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Understanding the ecological and social factors that influence group size is a major focus of primate behavioural ecology. Studies of species with fission–fusion social organizations have offered an insightful tool for understanding ecological drivers of group size as associations change over short temporal and spatial scales. Here we investigated how the fission–fusion dynamics of spider monkeys (Ateles geoffroyi) at Runaway Creek, Belize were affected by fruit availability. When males and females were analyzed together, we found no association between fruit availability and subgroup size. However, when females were analyzed separately, we found that when fruit availability increased, so did subgroup size. In all analyses, higher fruit availability did not influence subgroup spatial cohesion. Our results point to the complexity of understanding grouping patterns, in that while ecological factors make groups of specific sizes advantageous, social factors also play an important determining role.

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships. Publisher PDF

Spider monkeys (Ateles sp.) are characterized by high fission-fusion dynamics, meaning their social grouping pattern is fluid and consists of subgroups that vary in size, composition, and spatial cohesion over time. In this study, we quantify the fission-fusion dynamics of a group of spider monkeys at Runaway Creek Nature Reserve in Belize by measuring subgroup size, spatial cohesion, and stability using data spanning 5 years. We then test whether variation in these three subgroup measures differ according to season, subgroup sex composition, and the reproductive status of female subgroup members. Our results show that subgroups were larger in size and less stable in membership during the wet season compared to the dry season. All-female subgroups were less spatially cohesive but more stable in membership than all-male subgroups. Finally, we report that subgroups with one or more non-lactating females (i.e., without nursing young) were smaller on average than subgroups containing lactating females with nursing young. These data contribute to a growing body of research documenting the ecological and social dimensions along which grouping patterns might vary.

Popular and scientific interest in menopause in humans has led to an increased interest in the extent of post-fertile life in other animals, particularly in long-lived social species such as other primates and cetaceans. Information on maximum lifespan achieved and age at last birth are available from long-term observations of known individuals from 11 primate species in the wild. Comparable information from wild cetaceans are more difficult to obtain; however there are relevant fisheries data, as well as a small number of long-term individual-based studies. Using post-reproductive representation (PrR) as a population measure of post-fertile lifespan that allows comparisons across populations and species, this review confirms that among primates, only humans have a maximum lifespan significantly longer than 50 years, and only human female life history includes a significant post-fertile stage of life. We conclude that although a prolonged post-fertile stage of life is very rare in mammals, it does occur in some exceptionally long-lived taxa, such as humans and resident killer and short-finned pilot whales. Thus menopause evolved independently at least three times in mammals, and the reasons for its evolution may differ in different lineages.

In species in which males and females exhibit different association patterns, the use of vocalizations that regulate interindividual distance may differ between the sexes. Spider monkey social groups are characterized by high fission–fusion dynamics and sex differences in association patterns; female–female associations have been described as more passive than those between philopatric males. Individuals of both sexes produce whinny vocalizations, which may allow callers and receivers to mediate interindividual spacing based on existing social relationships. As such, we hypothesized individuals of each sex would use whinny vocalizations at different rates and in different contexts. To investigate sex differences in the rate of whinnying across behavioral contexts, we collected focal animal samples on Yucatan spider monkeys (Ateles geoffroyi yucatanensis) over 8 mo at Runaway Creek Nature Reserve, Belize. In addition, we recorded all changes in subgroup composition to investigate whether a female’s likelihood of calling was influenced by the number of conspecifics joining, or leaving their subgroup. We found that females called at higher rates than males in most behavioral contexts, especially foraging. The probability that females would call increased during subgroup fissions and fusions, and correlated positively with the number of individuals joining or leaving their subgroup. Male calling rates did not differ across contexts, and males generally called less than females. Our results suggest that whinnying by females may allow callers to mediate interindividual spacing in contexts where proximity risks increasing feeding competition. In species in which the sexes associate in qualitatively different ways, vocalizations may play a role in maintaining these differences.

