Reproductive consequences of variation in the composition of howler monkey (Alouatta spp.) groups

At least three general categories of environmental pressure - predation, resource distribution, and demographics - shape the costs and benefits of group-living for animals. Among the demographic factors that influence individual survival and reproduction, the composition of social groups can play an important role. Census data drawn from 26 populations of howler monkeys (Alouatta spp.) were used to determine if the composition of groups explained variation in their reproductive performance. Each group's reproductive performance was estimated by calculating the difference between the observed number of immatures and the number expected from its population average. Of four group structure variables tested, only one - the residual of the adult and subadult sex ratio - was a consistent correlate of reproductive performance across the howler monkey populations. Groups with a greater proportion of adult and subadult males contained more juveniles than expected from the population average. I propose that the survival or retention of immatures within howler monkey groups depends in part on the behavior of resident males. Of particular importance, the relative proportions of resident males and females were more informative than the absolute number of males or females. On this basis, I evaluate the possible role of males in protection from predation, conspecific aggression, and resource competition. The techniques used here can also be used to forecast major changes in demographic structure within populations.     

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.     

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.     

Smooth-billed ani (Crotophaga ani) predation on butterflies in Mato Grosso, Brazil: risk decreases with increased group size

Although most insects are vulnerable to predation by a variety of predators, including birds, there are few direct observational studies in the wild of avian predation on adult butterflies. We examined the predatory behavior of smooth-billed anis (Crotophaga ani) on butterflies, and the spacing behavior of the butterflies which were concentrated on a mineral-rich beach on the Cristalino River, in Mato Grosso, Brazil. We studied eight of the most regularly occurring butterfly species which came each morning to engage in "puddling." Most species of butterfly were closely associated with conspecifics, although nearest-neighbor distance varied among species. The pierids - "yellows" (Aphrissa statira, Phoebis trite), "oranges" (Phoebis argante), and sometimes "whites" (Daptoneura leucadia) - formed very dense groups (or clusters) of up to 1,000 individuals occasionally joined by a few kite swallowtails (Eurytides spp.). Most other butterfly species formed small groups (e.g., daggerwings, Marpesia spp.) or were dispersed individually and non-clumped over the beach (e.g., dingy purplewing, Eunica monima). Anis foraged using two strategies: rapid frontal attack on dense groups of butterflies (yellows, oranges, whites), and a stealthy approach to solitary butterflies (mainly purplewings) or those in small groups. For yellows, the most common butterfly caught by anis, the capture rate reached over 6 per 15 min per ani, and about 8% of those captured managed to escape. Capture rates were much lower for the other species. Time of day, age of the ani (adult or young-of-the-year), and total number of each butterfly species present accounted for variation in the number of each species captured by anis. The number of butterflies captured per 15 min increased as the number of butterflies present increased, but reached a threshold beyond which the capture rate did not increase. The capture rate per individual butterfly (individual risk) decreased with group size up to a group of 40 individuals and remained low with further increases. Thus a butterfly in a group of 100 was no less likely to be eaten than one in a group of 40. For individual ani forays into dense groups of pierids, an individual ani was unable to catch more than 16, regardless of group size. These data confirm the dilution effect of group size for butterflies; each individual yellow or orange was less at risk from ani predation when in a group.     

Seasonal variation in the degree of heterospecific association of two syntopic hyraxes (<Emphasis Type="Italic">Heterohyrax</Emphasis><Emphasis Type="Italic">brucei </Emphasis>and <Emphasis Type="Italic">Procavia capensis</Emphasis>) exhibiting synchronous parturition

Adult rock hyrax (Procavia capensis) and bush hyrax (Heterohyrax brucei) allocate much of their surface activity to being vigilant for vertebrate predators. Individuals of the two species associate for thermoregulatory basking on rock outcrops (koppies) and, in the Matobo National Park, Zimbabwe, frequently constitute heterospecific groups that produce offspring synchronously. Exposure to predators during basking is thought to put a high premium on vigilance, particularly during the presence of dependent offspring in nurseries. We predicted, therefore, an increase in the association of the two species of hyraxes when offspring were present because this would lead to larger groups, thus enhancing the ability to detect predators. Koppie aggregations of hyraxes were classified as homospecific or heterospecific according to basking group composition. Heterospecific association increased when offspring were present, and heterospecific groups were larger than homospecific ones. Fifty-one percent of nurseries were heterospecific for adults/subadults. During the pre-weaning phase (<2 months after birth), 85% of P. capensis and 65% of H. brucei juveniles were in nurseries of heterospecific basking groups. Heterospecific groups had more offspring than homospecific groups. Juvenile mortality is most evident after young are weaned and heterospecific associations break down. Heterospecific aggregation, through increased group size, may result in a higher probability of avoiding predators, thereby reducing the vulnerability of young.     

