Predation risk and the number of adult males in a primate group: a comparative test

The number of adult males in a bisexual primate group is thought to be determined mainly by the defensibility of mating access to the females. However, among primates, small groups sometimes contain several adult male. We evaluate the hypothesis that high predation risk may lead to greater male representation in primate groups, independent of the effect of group size. Male primates are known to be more vigilant than females, and may also be better at detecting potential predators. A comparative test was done using arboreal folivores in three continents, howler monkeys in the Neotropics, colobus monkeys in Africa and langurs in South and Southeast Asia. Howlers and colobus are exposed to predation by large monkey-eating eagles, whereas the langurs are not. We conducted regression analyses on group composition data of single populations and on mean group compositions among populations, and found that the arboreal langurs basically live in groups with only a single adult males whereas groups of howler and colobus monkeys of comparable size have multiple adult males (Fig. 3). Thus, the hypothesis was supported. Several alternative hypotheses do not account for this pattern.     

Predatory behavior of crowned hawk-eagles (Stephanoaetus coronatus) in Kibale National Park, Uganda

Evaluating the nature and significance of predation on populations of wild primates has been difficult given a paucity of data regarding the phenomenon. Here we addressed this problem in a 37-month study of the predatory behavior of crowned hawk-eagles living at the Ngogo study site in Kibale National Park, Uganda. We collected prey remains underneath the nests of two pairs of eagles and census data on potential prey species to investigate prey selection and the ecological impact of predation on the Ngogo primate population. Results indicate that primates form the vast majority of all prey items. Eagles prey selectively on monkeys according to sex and species. Male primates were taken more often than females, while two species, redtail monkeys and mangabeys, were captured significantly more and less, respectively, than chance expectation. In addition, there was no bias in the age of prey: adult and non-adults were killed in numbers roughly equal to their proportional representations in the forest. Further analyses indicate that a non-trivial fraction of the entire primate population at Ngogo succumbs to crowned hawk-eagle predation each year. These results reveal both parallels and contrasts with those reported previously. Some of the parallels are due to similarities in prey availability, while contrasts are likely related to methodological differences between studies, inter- individual variations in predator hunting styles, and differences in prey abundance, demography, and behavior. Received: 29 March 2000 / Revised: 6 June 2000 / Accepted: 15 October 2000     

Heavier birds react faster to predators: individual differences in the detection of stalking and ambush predators

The relationship between body mass and reactions speed in response to a predatory threat is poorly understood. Theory predicts that different vigilance patterns are optimal for the detection of different predator types. We suggest that birds of different individual state might also differ in their speed of response dependent upon predator type. We used laboratory trials of wild caught chaffinches (Fringilla coelebs) to determine how between individual differences in chaffinch behaviour and state correlate with latency to react to a ground predator model (domestic cat), thus providing a comparison with previous work in the same model system using aerial predator models. In experiment 1, we observed chaffinch responses to a moving cat model, simulating a stalking predator. In experiment 2, we used a camouflaged cat model simulating an ambush predator. Both experiments show evidence suggesting heavier individuals (which previous literature has linked to impaired flight performance) responded more quickly to the model cat. Heavier individuals also had shorter interscan intervals. In contrast to a previous study, both experiments found individuals with a higher intake rate were not faster at responding to the cat model. In addition, individuals in experiment 1 that head turned more while scanning were slower to respond to the stalking cat model. Our work suggests that although heavier individuals may have impaired escape performance they appear to show behavioural compensation by allocating more attention to anti-predator behaviour and by modifying their interscan intervals, resulting in faster response times to a ground predator. We suggest more experiments investigating response time to different predatory types and explicitly manipulating state to elucidate cause and effect.     

The costs and benefits of predator inspection behaviour in Thomson's gazelles

Summary When Thomson's gazelles (Gazella thomsoni) detect stalking predators, such as cheetahs (Acinonyx jubatus) and lions (Panthera leo), they often approach and follow the predator for up to 72 min (average 14 min). Coursing predators are rarely approached. Gazelle groups were more likely to approach cheetahs if the groups were larger, if the vegetation was low, or if the cheetahs came closer to the group. Immature gazelles were more likely to approach than adults, and a higher proportion of group members participated in inspection behaviour in small groups than in large ones. Gazelles approached closer in less risky situations: if they were in larger groups or if the vegetation was low. Inspection behaviour caused cheetahs to move further between rests and between hunting attempts. Approaching cheetahs was risky, particularly for younger gazelles (probability of being killed while inspecting a cheetah was 1 in 5000 approaches for adults and 1 in 417 approaches for half-grown/adolescent gazelles), and the risks were higher than monitoring cheetahs from a distance. The time costs of predator inspection were also considerable (less than 4.2% of daylight time budget), suggesting that the benefits must be substantial to offset these costs. The results suggested that inspection behaviour was multifunctional, causing stalking predators to move out of the vicinity, enabling gazelles to monitor the predators' movements, and providing an opportunity, particularly for younger animals, to learn about predators. By approaching, gazelles also inform predators that they have been detected and alert other gazelles to the predators' presence.     