Sexual segregation is a recognized dimension of the socioecology of many vertebrates, but it has not been systematically examined in primates. We investigated temporal patterns of sexual segregation in spider monkeys (Ateles geoffroyi yucatanensis) using a test that distinguishes sexual segregation from aggregation and random association between the sexes. We further investigated how sexual segregation varies over time as a function of food availability, and then tested other possible factors that might be causally linked to sexual segregation in spider monkeys. We predicted that male philopatry and cooperative territorial defence leads to sexual dimorphism in behavior, which in turn creates different optimal energetic requirements for males and females as reflected in differing activity budgets and diet. We investigated sexual segregation in a group of 33–35 spider monkeys at Runaway Creek Nature Reserve in Belize over 23 mo in 2008–2009. We used the sex compositions of subgroups recorded in scan samples to test the occurrence of sexual segregation at monthly and biweekly time scales.We found that males and females were significantly segregated in 15 out of the 23 mo of the study, and that periods of nonsegregation coincided with months of low food availability. The sexes differed significantly in activity and diet; males spent more time traveling, and less time resting and feeding than females, and they had a higher proportion of ripe fruits in their diets than did females. We propose that sexual segregation in spider monkeys is primarily a form of social segregation that results from males and females pursuing optimal dietary and behavioral strategies to satisfy sex-specific energetic demands. We further suggest that sexual segregation represents an important constraint on fission–fusion dynamics that should be considered when assessing the potential for variability in subgroup composition.

Financial sup-port for this research was received from the Natural Sciences andEngineering Research Council of Canada (NSERC), NationalGeographic, The Inter national Primatological Society, Sigma Xi,and The Depar tment of Anthropology, Faculty of Social Sciencesand Faculty of Graduate Studies at the University of Calgary.

Platyrrhine (New World) monkeys possess highly polymorphic color vision owing to allelic variation of the single-locus L/M opsin gene on the X chromosome. Most species consist of female trichromats and female and male dichromats. Howlers (genus Alouatta) are an exception; they are considered to be routinely trichromatic with L and M opsin genes juxtaposed on the X chromosome, as seen in catarrhine primates (Old World monkeys, apes, and humans). Yet it is not known whether trichromacy is invariable in howlers. We examined L/M opsin variation in wild howler populations in Costa Rica and Nicaragua (Alouatta palliata) and Belize (A. pigra), using fecal DNA. We surveyed exon 5 sequences (containing the diagnostic 277th and 285th residues for λmax) for 8 and 18 X chromosomes from Alouatta palliata and A. pigra, respectively. The wavelengths of maximal absorption (λmax) of the reconstituted L and M opsin photopigments were 564 nm and 532 nm, respectively, in both species. We found one M–L hybrid sequence with a recombinant 277/285 haplotype in Alouatta palliata and two L–M hybrid sequences in A. pigra. The λmax values of the reconstituted hybrid photopigments were in the range of 546~554 nm, which should result in trichromat phenotypes comparable to those found in other New World monkey species. Our finding of color vision variation due to high frequencies of L/M hybrid opsin genes in howlers challenges the current view that howlers are routine and uniform trichromats. These results deepen our understanding of the evolutionary significance of color vision polymorphisms and routine trichromacy and emphasize the need for further assessment of opsin gene variation as well as behavioral differences among subtypes of trichromacy. Electronic supplementary material The online version of this article (doi:10.1007/s10764-013-9705-9) contains supplementary material, which is available to authorized users.

As plants may contain low levels of some minerals including sodium, copper, and phosphorous, herbivores may become deficient in these nutrients. In 2001, Hurricane Iris hit the Monkey River Forest in Belize causing substantial damage to the food supply of the black howler monkey population (Alouatta pigra) living there. This included an 18-month absence in fruit production and a complete loss of figs that are high in calcium. In this article, we describe the post-hurricane diet of this monkey population and compare the mineral content of food items to each other and to recommendations for non-human primates [NRC 2003]. We also investigate food selection in relation to potentially limiting minerals. Behavioral data from four groups of howlers (2002-2006) and samples of all ingested food items were collected and a sample of 99 plant from 18 food species was analyzed for mineral content. Unexpectedly, the post-hurricane diet contained more mature leaves than new leaves despite the availability of new leaves. Leaves contained higher amounts of minerals than reproductive parts and with the exception of Cecropia peltata stems, plant parts were low in sodium. Cecropia peltata is a pioneer species that grows following habitat disturbance thus the ingestion of these stems may be a potential mechanism to avoid sodium deficiency in this damaged forest. Calcium and zinc were found above recommended values in most food items; however, both positively predicted food selection, which may reflect a difference between their abundance and their bioavailability. However, as mature leaves contained more calcium than other plant parts, their high post-hurricane consumption may also be a response to the absence of figs and the need to find an alternate calcium source. This study highlights how habitat disturbance may affect mineral abundance and the dietary choices of primates.

