Balancing the response to predation—the effects of shoal size,predation risk and habituation on behaviour of juvenile perch

Group size, predation risk and habituation are key drivers of behaviour and evolution in gregarious prey animals. However, the extent to which they interact in shaping behaviour is only partially understood. We analyzed their combined effects on boldness and vigilance behaviour in juvenile perch (Perca fluviatilis) by observing individuals in groups of one, two, three and five faced with four different levels of predation risk in a repeated measures design. The perch showed an asymptotic increase in boldness with increasing group size and the highest per capita vigilance in groups of two. With increasing predation risk, individuals reduced boldness and intensified vigilance. The interaction between group size and predation risk influenced vigilance but not boldness. In this context, individuals in groups of two elevated their vigilance compared to individuals in larger groups only when at higher risk of predation. Further, as only group size, they significantly reduced vigilance at the highest level of risk. With increasing habituation, solitary individuals became considerably bolder. Also, predation risk affected boldness only in the more habituated situation. Hence, repeated measures may be essential to correctly interpret certain relationships in behaviour. Our results suggest that perch may adjust boldness behaviour to group size and predation risk independently. This is rather unexpected since in theory, natural selection would strongly favour an interactive adjustment. Finally, vigilance might be particularly effective in groups of two due to the intense monitoring and detailed response to changing levels of risk.     

Cheetah mothers' vigilance: looking out for prey or for predators?

Summary Free-living cheetah (Acinonyx jubatus) cubs are killed by a number of predators, thus vigilance in cheetah mothers may be a form of anti-predator behaviour as well as a means of locating prey. Mothers' vigilance during the day was closely associated with measures of hunting but not with measures of anti-predator behaviour. In contrast, mothers' vigilance at kills was not related to hunting but was related to anti-predator behaviour. Both forms of vigilance decreased as cubs grew older. Vigilance during the day increased with litter size which supports a model of shared parental investment (Lazarus and Inglis 1986) because after prey had been located and caught by mothers, cubs shared the prey between them. Vigilance at kills did not increase with litter size when cubs were young; in these situations predators stole cheetahs' prey and rarely chased cubs so, at most, only a single cub would be taken. Mothers' anti-predator behaviour away from kills did increase with litter size at young cub ages however; more cubs are killed in these circumstances the greater is the size of the litter. When cubs were older and could outrun predators, neither vigilance at kills nor anti-predator behaviour increased with litter size. These results strongly support two models of unshared investment (Lazarus and Inglis 1986) and demonstrate, not only that superficially similar behaviour has different functions in different contexts, but that parental investment is shaped by the type of benefits accrued from it.     

Responses to threat by female bobucks,<Emphasis Type="Italic"> Trichosurus caninus</Emphasis>, during different stages of offspring development

The costs of reproduction are widely recognised as a major selective force in the evolution of various behavioural and life-history characteristics. In particular, the behaviour of reproductively active animals is likely to change when breeding increases risk of predation. We investigated the effect of an experimentally derived threat on the vigilance and escape behaviour of female Trichosurus caninus with and without dependent offspring and at different stages of offspring development. Females with offspring showed a heightened response to the threat in comparison to females without offspring. In addition, females with offspring displayed a stronger response at earlier stages of their offsprings development.Communicated by P. Bednekoff     

Vigilance and foraging substrate: anti-predatory considerations in a non-standard environment

Summary The commonly studied standard anti-predatory environment presents animals with spatially-distinct feeding sites and refuges from attack, neither of which necessarily obstructs predator detection. In contrast, tree-trunks provide animals with a markedly non-standard environment in which the foraging substrate itself may be a refuge from attack that unavoidably obstructs predator detection. Thus anti-predatory behavior in this environment should be influenced not only by a perceived risk of attack, but also by the nature of the refuge/foraging substrate itself. Downy woodpeckers (Picoides pubescens) are a common tree-trunk foraging animal, and an experimental analysis of their behavior suggests that they respond appropriately to their non-standard anti-predatory environment. In particular, anti-predatory vigilance varies strongly with changes in tree trunk diameter. Two modes of vigilance were apparent. In stationary vigilance, woodpeckers maintained the position of their feet while rotating their bodies side-to-side to peer around the trunk; mobile vigilance involved movement around the trunk itself. Both the frequency and angle of rotation of stationary vigilance increased with trunk diameter, as did the frequency of mobile vigilance. The woodpeckers also held their heads farther away from the trunk surface as diameter increased. All of these measures of vigilance increased under a greater perceived risk of predation. As might be expected given these results, downy woodpeckers avoided thick trunks; they did not, however, prefer the thinnest (least obstructive) available trunks. These preferences may reflect the influence of trunk diameter on thermo-ecological and/or anti-predator considerations not related to vigilance. Overall, this arboreal environment provides an unusual perspective on anti-predator decision-making with several implications for tree-trunk foraging animals in general.     