Towards an ecological solution to the folivore paradox: patch depletion as an indicator of within-group scramble competition in red colobus monkeys (Piliocolobus tephrosceles)

A number of socioecological models assume that within-group food competition is either weak or absent among folivorous primates. This assumption is made because their food resources are presumed to be superabundant and evenly dispersed. However, recent evidence increasingly suggests that folivore group size is food-limited, that the primates prefer patchily distributed high-quality foods, and display some of the expected responses to within-group scramble competition. To investigate this apparent contradiction between theoretical models and recent empirical data, we examined the foraging behaviour of red colobus monkeys (Piliocolobus tephrosceles) in Kibale National Park, Uganda. We found that red colobus monkeys foraged in a manner that suggests they deplete patches of preferred foods: intake rate slowed significantly during patch occupancy while movement rate, an index of foraging effort, increased. Furthermore, patch occupancy was related to the size of the feeding group and the size of the patch. These results suggest that within-group scramble competition occurs, may limit folivore group size, and should be considered in models of folivore behavioural ecology.     

Effects of predation risk and hunger on the behaviour of two species of tadpoles

Predation and hunger are threats for most organisms, and appropriate behavioural responses to both factors should be shaped by natural selection. In combination, however, the behavioural demands of predation avoidance and effective foraging often cannot be satisfied at the same time and lead to a conflict within organisms. We examined the behavioural responses of two closely-related species of tadpoles, Rana lessonae and R. esculenta, to simulated predation by fish and hunger. Tadpoles, hatched and reared in the laboratory, were tested in a three-way factorial (predation risk × hunger × species) experiment with four predation levels and four hunger levels. Both species decreased their swimming activity with increasing predation risk. Predation risk did not influence the amount of activity time invested in feeding but caused the tadpoles to spend less time in patches with food. Refuges were not used to avoid predation. R. esculenta was more sensitive to predation risk than R. lessonae. Hunger increased both the activity of tadpoles and the amount of activity time invested in feeding, thus indicating an increased energy intake. No interactions were observed between predation risk and hunger. These results show that tadpoles possess genetically-based behavioural mechanisms that allow them to respond in a graded manner to predation and hunger. However, they did not balance the two conflicting demands of predation avoidance and effective foraging; the two mechanisms appeared to act independently. Correspondence to: R.D. Semlitsch     

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.     

Ecological and social determinants of spacing behaviour in desert baboon groups

This paper investigates the determinants of individual spacing behaviour in a desert baboon population (Papio cynocephalus ursinus). Patterns of neighbour proximity and neighbour density were examined among adults in four groups under different ecological and social conditions (through instantaneous sampling during focal follows). Initial analysis of these data shows that (1) the use of vertical substrates (refuges such as tall trees and cliff faces) can confound patterns of spacing, and (2) individual differences in spacing can depend on the spatial scale over which it is measured. To minimise these substrate and scale effects, this analysis focuses on animals which are off refuges and examines spacing behaviour through its underlying statistical `dimensions' (identified through factor analysis). Analysis of these dimensions indicates that sex, group size, activity-habitat and female reproductive state can all have independent effects on spacing: (1) males are more dispersed than females in smaller groups, (2) male and female dispersion increases with time spent in foraging habitats, and (3) female dispersion is reduced during lactation. According to the hypotheses tested, these results indicate that feeding competition only affects spacing behaviour during foraging while predation risk plays little or no role in spacing. Most aspects of spacing behaviour are best explained by male reproductive strategies and their social repercussions. Received: 25 May 1998 / Accepted after revision: 18 July 1998     

