Antipredator Behavior Research Articles

The effects of prenatal predator cue exposure on offspring substrate preferences in the wolf spider Tigrosahelluo

Prey may gain fitness benefits from recognizing predators at an early age. Predator cues perceived by gravid prey have the potential to prime offspring to alter their behaviour in the presence of predation threats after birth. Wolf spiders (Araneae: Lycosidae) provide an opportunity to explore this phenomenon since females carry their eggsacs prior to eclosion and, after emergence, carry spiderlings for days as they disperse. During maternal care, mothers may prenatally expose offspring to predator odour cues and potentially influence their posteclosion dispersal when in the presence of these cues. Spiderlings of the wolf spider Tigrosa helluo are eaten by adults of the wolf spider Pardosa milvina . We measured differences in substrate preferences of spiderlings produced from egg-carrying T. helluo females that had or had not been exposed to cues of adult P. milvina . Over a 15-day period we counted the number of offspring climbing on substrates previously walked on by P. milvina , crickets or blank control substrates. For the first 10 out of 15 days, spiderlings of predator-exposed mothers climbed on Pardosa substrates significantly more compared to control mothers. We found no significant spiderling preference in time spent on cricket-cued or control substrates across treatments and no difference in chemical cue substrate preference of the mothers while spiderlings dispersed. Among wolf spiders, vertical climbing and contact with predator-cued substrates can induce adaptive tonic immobility (freeze response) that has been associated with increased survival in the presence of live predatory lycosids. Spider predator cues may prime spiderling antipredator behaviour either directly through prenatal exposure in the eggsac or indirectly by modifying the mother's behaviour prior to eclosion, but we found no evidence of mother substrate preference influencing spiderling distribution during dispersal. • Embryonic wolf spiders are primed to learn predator cues while in the eggsac. • Spiderling dispersal differed based on predator cue exposure during eggsac care. • Shifted antipredator responses persisted for at least 10 days postemergence.

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 responses of the tuco-tucos of the Talas (Ctenomys talarum Thomas, 1898) to predator cues. We found that individuals exposed to cat odors and immobilization entered less often and spent 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 C. talarum (naturally parasitized, deparasitized, or inoculated with Eimeria sp.). We did not find differences among the groups with regards to 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.

Living with the enemy: activity rhythms of the red fox and some potential preys in an urban environment

The present study aimed at investigating the activity rhythms of the red fox Vulpes vulpes and three potential preys (i.e. the European hedgehog Erinaceus europaeus, the wood mouse Apodemus sylvaticus, and the Norway rat Rattus norvegicus) in an urban environment. Data were collected as a part of a camera trapping survey, carried out within the municipality of Padua (northeastern Italy). In order to analyse species activity patterns, the R overlap package was used and then the Watson-Wheeler test was run to evaluate whether two overlaps were significantly different. Results show that all the investigated species have nocturnal activities, with “moderate” temporal activity overlap between the red fox and its potential prey. The Watson-Wheeler test showed that the hedgehog was the only potential prey that did not show significant differences in the hours of activity compared to those of the red fox. Instead, statistically significant differences were recorded when the activity rhythm of the red fox was compared with that of the wood mouse or the Norway rat. This may indicate the development of antipredator behaviour or the possibility that the red fox is seeking anthropogenic food sources instead of wild prey or, alternatively, other preferred food items.

Behavioral patterns in the early-stage antipredator response change after tail autotomy in adult wall lizards.