Anti-predatory vigilance and the limits to collective detection: visual and spatial separation between foragers

Collective detection concerns the idea that all members of a socially feeding group are alerted to an attack as long as at least one group member detects it. We found that collective detection in mixed flocks of emberizid sparrows is limited markedly by relatively small degrees of visual and spatial separation between foragers. These limits on collective detection appear to influence the degree to which flock members lower their vigilance with increasing group size (the group size effect). Specifically, the decrease in collective detection with increasing visual and spatial isolation between foragers is accompanied by a concomitant decrease in the strength of the vigilance group size effect. Explanations for the vigilance-related effects of such separation based upon a bird’s ability to monitor the vigilance behavior of flockmates can be ruled out for our experimental system. Our results also shed light on the issue of whether the vigilance group size effect is influenced more by collective detection or the simple dilution of risk with increasing group size. We argue that collective detection is not only an important determinant of the group size effect, but also that the phenomena of collective detection and risk dilution are interdependent. Received: 25 July 1995/Accepted after revision: 17 December 1995     

Individual variation in the relationship between vigilance and group size in eastern grey kangaroos

The mean vigilance of animals in a group often decreases as their group size increases, yet nothing is known about whether there is individual variability in this relationship in species that change group sizes frequently, such as those that exhibit fission–fusion social systems. We investigated variability in the relationship between group size and vigilance in the eastern grey kangaroo (Macropus giganteus) by testing whether all individuals showed decreased vigilance with increased group size, as has been commonly assumed. We carried out both behavioural observations of entire groups of kangaroos and focal observations of individually recognised wild female kangaroos. As in other studies, we found a collective group-size effect on vigilance; however, individuals varied in their vigilance patterns. The majority (57%) of the identified individual kangaroos did not show significant group-size effects for any of the recorded measures of vigilance. The females that did not show a negative group-size effect were, on average, more vigilant than those females that did show a group-size effect, but this difference was not significant. We propose that some females exhibit higher levels of social vigilance than others, and that this social vigilance increases with group size, cancelling out any group-size effect on anti-predator vigilance for those females. Our results therefore suggest that only some prey individuals may gain anti-predator benefits by reducing their time spent scanning when in larger groups. The large amount of variation that we found in the vigilance behaviour of individual kangaroos highlights the importance of collecting and analysing vigilance data at the individual level, which requires individual recognition.     

Predation, scramble competition, and the vigilance group size effect in dark-eyed juncos (Junco hyemalis)

In socially feeding birds and mammals, as group size increases, individuals devote less time to scanning their environment and more time to feeding. This vigilance “group size effect” has long been attributed to the anti-predatory benefits of group living, but many investigators have suggested that this effect may be driven by scramble competition for limited food. We addressed this issue of causation by focusing on the way in which the scan durations of free-living dark-eyed juncos (Junco hyemalis) decrease with group size. We were particularly interested in vigilance scanning concomitant with the handling of food items, since a decrease in food handling times (i.e. scan durations) with increasing group size could theoretically be driven by scramble competition for limited food resources. However, we showed that food-handling scan durations decrease with group size in an environment with an effectively unlimited food supply. Furthermore, this food-handling effect was qualitatively similar to that observed in the duration of standard vigilance scans (scanning exclusive of food ingestion), and both responded to changes in the risk of predation (proximity of a refuge) as one might expect based upon anti-predator considerations. The group size effects in both food-handling and standard scan durations may reflect a lesser need for personal information about risk as group size increases. Scramble competition may influence vigilance in some circumstances, but demonstrating an effect of competition beyond that of predation may prove challenging. Received: 22 September 1998 / Received in revised form: 1 February 1999 / Accepted: 14 February 1999     

