Quantitative analysis of fiddler crab flock movement: evidence for ‘selfish herd’ behaviour

The selfish herd hypothesis predicts that aggregations form because individuals move towards one another, and that this movement will minimize predation risk as measured by the domain of danger. To test the predictions of the selfish herd hypothesis in the field, we videotaped the movements of sand fiddler crab, Uca pugilator, flocks being attacked by predators. After recording 12 attacks on crabs by shorebird and human attackers, we digitized the video, and determined the positions of crabs before and after being frightened. We estimated the time of panic initiation by the rapid increase in the crabs' velocity. Crab flocks became more cohesive after panic initiation. The frequency distribution of the crabs' domains of danger shifted significantly towards smaller domains after panic initiation. The median domain of danger was significantly lower after panic initiation than beforehand. Two other indices of aggregation also showed statistically significant increases in flock cohesion following panic initiation. We conclude that fiddler crab behaviour is consistent with the selfish herd hypothesis. Therefore, our results support the selfish herd hypothesis as an explanation for gregarious behaviour. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Predation risk as a driving force for phenotypic assortment: a cross-population comparison

Frequency-dependent predation has been proposed as a general mechanism driving the phenotypic assortment of social groups via the ‘oddity effect’, which occurs when the presence of odd individuals in a group allows a predator to fixate on a single prey item, increasing the predator''s attack-to-kill ratio. However, the generality of the oddity effect has been debated and, previously, there has not been an ecological assessment of the role of predation risk in driving the phenotypic assortment of social groups. Here, we compare the levels of body length assortment of social groups between populations of the Trinidadian guppy (Poecilia reticulata) that experience differences in predation risk. As predicted by the oddity effect hypothesis, we observe phenotypic assortment by body length to be greater under high predation risk. However, we found that a number of low-predation populations were also significantly assorted by body length, suggesting that other mechanisms may have a role to play.     

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.     

Linking predator risk and uncertainty to adaptive forgetting: a theoretical framework and empirical test using tadpoles

Hundreds of studies have examined how prey animals assess their risk of predation. These studies work from the basic tennet that prey need to continually balance the conflicting demands of predator avoidance with activities such as foraging and reproduction. The information that animals gain regarding local predation risk is most often learned. Yet, the concept of ‘memory’ in the context of predation remains virtually unexplored. Here, our goal was (i) to determine if the memory window associated with predator recognition is fixed or flexible and, if it is flexible, (ii) to identify which factors affect the length of this window and in which ways. We performed an experiment on larval wood frogs, Rana sylvatica, to test whether the risk posed by, and the uncertainty associated with, the predator would affect the length of the tadpoles'' memory window. We found that as the risk associated with the predator increases, tadpoles retained predator-related information for longer. Moreover, if the uncertainty about predator-related information increases, then prey use this information for a shorter period. We also present a theoretical framework aiming at highlighting both intrinsic and extrinsic factors that could affect the memory window of information use by prey individuals.     

Evaluating the summer landscapes of predation risk and forage quality for elk (Cervus canadensis)

The recovery of carnivore populations in North American has consequences for trophic interactions and population dynamics of prey. In addition to direct effects on prey populations through killing, predators can influence prey behavior by imposing the risk of predation. The mechanisms through which patterns of space use by predators are linked to behavioral response by prey and nonconsumptive effects on prey population dynamics are poorly understood. Our goal was to characterize population‐ and individual‐level patterns of resource selection by elk (Cervus canadensis) in response to risk of wolves (Canis lupus) and mountain lions (Puma concolor) and evaluate potential nonconsumptive effects of these behavioral patterns. We tested the hypothesis that individual elk risk‐avoidance behavior during summer would result in exposure to lower‐quality forage and reduced body fat and pregnancy rates. First, we evaluated individuals'' second‐order and third‐order resource selection with a used‐available sampling design. At the population level, we found evidence for a positive relationship between second‐ and third‐order selection and forage, and an interaction between forage quality and mountain lion risk such that the relative probability of use at low mountain lion risk increased with forage quality but decreased at high risk at both orders of selection. We found no evidence of a population‐level trade‐off between forage quality and wolf risk. However, we found substantial among‐individual heterogeneity in resource selection patterns such that population‐level patterns were potentially misleading. We found no evidence that the diversity of individual resource selection patterns varied predictably with available resources, or that patterns of individual risk‐related resource selection translated into biologically meaningful changes in body fat or pregnancy rates. Our work highlights the importance of evaluating individual responses to predation risk and predator hunting technique when assessing responses to predators and suggests nonconsumptive effects are not operating at a population scale in this system.     