Infant tolerance by adult males has been observed in many primate species with multimale–multifemale mating systems, but males do not usually initiate interactions with infants. In male philopatric species, such as spider monkeys, adult males within a community exhibit high levels of cooperation and affiliation, and they might therefore be motivated to create bonds with potential future allies. Based on this hypothesis we predicted that adult male spider monkeys would participate in infant handling more than adult females and they would preferentially direct handling toward male infants. Between January 2008 and July 2010, we collected 884 h of observation on a community of wild spider monkeys at Runaway Creek Nature Reserve in Belize. During this period we observed 120 incidences of affiliative interactions between infants and adults other than their mother. The adult initiated the majority of nonmother adult–infant interactions (78 %). All available infants (5 males, 7 females) were handled during the study. All 9 of the community adult males handled infants but only 7 of 14 adult females did so. Adult males handled infants significantly more often than did adult females and males also handled young infants more often than older infants. Significant infant sex differences in handling appeared in infants >6 mo when adult males handled males significantly more than females. The patterns of infant handling among age–sex class dyads reflect the affiliative social patterns that we see in adult spider monkeys. These results provide support for the hypothesis that adult males preferentially handle male infants as a strategy for fostering social bonds.

Primates commonly consume leaves that are high in protein but low in digestion-inhibiting fibre. Due to the fact that mature leaves do not meet these criteria, they are typically avoided and many leaf-eating primates select for leaves high in protein and low in fibre leading to the theory that food selection is based on protein maximization. However, feeding records for a population of black howler monkey (Alouatta pigra) in Monkey River, Belize, collected over a 5-y period, together with synchronous phenological data, indicate that this population does not meet the expectation and actually prefer mature leaves. This study aims to describe the nutritional composition of the food supply and investigate the possibility that, rather than to maximize protein ingestion, mature leaves are eaten to balance nutrient intake. Macronutrient analyses (moisture, lipids, protein, NDF, ADF and simple sugars) were conducted on a sample of 96 plant samples from 18 food species of this population of black howler. Results reported here show that mature leaves eaten by howlers in this forest contain sufficient protein to meet minimum metabolic requirements (range: 11.6–24%; mean: 16.4% ± 3.8%) and have significantly higher concentrations of simple sugars than young leaves (means of 7.2% ± 2.7% vs. 4.4% ± 2.3% respectively). Thus, it appears that mature leaf ingestion is likely serving to balance energy and protein intake. This result may be due to the disruptive effects of a hurricane in 2001 that resulted in a loss of 80% of the howler population, changed forest composition and may have affected plant chemistry. Despite this, the data reported here suggest that the accepted view that mature leaves are simply fallback foods for primates, eaten only in times of preferred food scarcity, may have to be revised.

Although some environmental risks and resources are known to affect the evolution of primate social groups, we know little about the effect of major natural disturbances on primate populations. Hurricane Iris hit the Monkey River watershed in southern Belize in October 2001, presenting a unique opportunity to document the effects of a natural disaster under circumstances wherein some pre-hurricane data were available. We measured the characteristics of the population of black howlers in the affected forest 3.5 years after the storm and compared the population data with pre-hurricane data from a 52-ha study area, that may represent the larger continuous riverine forest and from which all monkeys were known. From February to May 2004, we sampled 28.77 km2 of the 96-km2 forest fragment via five transects walked 12 times each. From these data we estimate that the population in the watershed has dropped from 9784 to 1181 monkeys, a reduction of 88%, reflected by both a 79% drop in the number of social groups and a 38% reduction in group size. Before the storm, 75% of the social groups were multimale; after the storm, 74% of the groups were unimale. While the ratio of adult females to males improved slightly, the ratio of adults to immatures, and adult females to immatures more than doubled, indicating a much lower potential for growth. These data provide a quantitative assessment of how a major natural disturbance can affect a primate population.

