Simulated Predator Attack Research Articles

Are fast explorers slow reactors? Linking personality type and anti-predator behaviour

Response delays to predator attack may be adaptive, suggesting that latency to respond does not always reflect predator detection time, but can be a decision based on starvation-predation risk trade-offs. In birds, some anti-predator behaviours have been shown to be correlated with personality traits such as activity level and exploration. Here, we tested for a correlation between exploration behaviour and response latency time to a simulated fish predator attack in a fish species, juvenile convict cichlids (Amatitlania nigrofasciata). Individual focal fish were subjected to a standardized attack by a robotic fish predator while foraging, and separately given two repeated trials of exploration of a novel environment. We found a strong positive correlation between exploration and time taken to respond to the predator model. Fish that were fast to explore the novel environment were slower to respond to the predator. Our study therefore provides some of the first experimental evidence for a link between exploration behaviour and predator-escape behaviour. We suggest that different behavioural types may differ in how they partition their attention between foraging and anti-predator vigilance.

Yolk hormones have sex-specific long-term effects on behavior in the pied flycatcher ( Ficedula hypoleuca)

The hormonal environment during early development, such as maternally derived androgens in bird eggs, shapes the development and phenotype of the offspring in ways that may have important long-term consequences for behaviour. We studied the effects of yolk androgens on multiple behavioural traits in female and male pied flycatchers ( Ficedula hypoleuca) by experimentally elevating androgen levels (testosterone and androstenedione) in the eggs. The birds were housed in a common-garden environment in captivity until full independence, after which their behaviour was tested. We found that androgen-treated males were more likely than control males to explore a novel environment and showed higher activity in the presence of a novel object. In response to a simulated predator attack, androgen-treated males mainly showed freezing behaviour, while control males showed escape behaviour. Females from the androgen treatment and control group showed no differences in these behaviours. Androgen treatment did not affect neophobia (latency to approach the novel object) or dominance behaviour in either sex. Behaviour in the novel environment and towards a novel object was repeatable, but behaviours in the different experiments were mostly not inter-correlated. These results indicate that yolk androgens have various long-lasting effects on behaviour, especially in males, but that they do not induce a distinct behavioural syndrome. As behaviour is strongly linked with fitness, our results suggest that yolk androgens may play a role in determining fitness, and thus play a potentially adaptive role.

There will be blood: autohaemorrhage behaviour as part of the defence repertoire of an insect

AbstractArmoured ground crickets Acanthoplus discoidalis (Bradyporidae) have an arsenal of defence mechanisms in response to attack. Males but not females can stridulate when attacked, while both sexes will bite and regurgitate upon provocation. They will also autohaemorrhage. Here we have quantified these responses, examining how individuals of both sexes respond to repeated simulated predatory attack from the side (grabbing the legs with forceps) or from above (grabbing the animal by the pronotum). We found different responses depending on the method of attack. When attack was directed from the side (at the legs) the crickets can bite their attacker and males stridulate intensely. About 62% of such attacks elicited an autohaemorrhage response, where the crickets squirt 13±22 mg of acrid‐smelling haemolymph 43±63 mm from seams in the connective tissue between the trochanter and coxa of each leg and from under the pronotum. By contrast, animals attacked from above could not turn and bite their attacker, and stridulation was also reduced in males. About 86% of such attacks elicited an autohaemorrhage response with 19±19 mg of haemolymph projecting 10±30 mm from the body. Autohaemorrhaging is an effective form of chemical defence against bearded dragon lizards Pogona vitticeps (Agamidae) and Aca. discoidalis haemolymph applied to Gryllus bimaculatus nymphs (which have no such chemical defence) successfully saved them from predation by striped skinks Trachylepis punctatissima (Scincidae).

Flexibility in the colouration of the meninx (brain covering) in the guppy (Poecilia reticulata): investigations of potential function

Many organisms can change the apparent colour of their bodies by altering the aggregation of pigment in chromatophores in a process known as physiological colour change. In this study, we investigate a previously unstudied example of physiological colour change, from clear to black, of a brain covering, or meninx, in the guppy ( Poecilia reticulata Peters, 1859). UV protection in bright light was our primary hypothesis for the function of the meningeal colour, with a cost of increased conspicuousness to avian predators selecting for plasticity in the trait. An alternate hypothesis was that this flexible trait could be a physiological by-product of stress. Thus, we investigated the response of meningeal colour to light, stress, and simulated predator attacks, and also whether the black meninx affected conspicuousness to potential predators. Meningeal response to higher light levels did not differ from baseline responses. However, we did find that stress induced a sex-biased, rapid darkening of the meninx; this darkening then declined over time. These results suggest that meningeal blackness could be used as a novel, noninvasive indicator of stress level in guppies. We found no evidence for a role of predation in meningeal colour: meninx colour did not respond to the presence of a predator model and human “predators” detected similar numbers of guppies with black meninges and guppies with clear meninges.