Mechanisms for aggregation in animals: rule success depends on ecological variables

Under the threat of predation, animals often group tightly together,with all group members benefiting from a reduction in predationrisk through various mechanisms, including the dilution, encounter-dilution,and predator confusion effects. Additionally, the selfish herdhypothesis was first put forward by Hamilton (1971). He proposedthat in order to reduce its risk of predation, an individualshould approach its nearest neighbor, reducing its risk at theexpense of those around it. Despite extensive empirical support,the selfish herd hypothesis has been criticized on theoreticalgrounds: approaching the nearest neighbor does not result inthe observed dense aggregations, and the nearest neighbor inspace is not necessarily the one that can be reached fastest.Increasingly complex movement rules have been proposed, successfullyproducing dense aggregations of individuals. However, no studyto date has made a full comparison of the different proposedmovement rules within the same modeling environment. Further,ecologically relevant parameters, such as the size and densityof a population or group and the time it takes a predator toattack, have thus far been ignored. Here, we investigate thereduction in risk for animals aggregating using different strategiesand demonstrate the importance of ecological parameters on riskreduction in group-living animals. We find that complex rulesare most successful at reducing risk in small, compact populations,whereas simpler rules are most successful in larger, low-densitypopulations, and when predators attack quickly after being detectedby their prey.     

The response of a selfish herd to an attack from outside the group perimeter

According to the selfish herd hypothesis, animals can decrease predation risk by moving toward one another if the predator can appear anywhere and will attack the nearest target. Previous studies have shown that aggregations can form using simple movement rules designed to decrease each animal's Domain of Danger. However, if the predator attacks from outside the group's perimeter, these simple movement rules might not lead to aggregation. To test whether simple selfish movement rules would decrease predation risk for those situations when the predator attacks from outside the flock perimeter, we constructed a computer model that allowed flocks of 75 simulated fiddler crabs to react to one another, and to a predator attacking from 7 m away. We attacked simulated crab flocks with predators of different sizes and attack speeds, and computed relative predation risk after 120 time steps. Final trajectories showed flight toward the center of the flock, but curving away from the predator. Path curvature depended on the predator's size and approach speed. The average crab experienced a greater decrease in predation risk when the predator was small or slow moving. Regardless of the predator's size and speed, however, predation risk always decreased as long as crabs took their flock-mates into account. We conclude that, even when flight away from an external predator occurs, the selfish avoidance of danger can lead to aggregation.     

Mesopredator suppression by an apex predator alleviates the risk of predation perceived by small prey

Predators can impact their prey via consumptive effects that occur through direct killing, and via non-consumptive effects that arise when the behaviour and phenotypes of prey shift in response to the risk of predation. Although predators'' consumptive effects can have cascading population-level effects on species at lower trophic levels there is less evidence that predators'' non-consumptive effects propagate through ecosystems. Here we provide evidence that suppression of abundance and activity of a mesopredator (the feral cat) by an apex predator (the dingo) has positive effects on both abundance and foraging efficiency of a desert rodent. Then by manipulating predators'' access to food patches we further the idea that apex predators provide small prey with refuge from predation by showing that rodents increased their habitat breadth and use of ‘risky′ food patches where an apex predator was common but mesopredators rare. Our study suggests that apex predators'' suppressive effects on mesopredators extend to alleviate both mesopredators'' consumptive and non-consumptive effects on prey.     

