Antipredator Behavior Research Articles

Brown Mouse Lemurs (Microcebus rufus) May Lack Opportunities to Learn about Predator Calls

Diurnal primates commonly modify their behaviour in response to predator vocalizations, but little is known about how nocturnal primates perceive predator calls. Mouse lemurs do not innately perceive predator calls as dangerous but may learn to do so in the wild. I hypothesized that wild brown mouse lemurs (Microcebus rufus) in Ranomafana National Park, Madagascar, differentiate between predator and non-predator vocalizations and exposed 29 adult subjects to calls of 3 sympatric predators (goshawk, fossa and owl), 3 sympatric non-predators and 4 controls. Brown mouse lemurs did not differentiate among stimuli, and there was no evidence that any recording was associated with danger, as neither activity nor spatial preferences changed in response to a stimulus, nor did subjects exhibit obvious behaviours indicative of danger such as flight or position on the branches. The failure to perceive predator calls as dangerous is common among small nocturnal solitary prey species and could be explained by a lack of learning opportunities. In social species acquired behaviours can spread quickly by social learning. Solitary species like mouse lemurs have to individually learn to associate predator calls with danger which is dependent on encounter rates. Unlike diurnal prey mouse lemurs lack the opportunity to observe diurnal raptors and associate their calls with the bird, and owls are proficient predators, which are difficult to observe in a rain forest where they hunt cryptically from perches. While sometimes nocturnal, the fossa is solitary and largely silent, and is also particularly rare at my study site. Cryptic, rare or non-vocal predators provide prey with few opportunities to associate their calls with danger. Mouse lemurs are subject to high predation rates by a wide range of predators and need to balance the costs and benefits of antipredation behaviours. Their cryptic lifestyle and preference for dense vegetation lowers the likelihood of being detected by predators, and they utilize visual and olfactory predator cues to make decisions about risk. Furthermore, their high reproductive output compensates for the high predation rates.

Mixed-species herding levels the landscape of fear

Prey anti-predator behaviours are influenced by perceived predation risk in a landscape and social information gleaned from herd mates regarding predation risk. It is well documented that high-quality social information about risk can come from heterospecific herd mates. Here, we integrate social information with the landscape of fear to quantify how these landscapes are modified by mixed-species herding. To do this, we investigated zebra vigilance in single- and mixed-species herds across different levels of predation risk (lion versus no lion), and assessed how they manage herd size and the competition-information trade-off associated with grouping behaviour. Overall, zebra performed higher vigilance in high-risk areas. However, mixed-species herding reduced vigilance levels. We estimate that zebra in single-species herds would have to feed for approximately 35 min more per day in low-risk areas and approximately 51 min more in high-risk areas to compensate for the cost of higher vigilance. Furthermore, zebra benefitted from the competition-information trade-off by increasing the number of heterospecifics while keeping the number of zebra in a herd constant. Ultimately, we show that mixed-species herding reduces the effects of predation risk, whereby zebra in mixed-species herds, under high predation risk, perform similar levels of vigilance compared with zebra in low-risk scenarios.

Trait‐dependency of trophic interactions in zooplankton food webs

Anthropogenic change in the abundance or identity of dominant top predators may induce reorganizations in whole food webs. Predicting these reorganizations requires identifying the biological rules that govern trophic niches. However, we still lack a detailed understanding of the respective contributions of body size, behaviour (e.g. match between predator hunting mode and prey antipredator strategy), phylogeny and/or ontogeny in determining both the presence and strength of trophic interactions. Here, we address this question by measuring zooplankton numerical response to fish predators in lake enclosures. We compared the fit to zooplankton count data of models grouping zooplankters based either on 1) body sizes, 2) antipredator behaviour, 3) body size combined with antipredator behaviour or on 4) phylogeny combined with ontogeny (i.e. different life stages of copepods). Body size was a better predictor of zooplankton numerical response to fish than antipredator behaviour, but combining body size and behaviour provided even better predictions. Models based on phylogeny combined with ontogeny clearly outperformed those based on other zooplankton grouping rules, except when phylogeny was poorly resolved. Removing ontogenetic information plagued the predictive power of the highly‐resolved (genus‐level) phylogenetic grouping but not of medium‐resolved or poorly‐resolved phylogenetic grouping. Our results support the recent use of phylogeny as a superior surrogate for traits controlling trophic niches, and further highlight the added value of combining phylogeny with ontogenetic traits. Further improvements in our mechanistic understanding of how trophic networks are shaped are bound to uncovering the trophic traits captured by phylogeny and ontogeny, but that currently remain hidden to us.

