in capturability could be because traps can be regarded as a shelter in high-risk settings, but it can also be explained by the predator inspection behaviour. The increase in FCM concentrations during culpeo treatment can be linked to the adaptive mobilisation of energy to execute antipredator responses to increase survival chances.

The scent of fear makes sea urchins go ballistic

Background Classic ecological formulations of predator–prey interactions often assume that predators and prey interact randomly in an information-limited environment. In the field, however, most prey can accurately assess predation risk by sensing predator chemical cues, which typically trigger some form of escape response to reduce the probability of capture. Here, we explore under laboratory-controlled conditions the long-term (minutes to hours) escaping response of the sea urchin Paracentrotus lividus, a key species in Mediterranean subtidal macrophyte communities. Methods Behavioural experiments involved exposing a random sample of P. lividus to either one of two treatments: (i) control water (filtered seawater) or (ii) predator-conditioned water (with cues from the main P. lividus benthic predator—the gastropod Hexaplex trunculus). We analysed individual sea urchin trajectories, computed their heading angles, speed, path straightness, diffusive properties, and directional entropy (as a measure of path unpredictability). To account for the full picture of escaping strategies, we followed not only the first instants post-predator exposure, but also the entire escape trajectory. We then used linear models to compare the observed results from control and predators treatments. Results The trajectories from sea urchins subjected to predator cues were, on average, straighter and faster than those coming from controls, which translated into differences in the diffusive properties and unpredictability of their movement patterns. Sea urchins in control trials showed complex diffusive properties in an information-limited environment, with highly variable trajectories, ranging from Brownian motion to superdiffusion, and even marginal ballistic motion. In predator cue treatments, variability reduced, and trajectories became more homogeneous and predictable at the edge of ballistic motion. Conclusions Despite their old evolutionary origin, lack of cephalization, and homogenous external appearance, the trajectories that sea urchins displayed in information-limited environments were complex and ranged widely between individuals. Such variable behavioural repertoire appeared to be intrinsic to the species and emerged when the animals were left unconstrained. Our results highlight that fear from predators can be an important driver of sea urchin movement patterns. All in all, the observation of anomalous diffusion, highly variable trajectories and the behavioural shift induced by predator cues, further highlight that the functional forms currently used in classical predator–prey models are far from realistic.

Brain volume increase and neuronal plasticity underly predator-induced morphological defense expression in Daphnia longicephala

Predator-induced phenotypic plasticity describes the ability of prey to respond to an increased predation risk by developing adaptive phenotypes. Upon the perception of chemical predator cues, the freshwater crustacean Daphnia longicephala develops defensive crests against its predator Notonecta spec. (Heteroptera). Chemical predator perception initiates a cascade of biological reactions that leads to the development of these morphological features. Neuronal signaling is a central component in this series, however how the nervous system perceives and integrates environmental signals is not well understood. As neuronal activity is often accompanied by functional and structural plasticity of the nervous system, we hypothesized that predator perception is associated with structural and functional changes of nervous tissues. We observe structural plasticity as a volume increase of the central brain, which is independent of the total number of brain cells. In addition, we find functional plasticity in form of an increased number of inhibitory post-synaptic sites during the initial stage of defense development. Our results indicate a structural rewiring of nerve-cell connections upon predator perception and provide important insights into how the nervous system of prey species interprets predator cues and develops cost–benefit optimized defenses.

How do developmental and parental exposures to predation affect personality and immediate behavioural plasticity in the snail Physa acuta ?

Individuals differ in personality and immediate behavioural plasticity. While developmental environment may explain this group diversity, the effect of parental environment is still unexplored—a surprising observation since parental environment influences mean behaviour. We tested whether developmental and parental environments impacted personality and immediate plasticity. We raised two generations of Physa acuta snails in the laboratory with or without developmental exposure to predator cues. Escape behaviour was repeatedly assessed on adult snails with or without predator cues in the immediate environment. On average, snails were slower to escape if they or their parents had been exposed to predator cues during development. Snails were also less plastic in response to immediate predation risk on average if they or their parents had been exposed to predator cues. Group diversity in personality was greater in predator-exposed snails than unexposed snails, while parental environment did not influence it. Group diversity in immediate plasticity was not significant. Our results suggest that only developmental environment plays a key role in the emergence of group diversity in personality, but that parental environment influences mean behavioural responses to the environmental change. Consequently, although different, both developmental and parental cues may have evolutionary implications on behavioural responses.