Prey state shapes the effects of temporal variation in predation risk

The ecological impacts of predation risk are influenced by how prey allocate foraging effort across periods of safety and danger. Foraging decisions depend on current danger, but also on the larger temporal, spatial or energetic context in which prey manage their risks of predation and starvation. Using a rocky intertidal food chain, we examined the responses of starved and fed prey (Nucella lapillus dogwhelks) to different temporal patterns of risk from predatory crabs (Carcinus maenas). Prey foraging activity declined during periods of danger, but as dangerous periods became longer, prey state altered the magnitude of risk effects on prey foraging and growth, with likely consequences for community structure (trait-mediated indirect effects on basal resources, Mytilus edulis mussels), prey fitness and trophic energy transfer. Because risk is inherently variable over time and space, our results suggest that non-consumptive predator effects may be most pronounced in productive systems where prey can build energy reserves during periods of safety and then burn these reserves as ‘trophic heat’ during extended periods of danger. Understanding the interaction between behavioural (energy gain) and physiological (energy use) responses to risk may illuminate the context dependency of trait-mediated trophic cascades and help explain variation in food chain length.     

Prey bacteria shape the community structure of their predators

Although predator–prey interactions among higher organisms have been studied extensively, only few examples are known for microbes other than protists and viruses. Among the bacteria, the most studied obligate predators are the Bdellovibrio and like organisms (BALOs) that prey on many other bacteria. In the macroscopical world, both predator and prey influence the population size of the other''s community, and may have a role in selection. However, selective pressures among prey and predatory bacteria have been rarely investigated. In this study, Bacteriovorax, a predator within the group of BALOs, in environmental waters were fed two prey bacteria, Vibrio vulnificus and Vibrio parahaemolyticus. The two prey species yielded distinct Bacteriovorax populations, evidence that selective pressures shaped the predator community and diversity. The results of laboratory experiments confirmed the differential predation of Bacteriovorax phylotypes on the two bacteria species. Not only did Bacteriovorax Cluster IX exhibit the versatility to be the exclusive efficient predator on Vibrio vulnificus, thereby, behaving as a specialist, but was also able to prey with similar efficiency on Vibrio parahaemolyticus, indicative of a generalist. Therefore, we proposed a designation of versatilist for this predator. This initiative should provide a basis for further efforts to characterize the predatory patterns of bacterial predators. The results of this study have revealed impacts of the prey on Bacteriovorax predation and in structuring the predator community, and advanced understanding of predation behavior in the microbial world.     

Predator-driven fragmentation of fiddler crab droves into selfish miniherds of biased composition

An explanation for animal groups is the selfish herd, characterized by aggregation as each member tries to shield itself from a predator by moving into a tight gap between other members. We test the hypotheses that: (1) droves, the large feeding groups of fiddler crabs, are selfish herds; (2) the miniherds that form when droves fragment on approach of a large predator are selfish herds; (3) selfish herds form when refugia are unlikely to be reached before an approaching predator arrives; and (4) the composition of selfish miniherds is biased toward individuals most vulnerable to predation. The study was conducted in South Carolina (USA) by videotaping the movements of sand fiddler crabs Uca pugilator when approached by a human predator. In both droves and miniherds, interindividual distance decreases with predator approach, consistent with behavior in a selfish herd. However, two other expectations for selfish herds—herd cohesion and sacrificing distance from the predator in order to get closer to other herders—are only met in miniherds. Crabs farther from refugia are more likely to form and remain in miniherds, indicating that selfish herding is only favored when refugia cannot be quickly reached. The composition of the smallest miniherds, consisting of 2-18 crabs, is biased toward females and small males. These individuals may be more vulnerable to predation because they lack the enlarged claw of large males that deters some predators. The small miniherds are relatively homogeneous with respect to the size and sex of their members, which may enhance cohesion and effectiveness as selfish herds. Miniherds will be effective selfish groups when predator attack has a significant vertical component and when the strike distance is large relative to both the size of the prey and the distance between group members. Droves are not selfish herds but permit crabs to flee feeding grounds as members of selfish miniherds.     