Ecological constraints on the behaviour of mother long-tailed macaques (Macaca fascicularis)

Summary The ecological consequence of the effects of different social conditions on the behaviour of females with infants were examined in two different-sized groups of long-tailed macaques (Macaca fascicularis) that inhabited adjacent home ranges in Gunung Leuser National Park in Indonesia. This study aims to test predictions of the within-group competition/predation avoidance hypothesis of social organization. Females, particularly those carrying an infant, are considered to experience the most direct effects of environmental constraints on fitness prospects. Data on maintenance behaviour, height in canopy and spatial position were collected for five mothers in a small group and eight mothers in a large group. Comparisons were made on the basis of group size and dominance rank. Mothers from the large group spent less time feeding on clumped fruits and more time foraging on dispersed food items. Lower-ranking mothers, undergoing the highest rate of within-group competition, foraged most. For macaques in the study area, predation risk is considered to decrease with height in the canopy. Mothers in the small group, assumed to be more susceptible to predation, remained substantially higher in the canopy than mothers in the large group. In both groups, mothers adjusted their height to their spatial position in the group. Lower-ranking mothers were more often found without neighbours, presumably to avoid feeding competition. As a result they stay higher in the canopy than higher-ranking mothers. The results clearly demonstrate that individual females in the same reproductive state and living in the same area, but in different social environments, adapted their behaviour according to the hypothesis. Correspondence to: D.R. Vos     

Predator detection and dilution as benefits of associations between yellow mongooses and Cape ground squirrels

Associations among organisms are thought to form because the benefits, such as increased foraging efficiency or decreased risk of predation, outweigh any costs, such as resource competition. Though many interspecific associations have been described for closely related mammals, few studies have examined the associations between mammals in different orders. The yellow mongoose (Cynictus pencillata), a carnivore, and the Cape ground squirrel (Xerus inauris), a rodent, co-occur in arid and semi-arid South Africa where they share sleeping burrows, predators, a similar body size, and the capability to emit alarm calls in response to predators. To investigate enhanced predator avoidance as a potential benefit explaining the persistence of this association, we assessed individual mongoose vigilance alone and with squirrels or other mongooses, and with varying interspecific group size, using field observations. We also tested for responses to conspecific and heterospecific alarm calls in both study species using playback experiments. The proportion of time mongoose individuals spent vigilant decreased in the presence of squirrels or other mongooses and was negatively correlated with interspecific group size; a similar pattern was previously shown for conspecific groups of Cape ground squirrels. These results are predicted by both the dilution and collective detection hypotheses. In addition, hetero- and conspecific alarm calls elicited vigilance responses in both species. These results suggest that both species can benefit from the collective detection and dilution arising from their interspecific association and that this interspecific association could be mutualistic.     

Groups confuse predators by exploiting perceptual bottlenecks: a connectionist model of the confusion effect

Aggregation is a well documented behaviour in a number of animal groups. The confusion effect is one mechanism thought to mitigate the success of predators feeding on gregarious prey and hence favour aggregation. An artificial neural network model of prey targeting is developed to explore the advantages prey species might derive through a tendency to group. The network illustrates how an abstract model of the computational mechanisms mediating the perception of prey position is able to show a degradation in performance as group size increases. The relationship between group size and predator confusion has a characteristic decreasing decelerating shape. Prey oddity is shown to reduce the impact of the confusion effect, thereby allowing predators to target prey more accurately. Hence shoaling behaviour is most profitable to the prey when prey phenotypes are visually indistinguishable to a predator. Futhermore it is shown that prey oddity is relatively more costly in large groups than in small groups and the implications for assortative schooling are discussed. Both the model and the results are intended to make the general point that cognitive constraints will limit the information that a nervous system can process at a number of different levels of neural organization.     

