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.

Effect of Potential Sea Lamprey (Petromyzon marinus) Repellents on the Distribution of Juvenile Rainbow Trout (Oncorhynchus mykiss) in a Laboratory Environment

Recent studies have begun to consider the use of chemosensory alarm cues as potential repellents of invasive Sea Lamprey (Petromyzon marinus Linnaeus, 1758) in the Great Lakes Basin. An important factor in determining the efficacy of potential P. marinus repellents is whether they are species-specific. To that end, using laboratory stream channels, this study investigated whether a non-target species, the Rainbow Trout (Oncorhynchus mykiss Walbaum, 1792), would change their distribution in response to damage-released P. marinus alarm cues, potential mammalian predator cues, and damage-released conspecific cues. In groups of 10 individuals per replicate, with 10 replicates per stimulus type, subjects were exposed to one of the following treatment types: deionized water (control), P. marinus extract (heterospecific alarm cue), O. mykiss extract (conspecific alarm cue), 2-phenylethylamine hydrochloride (potential predator cue), and human saliva (potential predator cue). None of the stimuli induced a significant avoidance response during the stimulus observation period as compared to the control. These findings provide preliminary support for the species-specific nature of these proposed alternative P. marinus control measures.

Ocean Acidification Amplifies the Olfactory Response to 2-Phenylethylamine: Altered Cue Reception as a Mechanistic Pathway?

With carbon dioxide (CO2) levels rising dramatically, climate change threatens marine environments. Due to increasing CO2 concentrations in the ocean, pH levels are expected to drop by 0.4 units by the end of the century. There is an urgent need to understand the impact of ocean acidification on chemical-ecological processes. To date, the extent and mechanisms by which the decreasing ocean pH influences chemical communication are unclear. Combining behaviour assays with computational chemistry, we explore the function of the predator related cue 2-phenylethylamine (PEA) for hermit crabs (Pagurus bernhardus) in current and end-of-the-century oceanic pH. We demonstrate that this dietary predator cue for mammals and sea lampreys is an attractant for hermit crabs. Furthermore, we show that the potency of the cue increases at pH levels expected for the year 2100. In order to explain this increased potency, we assess changes to PEA’s conformational and charge-related properties as one potential mechanistic pathway. Using quantum chemical calculations validated by NMR spectroscopy, we characterise the different protonation states of PEA in water. We show how protonation of PEA could affect receptor-ligand binding, using a possible model receptor for PEA (human TAAR1). Investigating potential mechanisms of pH dependent effects on olfactory perception of PEA and the respective behavioural response, our study advances the understanding of how ocean acidification interferes with the sense of smell and thereby might impact essential ecological interactions in marine ecosystems.

Effect of predator cue on escape and oviposition behaviour of freshwater snail

When suitability of sites for parent is incompatible with that for their eggs, parent–offspring conflict occurs — the parent must choose between the optimal oviposition site for eggs and that suitable for itself. We examined effects of predator cue on parental habitat use and oviposition site in Physa acuta. We assessed desiccation risk in eggs and the relationship between water depth and predation risk. Predator cues induced the elevation of parental habitat away from the bottom but had no effect on the oviposition site. Oviposition site choice is not by-product of escape response. Eggs that were exposed to desiccation failed to hatch, indicating high desiccation risk. Eggs laid at deeper levels were at higher risk of stripping from oviposition substrates by crayfishes. Although the middle-water level would be suitable oviposition sites, the parents selected an oviposition site in the upper level. There are other benefits and costs of oviposition site selection.

Mobbing-like response to secondary predator cues is not a form of teaching in meerkats

Across many taxa, individuals learn how to detect, recognise and respond to predators via social learning. Learning to recognise and interpret predator cues is essential in the accurate assessment of risk. Cues can come directly from a predator’s presence (visual, acoustic) or from secondary predator cues (SPCs, such as hair/feathers, urine or faeces) left in the environment. Animals show various responses to encountering SPCs, which are thought to act in reducing risk to the individual. Meerkats, Suricata suricatta, show a response to SPCs not described in any other species: they display a mobbing-like behaviour. The function of this behaviour is unclear as unlike mobbing, the response it so closely resembles, it cannot serve to drive predators away. We used experiments to investigate whether adults may use this mobbing-like response to teach naïve young how to recognise and respond to predators. Meerkats are known to teach pups hunting skills, but there is as yet no evidence that any species other than humans teaches across multiple contexts. We used experimental presentations of SPCs to test whether wild adult meerkats respond more intensely to SPCs in the presence of naïve pups, as would be expected if the behaviour serves to promote learning. Contrary to this prediction, response intensity was lower when pups were present than when they were absent, and declined as the number of pups in the group increased, possibly due to costs associated with foraging with dependent young. Response intensity instead increased with increasing group size, number of group members interacting with the cue, and varied with predator cue type. These results suggest that the mobbing-like response to SPCs is not a form of teaching in meerkats. Instead, this behaviour may function to increase the recruitment of others to investigate the SPC. Exposing group members to SPCs may better inform them of the nature of the threat, facilitating more effective defensive group responses.

Distracted decision makers: ship noise and predation risk change shell choice in hermit crabs

Human-induced rapid environmental change such as noise pollution alters the ability of animals to integrate information cues. Many studies focus on how noise impacts single sensory channels but in reality animals rely on multimodal sources of information. In this study, we investigated the effect of anthropogenic noise and the visual presence of a predator on tactile information gathering during gastropod shell assessment in the European hermit crab Pagurus bernhardus. For hermit crabs, empty gastropod shells are a crucial resource affecting growth, reproduction, and survival. We measured shell assessment behavior and manipulated 1) the shell size (50% or 80% of the optimal), 2) sound condition (ship or ambient), and 3) visual predator cue (absence/presence). Overall we found that crabs were less likely to accept an optimal shell in the presence of ship noise, suggesting that exposure to ship noise disrupted the information gathering ability of the crabs. We also found a significant interaction between noise, predator presence, and shell size on the mean duration for the final decision to accept or reject the optimal shell. Hermit crabs in 50% shells took less time for their final decision when exposed to both ship noise and predator cue while crabs in 80% shells showed shorter decision time only when the predator cue was absent. Our results indicate that anthropogenic noise can interact with predation threat and resource quality to change resource acquisition, suggesting that noise pollution can disrupt behavior in a nonadditive way, by disrupting information use across multiple sensory channels.