The visual ecology of selective predation: Are unhealthy hosts less stealthy hosts?

Predators can strongly influence disease transmission and evolution, particularly when they prey selectively on infected hosts. Although selective predation has been observed in numerous systems, why predators select infected prey remains poorly understood. Here, we use a mathematical model of predator vision to test a long‐standing hypothesis about the mechanistic basis of selective predation in a Daphnia–microparasite system, which serves as a model for the ecology and evolution of infectious diseases. Bluegill sunfish feed selectively on Daphnia infected by a variety of parasites, particularly in water uncolored by dissolved organic carbon. The leading hypothesis for selective predation in this system is that infection‐induced changes in the transparency of Daphnia render them more visible to bluegill. Rigorously evaluating this hypothesis requires that we quantify the effect of infection on the visibility of prey from the predator''s perspective, rather than our own. Using a model of the bluegill visual system, we show that three common parasites, Metschnikowia bicuspidata, Pasteuria ramosa, and Spirobacillus cienkowskii, decrease the transparency of Daphnia, rendering infected Daphnia darker against a background of bright downwelling light. As a result of this increased brightness contrast, bluegill can see infected Daphnia at greater distances than uninfected Daphnia—between 19% and 33% further, depending on the parasite. Pasteuria and Spirobacillus also increase the chromatic contrast of Daphnia. These findings lend support to the hypothesis that selective predation by fish on infected Daphnia could result from the effects of infection on Daphnia''s visibility. However, contrary to expectations, the visibility of Daphnia was not strongly impacted by water color in our model. Our work demonstrates that models of animal visual systems can be useful in understanding ecological interactions that impact disease transmission.     

Geometry for mutualistic and selfish herds: the limited domain of danger

We present a two-dimensional individual-based model of aggregation behaviour in animals by introducing the concept of a "limited domain of danger", which represents either a limited detection range or a limited attack range of predators. The limited domain of danger provides a suitable framework for the analysis of individual movement rules under real-life conditions because it takes into account the predator's prey detection and capture abilities. For the first time, a single geometrical construct can be used to analyse the predation risk of both peripheral and central individuals in a group. Furthermore, our model provides a conceptual framework that can be equally applied to aggregation behaviour and refuge use and thus presents a conceptual advance on current theory that treats these antipredator behaviours separately. An analysis of individual movement rules using limited domains of danger showed that the time minimization strategy outcompetes the nearest neighbour strategy proposed by Hamilton's (J. Theor. Biol. 31 (1971) 295) selfish herd model, whereas a random strategy confers no benefit and can even be disadvantageous. The superior performance of the time minimization strategy highlights the importance of taking biological constraints, such as an animal's orientation relative to its neighbours, into account when searching for efficient movement rules underlying the aggregation process.     

Predator cannibalism can shift prey community composition toward dominance by small prey species

Cannibalism among predators is a key intraspecific interaction affecting their density and foraging behavior, eventually modifying the strength of predation on heterospecific prey. Interestingly, previous studies showed that cannibalism among predators can increase or reduce predation on heterospecific prey; however, we know less about the factors that lead to these outcomes. Using a simple pond community consisting of Hynobius retardatus salamander larvae and their associated prey, I report empirical evidence that cannibalism among predators can increase predation on large heterospecific prey but reduce that on small heterospecific prey. In a field‐enclosure experiment in which I manipulated the occurrence of salamander cannibalism, I found that salamander cannibalism increased predation on frog tadpoles but reduced that on aquatic insects simultaneously. The contrasting effects are most likely to be explained by prey body size. In the study system, frog tadpoles were too large for non‐cannibal salamanders to consume, while aquatic insects were within the non‐cannibals’ consumable prey size range. However, when cannibalism occurred, a few individuals that succeeded in cannibalizing reached large enough size to consume frog tadpoles. Consequently, although cannibalism among salamanders reduced their density, salamander cannibalism increased predation on large prey frog tadpoles. Meanwhile, salamander cannibalism reduced predation on small prey aquatic insects probably because of a density reduction of non‐cannibals primarily consuming aquatic insects. Body size is often correlated with various ecological traits, for instance, diet width, consumption, and excretion rates, and is thus considered a good indicator of species’ effects on ecosystem function. All this considered, cannibalism among predators could eventually affect ecosystem function by shifting the size composition of the prey community.     