What’s the buzz? Ultrasonic and sonic warning signals in caterpillars of the great peacock moth (Saturnia pyri)

Caterpillars have many natural enemies and, therefore, have evolved a diversity of antipredator strategies. Most research focuses on those strategies (crypsis, countershading, and warning coloration) targeting visually guided predators. In contrast, defensive sounds, although documented for more than a century, have been poorly studied. We report on a novel form of sound production--chirping--in caterpillars of the common European Great Peacock moth (Saturnia pyri). Chirps are broadband, with dominant peaks ranging between the sonic (3.7 kHz) and ultrasonic (55.1 kHz) and are generated by a rapid succession of mandibular "tooth strikes." Chirp trains are induced by simulated predator attacks and precede or accompany the secretion of a defensive chemical from integumental bristles, supporting our hypothesis that these sounds function in acoustic aposematism. We propose that these caterpillars generate multimodal warning signals (visual, chemical, and acoustic) to target the dominant sensory modalities of different predators, including birds, bats, and invertebrates.

Individual differences in exploratory and antipredator behaviour in juvenile smallmouth bass (Micropterus dolomieu)

Summary The correlation of individual behaviour in different contexts, known as a behavioural syndrome, constrains the optimization of behaviour within each context. Recent studies reveal that the strength of syndromes differs amongst populations and over individual ontogeny. In this study, exploratory behaviour in an unfamiliar environment and behavioural responses to a simulated predator attack in the presence of food were measured in juvenile smallmouth bass (Micropterus dolomieu). The results revealed a syndrome: individuals who actively explored the unfamiliar environment also behaved more boldly in the presence of the model predator. The syndrome implies a tradeoff between collecting information about one’s environment and risk of a predator attack. Additionally, the results revealed different anti-predator strategies. The simulated predator attack induced a longer period of activity (presumably to disperse away from the predator) by shy individuals, who were also more likely to utilize a refuge, had a longer latency to resume activity and were less likely to resume foraging than bold individuals. Larger conspecifics are the main predators of young-of-year smallmouth bass in the population from which subjects were collected. Predation pressure has been implicated as a cause of behavioral syndromes and the results of this study suggest that cannibalism in high density populations is sufficient to induce behavioural correlations.

Behaviour of damselfly larvae ( Enallagma cyathigerum) (Insecta, Odonata) after long-term exposure to PFOS

Perfluorooctane sulfonic acid (PFOS) is a persistent and ubiquitous environmental contaminant that has been detected in organisms worldwide. Here, we evaluate whether long-term (1 and 4 months) exposure to PFOS contamination affects the behavioural performance of freshwater larvae of the damselfly Enallagma cyathigerum (Insecta: Odonata). Our results show reduced behavioural performance with increasing PFOS concentration. In 1 month exposed larvae, no observed effect concentrations (NOECs) were 100 μg/L for general activity. In 4 months exposed larvae, NOECs were 10 μg/L, for each behavioural trait, except swimming acceleration of male larvae where the NOEC was 100 μg/L. When faced with PFOS concentrations above the NOEC, E. cyathigerum larvae were less active, less capable to escape a simulated predator attack and less efficient in foraging. Together, our results show that damselfly larvae suffer reduced survival-related behavioural performance.

A longitudinal study of antipredator behaviour in four successive generations of two populations of captive red junglefowl

Conservation breeding and reintroduction into the wild can only be an effective management tool if behaviours essential for a life in the wild are maintained in captivity. The aim of this study was to investigate how a protected captive environment influences antipredator behaviour over generations. The red junglefowl ( Gallus gallus) was used as a case study. Birds from two different captive populations were followed over four generations. In the last three generations, all birds were hatched and reared in the same indoor settings. Antipredator behaviour was measured in each generation in a standardised test where the birds were exposed to a simulated predator attack. The test was divided into three parts: pre-exposure period, exposure and post-exposure periods. There was an interaction effect between population and generation ( F 3,129 = 4.84, P < 0.01) on behaviour during the pre-exposure period, suggesting that the birds’ “baseline” agitation level may have been altered differently in the two populations. Population differences were also found during the post-exposure period but the populations tended to become more similar over successive generations in their behaviour after the exposure. Furthermore, there were significant effects of generation ( H (d.f. = 1, N = 137) = 10. 94, P < 0.05) as well as population ( H (d.f. = 1, N = 137) = 5.17, P < 0.05) on the immediate reaction to the simulated predator attack. In conclusion, over four successive generations, the two populations altered their antipredator behaviour and tended to become more similar. This study shows that antipredator behaviour may change over generations in a captive environment. This is likely to be one of the most crucial factors for successful reintroduction into the wild and hence, it is a very important aspect to consider for conservation breeding.