Cost-free vigilance during feeding in folivorous primates? Examining the effect of predation risk,scramble competition,and infanticide threat on vigilance in ursine colobus monkeys (<Emphasis Type="Italic">Colobus vellerosus</Emphasis>)

Vigilance often decreases with increasing group size, due to lower predation risk or greater scramble competition for food. A group size effect on vigilance is seldom seen in primates, perhaps because scanning and feeding often occur simultaneously or because the distinction between routine and induced vigilance has not been investigated. We analyzed feeding and resting observations separately while distinguishing between routine and induced scans in four groups of wild ursine colobus monkeys (Colobus vellerosus) experiencing scramble competition for food and infanticide risk. We used linear mixed-effect models to test the effect of group size, age–sex class, number of neighbors, number of adult male neighbors, and height in the canopy on scanning rates (vigilance) with and without evident conspecific threat. Food type was also examined in the feeding models. Perceived predation risk affected vigilance more than scramble competition for food and infanticide risk. Routine and induced vigilance were greatest at lower canopy heights during feeding and resting and increased when individuals had fewer neighbors while resting. A group size effect was found on induced vigilance while resting, but scanning increased with group size, which probably indicates visual monitoring of conspecifics. Scanning rates decreased while feeding on foods that required extensive manipulation. This supports the idea that vigilance is relatively cost free for upright feeders when eating food that requires little manipulation, a common feature of folivore diets. In the presence of threatening conspecific males, close proximity to resident males decreased individual vigilance, demonstrating the defensive role of these males in the group.     

Vigilance behaviour and fitness consequences: comparing a solitary foraging and an obligate group-foraging mammal

Vigilance behaviour in gregarious species has been studied extensively, especially the relationship between individual vigilance and group size, which is often negative. Relatively little is known about the effect of conspecifics on vigilance in non-obligate social species or the influence of sociality itself on antipredator tactics. We investigated predator avoidance behaviour in the yellow mongoose, Cynictis penicillata, a group-living solitary forager, and compared it with a sympatric group-living, group-foraging herpestid, the meerkat, Suricata suricatta. In yellow mongooses, the presence of conspecifics during foraging—an infrequent occurrence—reduced their foraging time and success and increased individual vigilance, contrary to the classical group-size effect. Comparing the two herpestids, sociality did not appear to affect overt vigilance or survival rates but influenced general patterns of predator avoidance. Whereas meerkats relied on communal vigilance, costly vigilance postures, and auditory warnings against danger, yellow mongooses avoided predator detection by remaining close to safe refuges and increasing “low-cost” vigilance, which did not interfere with foraging. We suggest that foraging group size in herpestids is constrained by species-distinct vigilance patterns, in addition to habitat and prey preference.     

Determinants of vigilance behavior in the ring-tailed coati (Nasua nasua): the importance of within-group spatial position

Individuals living in social groups are predicted to live under unequal predation risk due to their spatial location within the group. Previous work has indicated that individuals located at the edge of groups have higher “domains of danger”, thus are more likely to engage in vigilance or antipredator behavior. We studied the determinants of vigilance behavior in two groups of ring-tailed coatis in Iguazu National Park, Argentina. In addition to the expected pattern that coatis were more vigilant at the edge of the group, we found that individuals were particularly vigilant at the front edge of the group. This pattern conforms to predictions of differing predation risk caused by sit-and-wait predators with respect to mobile animal groups. In addition, coatis exhibited less vigilance when the number of neighbors within 5 m and group size increased. Of the three spatial variables tested, within-group spatial position was the most important predictor variable determining vigilance levels. These results confirm that spatial position has major effects on vigilance behavior, and that group directionality is an important factor which should be taken into account when measuring vigilance behavior. Coatis were more vigilant when juveniles less than 6 months old were in the groups. The presence of these young juveniles also affected the relationship between alarm response and vigilance levels. Coatis were more vigilant after strong alarm reactions, but only when young juveniles were not present in the groups. This may indicate that coatis give differential responses to alarm calls depending on the age of the caller. A comparison of antipredator vigilance between coatis and sympatric capuchin monkeys is consistent with the hypothesis that terrestriality leads to higher perceive predation risk for coatis.     