Autotomy is a drastic antipredator defense consisting of the voluntary shedding of a body part to escape from the predators. The loss of a body part may impair locomotion, feeding or mating, so animals may face a higher predation risk shortly after autotomy. Thus, until regeneration is completed, prey may adjust their behavior to reduce predation risk, and this could involve secondary costs. We assessed the effect of tail loss on the antipredator behavior of wall lizards (Podarcis muralis), comparing the behavior of tailed and tailless individuals exposed to a predatory snake (Coronella austriaca) scent, under controlled experimental conditions. Tailless lizards spent significantly more time performing behaviors with antipredatory significance (e.g., moving slowly), whereas tailed individuals performed exploratory walking for significantly more time. Moreover, tailless lizards spent more time basking, which probably increases the effectiveness of their cryptic design and decreases detection by predators. Lizards intensified the tongue flick rates when exposed to a pungent control or snake scents, as compared to their response to a neutral control. Besides, both tailed and tailless lizards intensified some aspects of their antipredator behavior (walking slowly and avoiding refuge use) when exposed to snake scent, which indicates discrimination of the smell of predatory snakes. Lizards decreased refuge use when exposed to predator scents, probably because the refuges are evaluated as unsafe due to a high concentration of snake scents. To conclude, our experiments showed that, after losing their tails, wall lizards modify their behavior in a way that likely minimizes predation risk.

Mobility-limiting antipredator response in the rock-paper-scissors model

Antipredator behavior is present in many biological systems where individuals collectively react to an imminent attack. The antipredator response may influence spatial pattern formation and ecosystem stability but requires an organism's cost to contribute to the collective effort. We investigate a nonhierarchical tritrophic system, whose predator-prey interactions are described by the rock-paper-scissors game rules. In our spatial stochastic simulations, the radius of antipredator response defines the maximum prey group size that disturbs the predator's action, determining the individual cost to participate in antipredator strategies. We consider that each organism contributes equally to the collective effort, having its mobility limited by the proportion of energy devoted to the antipredator reaction. Our outcomes show that the antipredator response leads to spiral patterns, with the segregation of organisms of the same species occupying departed spatial domains. We found that a less localized antipredator response increases the average size of the single-species patches, improving the protection of individuals against predation. Finally, our findings show that although the increase of the predation risk for a more localized antipredator response, the high mobility constraining benefits species coexistence. Our results may help ecologists understand the mechanisms leading to the stability of biological systems where locality is crucial to behavioral interactions among species.

Genomic characterization between strains selected for death-feigning duration for avoiding attack of a beetle

Predator avoidance is an important behavior that affects the degree of adaptation of organisms. We compared the DNA variation of one of the predator-avoidance behaviors, the recently extensively studied "death-feigning behavior”, between the long strain bred for feigning death for a long time and the short strain bred for feigning death for a short time. To clarify how the difference in DNA sequences between the long and short strains corresponds to the physiological characteristics of the death-feigning duration at the transcriptome level, we performed comprehensive and comparative analyses of gene variants in Tribolium castaneum strains using DNA-resequencing. The duration of death feigning involves many gene pathways, including caffeine metabolism, tyrosine metabolism, tryptophan metabolism, metabolism of xenobiotics by cytochrome P450, longevity regulating pathways, and circadian rhythm. Artificial selection based on the duration of death feigning results in the preservation of variants of genes in these pathways in the long strain. This study suggests that many metabolic pathways and related genes may be involved in the decision-making process of anti-predator animal behavior by forming a network in addition to the tyrosine metabolic system, including dopamine, revealed in previous studies.

Mate Choice, Sex Roles and Sexual Cognition in Vertebrates: Mate Choice Turns Cognition or Cognition Turns Mate Choice?

The idea of “smart is sexy,” meaning superior cognition provides competitive benefits in mate choice and, therefore, evolutionary advantages in terms of reproductive fitness, is both exciting and captivating. Cognitively flexible individuals perceive and adapt more dynamically to (unpredictable) environmental changes. The sex roles that females and males adopt within their populations can vary greatly in response to the prevalent mating system. Based on how cognition determines these grossly divergent sex roles, different selection pressures could possibly shape the (progressive) evolution of cognitive abilities, suggesting the potential to induce sexual dimorphisms in superior cognitive abilities. Associations between an individual’s mating success, sexual traits and its cognitive abilities have been found consistently across vertebrate species and taxa, providing evidence that sexual selection may well shape the supporting cognitive prerequisites. Yet, while superior cognitive abilities provide benefits such as higher feeding success, improved antipredator behavior, or more favorable mate choice, they also claim costs such as higher energy levels and metabolic rates, which in turn may reduce fecundity, growth, or immune response. There is compelling evidence in a variety of vertebrate taxa that females appear to prefer skilled problem-solver males, i.e., they prefer those that appear to have better cognitive abilities. Consequently, cognition is also likely to have substantial effects on sexual selection processes. How the choosing sex assesses the cognitive abilities of potential mates has not been explored conclusively yet. Do cognitive skills guide an individual’s mate choice and does learning change an individual’s mate choice decisions? How and to which extent do individuals use their own cognitive skills to assess those of their conspecifics when choosing a mate? How does an individual’s role within a mating system influence the choice of the choosing sex in this context? Drawing on several examples from the vertebrate world, this review aims to elucidate various aspects associated with cognitive sex differences, the different roles of males and females in social and sexual interactions, and the potential influence of cognition on mate choice decisions. Finally, future perspectives aim to identify ways to answer the central question of how the triad of sex, cognition, and mate choice interacts.

