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.     

Anti-predation behaviour of red colobus monkeys in the presence of chimpanzees

Predator-prey interactions are usually regarded as evolutionary “arms races”, but evidence is still scarce. We examined whether the anti-predation strategies of red colobus monkeys (Procolobus badius) are adapted to the hunting strategies of chimpanzees (Pan troglodytes) in the Taï National Park, Ivory Coast. Taï chimpanzees search for red colobus groups, approach them silently and hunt co-operatively. Our playback experiments and observations of natural encounters revealed that red colobus hid higher up the trees in positions where exposure to the forest floor is minimal and became silent, when chimpanzees were close. They moved away silently through the canopy, when chimpanzees were still at some distance. However, if a group of diana monkeys was nearby in the latter situation, red colobus sought their presence even if they had to move towards the chimpanzees. Chimpanzees refrained from hunting associated red colobus groups, probably because diana monkeys are excellent sentinels for predators approaching over the forest floor. Thus several elements of both the predator's and the prey's strategies correspond to each other. Finally, we compared the interactions between the two species in Taï and in Gombe, Tanzania. We suggest that the difference in size ratio between the two species at the two sites and adaptation of hunting techniques and of escape modes to different forest structures can explain why Gombe red colobus attack chimpanzees while Taï red colobus try to escape. We conclude that predator-prey interactions can indeed lead to evolutionary arms races, with the specific form of co-adaptations depending on environmental factors.     

The acoustic structure of chimpanzee pant-hooting facilitates chorusing

Duetting or chorusing behaviour occurs in a wide variety of animals and is posited to fulfil various important functions including territory defence and social bonding. The structure of calls produced in choruses might be shaped in a way that facilitates such joint vocal displays. In this study, we test the hypothesis that flexibility to modify the temporal structure of chimpanzee pant-hoots, vocalisations often given jointly with other individuals, facilitates chorusing. The results of this study, which was conducted on two communities of wild chimpanzees in Uganda, support this hypothesis. First, the duration of the build-up phase of the pant-hoot correlated with the latency with which the partner joined in the call, suggesting that males prolong the duration of the build-up to allow others to join in the call and to increase the likelihood of a chorus occurring. Second, the loud climax phases were significantly longer when produced in choruses than alone, which suggests that males prolong this part of the call when calling in choruses. Within chorus pant-hoots, there was a positive relationship between the number of climax elements given by two calling partners, suggesting that males adjust the temporal structure of their call to mirror their partner's call. We conclude that the basic acoustic structure of chimpanzee pant-hoots and the flexibility with which males adjust the duration of the constituent phases promote chorusing, and that the temporal structure of this rather stereotyped vocalisation is sensitive to fine details of the vocal responses of the audience.     

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.     

Predicting emergence, chorusing, and oviposition of periodical cicadas

Periodical cicadas in the genus Magicicada have an unusual life history that includes an exceptionally long life cycle and a massive, synchronized emergence. Distributions in woodland habitat are extremely patchy, and an unresolved problem is how the patchiness is generated and maintained. We undertook a study in Princeton, New Jersey, USA, to determine if habitat factors such as tree height, distance to the nearest neighbor, and amount of foliage influence distributions of nymphal emergences, centers of chorusing aggregations, and oviposition sites. Emerging nymphs were counted, chorus centers were identified by measuring decibel levels of their songs, and oviposition was estimated from the foliage "flags" that are produced by trees in response to the damage caused by egg-laying. All three distributions were mapped on 50 trees in a human-managed area of 75 x 130 m. We were unable to identify habitat features that were associated with the distribution of emergences, except that tulip trees (Liriodendron) had significantly fewer emergences than two other genera, ash (Fraxinus) and beech (Fagus). Using multiple linear regression analysis, we found that the distribution of emergences was the best predictor of the distribution of chorus centers and oviposition sites. In an analysis of ash trees alone, tree height and spacing, in addition to cicada emergences, predicted chorus centers and oviposition incidence. Thus the distribution of the offspring generation (oviposition) is shown to be similar to the parental generation (emergence). We suggest that their stability is maintained across generations by extremely low dispersal and mutual attraction. Aggregations may be thought of as self-perpetuating, randomly distributed assemblages, initially established through the interaction of factors, including successful exploitation of underground resources, and avoidance of fungal disease and aboveground predation in the development of high-density mating aggregations.     