Speed and Maneuverability of Adult Loggerhead Turtles (Caretta caretta) under Simulated Predatory Attack: Do The Sexes Differ?

Abstract Sex-biased predation rates have been documented in marine turtles, but no study to date has addressed the causes of such bias. In Shark Bay, male Loggerhead Turtles (Caretta caretta) display evidence of Tiger Shark (Galeocerdo cuvier) attack more often than do females, and sex-specific differences in swim speed or maneuverability have been posited as a possible reason for this pattern. We used simulated shark attacks (boat chases) in shallow water to test this hypothesis. Differences in speed and maneuverability between males and females were not detected, indicating that the heightened vulnerability to predation of male Loggerhead Turtles in Shark Bay requires a different explanation.

Increased predation risk modifies lizard scent‐mark chemicals

Variation in environmental factors plays a central role on organisms' physiological changes. However, the physiological response to predation risk has rarely been investigated in reptiles. Chemical senses are important for intraspecific communication in squamate reptiles. In male lizards Iberolacerta cyreni the maintenance of relative proportions of lipids in femoral gland secretions is costly, which may ensure honest signalling of quality. We hypothesized that increased predation risk should compromise the maintenance of such lipid proportions, as both a fear response and escaping behavior can have physiological consequences. We simulated predator attacks and found that relative proportions of lipids in femoral gland secretions changed in disturbed lizards but not in control ones. Thus, predator-prey interactions may modulate relative concentrations of chemicals in scents of lizards. Potential consequences of this effect on intraspecific chemical communication are suggested.

Spatial learning in the little brown skink, Scincella lateralis: the importance of experience

Previous studies have shown that squamates (lizards and snakes) are capable of spatial learning, but only after extensive training. In nature, squamates' capacity to learn may be better than that suggested by laboratory studies, because they have the opportunity to become familiar with the location of important landmarks and vital resources as they wander through their home range. I conducted three laboratory experiments to test the hypothesis that prior experience with a habitat improves spatial learning in little brown skinks. Individual lizards were subjected to a simulated predatory attack and tested for their ability to take refuge under one of two cardboard retreats (experiment 1) and to choose the ‘correct’ retreat without prior experience (experiment 2) and with 48 h of prior experience (experiment 3) in the ‘habitat’. Although little brown skinks learned to take refuge under cardboard retreats (experiment 1), inexperienced lizards did not learn to take refuge under the ‘correct’ retreat (experiment 2). However, experienced lizards did learn to take refuge under the correct retreat (experiment 3) and did so after only a few trials. I discuss the influence of experience, the ecological relevance of stimuli used in learning experiments, and other methodological issues.

To run or to fly: low cost versus low risk escape strategies in blackbirds

When escaping from predators, ground-foraging birds could choose between two escape strategies with different costs: running or flying. We simulated predator attacks on blackbirds Turdus merula to investigate the factors influencing blackbirds to select between these strategies. The probability that blackbirds would fly increased as flight initiation distance decreased, suggesting that they may trade-off benefits of delaying escape with a costly escape strategy. The probability of flying also increased as the number of potential predators increased, indicating an increase in perceived predation risk with the number of non-attacking predators. Running was more likely to be used in the mornings and flying in the afternoons, suggesting a possible mass-dependent predation risk effect or restrictions in the use of costly escape strategies when energetic reserves are lower. Juvenile blackbirds tended to fly away more often than adults, probably to compensate for their less reliable risk assessments due to lack of experience. We conclude that different factors act independently on choosing an optimal escape strategy, and that the decision about when to escape (flight initiation distance) is associated with the decision about how to escape (escape strategy), which in turn can affect the decision about how far to escape (distance fled).