Behavioural responses of Diana monkeys to male long-distance calls: changes in ranging,association patterns and activity

Although much is known about the relationship between vigilance, group size and predation risk, behavioural responses to predation risk and their resultant costs are less clear. We investigated the response of Diana monkeys to increased predation risk by looking at behavioural changes associated with male long-distance calls, which are reliably given to certain predators. After male long-distance calls, group spread and nearest-neighbour distance decreased whilst travel and association rates for the group increased. The average height and exposure level of individuals in the group did not change after calls. Individual Diana monkeys changed their behaviour and were more likely to be vigilant or travel and less likely to engage in social or resting behaviours after long-distance calls. In addition, movement rates increased with the number of species the Diana monkeys were associated with. Diana monkey long-distance calls facilitate the joining of groups of other species. Black and white colobus and lesser spot-nosed monkeys were more likely to be in an association following a long-distance call than before. Behavioural responses, such as increased travel or association rates, that reduce foraging efficiency are interpreted as evidence of a non-lethal impact of increased predation risk.     

Information transfer and gain in flocks: the effects of quality and quantity of social information at different neighbour distances

We assessed experimentally how the quality and quantity of social information affected foraging decisions of starlings (Sturnus vulgaris) at different neighbour distances, and how individuals gained social information as a function of head position. Our experimental set up comprised three bottomless enclosures, each housing one individual placed on a line at different distances. The birds in the extreme enclosures were labelled senders and the one in the centre receiver. We manipulated the foraging opportunities of senders (enhanced, natural, no-foraging), and recorded the behaviour of the receiver. In the first experiment, receivers responded to the condition of senders. Their searching rate and food intake increased when senders foraged in enhanced conditions, and decreased in no-foraging conditions, in relation to natural conditions. Scanning was oriented more in the direction of conspecifics when senders behaviour departed from normal. In the second experiment, responses were dose dependent: receivers increased their searching rate and orientated their gaze more towards conspecifics with the number of senders foraging in enhanced food conditions. In no-foraging conditions, receivers decreased their searching and intake rates with the number of senders, but no variation was found in scanning towards conspecifics. Differences in foraging and scanning behaviour between enhanced and no-foraging conditions were much lower when neighbours were separated farther. Overall, information transfer within starling flocks affects individual foraging and scanning behaviour, with receivers monitoring and copying senders behaviour mainly when neighbours are close. Information transfer may be related to predation information (responding to the vigilance of conspecifics) and foraging information (responding to the feeding success of conspecifics). Both sources of information, balanced by neighbour distance, may simultaneously affect the behaviour of individuals in natural conditions.Communicated by H. Kokko     

Flocking behaviour of passerines: a dynamic model for the non-reproductive season

Summary The behaviour of a small male passerine bird over a typical winter day is studied by a dynamic programming model. The bird can be either unpaired or paired; an unpaired bird can forage in a flock, forage alone or sing to attract a mate. Foraging increases his reserves, while singing reduces them. The optimal policy and the expected behaviour of birds depend both on time and reserves. The model predicts that birds will flock, especially in the morning, if flocking birds find more food (foraging efficiency), and also more flocking can be expected when the predation risk is lower in a flock (antipredator benefit). Where flocking gives lower variance in food intake, with the same mean (reduced variance benefit), birds with low reserves at the end of the day choose to forage alone (high variance option), while otherwise they are risk-averse and forage in a flock. The cost of flocking increases with time in a day and with the probability of mate attraction through singing. Decisions inevitably involve trade-offs. Where flocking results in antipredator benefit, but also lower foraging gain, birds with low reserves forage alone, but birds with high reserves flock. Offprint requests to: A.I. Houston     

Intra-sexual variability in feeding behaviour of a mountain ungulate: size matters

Many studies comparing the behaviour of individuals of different genders or species showed that animal body mass and forage quality/quantity are key elements of the foraging ecology of herbivores. Since body mass could also influence the animal’s sensitivity to predation risk, its vigilance behaviour should consequently be affected. Alpine ibex (Capra ibex) is characterised by a strong dimorphism among males of different ages, thus representing an ideal case study for testing the Jarman-Bell principle, avoiding possibly misleading effects resulting from the comparison between different species or genders. We analysed the fine-scale foraging behaviour of male ibex in order to assess the effect of body mass and the effects of vegetation quality/quantity on both foraging and vigilance behaviour. Our results showed that smaller males were more selective than larger ones, on account of their lower capability of digesting plant. Smaller males scanned the environment more frequently than larger ones. Male ibex grazed more selectively in sites with high quality forage and their bite rate increased as forage biomass decreased. Vigilance frequency increased with increasing forage biomass as, under these circumstances, ibex are able to prolong anti-predator vigilance while chewing bites that have already been cropped. Our findings highlight the effects of body mass per se on both foraging and anti-predator behaviours in herbivores, thus supporting the Jarman-Bell principle. Foraging can arguably be considered a very flexible behaviour with high evolutionary relevance as it enables herbivores to optimally adjust their total energy intake under varying conditions of food resources.     