Prey responses to pulses of risk and safety: testing the risk allocation hypothesis

The risk allocation hypothesis predicts that prey responses to predation risk should depend on the temporal pattern of risk. In systems where activity is dangerous, predicted activity levels should be ranked as follows: activity during a pulse of safety>activity during continual safety>activity during continual risk>activity during a pulse of risk. We conducted the first experimental test of the basic predictions of the risk allocation hypothesis by examining responses of freshwater physid snails, Physa gyrina, to chemical cues associated with predation on snails by predatory crayfish,Orconectes juvenilis . As predicted, the snails' pattern of activity, microhabitat use and response to risk depended on the temporal pattern of risk. Snails held in continual risk had very low activity levels, but showed an immediate, large increase in activity during a brief period of safety. In contrast, snails held in continual safety showed moderate levels of activity, but surprisingly, only a weak reduction in activity when exposed to a pulse of danger. Further studies are needed to identify general patterns for how temporal variation in risk influences antipredator behaviour.     

Simulated evolution of selfish herd behavior

Single species aggregations are a commonly observed phenomenon. One potential explanation for these aggregations is provided by the selfish herd hypothesis, which states that aggregations result from individual efforts to reduce personnel predation risk at the expense of group-mates. Not all movement rules based on the selfish herd hypothesis are consistent with observed animal behavior. Previous work has shown that herd-like aggregations are not generated by movement rules limited to local interactions between nearest neighbors. Instead, rules generating realistic herds appear to require delocalized interactions. To date, it has been an open question whether or not the necessary delocalization can emerge from local interactions under natural selection. To address this question, we study an individual-based model with a single quantitative genetic trait that controls the influence of neighbors as a function of distance. The results indicate that predation-based selection can increase the influence of distant neighbors relative to near neighbors. Our results lend support for the idea that selfish herd behavior can arise from localized movement rules under natural selection.     

Cool Headed Individuals Are Better Survivors: Non-Consumptive and Consumptive Effects of a Generalist Predator on a Sap Feeding Insect

Non-consumptive effects (NCEs) of predators are part of the complex interactions among insect natural enemies and prey. NCEs have been shown to significantly affect prey foraging and feeding. Leafhopper''s (Auchenorrhyncha) lengthy phloem feeding bouts may play a role in pathogen transmission in vector species and also exposes them to predation risk. However, NCEs on leafhoppers have been scarcely studied, and we lack basic information about how anti-predator behaviour influences foraging and feeding in these species. Here we report a study on non-consumptive and consumptive predator-prey interactions in a naturally co-occurring spider–leafhopper system. In mesocosm arenas we studied movement patterns during foraging and feeding of the leafhopper Psammotettix alienus in the presence of the spider predator Tibellus oblongus. Leafhoppers delayed feeding and fed much less often when the spider was present. Foraging movement pattern changed under predation risk: movements became more frequent and brief. There was considerable individual variation in foraging movement activity. Those individuals that increased movement activity in the presence of predators exposed themselves to higher predation risk. However, surviving individuals exhibited a ‘cool headed’ reaction to spider presence by moving less than leafhoppers in control trials. No leafhoppers were preyed upon while feeding. We consider delayed feeding as a “paradoxical” antipredator tactic, since it is not necessarily an optimal strategy against a sit-and-wait generalist predator.     