Social learning of acoustic anti-predator cues occurs between wild bird species.

In many species, individuals gather information about their environment both through direct experience and through information obtained from others. Social learning, or the acquisition of information from others, can occur both within and between species and may facilitate the rapid spread of antipredator behaviour. Within birds, acoustic signals are frequently used to alert others to the presence of predators, and individuals can quickly learn to associate novel acoustic cues with predation risk. However, few studies have addressed whether such learning occurs only though direct experience or whether it has a social component, nor whether such learning can occur between species. We investigate these questions in two sympatric species of Parids: blue tits (Cyanistes caeruleus) and great tits (Parus major). Using playbacks of unfamiliar bird vocalizations paired with a predator model in a controlled aviary setting, we find that blue tits can learn to associate a novel sound with predation risk via direct experience, and that antipredator response to the sound can be socially transmitted to heterospecific observers, despite lack of first-hand experience. Our results suggest that social learning of acoustic cues can occur between species. Such interspecific social information transmission may help to mediate the formation of mixed-species aggregations.

Intraspecific variation in tree lizard escape behaviour in relation to habitat and temperature

Abstract Optimal escape theory has proven useful for understanding the dynamics of antipredator behaviour in animals; however, approaches are often limited to single-population studies. We studied how the escape behaviour of tree lizards (Urosaurus ornatus) varied across a disturbance gradient. We also considered how sex, body temperature, and perch temperature affected their escape decisions. Both sexes exhibited similar response patterns; however, lizards in the most-disturbed habitat, as well as cooler (body or perch temperature) lizards, initiated escape earlier (but did not flee further) than other animals. Increased wariness as indicated by earlier escape suggests that frequently-disturbed, more-open localities may be stressful habitats for species like U. ornatus. In addition, because cooler temperatures limit locomotor performance capacity, escape decisions should also depend on a species’ thermal ecology. Overall, we stress the importance of multi-population approaches for capturing the variety of ways species adaptively respond to the threat of predation across habitat gradients.

Otolith morphological divergences of successful Lessepsian fishes on the Mediterranean coastal waters

Here we used a method of morphological niche analysis, previously shown to be an effective predictor of invasion success, to investigate morphological relationships of sagittae otoliths of Lessepsian (Red sea species entering the Mediterranean through the Suez Canal) fishes within the morphospace of the corresponding receiving taxonomic groups. Overall, sagittae of 13 Lessepsian species and 49 closely related native fishes/taxa, distributed in 9 different families or subfamilies were considered, for a total of 305 analyzed otoliths. Based on wavelet functions of 512 Cartesian coordinates, we quantified the degree of morphological disparity produced by the introduction of these species in the hosting community. Lessepsian otoliths tended to be added outside or at the margins of the receiving morphospace, being morphologically divergent from the ones of native species. Considering that many ecological traits of fishes (especially feeding) are mirrored in the shape of otoliths, our findings agree with the idea that these successful invaders may count on novel sensory strategies to compete for available resources and to thrive in newly colonized habitats. Nevertheless, different measurements of morphological disparity did not show any variation before and after invasion and with the specific richness and further investigation is needed to understand to what extent these differentiated sensorial adaptations are linked to novel opportunities along the niche axes, such as in relation to feeding, predatory and anti-predatory behaviour and exploitation of the temporal niche.

Precipitation and predation risk alter the diversity and behavior of pollinators and reduce plant fitness.