Environmental and social factors influence chorusing behaviour in a tropical frog: examining various temporal and spatial scales

Many animals use conspicuous display to attract mates, and there should be selection for displays to occur at times and places that maximise the probability of mating, while minimising energetic costs and predator attraction. To select the best times for display, individuals may use environmental cues, the presence of other individuals, or both, but few studies have examined these sources of variation in display activity. In this study, we examined physical environmental and social factors triggering displays in a tropical, terrestrially breeding frog, Cophixalus ornatus. To measure the influence of physical environmental conditions on calling activity, we recorded temperature, rainfall, moon illumination/visibility, humidity, barometric pressure and intensity of calling activity throughout a breeding season at six locations along a 560-m transect. The intensity of calling varied daily, seasonally, and at a small spatial scale. Variation in calling activity from day to day was large. There was also a strong seasonal trend in calling activity: few males called at the start of the season, activity peaked shortly after the beginning of the season, and then declined linearly from the peak to the end of the season. There was also consistent variation among sites along the transect, which may have been due to variations in frog density at each site, or to consistent microscale variations in physical conditions, or both. After statistically removing consistent local variation among sites, a principal components analysis suggested that a maximum of 35.8% of the variation in calling activity among days was due to factors common to all sites, such as weather, moon illumination, or large-scale social facilitation (e.g. of choruses by other choruses). The remainder of the variation among sites (64.2%) was due to site-specific factors, such as small-scale social facilitation or unmeasured, apparently stochastic effects, such as microenvironmental physical factors that do not vary consistently over sites. Regressions of environmental variables on residual calling activity (after removing consistent effects of site and season), alone or in combination, accounted for very little of the variation in the number of calling males (maximum 10%). Thus, our data, showing strong seasonal effects and consistent variation among sites combined with large amounts of variation in the number of calling males at small spatial scales, suggest that environmental conditions, such as temperature, rainfall, moon illumination and barometric pressure, which act over large spatial scales, may determine the overall environmental envelope within which calling can occur but do not account for most of the variation in the number of calling males on a day-to-day or site-to-site basis. Similarly, variations in the number of calling males at small spatial scales suggest that social facilitation is a relatively unimportant trigger for displays on a large scale in these frogs. On the other hand, our data suggest that social facilitation may have important effects on variation in the number of calling males on a day-to-day and site-to-site basis. We used playback experiments to assess whether the sound of calling could initiate displays. We played either a taped chorus or white noise in areas where few (zero to two) males were calling. The number of calling males increased both during and after the chorus stimulus, whereas there was no increase in calling in response to white noise. These data suggest that examining variation in calling activity at small spatial scales can reveal the sources of variation for the number of calling males, and indicate that, in these frogs, males tend to use the calling of other individuals as a cue to determine when to display. Received: 19 October 1999 / Revised: 30 June 2000 / Accepted: 26 August 2000     

Mother-infant behavior in vervet monkeys

Summary Mother-infant behavior of 9 vervet monkey mothers who had failed in their last pregnancy were compared to the behavior of 14 mothers who had been successful in the prior year and to 11 primiparous mothers. The results indicated that females responded to the loss of one infant by increasing their level of care for their next infant. Females who had failed in their last pregnancy encouraged ventral contact and were more restrictive of their infant's movements, they gave more care and attention to their infants, and they played a greater part in keeping their infants near, compared to mothers who had been successful in their last pregnancy. Mothers who had failed in their last pregnancy were also more attentive and protective toward their infants than primiparous mothers who had had no prior reproductive experience. The increase in maternal care by females who had failed in their last pregnancy was accompanied by an increase in the interval to the birth of their next infant. These differences could not be completely explained by differences in the mothers' age or in the presence of other immature offspring. They suggest that vervet mothers can adjust their level of parental care based on the quality of their past experience, and that these adjustments have an effect on the mother's future reproductive potential.     