Variation in the food hoarding behaviour of red squirrels

Summary To investigate variation in food storing behaviour within a population of red squirrels (Tamiasciurus hudsonicus) we intensively sampled the size and spatial dispersion of hoards. Single-item and large hoards were far more prevalent than expected by chance (Figs. 1 and 2) and appeared to be distinct components of the hoarding tactic employed in this population. Scattered single-item hoards represented more than half of all hoards constructed and approximately one-fifth of all cones stored. Large hoards (> 10 cones) comprised less than 15% of all hoards, and about 50% of all cones stored. In response to experimental manipulations, squirrels altered their hoarding behaviour in order to concentrate cones in the litter and brush heaps we provided, but still scattered a large proportion of their stores. We conclude that hoarding patterns in red squirrels are more variable and plastic than has previously been recognized, and discuss this variability in terms of adaptive explanations. Offprint requests to: R.J. Robertson     

Nest concealment and parental behaviour interact in affecting nest survival in the blackcap (Sylvia atricapilla): an experimental evaluation of the parental compensation hypothesis

Nest concealment varies strongly within populations of many species. Although some studies have revealed the beneficial effects of concealment in mitigating predation pressure on nests, other studies were unable to find similar effects. One potential reason for the mixed results is that parental behaviour may compensate for the effects of nest cover, and specifically designed experimental studies are needed to reveal this compensation. I studied the effects of concealment on the probability of nest survival in the blackcap (Sylvia atricapilla), by experimentally manipulating the degree of nest-foliage cover. There was a significant effect of the treatment depending on nest type and the phase of nesting. Whereas there was no effect of concealment on nest survival in natural nests, there was a positive effect in real nests baited with plasticine clutches (i.e. without parental activity). Parents probably behaviourally compensated for poor concealment in natural nests (nest guarding, defence). In line with this, there was no effect of concealment on nest survival during incubation, whereas there was probably a positive effect in the nestling phase. Parents spent more time on the nest during incubation (80%) than during the care of nestlings (40%) and, consequently, had more opportunities to compensate for poor cover. In general, we cannot use single measures of behaviours or states (nest concealment) as an indication of predation risk because of the capacity for compensation in other behaviours.Communicated by C. Brown     

Between-group contest competition for food in a highly folivorous population of black and white colobus monkeys (Colobus guereza)

In theory, between-group contest (BGC) competition for food can greatly influence female social relationships and reproductive success in primates, but few studies have investigated whether such effects occur and, if so, under what ecological conditions. There is evidence that adult male black and white colobus monkeys (Colobus guereza, “guerezas”) defend the food their mates need against other groups, suggesting that BGC competition is important in this species. Using data on feeding, ranging, vegetation patterns, and intergroup encounters between six neighboring guereza groups, I provide evidence that the highly folivorous guerezas at Kanyawara, Kibale National Park, Uganda, engaged in BGC competition over unevenly dispersed, relatively high-quality feeding areas or “core areas”. Intergroup aggression was common, and groups’ home ranges overlapped. Groups were more likely to initiate high-level aggression if they encountered another group within or near their core area, and groups that initiated and won encounters often fed in the same areas in which losing groups had fed. Guerezas fed selectively on species with contagious (clumped) distributions and concentrated their feeding efforts in areas of the forest that contained the most food (core areas). Groups could be ranked in a linear dominance hierarchy, and group rank number was inversely related to the quantity and quality of food in groups’ core areas. This study not only provides good evidence that BGC competition occurs in primates but it also reinforces the idea that folivore food resources may be worth defending.     

Rats on the run: removal of alien terrestrial predators affects bush rat behaviour

Predators can strongly influence the microhabitat use and foraging behaviour of prey. In a large-scale replicated field experiment in East Gippsland, Australia, we tested the effects of reduced alien red fox (Vulpes vulpes) and alien wild dog (Canis lupus familiaris) abundance (treatment) on native bush rat (Rattus fuscipes) behaviour. Bush rats are exposed to two main guilds of predators, namely mammalian carnivores and birds of prey. Tracking rat movements using the spool-and-line technique revealed that, in treatment sites, rats used ground cover, which provides shelter from predators, less often than at unmanipulated fox and wild dog abundance (non-treatment sites). In treatment sites, rats more frequently moved on logs where they would have been exposed to hunting foxes and dogs than in non-treatment sites. Furthermore, in treatments, rats showed a preference for understorey but not in non-treatments. Hence, bush rats adapted their behaviour to removal of alien terrestrial predators. Giving-up densities (GUDs) indicated no treatment effects on the marginal feeding rate of bush rats. Interestingly, GUDs were higher in open patches than in sheltered patches, suggesting higher perceived predation risk of bush rats during foraging at low versus high cover. The lack of treatment effects on GUDs but the clear response of bush rats to cover may be explained by the impact of predators other than foxes and wild dogs.     