Comparative analysis of Dipodomys species indicates that kangaroo rat hindlimb anatomy is adapted for rapid evasive leaping.

Body size is a key factor that influences antipredator behavior. For animals that rely on jumping to escape from predators, there is a theoretical trade-off between jump distance and acceleration as body size changes at both the inter- and intraspecific levels. Assuming geometric similarity, acceleration will decrease with increasing body size due to a smaller increase in muscle cross-sectional area than body mass. Smaller animals will likely have a similar jump distance as larger animals due to their shorter limbs and faster accelerations. Therefore, in order to maintain acceleration in a jump across different body sizes, hind limbs must be disproportionately bigger for larger animals. We explored this prediction using four species of kangaroo rats (Dipodomys spp.), a genus of bipedal rodent with similar morphology across a range of body sizes (40-150g). Kangaroo rat jump performance was measured by simulating snake strikes to free-ranging individuals. Additionally, morphological measurements of hind limb muscles and segment lengths were obtained from thawed frozen specimens. Overall, jump acceleration was constant across body sizes and jump distance increased with increasing size. Additionally, kangaroo rat hind limb muscle mass and cross-sectional area scaled with positive allometry. Ankle extensor tendon cross-sectional area also scaled with positive allometry. Hind limb segment length scaled isometrically, with the exception of the metatarsals, which scaled with negative allometry. Overall, these findings support the hypothesis that kangaroo rat hind limbs are built to maintain jump acceleration rather than jump distance. Selective pressure from single-strike predators, such as snakes and owls, likely drives this relationship.

The impact of headstarting on the survival and naiveté of an endangered terrestrial mammal after return to the wild

AbstractComplete separation of endangered prey from introduced predators improves prey survival at the cost of reduced predator recognition and antipredator behaviours, termed ‘prey naiveté’. Headstarting is a conservation strategy that has been used to improve the survival of juveniles for numerous species, whereby prey is separated from predators only in their vulnerable early life stage before release to the wild. However, by isolating prey from predators headstarting could compromise prey individuals’ antipredator behaviour. Here, we evaluate the effects that headstarting has on the survival, dispersal, body condition and flight initiation distance (FID) of a terrestrial mammal, the bridled nailtail wallaby Onychogalea fraenata. Young bridled nailtail wallabies were isolated from predators in a 9.2 ha predator‐free fenced exclosure and were released into the wild once their body mass exceeded 3 kg. There was no difference in dispersal, body condition or survival of headstarted wallabies compared to wild‐raised wallabies. FID of headstarted wallabies assessed using night‐vision goggles was lower than wild‐raised wallabies in the week following release, but converged with that of wild‐raised wallabies within 4 weeks post‐release. Our results show that headstarting can be an effective conservation strategy for terrestrial mammals whose early life stages are vulnerable to introduced predators.