Biotic and abiotic factors may individually or interactively disrupt plant-pollinator interactions, influencing plant fitness. Although variations in temperature and precipitation are expected to modify the overall impact of predators on plant-pollinator interactions, few empirical studies have assessed if these weather conditions influence anti-predator behaviors and how this context-dependent response may cascade down to plant fitness. To answer this question, we manipulated predation risk (using artificial spiders) in different years to investigate how natural variation in temperature and precipitation may affect diversity (richness and composition) and behavioral (visitation) responses of flower-visiting insects to predation risk, and how these effects influence plant fitness. Our findings indicate that predation risk and an increase in precipitation independently reduced plant fitness (i.e., seed set) by decreasing flower visitation. Predation risk reduced pollinator visitation and richness, and altered species composition of pollinators. Additionally, an increase in precipitation was associated with lower flower visitation and pollinator richness but did not alter pollinator species composition. However, maximum daily temperature did not affect any component of the pollinator assemblage or plant fitness. Our results indicate that biotic and abiotic drivers have different impacts on pollinator behavior and diversity with consequences for plant fitness components. Even small variation in precipitation conditions promotes complex and substantial cascading effects on plants by affecting both pollinator communities and the outcome of plant-pollinator interactions. Tropical communities are expected to be highly susceptible to climatic changes, and these changes may have drastic consequences for biotic interactions in the tropics.

The effect of antrophogenic noise on Sumatran Elephant’s anti-predator behavior in the Elephant Conservation Center

The increase of human activity around forest area causes noise anthropogenic effect to animals. This long-term effect can lead to decrease behavior and impact on species composition and inter-species interactions. Sumatran Elephants are classified as endangered animal. This study aims to determine the effect of noise on the Sumatran elephant’s anti-predator behavior and the difference in behavioral response based on the difference noise exposure time. The observation was conducted to Sumatran Elephants in Elephant Conservation Center Saree, Aceh Besar District. Observation method was animal focal sampling technique. The data was analyzed using the chi square test with a significant level of 5%. Based on the results of the chi-square test, the value of sig is 0.000 or smaller than 0.05, indicate that there is an effect of noise toward anti-predator behavior. The observed Sumatran elephants also look more responsive to the noise that is sounded in the morning. Noise can interfere with prey perceptions of predators and correlate with increased energy use.

Native and invasive squirrels show different behavioural responses to scent of a shared native predator.

Invasive species pose a serious threat to native species. In Europe, invasive grey squirrels (Sciurus carolinensis) have replaced native red squirrels (Sciurus vulgaris) in locations across Britain, Ireland and Italy. The European pine marten (Martes martes) can reverse the replacement of red squirrels by grey squirrels, but the underlying mechanism of how pine martens suppress grey squirrels is little understood. Research suggests the reversal process is driven by direct predation, but why the native red squirrel may be less susceptible than the invasive grey squirrel to predation by a commonly shared native predator, is unknown. A behavioural difference may exist with the native sciurid being more effective at avoiding predation by the pine marten with which they have a shared evolutionary history. In mammals, olfactory cues are used by prey species to avoid predators. To test whether anti-predator responses differ between the native red squirrel and the invasive grey squirrel, we exposed both species to scent cues of a shared native predator and quantified the responses of the two squirrel species. Red squirrels responded to pine marten scent by avoiding the feeder, increasing their vigilance and decreasing their feeding activity. By contrast, grey squirrels did not show any anti-predator behaviours in response to the scent of pine marten. Thus, differences in behavioural responses to a shared native predator may assist in explaining differing outcomes of species interactions between native and invasive prey species depending on the presence, abundance and exposure to native predators.