Synergistic interactions between chemical alarm cues and the presence of conspecific and heterospecific fish shoals

Chemical and visual sources of information are used by aquatic prey during risk assessment. Here, we test the behavioral response of littoral prey fish to combinations of chemical alarm cues (skin extract) and the visual presence of a fish shoal. We scented minnow traps with either alarm cues or water (control) placed inside the trap, a jar that contained either a fish shoal or nothing (control), and recorded the number and species of fish captured. We predicted that chemical alarm cues would reduce the number of fish captured and that a fish shoal would increase the number of fish captured. The predicted effect of chemical and visual cues combined depended on the nature of the interaction. We found that the lowest catch rate was for the combination of alarm cue + no shoal, but the highest catch rate occurred for the combination of alarm cue + shoal. Fish shoal + water had the second highest catch rate and no shoal + water had the second lowest catch rate. We conclude that chemical alarm cues induce area avoidance in the absence of a shoal, but a strong behavioral proclivity to increase shoal cohesion in the presence of a shoal. The presence of a shoal in the traps induced alarmed fish to shoal with them and thus, enter the traps. This occurred even though traps were the source of the alarm cue.Communicated by A. Mathis     

Determinants of group size in the red colobus monkey (Procolobus badius): an evaluation of the generality of the ecological-constraints model

The ecological-constraints model proposes that increased group size increases within-group feeding competition, necessitating increased travel and, consequently, constraining group size. Previous studies have supported the model for frugivores, but its applicability to folivores remains untested. This study evaluated the generality of the model by re-examining the relationship between day range and group size for a folivorous species for which published accounts have not found a relationship between these factors. This study differs from earlier studies by accounting for variation in food availability, which may drive changes in day range. We quantified the relationships among food availability, day range, and group size for two red colobus groups at Kibale National Park, Uganda. Mean day range and home range were significantly greater for the group of 48 individuals compared to the group of 24 individuals. The large group traveled more and rested less than the small group. The large group also traveled more rapidly than the small group. Food availability significantly predicted mean day range for the large group, but not for the small group. Analyses of covariance demonstrated that the large and small group responded differently to changes in food availability. These observations suggest that the large red colobus group experiences greater levels of within-group feeding competition than the small group. This study provides added support for the generality of the ecological-constraints model and contributes toward an understanding of the mechanisms controlling feeding competition and social organization in primates.     

Elk decision-making rules are simplified in the presence of wolves

The risk of predation drives many behavioral responses in prey. However, few studies have directly tested whether predation risk alters the way other variables influence prey behavior. Here we use information theory (Akaike’s Information Criterion, AICc) in a novel way to test the hypothesis that the decision-making rules governing elk behavior are simplified by the presence of wolves. With elk habitat use as the dependent variable, we test whether the number of independent variables (i.e., the size of the models) that best predict this behavior differ when wolves are present vs absent. Thus, we use AICc scores simply to determine the number of variables to which elk respond when making decisions. We measured habitat use using 2,288 locations from GPS collars on 14 elk, over two winters (14 elk winters), in the Gallatin Canyon portion of the Greater Yellowstone Ecosystem. We found that the use of three major habitat components (grass, conifer, sage) was sensitive to many variables on days that wolves were locally absent, with the best models (ΔAICc≤2) averaging 7.4 parameters. In contrast, habitat use was sensitive to few variables on days when wolves were present: the best models averaged only 2.5 parameters. Because fewer variables affect elk behavior in the presence of wolves, we conclude that elk use simpler decision-making rules in the presence of wolves. This simplification of decision-making rules implies that predation risk imposes selection pressures that do not allow prey to respond to other pressures in ways that they otherwise would. If the affected processes are important, then this indirect effect of predation is likely to be important.     

Sex, intimidation and severed limbs: the effect of simulated predator attack and limb autotomy on calling and emergence behaviour in the field cricket Gryllus bimaculatus

Crickets can autotomize a limb in order to evade predation; however, this autotomy compromises their escape speed and, therefore, their ability to avoid subsequent predation events. We recorded two measures of predator-avoidance behaviour in field crickets (Gryllus bimaculatus) exposed to varying levels of predation threat, with the most extreme level leading to autotomy of a limb. Our first measure of caution was time to emergence from cover, which was affected by perceived predation treatment, with both autotomized males and females being significantly more cautious than intact individuals. For males (but not females), the presence of a calling conspecific encouraged earlier emergence. Our second measure of caution was alteration of male calling behaviour. Autotomized males remained silent for significantly longer time after disturbance than intact males, but there was no difference in call rate once they had resumed calling, suggesting that behavioural changes were not merely a result of injury response but a controlled modification of behaviour as a result of autotomy. These data suggest that autotomy in field crickets results in altered calling behaviour, which was not significantly altered with different acoustic environments.     