Behaviour and metabolism during tonic immobility (death-feigning) in Eucryptorrhynchus scrobiculatus and E. brandti (Coleoptera: Curculionidae)

The antipredator behaviour, tonic immobility (TI) is a valuable defence that enables insects to increase their chance of survival and is a trade-off between fleeing and protection. How the TI strategies of insects respond to environmental factors, however, remains a largely understudied subject. In this paper the effect of four factors (mechanical stimulation, light, sound and temperature) and metabolic responses were used to evaluate TI behavioural and physiological adaptions in Eucryptorrhynchus scrobiculatus (ESCR) and Eucryptorrhynchus brandti (EBRA). In the behavioural experiment, the metaventrite, which is the stimulus-sensing region in ESCR and EBRA, was subjected to mechanical stimulation. Light lengthened the TI duration in ESCR males, while sound had the opposite effect in ESCR and EBRA. The effect of temperature on the duration of TI was variable: in ESCR, the duration was shorter at low (15°C) and high (32°C) temperatures, but in EBRA, it was longer at the low (15°C) temperature. In the metabolism experiment, ESCR and EBRA metabolic rates (MR), was significantly dependent on whether they were in a state of TI or not. The TIMR declined to 76.90% in ESCR and 71.40% in EBRA. These results indicate that TI in ESCR and EBRA differed under different external conditions and contributes to the understanding of the physiological regulation of ecological traits of insect TI.

Modelling collective decision-making: Insights into collective anti-predator behaviors from an agent-based approach

Collective decision-making is a widespread phenomenon across organisms. Studying how animal societies make group decisions to the mutual benefit of group members, while avoiding exploitation by cheaters, can provide unique insights into the underlying cognitive mechanisms. As a step toward dissecting the proximate mechanisms that underpin collective decision-making across animals, we developed an agent-based model of antipredatory alarm signaling and mobbing during predator-prey encounters. Such collective behaviors occur in response to physical threats in many distantly related species with vastly different cognitive abilities, making it a broadly important model behavior. We systematically assessed under which quantitative contexts potential prey benefit from three basic strategies: predator detection, signaling about the predator (e.g., alarm calling), and retreating from vs. approaching the predator. Collective signaling increased survival rates over individual predator detection in several scenarios. Signaling sometimes led to fewer prey detecting the predator but this effect disappeared when prey animals that had seen the predator both signaled and approached it, as in mobbing. Critically, our results highlight that collective decision-making in response to a threat can emerge from simple rules without needing a central leader or needing to be under conscious control.

No evident effect of domestication on the anti-predator behaviour of European abalone (Haliotis tuberculata): Implications for stock enhancement programs

Stock-enhancement programs for the European abalone (Haliotis tuberculata) might be an efficient way to restore collapsed natural populations or preserve fishing activities. Specifically, this practice consists of releasing hatchery-reared juveniles from wild or farmed broodstock into natural environments. However, the process of selection and adaptation to farming conditions may result in domestication, thus leading to genetic and behavioural changes in farmed animals. Therefore, evaluating the effects of the domestication process on juveniles is a critical first step toward the development of successful abalone stock-enhancement programs. To this end, the behaviour and survival of sixteen-month-old H. tuberculata juveniles from wild and from farmed broodstock (the product of three generations of shell-length based selection) were compared. We used three assays at different spatial and temporal scales: (1) short-term responses to simulated contact with predators, (2) the activity pattern in the presence of a natural predator (the velvet crab Necora puber) in aquariums during a 2-week trial, and (3) survival in large mesocosms in the presence of predators during a 3-week trial. No significant effects of the broodstock origin of the juveniles were detected on any of the studied parameters (P > 0.05). In addition, the estimated size effects were small compared to the overall mean for most of the variables, suggesting that the domestication process was too recent to induce important behavioural changes in juveniles from farmed broodstock.Introducing crabs into the mesocosms significantly decreased abalone survival rates (P < 0.05). In the activity pattern trial, most of the abalone mortality in aquariums with crabs (55%) occurred within the first three days, which was largely attributed to initial exploration of areas outside of shelters by the abalone. In the second week, abalone spent much less time moving when crabs were present (P < 0.05).These results suggest that juveniles from both origins would likely have the same survival rates if released in the wild. The commonly reported high abalone mortality immediately after seeding is likely due to a lack of hiding behaviour or exploration of the new environment during the first few days of exposure to predators in the wild. Therefore, current release systems may need to be adjusted to the ethological characteristics of abalone juveniles to avoid high mortalities due to an initial lack of predator avoidance.