The establishment of foraging flocks in house sparrows: risk of predation and daily temperature

Summary The foraging decisions of animals often reflect a trade-off between the risk of predation and efficient foraging. One way an animal may reduce the risk of predation, and hence exploit a resource patch in relative safety, is by foraging in a group. Solitary pioneer sparrows often recruit others to a food source by making chirrup calls in order to establish foraging flocks. This study describes the decisions of house sparrows that arrive at food resources of different risks of predation. Four feeding sites at different distances from a perching site and from an observer were presented to sparrows. When the feeder was adjacent to the perching site and far from the observer, the pioneers chirruped less frequently and were more likely to forage alone than when the feeder was in the other three positions. There were differences in the scanning behaviour of sparrows at these sites, suggesting that they were responding to different risks of predation. Furthermore, the chirrup rates of pioneer sparrows in this study and a previous study were found to be negatively correlated with maximum daily temperature. This is consistent with the hypothesis that energy requirements may affect the flock establishment decisions of sparrows, and that the benefits of foraging in flocks may be greater at lower temperatures.     

Do kin always make better neighbours?: The effects of territory quality

Summary The effects of territory quality on kin-biased territorial defence behaviour and fitness of juvenile rainbow trout (Oncorhynchus mykiss) were examined by manipulating food and predation risk levels in an artificial stream channel. Groups of related (full sibling) or unrelated fry were observed in the channel under one of four treatments: (1) high food-low predator (high territory quality); (2) high food-high predator; (3) low food-low predator; and (4) low food-high predator (low territory quality). Fish within kin groups always initiated fewer aggressive interactions, defended smaller territories, exhibited higher proportions of threat type territorial defence behaviours (as opposed to overtly aggressive behaviours) and had a higher mean weight increase than non-kin groups. Within both kin and non-kin groups, decreasing territory quality significantly increased the frequency of aggressive interactions, the size of territories and decreased growth. It is argued that while kin-biased territorial defence behaviours are always present, decreased availability of resources and increased predation risk serve to reduce the magnitude of this kin bias. However, even in low-quality territories, the benefit of associating with kin may increase the probability of overwintering survival (increased fitness) of the young fish by increasing body size.     

Ontogenetic changes in social behaviour in the forest tent caterpillar,<Emphasis Type="Italic"> Malacosoma disstria</Emphasis>

Many animals, including gregarious caterpillars, begin life in groups and become increasingly solitary as they grow larger. These ontogenetic changes in social behaviour suggest that the costs and benefits of grouping change with increasing individual size. Forest tent caterpillar (Malacosoma disstria) colonies exhibit complex social behaviour during the early larval instars, using pheromone trails to move together between temporary bivouacs and feeding sites, and break up as the caterpillars grow. We demonstrate changes in individual responses to cues from conspecifics that explain changes in aggregation during caterpillar development. We used Markov chain analysis to test the influence of pheromone trails and colony-mates on an individual caterpillars tendency to switch between quiescence, searching, walking and spinning. Pheromone-laden silk trails increased the tendency to begin locomotion, whereas colony-mates increased switching from activity to quiescence. Trails also influenced the form taken by locomotor behaviour, and promoted directed walking over searching. Social cues thus increase the efficiency of individual locomotion. Younger larvae were more quiescent and more reluctant to walk in the absence of trails than were older insects. An increase in independent locomotion as the larvae grow provides a mechanism to explain colony break-up and points to an ontogenetic shift in the internal processes driving behaviour. Scaling relationships suggest that many of the benefits associated with group-living in caterpillars decrease as individuals grow larger, providing an adaptive explanation for observed ontogenetic changes in social behaviour.Communicated by N. Wedell