萼花臂尾轮虫对晶囊轮虫反捕食行为及形态响应的母体效应

为研究轮虫通过母体效应诱导能否产生行为响应, 以萼花臂尾轮虫(Brachionus calyciflorus)为例, 研究其反捕食漂浮行为响应的母体效应。通过控制轮虫母体在捕食者诱导液中的暴露时间及带卵状态, 收集母体产生的后代, 再将这些后代再次用捕食者诱导液处理, 观察后代的漂浮行为及形态特征。研究发现: 暴露于捕食者诱导液诱导较长时间的母体产生的后代个体, 当再次暴露于捕食者诱导液时, 其产生的行为响应强于没有母体暴露经历的后代; 母体暴露时间越长, 后代形态和行为响应均更加强烈。研究显示萼花臂尾轮虫可通过母体效应产生漂浮行为响应。     

Modeling the Fear Effect in Predator–Prey Interactions with Adaptive Avoidance of Predators

Recent field experiments on vertebrates showed that the mere presence of a predator would cause a dramatic change of prey demography. Fear of predators increases the survival probability of prey, but leads to a cost of prey reproduction. Based on the experimental findings, we propose a predator–prey model with the cost of fear and adaptive avoidance of predators. Mathematical analyses show that the fear effect can interplay with maturation delay between juvenile prey and adult prey in determining the long-term population dynamics. A positive equilibrium may lose stability with an intermediate value of delay and regain stability if the delay is large. Numerical simulations show that both strong adaptation of adult prey and the large cost of fear have destabilizing effect while large population of predators has a stabilizing effect on the predator–prey interactions. Numerical simulations also imply that adult prey demonstrates stronger anti-predator behaviors if the population of predators is larger and shows weaker anti-predator behaviors if the cost of fear is larger.     

Behavioural and life history effects of predator diet cues during ontogeny in damselfly larvae

A central issue in predator–prey interactions is how predator associated chemical cues affect the behaviour and life history of prey. In this study, we investigated how growth and behaviour during ontogeny of a damselfly larva (Coenagrion hastulatum) in high and low food environments was affected by the diet of a predator (Aeshna juncea). We reared larvae in three different predator treatments; no predator, predator feeding on conspecifics and predator feeding on heterospecifics. We found that, independent of food availability, larvae displayed the strongest anti-predator behaviours where predators consumed prey conspecifics. Interestingly, the effect of predator diet on prey activity was only present early in ontogeny, whereas late in ontogeny no difference in prey activity between treatments could be found. In contrast, the significant effect of predator diet on prey spatial distribution was unaffected by time. Larval size was affected by both food availability and predator diet. Larvae reared in the high food treatment grew larger than larvae in the low food treatment. Mean larval size was smallest in the treatment where predators consumed prey conspecifics, intermediate where predators consumed heterospecifics and largest in the treatment without predators. The difference in mean larval size between treatments is probably an effect of reduced larval feeding, due to behavioural responses to chemical cues associated with predator diet. Our study suggests that anti-predator responses can be specific for certain stages in ontogeny. This finding shows the importance of considering where in its ontogeny a study organism is before results are interpreted and generalisations are made. Furthermore, this finding accentuates the importance of long-term studies and may have implications for how results generated by short-term studies can be used.     

Predator–prey interactions and metabolic rates are altered in stable and unstable groups in a social fish

Understanding the determinants and consequences of predation effort, success and prey responses is important since these factors affect the fitness of predators and prey. When predators are also invasive species, the impacts on prey can be particularly far-reaching with ultimate ecosystem-level consequences. However, predators are typically viewed as behaviourally fixed within this interaction and it is unclear how variation in predator social dynamics affects predator–prey interactions. Using the invasive eastern mosquitofish Gambusia holbrooki and a native glass shrimp Paratya australiensis in Australia, we investigated how varying levels of social conflict within predator groups influences predator–prey interactions. By experimentally manipulating group stability of G. holbrooki, we show that rates of social conflict were lower in groups with large size differences, but that routine metabolic rates were higher in groups with large size differences. Predation effort and success did not vary depending on group stability, but in stable groups predation effort by aggressive dominants was greater than subordinates. The anti-predator responses of prey to the stability of predator groups were mixed. While more prey utilized shelters when exposed to stable compared to unstable groups of predators, a greater proportion were sedentary when predator groups were unstable. Overall, this study demonstrates predator group stability is modulated by differences in body size and can influence prey responses. Further, it reveals a hidden metabolic cost of living in stable groups despite reduced overt social conflict. For invasive species management, it is therefore important to consider the behavioural and physiological plasticity of the invasive predators, whose complex social interactions and metabolic demands can modulate patterns of predator–prey interactions.     