Solving the Uncapacitated Single Allocation p-Hub Location Problem with Fixed Cost Using Anti-Predatory NIA

Background: Hub Location Problem (HLP) deals with long-term strategic decision planning in various application domains with the aim of reducing overall transportation cost. It deals with identifying hubs and allocating spokes to hubs in order to route the flow of goods between origin-destination locations. Due to the complex nature of the problem, meta-heuristic algorithms are best suited to solve HLPs. The existing algorithms face the accuracy and consistency related issues for solving the HLPs. Objective: This paper attempts to solve a variant of HLP, which is known as Uncapacitated Single Allocation p-Hub Location Problem with Fixed Cost (USApHLP-FC), using Anti-Predatory Nature- Inspired Algorithm (APNIA) to improve accuracy and consistency in results. Methods: APNIA is a recently proposed meta-heuristic nature-inspired algorithm, which is based on the anti-predatory behavior of frogs. For solving the HLP, APNIA is used for both identifying the hubs and allocating the spokes to hubs in order to reduce the total cost of goods transportation. Results: A numerical problem with 10 locations is used for empirical study. The experimental result shows that APNIA outperforms other leading proposals in terms of total cost and gap value. The obtained results of APNIA are compared with the genetic algorithm, particle swarm optimization, artificial bee colony, firefly algorithm, teacher learning based optimization and Jaya algorithm. The comparative study indicates at least 0.86% improvement in accuracy and at least a 10% gain in consistency by APNIA for the different number of generations. Conclusion: The experimental evaluation and performance comparison signify that APNIA based approach has improved accuracy and consistency in solutions than other compared algorithms. It establishes the robustness of anti-predatory NIA for solving the hub location problems.

Factors influencing the flush response and flight initiation distance of three owl species in the Andaman Islands

Effects of anthropogenic pressures on birds of the Andaman Islands have been documented to some extent, however studies on the effect of human activities on the behavioural response of these birds are limited. This study assessed the anti-predatory behaviour (flush response - FR and flight initiation distance - FID) of three owl species (Otus sunia, Otus balli, and Ninox obscura) in response to human stimuli and factors influencing it on the Andaman Islands. In total, 63 % of owls flushed from their roost sites in response to approaching human, and such a response varied between species. Similarly, FID varied widely among the species ranging from 4.23 to 6.73 m. The FR of N. obscura was influenced by the count of climbers, presence of spine, and branch status, while roost height, ambient temperature, and lower count of climbers contributed to a higher FID. For the two Otus species, camouflage and pairing were found to influence their FR while FID of O. balli was influenced by roost height, pairing, and presence of spines. Our results indicated that the anti-predatory behaviour of owls on the Andaman Islands was species- and site-specific and prolonged disturbance to their roost sites may affect the survival and reproductive rate of these owls.

Anti-predator behaviour of Rhinella major (Müller and Hellmich 1936), with insights into the Rhinella granulosa group

In anurans, the different types of anti-predator behaviour have been documented in isolation, but some species have shown synergistic strategies in different situations. The display of these types of behaviour may be related to the types of predators in the habitat, which boost defensive responses in their prey. However, most reports are mostly opportunistic and punctual observations, not systematic. Here, we report the occurrence of anti-predator behaviour in the toadRhinella major(Müller and Hellmich 1936) (Amphibia, Anura, Bufonidae) in the face of different handling modes. Probably the disturbance caused by handling had elicited a predator deterrence response in the individual, causing it to rapidly exhibit such behaviour. These conditions are discussed along with an overview of anti-predator behaviour in species of theR. granulosagroup and we re-interpreted these strategies for two species in the group.

Urban-nesting mountain chickadees have a reduced response to a simulated predator

Abstract Anti-predator behaviour is common among birds, but little research exists on whether differences in the predator landscape between urban and rural habitats results in differential anti-predator behaviour. We compared nest-defence behaviour of mountain chickadees (Poecile gambeli) in urban and rural habitats in Kamloops, BC, Canada to a simulated predator model (snake) on top of nest boxes while incubating females were away from nests on foraging bouts. Upon their return, we recorded proximity to the predator model, latency to contact the nest box and enter the nest, and number of gargle and chick-a-dee calls as measures of anti-predator behaviour and compared multivariate “predator aversion scores” across birds occupying either rural or urban landscapes. Rural-nesting birds had more aversive reactions to the predator model than the urban-nesting birds, which may suggest differences in perceived threat of the model, in combination with increased boldness associated with urban-nesting birds.