Carbohydrate and calling: Depletion of muscle glycogen and the chorusing dynamics of the neotropical treefrog Hyla microcephala

Chorusing males of the neotropical treefrog Hyla microcephala call in distinct bouts punctuated by periods of silence, a pattern known as unison bout singing. Schwartz (1991) previously tested and refuted the hypotheses that males periodically stop calling either because of a female preference for males that call cyclically, or because high ambient noise levels inhibit vocal activity. Males of H. microcephala are vocally responsive to the calls of other males, and during calling bouts their rate of note production can exceed 10,000 per hour. In natural choruses females preferentially pair with males that call at the higher rates. Because females can pair with males over many hours, males may stop calling periodically to save energy so they can continue to call for the entire period that females are available. We directly tested this energy conservation hypothesis by collecting samples of males early in the evening just after chorusing commenced and later when chorusing had ended for the night. Trunk muscles (internal and external oblique), which are responsible for the airflow associated with note production, were dissected, frozen, and their glycogen content measured. Data on calling behavior were obtained for late-evening samples. Individual calling behavior was not correlated with a males final glycogen level. In addition, many males ended their calling before glycogen reserves were exhausted, indicating that factors other than energy can determine when males finally stop chorusing, However, the biochemical assays supported the energy conservation hypothesis. Unless chorusing was punctuated by pauses, most males would have been unable to sustain high rates of calling for an entire evening without exhausting glycogen reserves in their trunk muscles. Because the time females pair with males is probably unpredictable to males, the ability to call for long periods may improve a males chances of mating.     

An agent-based model of red colobus resources and disease dynamics implicates key resource sites as hot spots of disease transmission

The effect of anthropogenic landscape change on disease in wildlife populations represents a growing conservation and public health concern. Red colobus monkeys (Procolobus rufomitratus), an endangered primate species, are particularly susceptible to habitat alteration and have been the focus of a great deal of disease and ecological research as a result. To infer how landscape changes can affect host and parasite dynamics, a spatially explicit agent-based model is created to simulate movement and foraging of this primate, based on a resource landscape estimated from extensive plot-derived tree population data from Kibale National Park, Uganda. Changes to this resource landscape are used to simulate effects of anthropogenic forest change. With each change in the landscape, disease outcomes within the simulated red colobus population are monitored using a hypothetical microparasite with a directly transmitted life cycle. The model predicts an optimal distribution of resources which facilitates the spread of an infectious agent through the simulated population. The density of resource rich sites and the overall heterogeneity of the landscape are important factors contributing to this spread. The characteristics of this optimal distribution are similar to those of logged sections of forest adjacent to our study area.     

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.     

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.     

Birth synchrony in squirrel monkeys (Saimiri oerstedi)

Summary The vigilance behaviors and association patterns of adult female squirrel monkeys (Saimiri oerstedi) in Parque Nacional Corcovado, Costa Rica were studied over the annual reproductive cycle to identify a possible adaptive function associated with the unusually close within-group birth synchrony prevalent in Saimiri populations. Raptor association with the troops, predation attempts, and monthly changes in food abundance were also documented. Seasonal fluctuations in food abundance probably constrained the timing of births among three contiguous troops to a two month period. The close within-troop birth synchrony (majority of births occurring within a week) is suggested to be advantageous because of intense predation pressure on neonate squirrel monkeys. Adult females with neonates cooperate in anti-predator vigilance and defense of neonates. Participation in these maternal associations may increase the probability of neonate survivorship. Variable gestation length in squirrel monkeys may reflect a lability in the duration of gestation to allow coordination of the timing of births among females in a troop.     

Mating patterns in squirrel monkeys (Saimiri oerstedi)

Summary The mating system of squirrel monkeys (Saimiri oerstedi) in Parque Nacional Corcovado, Costa Rica was studied and used to develop a model to interpret the evolution of seasonal sexual dimorphism in squirrel monkeys (Saimiri spp.). Adult male body weights in captivity and the wild may increase more than 20%, beginning approximately two months prior to and continuing through the annual two month, breeding season. Female inter-troop transfer was common in the study population, but male troop residence was stable. Instances of agression among adult males in the troop, even in sexual contexts, were rare. Reproductively mature males enlarged to varying degrees by the start of the breeding season and cooperated in mobbing females to olfactorily evaluate female, estrous condition. Female mate preference corresponded to a ranking based on relative male enlargement. The largest male obtained 70% of the copulations observed in the 1984 breeding season. Little evidence exists that females typically mate with more than one male during the period of peak receptivity. Seasonal enlargement in males is suggested to be the result, of both male intrasexual competition and female choice.     