Researchers consider group size in primates to be determined by complex relationships among numerous ecological forces. Antipredator benefits and better resource defense are the primary pressures for large groups. Conversely, intragroup limited food availability, can result in greater intragroup feeding competition and individual energy expenditure in larger groups, creating energetic advantages for individuals in small groups and placing an upper limit group size. However, the extent to which food availability constrains group size remains unclear for many species, including black howlers (Alouatta pigra), which ubiquitously live in small social groups (≤10 individuals). We studied the relationship between group size and 2 key indices of feeding competition—day journey length and activity budgets—in 3 groups of wild Alouatta pigra at a hurricane-damaged site in Belize, Central America. We controlled for differences in food availability between home ranges (food tree density) and compared both indicators of feeding competition directly with temporal variation in food availability for each group. Our results show no consistent association between resource availability, group size, and either index of competition, indicating that feeding competition does not limit group size at the site—i.e., that larger groups can form without increased costs of feeding competition. The results support the search for other explanations, possibly social ones, for small group size in the primates, and we conclude with suggestions and evidence for such alternative explanations.

Hurricanes frequently affect the forests of South and Central America; however, few studies have quantified their effects to forest structure, especially when concentrating on the food supply of an animal population. Hurricane Iris made landfall in Southern Belize on 8 October 2001, severely damaging a 52 hectare site where the behavioral ecology of a population of Central American Black Howlers (Alouatta pigra) had been under study for 2.5 yr. The hurricane resulted in a mortality rate of 35 percent for major food trees, which was primarily attributed to uprooting, snapping, and major delimbing. This damage accounted for 97 percent of the food tree loss between the two sample periods. Tree species differences were found in both the percentage loss and category of damage to food trees. Trees of different heights also experienced different percentage loss and levels of damage; subcanopy and emergent trees experienced higher loss than canopy trees, and subcanopy trees were frequently uprooted. This was partially attributed to a lack of buttressing on these subcanopy trees. Buttressing was found to decrease the frequency of uprooting. Tree size was the only factor that did not influence either damage or death. Trees from which fruit were eaten by black howlers died more than twice as often as did trees eaten for leaves.

The diet and activity of a population of Alouatta pigra were compared before and immediately after a major hurricane to begin to explore how the monkeys cope with severe habitat destruction. Focal animal data were collected from January to April (dry season) for two seasons before (368 h) and one season after the storm (149 h) on a population of black howlers in Monkey River, Belize. During the first dry season after the storm, the monkeys changed their diet in direct accordance with the availability of food. The absence of fruit and flower production and the increase in new leaf availability forced the monkeys to adopt a completely folivorous diet. The activity budget of the monkeys also changed, and they spent more time inactive, which may be linked to the change in the distribution and type of food available. They also spent less time in social interactions, which may be due to the lower number of juveniles in the population or to the formation of new groups between unfamiliar individuals following the hurricane. The ability to live for long periods of time on leaves alone has allowed the remaining population to survive in the short term.

The ecological-constraints model assumes that food items occur in depletable patches and proposes that an increase in group size leads to increased day range due to more rapid patch depletion. Smaller groups become advantageous when an increase in travel costs is not repaid by an increase in energy gained or some other fitness advantage. On the other hand, we also know that group size can be influenced by social factors. Here we contrast the diet and group size of red colobus (Procolobus badius) and black-and-white colobus (Colobus guereza) in Kibale National Park, Uganda to consider how ecological and social factors are affecting their group sizes. Subsequently, we examine whether the insights gained from this detailed comparison can provide an understanding of why the social organization and group size of mantled howlers (Alouatta palliata) and black howlers (A. pigra) differ. Two groups of red colobus and two groups of black-and-white colobus were studied over 10 months. Red colobus groups were larger (48 and 24) than black-and-white colobus groups (9 and 6). The two groups of red colobus overlap home ranges with the two groups of black-and-white colobus; 75% and 95% of their home ranges were within red colobus's home range. There was a great deal of similarity in the plant parts eaten by the two species and both species fed primarily on young leaves (red colobus 70%, black-and-white colobus 76%). In terms of the actual species consumed, again there was a great deal of similarity between species. The average dietary overlap among months for the two neighboring groups of red colobus was 37.3%, while the dietary overlap between the red colobus and the black-and-white colobus group that had its home range almost entirely within the home range of the red colobus groups averaged 43.2% among months. If ecological conditions were responsible for the difference in group size between the two colobine species, one would expect the density of food trees to be lower in the home ranges of the black-and-white colobus monkeys, since they have the smaller group size. We found the opposite to be true. Both black-and-white colobus groups had more food trees and the cumulative size of those trees was greater than those in the red colobus's home ranges. We quantify how these differences parallel differences in mantled and black howlers. The average group size for mantled howlers was 12.9 individuals, and for black howlers it was 5.3 individuals. We explore possible social constraints, such as infanticide, that prevent black-and-white colobus and black howlers from living in large groups.