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.     

Diana monkeys, Cercopithecus diana, adjust their anti-predator response behaviour to human hunting strategies

In Taï National Park, Ivory Coast, humans with guns hunt monkeys for their meat. The poachers imitate animal calls to feign the presence of eagles or leopards, two predators to which monkeys react with high calling rates and approach. In the presence of humans, monkeys become silent and move off. A small area of the park is now avoided by poachers, due to the establishment of a field project on chimpanzees in 1979. This offered the opportunity to investigate whether sudden changes in predation pressure lead to a rapid alteration in prey behaviour. Playback experiments, using groups of Diana monkeys, Cercopithecus diana, as subjects, revealed that the poachers' strategy works well in the home range of the habituated chimpanzee group. However, monkeys which are frequently exposed to poachers are rarely fooled by the imitations. Adaptive discrimination abilities can thus be acquired or lost within the lifespan of individual monkeys.     

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.     

Anti-predator benefits of group living in white-nosed coatis (Nasua narica)

Predation is often considered an important factor in the evolution of sociality among animals. We studied mortality patterns and grouping behavior of white-nosed coatis (Nasua narica) at sites in southern Arizona, USA, and western Jalisco, México. Coatis were monitored by radio-tracking and recaptures for more than 3 years at each site. In both populations, predation by large felids, including jaguars (Panthera onca) and pumas (Puma concolor), accounted for more than 50% of mortality of adult coatis. Predation rates were significantly higher on solo coatis than on coatis in groups at both study sites. Predation rates were negatively related to group size in Arizona. However, mortality of juveniles, as measured by the ratios of juveniles to adult females, was not related to the number of adult females per group in Arizona or Jalisco. Coatis exhibit a suite of behaviors, including foraging with the juveniles in the center of the group, sharing vigilance, alarm calling, mobbing and attacking predators, and a highly synchronous birth season, that are all consistent with the hypothesis that predation has played an important role in shaping coati social behavior.     

Effects of howler monkey reintroduction on ecological interactions and processes

Rewilding has been an increasingly popular tool to restore plant–animal interactions and ecological processes impaired by defaunation. However, the reestablishment of such processes has seldom been assessed. We investigated the restoration of ecological interactions following the reintroduction of the brown howler monkey (Alouatta guariba) to a defaunated Atlantic forest site. We expected the reintroduction to restore plant–animal interactions and interactions between howlers and dung beetles, which promote secondary seed dispersal. We estimated the number of interactions expected to be restored by the reintroduction to provide the baseline interaction richness that could be restored. We followed the reintroduced howler monkeys twice a week for 24 months (337 hours total) to assess their diet. We used howler monkey dung in secondary seed dispersal experiments with 2484 seed mimics to estimate the removal rates by dung beetles and collected the beetles to assess community attributes. We compared the potential future contribution of howler monkeys and other frugivores to seed dispersal based on the seed sizes they disperse in other areas where they occur. In 2 years, howler monkeys consumed 60 animal-dispersed plant species out of the 330 estimated. Twenty-one dung beetle species were attracted to experimentally provided dung; most of them were tunnelers, nocturnal, and large-sized (>10 mm). On average 30% (range 0–100%) of the large seed mimics (14 mm) were moved by dung beetles. About 91% of the species consumed by howlers (size range 0.3–34.3 mm) overlapped in seed size with those removed by dung beetles. In our study area, howler monkeys may consume more large-seeded fruit species than most other frugivores, highlighting their potential to affect forest regeneration. Our results show reintroductions may effectively restore ecological links and enhance ecological processes.     

Habitat fragmentation and effects of herbivore (howler monkey) abundances on bird species richness

Habitat fragmentation can alter herbivore abundances, potentially causing changes in the plant community that can propagate through the food web and eventually influence other important taxonomic groups such as birds. Here we test the relationship between the density of red howler monkeys (Alouatta seniculus) and bird species richness on a large set of recently isolated land-bridge islands in Lago Guri, Venezuela (n = 29 islands). Several of these islands host relict populations of howler monkeys at densities up to more than 30 times greater than those on the mainland. These "hyperabundant" herbivores previously have been shown to have a strong positive influence on aboveground plant productivity. We predicted that this should lead to a positive, indirect effect of howler monkey density on bird species richness. After accounting for passive sampling (the tendency for species richness to be positively associated with island area, regardless of differences in habitat quality) we found a significant positive correlation between howler monkey density and bird species richness. A path analysis incorporating data on tree growth rates from a subset of islands (n = 9) supported the hypothesis that the effect of howler monkeys on the resident bird communities is indirect and is mediated through changes in plant productivity and habitat quality. These results highlight the potential for disparate taxonomic groups to be related through indirect interactions and trophic cascades.     