Time as a constraint on group size in spider monkeys

An animal can only survive in a given habitat if it has enough time to find, process and digest food whilst avoiding predation. The time it has for food acquisition is affected by the vegetation and competition with conspecifics, which depends on aggregation tendencies. We used the relationships between time allocations, on the one hand, and climatic variables (as a proxy for habitat quality) and group size, on the other, to develop a model that predicts maximum ecologically tolerable group size at different locations for spider monkeys. Spider monkeys are particularly interesting because the social communities often split up into small units. Temperature variation and rainfall variation were the main determinants of time budgets. Community size and average annual rainfall determined party size. The model correctly predicted presence or absence of spider monkeys at 78–83% of 217 New World forest sites. Within the geographical range of the species, this time budget model predicted the presence of spider monkeys better than a model based directly on climate variables. Predicted community and party sizes were significantly larger at sites where spider monkeys are present than at sites where they are absent. As required by the model, predicted maximum community sizes were significantly larger than observed community sizes. Moving time showed a U-shaped relationship with party size, which suggests that moving time is the factor that keeps spider monkey communities from travelling together in a tight group.     

Male responsiveness to infant distress calls in free-ranging vervet monkeys

Summary Playback experiments were conducted of five groups of free-ranging vervet monkeys (Cercopithecus aethiops) to determine whether an adult male's responsiveness to infant distress calls was a function of (1) paternal certainty, (2) dominance rank, (3) predator presence, (4) number of males, (5) number of infants, (6) infant's mother's rank and/or (7) infant's age. Results from these experiments reveal that paternal certainty was the only factor that could directly explain the differences between males in the duration of response to distress calls.     

Genetic differentiation among matrilines in social groups of rhesus monkeys

Summary In rhesus monkey populations, animals related by descent to some female comprise a matriline or genealogy. Data on blood protein polymorphisms in the Cayo Santiago rhesus colony indicate that allele frequency variations among matrilines in social groups are large. These variations occur despite high levels of outbreeding. Computer simulation analyses indicate that pedigree or linear effect account for much of the observed genetic differentiation among genealogies. A sampling with correlation model in which genealogy sizes and average kinship levels are parameters predicts among matriline genetic differentiation. This study indicates that substantial genetic substructure is present within rhesus social groups. Our analyses also predict that large variances in allele frequencies should be common among social or trait groups based on kinship relationships.     

Facial asymmetry is negatively related to condition in female macaque monkeys

The face is an important visual trait in social communication across many species. In evolutionary terms, there are large and obvious selective advantages in detecting healthy partners, both in terms of avoiding individuals with poor health to minimise contagion and in mating with individuals with high health to help ensure healthy offspring. Many models of sexual selection suggest that an individual's phenotype provides cues to their quality. Fluctuating asymmetry is a trait that is proposed to be an honest indicator of quality, and previous studies have demonstrated that rhesus monkeys gaze longer at symmetric faces, suggesting preferences for such faces. The current study examined the relationship between measured facial symmetry and measures of health in a captive population of female rhesus macaque monkeys. We measured asymmetry from landmarks marked on front-on facial photographs and computed measures of health based on veterinary health and condition ratings, number of minor and major wounds sustained and gain in weight over the first 4?years of life. Analysis revealed that facial asymmetry was negatively related to condition-related health measures, with symmetric individuals being healthier than more asymmetric individuals. Facial asymmetry appears to be an honest indicator of health in rhesus macaques, and asymmetry may then be used by conspecifics in mate-choice situations. More broadly, our data support the notion that faces are valuable sources of information in non-human primates and that sexual selection based on facial information is potentially important across the primate lineage.     

Fissioning minimizes ranging costs in spider monkeys: a multiple-level approach

The adjustment to deal with intragroup food competition is probably the most plausible explanation of high levels of fission–fusion dynamics. However, studies did not always support expected relations between food availability, ranging costs, and subgroup size. We used several levels of analysis differing in the time and spatial scale in order to investigate this explanation in spider monkeys. In our study, subgroups were larger when food availability was higher across most levels of analyses used. We also found a fine-scale adjustment: compared to the food patch previously visited, spider monkeys traveled to larger patches just after fusions. This was not without an immediate travel cost: the interpatch distance and travel time after a fusion were longer than that before the fusion. This rapid adjustment shows the flexibility that fission–fusion dynamics can offer. Spider monkeys are in large subgroups only when food conditions are favorable, as evidenced by the fact that at all the other time-scale levels larger subgroups did not experience greater ranging costs than smaller subgroups. Our results indicate that on the whole spider monkeys successfully minimize ranging costs by fission and fusion of subgroups.