Effects of protective nesting associations with Whiskered Terns on the breeding success of Great Crested Grebes

At Anzali Lagoon, on the southwest coast of the Caspian Sea, Great Crested Grebes Podiceps cristatus were observed breeding both in monospecific colonies and in a mixed colony with Whiskered Terns Chlidonias hybridus. In the mixed colony, Great Crested Grebes bred later than in their monospecific colonies, while laying clutches of similar size, but significantly fewer of their nests disappeared during incubation and their chicks had higher survival rates up to at least 20 days old. Human disturbance and the resulting increases in predation likely caused greater losses at monospecific colonies of Great Crested Grebes where there is no common anti-predatory activity; while the strong anti-predatory behaviour of Whiskered Terns in the mixed colony might have offered enhanced protection to the chicks. Unfortunately, we could not separate the effects of the seasonal differences in human disturbance and of the protective presence of terns on the Great Crested Grebe's reproductive output.

Screening anti-predator behaviour in fish larvae exposed to environmental pollutants

Predation is one of the main sources of mortality for fish larvae. During evolution, they have developed different anti-predator behaviours, as the vibrational-evoked startle response and its habituation, for promoting survival to predator's strikes. Whereas these two behaviours can be altered by the exposure to some neurotoxicants, it is currently unknown if the exposure to environmentally relevant concentration (ERC) of neurotoxic pollutants could impair them. In this study thirty neurotoxic environmental pollutants from nine chemical groups, including: herbicides; carbamate, organophosphate (OP), organochlorine (OC), neonicotinoid and pyrethroid insecticides; toxins; metal and non-metal elements, have been screened at two concentrations, including one environmental relevant concentration (ERC), for adverse effects on anti-predator behaviours by using the Vibrational Startle Response Assay on zebrafish larvae. Significant effects over anti-predator responses were equally observed in both exposure concentrations. Focusing on the ERC scenario, it was found that the startle response was the less affected behaviour, where ten pollutants from all chemical groups except for organochlorine, neonicotinoid and pyrethroids, altered this response. Interestingly, organic and inorganic pollutants showed opposite effects on this response: whereas all organic pollutants decreased the startle response, the three remaining inorganic pollutants increased it. On the other hand, more pollutants affected habituation of the startle response of the larvae, where thirteen of the pollutants from all groups, except for herbicides, altered this behaviour at ERC, generally resulting in a faster habituation except for one OP and one marine toxin, which were able to delay this response. Ultimately, only one chemical from the OP, toxin, metal and non-metal element groups altered both the startle response and its habituation at both ERC and WSC. These results emphasize the environmental risk of the current levels of some neurotoxicants present in our aquatic ecosystems, as they are high enough to impair essential anti-predator behaviours in fish larvae.

Chronic Exposure to Oxazepam Pollution Produces Tolerance to Anxiolytic Effects in Zebrafish (Danio rerio).

Environmental concentrations of the anxiolytic drug oxazepam have been found to disrupt antipredator behaviors of wild fish. Most experiments exposed fish for a week, while evidence from mammals suggests that chronic exposure to therapeutic concentrations of benzodiazepines (such as oxazepam) results in the development of tolerance to the anxiolytic effects. If tolerance can also develop in response to the low concentrations found in the aquatic environment, it could mitigate the negative effects of oxazepam pollution. In the current study, we exposed wild-caught zebrafish to oxazepam (∼7 μg L-1) for 7 or 28 days and evaluated behavioral and physiological parameters at both time points. Females showed reduced diving responses to conspecific alarm pheromone after 7 days, but not after 28 days, indicating that they had developed tolerance to the anxiolytic effects of the drug. Zebrafish males were not affected by this oxazepam concentration, in line with earlier results. Serotonin turnover (ratio 5-HIAA/5-HT) was reduced in exposed females and males after 28 days, indicating that brain neurochemistry had not normalized. Post-confinement cortisol concentrations and gene expression of corticotropin-releasing hormone (CRH) were not affected by oxazepam. We did not find evidence that chronically exposed fish had altered relative expression of GABAA receptor subunits, suggesting that some other still unknown mechanism caused the developed tolerance.