Is the antipredatory response in behaviour reflected in stress measured in faecal corticosteroids in a small rodent?

Predation risk has been shown to alter various behaviours in prey. Risk alters activity, habitat use and foraging, and weight decrease might be a consequence of that. In mammals, studies on physiological measures affected by risk of predation, other than weight, are rare. We studied in two separate laboratory experiments foraging, hoarding behaviour and expression of stress measured non-invasively from the faeces in the bank vole (Clethrionomys glareolus), a common boreal rodent. Voles were exposed to predation risk using odours of the least weasels (Mustela nivalis nivalis). Distilled water served as control. In the first experiment, we found that foraging effort, measured as sunflower seeds taken from seed trays filled with sand, was significantly lower in trays scented with weasel odour. Both immediate consumption of seeds and hoarding were affected negatively by the weasel odour. Females hoarded significantly more than males in autumn. In the second experiment, the negative effect of weasel odour on foraging was consistent over a 3-day experiment, but the strongest effect was observed in the first night. Foraging increased over the time of the experiment, which might reflect either energetic compensation during a longer period of risk, predicted in the predation risk allocation hypothesis, or habituation to the odour-simulated risk. Despite decreased foraging under predation risk, stress measured as corticosteroid metabolite concentration in vole faeces was not affected by the weasel odour treatment. In conclusion, we were able to verify predation-risk-mediated changes in the foraging effort of bank voles but no physiological stress response was measured non-invasively, probably due to great individual variation in secretion of stress hormones.     

Influences of moonlight,ambient temperature,and food availability on the diurnal and nocturnal activity of owl monkeys (<Emphasis Type="Italic">Aotus azarai</Emphasis>)

The study of activity rhythms, their potential zeitgebers and masking factors among free-ranging primates has received relatively little attention in the past. Most primates are diurnal, a few of them nocturnal, and even fewer are cathemeral. Owl monkeys (Aotus azarai azarai) regularly show diurnal, as well as nocturnal, activity in the Argentinean and Paraguayan Chaco. The goal of this study was to examine how changes in activity patterns in owl monkeys of Formosa, Argentina are related to daily, monthly, and seasonal changes in temperature, light and food availability . During 1 year, I collected activity data from five groups followed continuously from dawn to dusk, dusk to dawn or uninterruptedly during 24 or 36 h for approximately 1,500 h. I kept hourly and daily records of temperature and light conditions, and I gathered monthly information on the density, distribution and abundance of food resources available to the monkeys. I found that the area of study is highly seasonal, and characterized by significant fluctuations in rainfall, temperature, photoperiod, and food availability. Owl monkeys had on average 5 h of activity during the day and 4 h during the night. The amount of diurnal activity remained fairly constant through the year despite seasonal changes in exogenous factors. Owl monkeys did not show changes in their activity patterns that could be attributed to changes in food availability. Nocturnal activity increased as the amount of moonlight increased, whereas diurnal activity decreased following a full-moon night. Ambient temperature was a good predictor of activity only when the moon was full. These results argue convincingly for an interaction between ambient temperature and moonlight in determining the observed activity pattern. It is then highly advisable that any evaluation of diurnal activity in cathemeral animals be analyzed controlling for the possible effects of moonlight during the previous night.Communicated by P. Kappeler     

Cyclicity in the structure of female baboon social networks

There is an established and very influential view that primate societies have identifiable, persistent social organizations. It assumes that association patterns reflect long-term strategic interests that are not qualitatively perturbed by short-term environmental variability. We used data from two baboon troops in markedly different habitats over three consecutive seasons to test this assumption. Our results demonstrate pronounced cyclicity in the extent to which females maintained differentiated relationships. When food was plentiful, the companionships identified by social network analysis in the food-scarce season disappeared and were replaced by casual acquaintanceships more representative of mere gregariousness. Data from the fourth, food-scarce, season at one site indicated that few companions were re-united. It is likely that this reflected stochastic variation in individual circumstances. These results suggest that attention could profitably be paid to the effects of short-term local contingencies on social dynamics, and has implications for current theories of primate cognitive evolution. This contribution is part of the special issue “Social Networks: new perspectives” (Guest Editors: J. Krause, D. Lusseau and R. James).     

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