Interspecific infanticide deters predators

It is well known that young, small predator stages are vulnerable to predation by conspecifics, intra-guild competitors or hyperpredators. It is less known that prey can also kill vulnerable predator stages that present no danger to the prey. Since adult predators are expected to avoid places where their offspring would run a high predation risk, this opens the way for potential prey to deter dangerous predator stages by killing vulnerable predator stages. We present an example of such a complex predator–prey interaction. We show that (1) the vulnerable stage of an omnivorous arthropod prey discriminates between eggs of a harmless predator species and eggs of a dangerous species, killing more eggs of the latter; (2) prey suffer a minor predation risk from newly hatched predators; (3) adult predators avoid ovipositing near killed predator eggs, and (4) vulnerable prey near killed predator eggs experience an almost fourfold reduction of predation. Hence, by attacking the vulnerable stage of their predator, prey deter adult predators and thus reduce their own predation risk. This provides a novel explanation for the killing of vulnerable stages of predators by prey and adds a new dimension to anti-predator behaviour.     

Generalization of predator recognition: Velvet geckos display anti-predator behaviours in response to chemicals from non-dangerous elapid snakes

Many prey species detect chemical cues from predators and modify their behaviours in ways that reduce their risk of predation. Theory predicts that prey should modify their anti-predator responses according to the degree of threat posed by the predator. That is, prey should show the strongest responses to chemicals of highly dangerous prey, but should ignore or respond weakly to chemicals from non-dangerous predators. However, if anti-predator behaviours are not costly, and predators are rarely encountered, prey may exhibit generalised antipredator behaviours to dangerous and non-dangerous predators. In Australia, most elapid snakes eat lizards, and are therefore potentially dangerous to lizard prey. Recently, we found that the nocturnal velvet gecko Oedura lesueurii responds to chemicals from dangerous and non-dangerous elapid snakes, suggesting that it displays gen-eralised anti-predator behaviours to chemicals from elapid snakes. To explore the generality of this result, we videotaped the be-haviour of velvet geckos in the presence of chemical cues from two small elapid snakes that rarely consume geckos: the nocturnal golden-crowned snake Cacophis squamulosus and the diurnal marsh snake Hemiaspis signata. We also videotaped geckos in tri-als involving unsceted cards (controls) and cologne-scented cards (pungency controls). In trials involving Cacophis and Hemi-aspis chemicals, 50% and 63% of geckos spent long time periods (> 3 min) freezing whilst pressed flat against the substrate, re-spectively. Over half the geckos tested exhibited anti-predator behaviours (tail waving, tail vibration, running) in response to Ca-cophis (67%) or Hemiaspis (63%) chemicals. These behaviours were not observed in control or pungency control trials. Our re-sults support the idea that the velvet gecko displays generalised anti-predator responses to chemical cues from elapid snakes. Generalised responses to predator chemicals may be common in prey species that co-occur with multiple, ecologically similar, dangerous predators.     