Comparative Analysis of Anti-predator Behaviour and Life History Traits of the Tadpoles Exposed to Predation Risk and Corticosterone

Anuran tadpoles show behavioural and morphological alterations in the presence of predatory cues (perceived predation risk). Recent studies suggested the possible role of stress hormone corticosterone (CORT) in anti-predator responses. We speculated that the anti-predator responses of prey tadpoles exposed to predation risk and CORT will be similar if they are mediated through CORT. In the present study, we compared behavioural and life history responses of Duttaphrynus melanostictus tadpoles exposed to (i) predatory tadpoles of Hoplobatrachus crassus, and (ii) two concentrations (1 and 10 µg/L) of CORT. The results revealed that exposure of the tadpoles to predation risk and CORT have similar effects on behaviour and life history traits. Tadpoles exposed to predation risk and CORT did not alter behaviour in response to alarm cues. Tadpoles exposed to predation risk and different concentrations of CORT delayed metamorphosis with a reduction in size. CORT influenced metamorphosis and size of the tadpoles in concentration dependent manner. These results suggest that the presence of non-lethal predators affects life history traits possibly through the stress hormone.

Emerging investigator series: use of behavioural endpoints in the regulation of chemicals.

Interest in behavioural ecotoxicology is growing, partly due to technological and computational advances in recording behaviours but also because of improvements of detection capacity facilitating reporting effects at environmentally relevant concentrations. The peer-reviewed literature now contains studies investigating the effects of chemicals, including pesticides and pharmaceuticals, on migration, dispersal, aggression, sociability, reproduction, feeding and anti-predator behaviours in vertebrates and invertebrates. To understand how behavioural studies could be used in regulatory decision-making we: (1) assessed the legal obstacles to using behavioural endpoints in EU chemicals regulation; (2) analysed the known cases of use of behavioural endpoints in EU chemicals regulation; and (3) provided examples of behavioural endpoints of relevance for population level effects. We conclude that the only legal obstacle to the use of behavioural endpoints in EU chemicals regulation is whether an endpoint is considered to be relevant at the population level or not. We also conclude that ecotoxicity studies investigating behavioural endpoints are occasionally used in the EU chemicals regulation, and underscore that behavioural endpoints can be relevant at the population level. To improve the current use of behavioural studies in regulatory decision-making contribution from all relevant stakeholders is required. We have the following recommendations: (1) researchers should conduct robust, well-designed and transparent studies that emphasize the relevance of the study for regulation of chemicals; (2) editors and scientific journals should promote detailed, reliable and clearly reported studies; (3) regulatory agencies and the chemical industry need to embrace new behavioural endpoints of relevance at the population level.

Predator recognition and anti-predatory behaviour in a recent aquatic invader, the killer shrimp (Dikerogammarus villosus)

Abstract The killer shrimp (Dikerogammarus villosus) is one of the most recent, but also most damaging, aquatic invasive species in Europe, but information on how the species responds to novel predation pressures in recently invaded areas is very limited. We employed an open test arena to examine predator recognition and anti-predatory behaviour in killer shrimp exposed to either blank water or water conditioned with fish kairomones to simulate a predator threat. Within five years after their introduction, killer shrimp spent much more time hiding in the presence of fish kairomones than when they were exposed to blank water. However, no significant difference was found in aggregation behaviour, and killer shrimp were strongly attracted to the scent of conspecifics regardless of predator threat. Given the strong selective pressures that fish predators can exert on native and invasive gammarids, our findings highlight the need to consider prey-predator interactions to better predict the dispersal and likely impact of killer shrimp into invaded ecosystems.

Anthropogenic influences on primate antipredator behavior and implications for research and conservation.

Predation risk affects prey species' behavior, even in the absence of a direct threat, but human-induced environmental change may disturb ecologically significant predator-prey interactions. Here, we propose various ways in which knowledge of antipredator tactics, behavioral risk effects, and primate-predator interactions could assist in identifying human-caused disruption to natural systems. Using behavior to evaluate primate responses to the ongoing environmental change should be a potentially effective way to make species conservation more predictive by identifying issues before amore dramatic population declines. A key challenge here is that studies of predation on primates often use data collected via direct observations of habituated animals and human presence can deter carnivores and influence subjects' perception of risk. Hence, we also review various indirect data collection methods to evaluate their effectiveness in identifying where environmental change threatens wild species, while also minimizing observer bias.