Behavioral “bycatch” from camera trap surveys yields insights on prey responses to human‐mediated predation risk

Human disturbance directly affects animal populations and communities, but indirect effects of disturbance on species behaviors are less well understood. For instance, disturbance may alter predator activity and cause knock‐on effects to predator‐sensitive foraging in prey. Camera traps provide an emerging opportunity to investigate such disturbance‐mediated impacts to animal behaviors across multiple scales. We used camera trap data to test predictions about predator‐sensitive behavior in three ungulate species (caribou Rangifer tarandus; white‐tailed deer, Odocoileus virginianus; moose, Alces alces) across two western boreal forest landscapes varying in disturbance. We quantified behavior as the number of camera trap photos per detection event and tested its relationship to inferred human‐mediated predation risk between a landscape with greater industrial disturbance and predator activity and a “control” landscape with lower human and predator activity. We also assessed the finer‐scale influence on behavior of variation in predation risk (relative to habitat variation) across camera sites within the more disturbed landscape. We predicted that animals in areas with greater predation risk (e.g., more wolf activity, less cover) would travel faster past cameras and generate fewer photos per detection event, while animals in areas with less predation risk would linger (rest, forage, investigate), generating more photos per event. Our predictions were supported at the landscape‐level, as caribou and moose had more photos per event in the control landscape where disturbance‐mediated predation risk was lower. At a finer‐scale within the disturbed landscape, no prey species showed a significant behavioral response to wolf activity, but the number of photos per event decreased for white‐tailed deer with increasing line of sight (m) along seismic lines (i.e., decreasing visual cover), consistent with a predator‐sensitive response. The presence of juveniles was associated with shorter behavioral events for caribou and moose, suggesting greater predator sensitivity for females with calves. Only moose demonstrated a positive behavioral association (i.e., longer events) with vegetation productivity (16‐day NDVI), suggesting that for other species bottom‐up influences of forage availability were generally weaker than top‐down influences from predation risk. Behavioral insights can be gleaned from camera trap surveys and provide complementary information about animal responses to predation risk, and thus about the indirect impacts of human disturbances on predator–prey interactions.     

Diet quality in a wild grazer declines under the threat of an ambush predator

Predators influence prey populations not only through predation itself, but also indirectly through prompting changes in prey behaviour. The behavioural adjustments of prey to predation risk may carry nutritional costs, but this has seldom been studied in the wild in large mammals. Here, we studied the effects of an ambush predator, the African lion (Panthera leo), on the diet quality of plains zebras (Equus quagga) in Hwange National Park, Zimbabwe. We combined information on movements of both prey and predators, using GPS data, and measurements of faecal crude protein, an index of diet quality in the prey. Zebras which had been in close proximity to lions had a lower quality diet, showing that adjustments in behaviour when lions are within short distance carry nutritional costs. The ultimate fitness cost will depend on the frequency of predator–prey encounters and on whether bottom-up or top-down forces are more important in the prey population. Our finding is the first attempt to our knowledge to assess nutritionally mediated risk effects in a large mammalian prey species under the threat of an ambush predator, and brings support to the hypothesis that the behavioural effects of predation induce important risk effects on prey populations.     

Anthropogenic noise affects risk assessment and attention: the distracted prey hypothesis

Many studies have focused on the effects of anthropogenic noise on animal communication, but only a few have looked at its effect on other behavioural systems. We designed a playback experiment to test the effect of noise on predation risk assessment. We found that in response to boat motor playback, Caribbean hermit crabs (Coenobita clypeatus) allowed a simulated predator to approach closer before they hid. Two hypotheses may explain how boat noise affected risk assessment: it masked an approaching predator''s sound; and/or it reallocated some of the crabs'' finite attention, effectively distracting them, and thus preventing them from responding to an approaching threat. We found no support for the first hypothesis: a silent looming object still got closer during boat motor playbacks than during silence. However, we found support for the attentional hypothesis: when we added flashing lights to the boat motor noise to further distract the hermit crabs, we were able to approach the crabs more closely than with the noise alone. Anthropogenic sounds may thus distract prey and make them more vulnerable to predation.