Behavioral responses of native prey to disparate predators: naiveté and predator recognition

It is widely accepted that predator recognition and avoidance are important behaviors in allowing prey to mitigate the impacts of their predators. However, while prey species generally develop anti-predator behaviors through coevolution with predators, they sometimes show accelerated adoption of these behaviors under strong selection pressure from novel species. We used a field manipulation experiment to gauge the ability of the common ringtail possum (Pseudocheirus peregrinus), a semi-arboreal Australian marsupial, to recognize and respond to olfactory cues of different predator archetypes. We predicted that ringtails would display stronger anti-predator behaviors to cues of the invasive European red fox (Vulpes vulpes) in areas where fox impacts had been greatest, and to cues of the native lace monitor (Varanus varius) in areas of sympatry compared with allopatry. We found that ringtails fled quickly and were more alert when exposed to the fecal odors of both predators compared to neutral and pungent control odors, confirming that predator odors are recognized and avoided. However, these aversive responses were similar irrespective of predator presence or level of impact. These results suggest that selection pressure from the fox has been sufficient for ringtails to develop anti-predator behaviors over the few generations since foxes have become established. In contrast, we speculate that aversive responses by ringtails to the lace monitor in areas where this predator is absent reflect recent coexistence of the two species. We conclude that rapid evolution of anti-predator behaviors may occur when selection is strong. The maintenance of these behaviors should allow re-establishment of predator–prey relationships if the interactants regain sympatry via range shifts or management actions to reintroduce them to their former ranges.     

Anti-predator behaviour in response to conspecific chemical alarm cues in an esociform fish, <Emphasis Type="Italic">Umbra limi</Emphasis> (Kirtland 1840)

When a predators attack prey, damaged prey tissue releases chemical information that reliably indicates an actively foraging predator. Prey use these semiochemicals to cue anti-predator behaviour and reduce their probability of predation. Here, we test central mudminnows, Umbra limi (Kirtland 1840), for anti-predator behavioural responses to chemical cues in conspecific skin extract. In a field experiment, traps scented with mudminnow skin extract (alarm cue) caught fewer mudminnows than traps scented with water (control). Under controlled laboratory conditions, mudminnows showed a significant reduction in activity and movement to the bottom in response to alarm cues relative to water controls. Reduced activity and increased time on the bottom of the tank are both known components of an anti-predator response. Thus, based on field and lab data, mudminnows exhibited anti-predator behavioural responses to chemical alarm cues released by damaged epidermal tissue. Histological preparations of epidermal tissue did not reveal the presence of specialised “alarm substance” cells for the production of chemical alarm cues. This is the first report of an alarm reaction in an esociform, an order with a long evolutionary history of piscivory.     

四种鲤科鱼类对捕食胁迫行为响应的种间比较

为了比较早期捕食胁迫经历和当前环境中存在的捕食者对鱼类行为的影响, 并考查这些影响是否存在种间差异, 研究分别考查了测定环境(有、无捕食者存在)对有、无捕食胁迫经历的鳊(Parabramis pekinensis)、草鱼(Ctenopharyngodon idellus)、鲫(Carassius auratus)和中华倒刺鲃(Spinibarbus sinensis)等4种鲤科鱼类探索性、活跃性和勇敢性的影响。结果发现: 早期捕食胁迫经历与当前环境条件对鱼类行为产生截然不同的影响, 且存在较大的种间差异。无捕食胁迫经历的鳊、草鱼和中华倒刺鲃均会对陌生的捕食者乌鳢(Channa argus)做出行为响应, 提示这3种鱼可能对陌生捕食者具有一定的识别能力, 但这种识别与猎物鱼通过捕食胁迫经历获得的识别仍具有一定差距; 具有捕食胁迫经历的鳊和中华倒刺鲃在空白环境中未表现出反捕食行为, 可能是节约能量的一种策略。总体而言, 草鱼对捕食胁迫经历和测定环境处理反应更为敏感, 而中华倒刺鲃的反应则相对保守。但当周围环境中存在捕食者时, 4种鲤科鱼类均会通过维持较高运动状态的方式来应对捕食者。维持这种应激状态可能对猎物鱼保持与捕食者的距离, 并随时保持警惕较为关键。     

A community-level evaluation of the impact of prey behavioural and ecological characteristics on predator diet composition

Although predation avoidance is the most commonly invoked explanation for vertebrate social evolution, there is little evidence that individuals in larger groups experience lower predation rates than those in small groups. We compare the morphological and behavioural traits of mammal prey species in the Taï forest, Ivory Coast, with the diet preferences of three of their non-human predators: leopards, chimpanzees and African crowned eagles. Individual predators show marked differences in their predation rates on prey species of different body sizes, but clear patterns with prey behaviour were apparent only when differences in prey habitat use were incorporated into the analyses. Leopard predation rates are highest for terrestrial species living in smaller groups, whereas eagle predation rates are negatively correlated with group size only among arboreal prey. When prey predation rates are summed over all three predators, terrestrial species incur higher predation rates than arboreal species and, within both categories, predation rates decline with increasing prey group size and decreasing density of groups in the habitat. These results reveal that it is necessary to consider anti-predator strategies in the context of a dynamic behavioural interaction between predators and prey.     