Impaired escape flight ability in butterflies due to low flight muscle ratio prior to hibernation

For an animal to escape an attacking predator, speed and manoeuvrability are likely to be crucial factors. Previous studies on reptiles and birds have revealed that gaining weight, due to for instance egg load or lipid accumulation, leads to impaired escape ability and possibly increases the risk of being caught by predators. Here we tested whether the flight performance of an insect, the small tortoiseshell butterfly (Aglais urticae), is affected by variations in body mass due to feeding by comparing flight performance parameters between individuals that (i) took flight spontaneously or after being subjected to a simulated predator attack and (ii) varied in flight muscle ratio (FMR: thorax mass/total body mass). The results show that butterflies that were subjected to a simulated predator attack flew at higher velocities and straighter than butterflies that were allowed to take off spontaneously. Furthermore, our study suggests, for the first time, that butterflies may experience impaired escape ability after feeding, which directly leads to a decrease in FMR; a reduction from 0.5 to 0.3 reduced escape flight velocity by about 37% at 0.5 m from the start. Finally, this study shows that FMR affects take-off angle and sinuosity, with steeper angles and more turning in butterflies with low FMR.

Differences in morphology, performance and behaviour between recently diverged populations of Podarcis sicula mirror differences in predation pressure

We investigated the possible role of variation in predation pressure in the phenotypic divergence of two island populations of the Italian wall lizard, Podarcis sicula. In 1971, ten adult specimens from the island of Pod Kopište (Adriatic Sea, Croatia) were transported to the island of Pod Mrčaru, 3.5 km east, where they founded a new population. Although the two islands resemble each other in general physiognomy (size, elevation, microclimate) and in the absence of terrestrial predators, lizards from the newly established population are now on average larger and have shorter hind limbs. They also exhibit lower maximal sprint speed as measured on a racetrack, and fatigue faster when chased in a torus track. In the field, lizards from the original population of Pod Kopište respond to a simulated predatory attack by fleeing at larger approach distances and by running further from the predator than lizards from Pod Mrčaru. These changes in morphology, behaviour and performance may result from the relaxed predation intensity on the latter island. Our analysis of the structural features of the microhabitats suggests that the vegetation on Pod Mrčaru offers more protection to lizards. Also, plasticine models of lizards, laid out on the islands, less often exhibited signs of being attacked by birds on Pod Mrčaru than on Pod Kopište. Our findings provide an example of how changes in (possibly a single) environmental factor may simultaneously produce responses in behaviour, morphology and whole‐animal physiology, and this on a surprisingly small spatial and temporal scale.

Not All Signals are Equal: Male Brown Anole Lizards (Anolis sagrei) Selectively Decrease Pushup Frequency Following a Simulated Predatory Attack

AbstractThe use of conspicuous communication signals often increases a signaler's risk of predation. Many species communicate with a repertoire of signals that may differ in their conspicuousness to predators. Few studies have examined the ability of prey to selectively decrease the use of individual signals in their displays under heightened predation risk. Here, I examined the behavior of male brown anole lizards (Anolis sagrei) in response to a simulated predatory attack from a model kestrel. This species communicates with three major visual signal types, the head‐bob, pushup, and dewlap extension, which vary in their motion and spectral characteristics. I predicted that lizards would decrease frequencies of the dewlap extension and pushup following the attack, but not the head‐bob. Males modulated their use of individual signals by decreasing pushup rates, but not head‐bob rates. Decreases in dewlap frequency were marginally significant. One explanation for these results is that lizards decrease frequencies of signal types based partly on their conspicuousness. The energetic cost of each signal type may be an equally important factor that determines the signaler's response to predators, particularly if a predatory attack is perceived as imminent.

Boldness is influenced by social context in threespine sticklebacks (Gasterosteus aculeatus)

Summary Boldness refers to the extent to which animals balance risk against benefits when engaging in such behaviors as foraging, exploration or resource competition. Evidence suggests that individuals can behave strategically, acting boldly in situations when doing so is adaptive, whilst avoiding risk when the rewards are correspondingly lower. In this study we sought to determine the effects of social context upon the boldness of threespine sticklebacks (Gasterosteus aculeatus). We found that when individuals were tested alone, those that were more active were more likely to resume foraging sooner when subjected to a simulated predator attack in a separate test, and also consumed more prey in foraging competition trials. We found no effect of group size upon the relative ability of individuals to effectively compete for prey. Group size did affect other behaviours however: focal fish were more active and resumed foraging more rapidly when tested in groups that they did when tested alone. Finally, individual social information use was not correlated with behaviour in other contexts. Two competing hypotheses, the adaptation and the constraint hypotheses have been posited to explain the presence and prevalence of individual variation in boldness; our findings offer partial support for the former of these.