A novel swarm intelligence optimization approach: sparrow search algorithm

ABSTRACT In this paper, a novel swarm optimization approach, namely sparrow search algorithm (SSA), is proposed inspired by the group wisdom, foraging and anti-predation behaviours of sparrows. Experiments on 19 benchmark functions are conducted to test the performance of the SSA and its performance is compared with other algorithms such as grey wolf optimizer (GWO), gravitational search algorithm (GSA), and particle swarm optimization (PSO). Simulation results show that the proposed SSA is superior over GWO, PSO and GSA in terms of accuracy, convergence speed, stability and robustness. Finally, the effectiveness of the proposed SSA is demonstrated in two practical engineering examples.

First observation of a Brolga Antigone rubicunda preying on eggs and of ‘water-kicking’ behaviour by Australasian Grebes Tachybaptus novaehollandiae as a nest-defence

We report a novel observation of Australian waterbird behaviour: a Brolga Antigone rubicunda preying on eggs of the Australasian Grebe Tachybaptus novaeholliandiae , the first record of birds’ eggs in the diet of a crane in Australia. We also report ‘water-kicking’ by the Australasian Grebe, the first record of this anti-predator behaviour in the species. Neither Brolga diet nor display behaviours of the Australasian Grebe have been systematically investigated, and we suggest avenues for further studies of egg predation and parental defence behaviours in waterbird breeding wetlands.

Low-frequency electroencephalogram oscillations govern left-eye lateralization during anti-predatory responses in the music frog.

Visual lateralization is widespread for prey and anti-predation in numerous taxa. However, it is still unknown how the brain governs this asymmetry. In this study, we conducted behavioral and electrophysiological experiments to evaluate anti-predatory behaviors and dynamic brain activities in Emei music frogs (Nidirana daunchina), to explore the potential eye bias for anti-predation and the underlying neural mechanisms. To do this, predator stimuli (a model snake head and a leaf as a control) were moved around the subjects in clockwise and anti-clockwise directions at steady velocity. We counted the number of anti-predatory responses and measured electroencephalogram (EEG) power spectra for each band and brain area (telencephalon, diencephalon and mesencephalon). Our results showed that (1) no significant eye preferences could be found for the control (leaf); however, the laterality index was significantly lower than zero when the predator stimulus was moved anti-clockwise, suggesting that left-eye advantage exists in this species for anti-predation; (2) compared with no stimulus in the visual field, the power spectra of delta and alpha bands were significantly greater when the predator stimulus was moved into the left visual field anti-clockwise; and, (3) generally, the power spectra of each band in the right-hemisphere for the left visual field were higher than those in the left counterpart. These results support that the left eye mediates the monitoring of a predator in music frogs and lower-frequency EEG oscillations govern this visual lateralization.

Anti-Predatory NIA for Unconstrained Mathematical Optimization Problems

Nature-Inspired Algorithms (NIAs) are one of the most efficient methods to solve the optimization problems. A recently proposed NIA is the anti-predatory NIA, which is based on the anti-predatory behavior of frogs. This algorithm uses five different types of self-defense mechanisms in order to improve its anti-predatory strength. This paper demonstrates the computation steps of anti-predatory for solving the Rastrigin function and attempts to solve 20 unconstrained minimization problems using anti-predatory NIA. The performance of anti-predatory NIA is compared with the six competing meta-heuristic algorithms. A comparative study reveals that the anti-predatory NIA is a more promising than the other algorithms. To quantify the performance comparison between the algorithms, Friedman rank test and Holm-Sidak test are used as statistical analysis methods. Anti-predatory NIA ranks first in both cases of “Mean Result” and “Standard Deviation.” Result measures the robustness and correctness of the anti-predatory NIA. This signifies the worth of anti-predatory NIA in the domain of mathematical optimization.