The temporal selfish herd: predation risk while aggregations form

The hypothesis of the selfish herd has been highly influential to our understanding of animal aggregation. Various movement strategies have been proposed by which individuals might aggregate to form a selfish herd as a defence against predation, but although the spatial benefits of these strategies have been extensively studied, little attention has been paid to the importance of predator attacks that occur while the aggregation is forming. We investigate the success of mutant aggregation strategies invading populations of individuals using alternative strategies and find that the invasion dynamics depend critically on the time scale of movement. If predation occurs early in the movement sequence, simpler strategies are likely to prevail. If predators attack later, more complex strategies invade. If there is variation in the timing of predator attacks (through variation within or between individual predators), we hypothesize that groups will consist of a mixture of strategies, dependent upon the distribution of predator attack times. Thus, behavioural diversity can evolve and be maintained in populations of animals experiencing a diverse range of predators differing solely in their attack behaviour. This has implications for our understanding of predator–prey dynamics, as the timing of predator attacks will exert selection pressure on prey behavioural responses, to which predators must respond.     

The anatomy of predator-prey dynamics in a changing climate

Humans are increasingly influencing global climate and regional predator assemblages, yet a mechanistic understanding of how climate and predation interact to affect fluctuations in prey populations is currently lacking. Here we develop a modelling framework to explore the effects of different predation strategies on the response of age-structured prey populations to a changing climate. We show that predation acts in opposition to temporal correlation in climatic conditions to suppress prey population fluctuations. Ambush predators such as lions are shown to be more effective at suppressing fluctuations in their prey than cursorial predators such as wolves, which chase down prey over long distances, because they are more effective predators on prime-aged adults. We model climate as a Markov process and explore the consequences of future changes in climatic autocorrelation for population dynamics. We show that the presence of healthy predator populations will be particularly important in dampening prey population fluctuations if temporal correlation in climatic conditions increases in the future.     

Rapid acquisition of an alarm response by a neotropical primate to a newly introduced avian predator

Predation is an important selective pressure in natural ecosystems. Among non-human primates, relatively little is known about how predators hunt primate prey and how primates acquire adaptive responses to counteract predation. In this study we took advantage of the recent reintroduction of radio-tagged harpy eagles (Harpia harpyja) to Barro Colorado Island (BCI), Panama to explore how mantled howler monkeys (Alouatta palliata), one of their primary prey, acquire anti-predator defences. Based on the observation that harpies follow their prey prior to attack, and often call during this pursuit period, we broadcast harpy eagle calls to howlers on BCI as well as to a nearby control population with no harpy predation. Although harpies have been extinct from this area for 50-100 years, results indicate that BCI howlers rapidly acquired an adaptive anti-predator response to harpy calls, while showing no response to other avian vocalizations; howlers maintained this response several months after the removal of the eagles. These results not only show that non-human primates can rapidly acquire an alarm response to a newly introduced predator, but that they can detect and identify predators on the basis of acoustic cues alone. These findings have significant implications both for the role of learning mechanisms in the evolution of prey defence and for conservation strategies, suggesting that the use of 'probing' approaches, such as auditory playbacks, may highly enhance an a priori assessment of the impact of species reintroduction.     