Social influence on anti-predatory behaviors of juvenile bighead carp (Hypophthalmichthys nobilis) are influenced by conspecific experience and shoal composition

Social influence on anti-predatory behaviors of juvenile bighead carp (Hypophthalmichthys nobilis) are influenced by conspecific experience and shoal composition

Predator–Prey Reunion: Non-native Coquí Frogs Avoid Their Native Predators

When non-native species are introduced to new areas without their native predators, they may lose their ability to detect and avoid those predators, especially if the behaviors impose some sort of cost. Few studies have investigated whether non-native populations have lost the ability to avoid their native predators. Coquí frogs, which are endemic to Puerto Rico, were introduced to Hawaii in the late 1980s. Our goal was to investigate whether Coquís from Hawaii avoid predators from their native Puerto Rico. To test this, we collected frogs from both ranges and two arthropod predators from Puerto Rico (tailless whip scorpions and tarantulas). We determined experimentally whether frogs from Hawaii and Puerto Rico exhibited the same avoidance behaviors to these predators. We found that frogs from both ranges avoid attack by moving away from predators and that there was no difference in behaviors between the two ranges. Results suggest that, after nearly 20 generations, frogs from Hawaii have not lost their ability to detect and avoid native predators. The antipredator behaviors Coquís exhibit may help them avoid novel predators in their introduced range and may have contributed to their successful invasion.

Predator-induced maternal effects determine adaptive antipredator behaviors via egg composition

In high-risk environments with frequent predator encounters, efficient antipredator behavior is key to survival. Parental effects are a powerful mechanism to prepare offspring for coping with such environments, yet clear evidence for adaptive parental effects on offspring antipredator behaviors is missing. Rapid escape reflexes, or "C-start reflexes," are a key adaptation in fish and amphibians to escape predator strikes. We hypothesized that mothers living in high-risk environments might induce faster C-start reflexes in offspring by modifying egg composition. Here, we show that offspring of the cichlid fish Neolamprologus pulcher developed faster C-start reflexes and were more risk averse if their parents had been exposed to cues of their most dangerous natural predator during egg production. This effect was mediated by differences in egg composition. Eggs of predator-exposed mothers were heavier with higher net protein content, and the resulting offspring were heavier and had lower igf-1 gene expression than control offspring shortly after hatching. Thus, changes in egg composition can relay multiple putative pathways by which mothers can influence adaptive antipredator behaviors such as faster escape reflexes.

The influence of maternal glucocorticoids on offspring phenotype in high- and low-risk environments.

Elevated maternal glucocorticoid levels during gestation can lead to phenotypic changes in offspring via maternal effects. Although such effects have traditionally been considered maladaptive, maternally derived glucocorticoids may adaptively prepare offspring for their future environment depending upon the correlation between maternal and offspring environments. Nevertheless, relatively few studies test the effects of prenatal glucocorticoid exposure across multiple environments. We tested the potential for ecologically relevant increases in maternal glucocorticoids in the eastern fence lizard (Sceloporus undulatus) to induce adaptive phenotypic changes in offspring exposed to high or low densities of an invasive fire ant predator. Maternal treatment had limited effects on offspring morphology and behavior at hatching, but by 10 days of age, we found maternal treatment interacted with offspring environment to alter anti-predator behaviors. We did not detect differences in early-life survival based on maternal treatment or offspring environment. Opposing selection on anti-predator behaviors from historic and novel invasive predators may confound the potential of maternal glucocorticoids to adaptively influence offspring behavior. Our test of the phenotypic outcomes of transgenerational glucocorticoid effects across risk environments provides important insight into the context-specific nature of this phenomenon and the importance of understanding both current and historic evolutionary pressures.