Does sex affect both individual and collective vigilance in social mammalian herbivores: the case of the eastern grey kangaroo?

In several vertebrate taxa, males and females differ in the proportions of time they individually devote to vigilance, commonly attributed to sex differences in intra-specific competition or in absolute energy requirements. However, an effect of sex on collective vigilance is less often studied (and therefore rarely predicted), despite being relevant to any consideration of the adaptiveness of mixed- vs single-sex grouping. Controlling for group size, we studied the effect of sex on vigilance in the sexually dimorphic eastern grey kangaroo Macropus giganteus, analysing vigilance at two structural levels: individual vigilance and the group’s collective vigilance. Knowing that group members in this species tend to synchronise their bouts of vigilance, we tested (for the first time) whether sex affects the degree of synchrony between group members. We found that females were individually more vigilant than males and that their vigilance rate was unaffected by the presence of males. Collective vigilance did not differ between female-only and mixed-sex groups of the same size. Vigilance in mixed-sex groups was neither more nor less synchronous than in single-sex groups of females, and the presence of males seemed not to affect the degree of synchrony between females. Sixty-six percent of vigilant acts were unique (performed when no other kangaroo was alert), and only about one unique vigilant act in every three induced a collective wave of vigilance. The proportions of vigilant acts that were unique were 60% for females but only 46% for males. However, the sexes differed little in the rates at which their unique vigilant acts were copied. This limited study shows that the differences in vigilance between male and female kangaroos had no discernible effect upon collective vigilance.     

The relationship between dissolved oxygen concentration and maximum size in deep-sea turrid gastropods: an application of quantile regression

Bathymetric gradients in body size are the most well-known patterns of geographic variation in deep-sea organisms. The causes of size-depth relationships remain uncertain, but most have been attributed to rates of nutrient input. Chapelle and Peck (1999, Nature 399:114-115) recently hypothesized that body size in marine invertebrates is a function of dissolved oxygen concentration. We tested this hypothesis by using quantile regression techniques to assess the relationship of dissolved oxygen levels to maximum size in deep-sea turrid gastropods collected from the North Atlantic. Relationships were examined for a group of nine turrid species and within the abundant lower bathyal species Benthomangelia antonia (Dall, 1881). We controlled the analysis for depth because size in deep-sea gastropods varies bathymetrically. When the effects of depth are accounted for statistically, maximum size in B. antonia increases with increasing levels of dissolved oxygen. In turrids as a group, both depth and oxygen appear to explain significant proportions of the variance in maximum size. These findings suggest that a suite of factors, including dissolved oxygen concentration, may influence maximum size in deep-sea organisms.     

Vigilance of mustached tamarins in single-species and mixed-species groups—the influence of group composition

Species that participate in mixed-species groups (MSG) may have complementary roles in antipredator strategies. We studied vigilance in mustached tamarins (Saguinus mystax), small arboreal primates that form stable mixed-species groups with saddleback tamarins (Saguinus fuscicollis), in order to examine how the direction of vigilance changes with different species group compositions and whether the division of labor between the two species can be confirmed. We did so by comparing quantitative and qualitative differences in vigilance behavior between same individuals in and out of association (case A); MSG and single-species groups of the same total group size from two different populations (case B); and MSG of the same group size but with a different ratio of conspecifics to heterospecifics (case C). We predicted that individuals would increase downward scanning when heterospecifics are absent or their percentage is low, but total vigilance would increase only in case A due to the group size effect. However, mustached tamarins increased total vigilance due to horizontal scanning in cases A and C, and the predictions were confirmed only in small-sized groups in case B. Thus, we found indications that associating tamarin species in MSG might complement each other in the direction of vigilance, but the division of labor alone does not satisfactorily explain all the findings. There appear to be other mechanisms at work that define how direction of vigilance changes with group size and species composition. Complementarity of species probably occurs due to species vertical stratification rather than differences in the direction of vigilance.     

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.     

Mean colony relatedness is a poor predictor of colony structure and female philopatry in the communally breeding Bechstein's bat (Myotis bechsteinii)

In order to understand why animals are social and how group members interact with each other it is important to know their relatedness. However, few studies have investigated the genealogy in complete social groups of free-living animals with low reproductive skew. This holds particularly true for bats. Although almost all bat species are social, their sociobiology is not well understood. Because they are volant, nocturnal and have a rather cryptic life-style, bats are difficult to observe in the wild. Furthermore females are generally gregarious making genetic parent-offspring assignment a challenging task. We used genetic markers in combination with knowledge about age and colony membership of individually marked bats to construct pedigrees in completely sampled maternity colonies of Bechstein's bats (Myotis bechsteinii). Despite considerable fluctuations in population size, no immigration occurred over 5 years in four colonies living in close proximity. Additionally, confrontation tests showed that females of one maternity colony were able to detect and attempted to prevent the intrusion of foreign females into a roost they occupy. Although colonies were absolutely closed, and 75% of the colony members lived together with close relatives (rS=0.25), mean colony relatedness was nearly zero (0.02). Average relatedness therefore is a poor estimator for the potential of kin selection in Bechstein's bat colonies and may be misleading when attempting to understand the social structure of animals living in groups where many members breed. Based on our results we discuss the potential adaptive value of living in closed societies with low reproductive skew.     