Effects of an infectious fungus, Batrachochytrium dendrobatidis, on amphibian predator-prey interactions

The effects of parasites and pathogens on host behaviors may be particularly important in predator-prey contexts, since few animal behaviors are more crucial for ensuring immediate survival than the avoidance of lethal predators in nature. We examined the effects of an emerging fungal pathogen of amphibians, Batrachochytrium dendrobatidis, on anti-predator behaviors of tadpoles of four frog species. We also investigated whether amphibian predators consumed infected prey, and whether B. dendrobatidis caused differences in predation rates among prey in laboratory feeding trials. We found differences in anti-predator behaviors among larvae of four amphibian species, and show that infected tadpoles of one species (Anaxyrus boreas) were more active and sought refuge more frequently when exposed to predator chemical cues. Salamander predators consumed infected and uninfected tadpoles of three other prey species at similar rates in feeding trials, and predation risk among prey was unaffected by B. dendrobatidis. Collectively, our results show that even sub-lethal exposure to B. dendrobatidis can alter fundamental anti-predator behaviors in some amphibian prey species, and suggest the unexplored possibility that indiscriminate predation between infected and uninfected prey (i.e., non-selective predation) could increase the prevalence of this widely distributed pathogen in amphibian populations. Because one of the most prominent types of predators in many amphibian systems is salamanders, and because salamanders are susceptible to B. dendrobatidis, our work suggests the importance of considering host susceptibility and behavioral changes that could arise from infection in both predators and prey.     

Metamorphosing reef fishes avoid predator scent when choosing a home

Most organisms possess anti-predator adaptations to reduce their risk of being consumed, but little is known of the adaptations prey employ during vulnerable life-history transitions when predation pressures can be extreme. We demonstrate the use of a transition-specific anti-predator adaptation by coral reef fishes as they metamorphose from pelagic larvae to benthic juveniles, when over half are consumed within 48 h. Our field experiment shows that naturally settling damselfish use olfactory, and most likely innate, predator recognition to avoid settling to habitat patches manipulated to emit predator odour. Settlement to patches emitting predator odour was on average 24-43% less than to control patches. Evidence strongly suggests that this avoidance of sedentary and patchily distributed predators by nocturnal settlers will gain them a survival advantage, but also lead to non-lethal predator effects: the costs of exhibiting anti-predator adaptations. Transition-specific anti-predator adaptations, such as demonstrated here, may be widespread among organisms with complex life cycles and play an important role in prey population dynamics.     

Background evolution in camouflage systems: A predator-prey/pollinator-flower game

A common predator or anti-predator strategy involves camouflage based on background matching. In some systems, the background is an organism whose fitness is affected by the predator-prey interaction. In these cases, the phenotype of the background species may evolve to affect the degree of background matching in the predator-prey interaction. For example, some flower species (the background) are inhabited by camouflaged ambush predators that attack visiting pollinators. These flowers have a fitness interest in the outcome of the predator-prey interaction because flowers depend on pollinator visitations for reproduction. Therefore, floral colour might evolve relative to predator colour so as to influence the detectability of resident predators. I have created a three-player game, based on Signal Detection Theory, to model the co-evolution of predator and prey/pollinator behavioural strategies with floral colour. This model makes two general predictions: (1) Constraints on predator distributions favour the evolution of flowers that match the predators’ colour because they prevent predators from overexploiting these flowers; (2) factors that produce less discriminating pollinators also favour the evolution of flowers that match the predators’ colour because these pollinators are willing to land on these flowers even if the safety of the flower is in doubt.     

Plastic Responses of a Sessile Prey to Multiple Predators: A Field and Experimental Study

Background

Theory predicts that prey facing a combination of predators with different feeding modes have two options: to express a response against the feeding mode of the most dangerous predator, or to express an intermediate response. Intermediate phenotypes protect equally well against several feeding modes, rather than providing specific protection against a single predator. Anti-predator traits that protect against a common feeding mode displayed by all predators should be expressed regardless of predator combination, as there is no need for trade-offs.

Principal Findings

We studied phenotypic anti-predator responses of zebra mussels to predation threat from a handling-time-limited (crayfish) and a gape-size-limited (roach) predator. Both predators dislodge mussels from the substrate but diverge in their further feeding modes. Mussels increased expression of a non-specific defense trait (attachment strength) against all combinations of predators relative to a control. In response to roach alone, mussels showed a tendency to develop a weaker and more elongated shell. In response to crayfish, mussels developed a harder and rounder shell. When exposed to either a combination of predators or no predator, mussels developed an intermediate phenotype. Mussel growth rate was positively correlated with an elongated weaker shell and negatively correlated with a round strong shell, indicating a trade-off between anti-predator responses. Field observations of prey phenotypes revealed the presence of both anti-predator phenotypes and the trade-off with growth, but intra-specific population density and bottom substrate had a greater influence than predator density.