This study reports on the diet and activity budgets of Central American black howling monkeys ( Alouatta pigra) at Monkey River, Belize. This is a previously unstudied population, close to the southern boundary of the species range, and it provides comparative data on A. pigra from a new study site. Both diet and activity are within the ranges reported for other A.pigra sites and for mantled howlers ( A. palliata). No age-sex differences could be discerned in either diet or activity, though monthly variation was apparent. The monkeys switch from consuming leaves 86% of the time in January to March to consuming 67% fruit in April to July. This difference was statistically significant, and provided the opportunity to compare activity levels of the monkeys over two dietary periods, one characterized primarily by folivory, the other by frugivory. Howlers are often seen as a relatively inactive species, something that is associated with a low quality, folivorous diet. However, A. pigra have been described as being as frugivorous as possible and as folivorous as necessary. Yet, despite the opportunistic consumption of large quantities of high-energy foods, A. pigra has been observed as conforming to the howler lifestyle, resting as much as 80% of the day. The data in this paper support both of these reports. Black howlers at Monkey River Belize are typically inactive, maintaining high levels of inactivity even during months characterized by frugivory, suggesting that diet is more flexible and varied than is behavior and calling into question the assumption that howler inactivity is due to the digestion of large quantities of leaves.

The opportunity to study the effects of a powerful hurricane on monkey populations, diet, and behavior via pre- and post-hurricane data was presented when hurricane Iris virtually destroyed the forest along Monkey River in southern Belize on October 8, 2001, including a 52-ha area where black howlers have been subjects since 1999. Before the hurricane, 8 social groups, averaging 6.37 members, had been stable in both group composition and range for ≥q 2 years. The hurricane, which levelled much of the forest, resulted in the complete loss of the forest canopy. The trees that remained standing lost most or all branches and were 100% defoliated. The monkey population in the study area was reduced by 42% and survivers experienced a period of extended social disorganization involving transient individuals, high numbers of solitary monkeys, and small fragmentary social groups. The period of disorganization lasted 12 weeks, after which the number of solitaries reduced and stability of the large groups increased. Within the study area, 5 social groups have been more or less stable since ca. week 15; however, home ranges had yet to stabilize at week 35. The social and ranging effects are similar to what has been described for translocated primates. Post-hurricane diet was limited to fruit and leaves remaining in the deadfall for the first 2 weeks and to new leaves and leaf buds for many weeks after that. Normal fruit consumption in April and May was prevented by the failure of surviving trees to produce fruit. With the loss of forest canopy there has been increased use of low foliage and ground travel, and with the reduction in population density there has been a reduction in vocalization frequency.