Vigilance for predators: detection and dilution effects

Summary Grouped individuals are less vigilant for predators than solitary conspecifics because (1) grouping increases the likelihood of predator detection (detection effect) and (2) grouping makes it less likely that any given individual will be preyed upon (dilution effect). However, many models of vigilance behaviour consider only the detection effect, and the interaction of the two effects has been insufficiently considered. I present two models of vigilance behaviour and test them using data on the vigilance of elk, Cervus elaphus. The first model, based on the detection effect alone, is implicit in many published formulations of the relationship between vigilance and group size. Although it predicts the direction of the relationship between vigilance and group size, it provides a poor explanation of the form of the relationship. The second model incorporates both detection and dilution effects. Regression analysis on this security model indicates that the model provides a good prediction of both the direction and the form of the relationship between vigilance and group size, explaining 69% of the variance in vigilance frequency. The security model demonstrates that both detection and dilution are important in determining the frequency of vigilance behaviour but that the relative importance of these two effects changes across group size, with detection providing relatively less benefit as group size increases. However, even when groups are large, individuals should exhibit at least some vigilance because although dilution alone provides much protection from predation, even a low level of vigilance greatly increases the likelihood that an individual will survive repeated predation attempts.     

Carotenoid-based status signalling in red-shouldered widowbirds (<Emphasis Type="Italic">Euplectes axillaris</Emphasis>): epaulet size and redness affect captive and territorial competition

In breeding plumage, the African male red-shouldered widowbirds (Euplectes axillaris) are black except for red carotenoid-based epaulets ('shoulder patches'), similar to the well-studied American red-winged blackbirds (Agelaius phoeniceus). To experimentally test the signal function of the red epaulets in male red-shouldered widowbirds, we manipulated epaulet colour and size (within natural variation), and observed the effects in two competitive contexts. First, in captivity, unfamiliar males with epaulets of different size or redness were staged in dyadic contests over food. Only epaulet manipulations significantly affected contest outcome; red epaulet males out-competed orange and control males, which in turn dominated blackened (no epaulet) males. Epaulet size manipulations had particularly strong effects; enlarged epaulet males vigorously defeated smaller epaulet males within colour treatments, whereas the independent effect of 'redness' (i.e., within size treatments) was much weaker. Second, in a field experiment, epaulets were manipulated prior to territory establishment. Males with enlarged epaulets acquired territories, whereas most males with blackened or reduced signals failed to obtain territories. Furthermore, among the territorial males, birds with enlarged epaulets defended larger territories and spent less time in boundary signalling, yet they received fewer intrusions from conspecifics. In contrast, epaulet manipulations had no effect on either female visitation rates or subsequent female settlement. These results concur with recent studies and suggest that the carotenoid-based epaulets of red-shouldered widowbirds are status signals, sexually selected through male contest competition for territories.     

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.     

Predator-specific alarm calls in Campbell's monkeys, Cercopithecus campbelli

One of the most prominent behavioural features of many forest primates are the loud calls given by the adult males. Early observational studies repeatedly postulated that these calls function in intragroup spacing or intergroup avoidance. More recent field experiments with Diana monkeys (Cercopithecus diana) of Taï Forest, Ivory Coast, have clearly shown that loud male calls function as predator alarm calls because calls reliably (1) label different predator classes and (2) convey semantic information about the predator type present. Here, I test the alarm call hypothesis another primate, the Campbell's monkey (C. campbelli). Like Diana monkeys, male Campbell's monkeys produce conspicuous loud calls to crowned hawk eagles (Stephanoaetus coronatus) and leopards (Panthera pardus), two of their main predators. Playback experiments showed that monkeys responded to the predator category represented by the different playback stimuli, regardless of whether they consisted of (1) vocalisations of the actual predators (crowned hawk eagle shrieks or leopard growls), (2) alarm calls to crowned hawk eagles or leopards given by other male Campbell's monkeys or (3) alarm calls to crowned hawk eagles or leopards given by sympatric male Diana monkeys. These experiments provide further evidence that non-human primates have evolved the cognitive capacity to produce and respond to referential labels for external events.