Conclusions

Our results show that two different predators can exert both functionally equivalent and inverse selection pressures on a single prey. Our field study suggests that abiotic factors and prey population density should be considered when attempting to explain phenotypic diversity in the wild.     

The ecology of fear and inverted biomass pyramids

In inverted biomass pyramids (IBPs) prey are outnumbered by their predators when measured by biomass. We investigate how prey should behave in the face of danger from higher predator biomass, and how anti-predator behavior (in the form of vigilance) can, in turn, affect the predator–prey system. In this study, we incorporate anti-predator behaviors into a Lotka–Volterra predator–prey model in the form of fixed and facultative vigilance. Facultative vigilance models behavior as a dynamic foraging game, allowing us to assess optimal behavioral responses in the context of IBPs using a dynamical fitness optimization approach. We model vigilance as a tradeoff between safety and either the prey's maximum growth rate or its carrying capacity. We assess the population dynamics of predators and prey with fear responses, and investigate the role fear plays on trophic structure. We found that the ecology of fear plays an important role in predator–prey systems, impacting trophic structure and the occurrence of IBPs. Fixed vigilance works against IBP structure by always reducing the predator–prey biomass ratio at equilibrium with increasing levels of vigilance. Facultative vigilance can actually promote IBPs, as prey can now adjust their vigilance levels to cope with increased predation and the costs associated with vigilance. This is especially true when the effectiveness of vigilance is low and predators are very lethal. In general, these trends are true whether the costs of vigilance are felt on the prey's maximum growth rate or its carrying capacity. Just as the ecology of fear, when first introduced, was used to explain why top carnivores are rare in terrestrial systems, it can also be used to understand how big fierce predators can be common in IBPs.     

Fear in animals: a meta-analysis and review of risk assessment

The amount of risk animals perceive in a given circumstance (i.e. their degree of 'fear') is a difficult motivational state to study. While many studies have used flight initiation distance as a proxy for fearfulness and examined the factors influencing the decision to flee, there is no general understanding of the relative importance of these factors. By identifying factors with large effect sizes, we can determine whether anti-predator strategies reduce fear, and we gain a unique perspective on the coevolution of predator and anti-predator behaviour. Based on an extensive review and formal meta-analysis, we found that predator traits that were associated with greater risk (speed, size, directness of approach), increased prey distance to refuge and experience with predators consistently amplified the perception of risk (in terms of flight initiation distance). While fish tolerated closer approach when in larger schools, other taxa had greater flight initiation distances when in larger groups. The presence of armoured and cryptic morphologies decreased perception of risk, but body temperature in lizards had no robust effect on flight initiation distance. We find that selection generally acts on prey to be sensitive to predator behaviour, as well as on prey to modify their behaviour and morphology.     

Predator-prey shell games: large-scale movement and its implications for decision-making by prey

Many classical models of food patch use under predation risk assume that predators impose patch-specific predation risks independent of prey behavior. These models predict that prey should leave a chosen patch only if and when the food depletes below some critical level. In nature, however, prey individuals may regularly move among food patches, even in the apparent absence of food depletion. We suggest that such prey movement is part of a predator-prey "shell game", in which predators attempt to learn prey location, and the prey attempt to be unpredictable in space. We investigate this shell game using an individual-based model that allows predators to update information about prey location, and permits prey to move with some random component among patches, but with reduced energy intake. Our results show the best prey strategy depends on what the predator does. A non-learning (randomly moving) predator favors non-moving prey – moving prey suffer higher starvation and predation. However, a learning predator favors prey movement. In general, the best prey strategy involves movement biased toward, but not completely committed to, the richer food patch. The strategy of prey movement remains beneficial even in combination with other anti-predator defenses, such as prey vigilance.