Health-dependent vulnerability to predation affects escape responses of unguarded chinstrap penguin chicks

Predators may select more often to attack the more vulnerable prey or those with an inferior health status. Thus, prey should be able to assess their own vulnerability to predation and modify their antipredatory behavior accordingly. When approached by predator skuas, unguarded penguin chicks flee short distances, and usually aggregate in dense packs, but there is a clear interindividual variability in their responses under similar conditions. We hypothesized that this variability in escape responses might be related to the perceived vulnerability to predation of each individual chick. We simulated predator attacks to chinstrap penguin chicks and analyzed the sources of variation in their escape response, such as the presence of adults or the density of other chicks, and the sex, age, body condition, and health status of responding chicks. Chicks allowed shorter approach distances when they had a better health condition (i.e., a greater T-cell-mediated immunity, CMI), when they were younger, and when the density of adults around was higher. Sex and density of other chicks were not important. Similarly, chicks fled from the experimenter to longer distances when they had a lower CMI and when the density of adults was lower. Therefore, escape characteristics of chicks depended on the presence of adults that can deter predators and on the health-dependent vulnerability of chicks.

Pheromone-Induced Priming of a Defensive Response in Western Flower Thrips

The Western flower thrips Frankliniella occidentalis produces conspicuous anal droplets that function as a direct defense against various predators. These droplets also function in pheromonal communication in that they contain a mixture of decyl acetate and dodecyl acetate, which acts as an alarm. Exposure of thrips to synthetic pheromone is known to promote takeoff or refuge seeking, but the effect of the natural pheromone has not yet been studied. Here, we not only studied the response to natural pheromone, but also tested the new hypothesis that the alarm pheromone primes a defensive response in thrips. This test was carried out by measuring the reaction time to a simulated predator attack after exposure to synthetic or natural alarm pheromone (against a control with no pheromone at all). The reaction was quantified in terms of the time it takes a thrips larva to produce a droplet after attack. We found that thrips larvae produce droplets of alarm pheromone faster when cues associated with danger are present. There were no significant differences in reaction times of responses to synthetic pheromone, natural pheromone, or odors from a patch with a predator attacking a thrips larva. This implies that the synthetic pheromone mimics the natural pheromone, and that other cues emanating from the predator play a minor role. We conclude that the alarm pheromone increases the vigilance of the thrips, and this may promote its survival.

Direct Exposure to Corticosterone During Embryonic Development Influences Behaviour in an Ovoviviparous Lizard

AbstractIt is becoming increasingly clear that conditions experienced during embryonic development can be of major importance for traits subsequent to parturition or hatching. For example, in mammals, offspring from stressed mothers show a variety of changes in behavioural, morphological, and life‐history traits. The effects of maternal stress on trait development are believed to be mediated via transfer of glucocorticoids, the main hormones released during the stress response, from mother to offspring. However, also other physiological maternal responses during stress could be responsible for changes in offspring phenotype. We investigated the direct effects of corticosterone on offspring development, without other confounding factors related to increased maternal stress, by injection of corticosterone in eggs of the ovoviviparous lizardLacerta vivipara. Corticosterone‐manipulated offspring did not show impaired development, reduced body size or body condition at parturition. However, corticosterone‐treated offspring showed altered anti‐predator behaviour, as measured by the time required to emerge from shelter after a simulated predator attack. Differential steroid exposure during development, possibly mediated by maternal stress response, may explain some of the variation in behaviour among individuals in natural populations.

Can Wall Lizards Combine Chemical and Visual Cues to Discriminate Predatory from Non‐Predatory Snakes Inside Refuges?

AbstractThe ability to use multiple cues in assessing predation risk is especially important to prey animals exposed to multiple predators. Wall lizards, Podarcis muralis, respond to predatory attacks from birds in the open by hiding inside rock crevices, where they may encounter saurophagous ambush smooth snakes. Lizards should avoid refuges with these snakes, but in refuges lizards can also find non‐saurophagous viperine snakes, which lizards do not need to avoid. We investigated in the laboratory whether wall lizards used different predator cues to detect and discriminate between snake species within refuges. We simulated predatory attacks in the open to lizards, and compared their refuge use, and the variation in the responses after a repeated attack, between predator‐free refuges and refuges containing visual, chemical, or visual and chemical cues of saurophagous or non‐saurophagous snakes. Time to enter a refuge was not influenced by potential risk inside the refuge. In contrast, in a successive second attack, lizards sought cover faster and tended to increase time spent hidden in the refuge. This suggests a case of predator facilitation because persistent predators in the open may force lizards to hide faster and for longer in hazardous refuges. However, after hiding, lizards spent less time in refuges with both chemical and visual cues of snakes, or with chemical cues alone, than in predator‐free refuges or in refuges with snake visual cues alone, but there were no differences in response to the two snake species. Therefore, lizards could be overestimating predation risk inside refuges. We discuss which selection pressures might explain this lack of discrimination of predatory from similar non‐predatory snakes.