Evolutionary biologists often argue that menopause evolved in the human female as the result of selection for a postreproductive phase of life, during which increased maternal investment in existing progeny could lead to enhanced survivorship of descendents. Adaptive theories relating menopause to enhanced maternal investment are known as the mother (first-generation) and grandmother (second-generation-offspring) hypotheses. Although menopause—universal midlife termination of reproduction—has not been documented in primates other than humans, some researchers have argued that postreproductive alloprimates also have a positive impact on the survivorship of first and second generation progeny. We tested the maternal investment hypotheses in Japanese macaques by comparing the survivorship of offspring, final infants, and great-offspring of females that terminated reproduction before death with females that continued to reproduce until death. SURVIVAL analyses revealed no significant difference in the survivorship of descendents of postreproductive and reproductive females, though final infants of postreproductive females were 13% more likely to survive than final infants of females that reproduced until death were. We also explored possible differences between these two groups of females, other than survivorship of progeny. We found no difference in dominance rank, matrilineal affiliation, body weight, infant sex ratio, age at first birth, fecundity rate or lifetime reproductive success. However, postreproductive females are significantly longer-lived than reproductive females and as a result experienced more years of reproduction and produced more infants in total. Apart from final infants, offspring survival is marginally lower in postreproductive females. Since offspring survival is not significantly enhanced in postreproductive females, the greater number of infants produced did not translate into greater lifetime reproductive success. Our findings fail to support the maternal investment hypotheses and instead suggest that reproductive termination in this population of Japanese macaques is most closely associated with enhanced longevity and its repercussions.

This study explores the question of reproductive termination (loss of reproductive ability) in female Japanese macaques (Macaca fuscata) from the Arashiyama West (Texas) troop. We used a large sample of completed lives to identify reproductively terminated female Japanese macaques and to consider reproductive termination in Japanese macaques from a comparative life history perspective, which permits meaningful comparisons to be made with human female menopause. We classified a female as reproductively terminated if the time lag between last parturition and death exceeded two standard deviations of the female's own mean lifetime interbirth interval (Caro et al. [1995] Int. J. Primatol. 16:205-220). Seventy of the 95 females in the sample had at least 3 infants over their lifetime (the minimum required for the calculation of a mean and standard deviation), and thus were included in the analysis. Of these 70 females, 20 showed reproductive termination. Reproductively terminated females ranged in age from 14.5-32.7 years, although in females under age 25, reproductive termination was unlikely. The majority of females up to age 25 showed continued parturition. However, after age 25, reproductive termination was population-wide. Length of postreproductive life for reproductively terminated females varied from 0.07-4.4 years, with a mean of 2.08 years. Variation in length of postreproductive life was not related to the age at death of the female. While the occurrence of population-wide reproductive termination after 25 years does suggest similarities with human female menopause, the age at which this termination occurs is very late in the life span, and it was experienced by only 2.9% of the population. Female Japanese monkeys over age 25 are visibly aged and show outward signs of weakness and deterioration, quite unlike the healthy middle age of menopausal human females. Accordingly, as a life history characteristic, reproductive termination in Japanese macaques does not appear to coincide with menopause as experienced by human females.

Primates in fragments, because of their increased vulnerability to stochasticity, are in double jeopardy with the expected increases in severe weather patterns due to global climate change. It is thus increasingly important to have a better understanding of how severe weather events affect primate populations, especially those in fragments. This study explores the interacting effects of diet, cortisol levels, and parasites on the density of a black howler (Alouatta pigra) population following a major hurricane. In October 2001, Hurricane Iris made landfall in Southern Belize resulting in substantial damage to the 96-km2 Monkey River watershed forest fragment and a loss of nearly 80 % of the population by 3 years after the storm. Late in 2004 the population stabilized and began to recover. From 2001 to 2006, demographic, behavioral, and dietary data along with fecal samples were collected from six monkey groups in an 86-ha study site in the Monkey River forest. Changes in population density over the 5-year period were explained primarily by fruit consumption both directly through inadequate fruit intake leading to energy malnutrition and indirectly through physiological stress (measured through fecal cortisol). Cortisol levels had a lesser direct effect on population density and were affected not only by low fruit consumption, but by multispecies parasite infections. This study highlights the importance of taking a multifactorial approach to understanding population density and shows how diet, stress, and parasites can have interacting effects in influencing primate population dynamics.

This paper presents a perspective on the topic of intergenerational relations among nonhuman primate females, reporting on a study of the social manifestations of aging in female Japanese monkeys. Japanese monkeys are representative of many of the well-studied old world monkeys, living in female-bonded societies characterized by the dispersal of natal males. The intergenerational relationships among female kin represent the most fundamental and enduring relationships in the group. The life-time bonds between mothers and daughters are characterized by affiliative behaviors and by mutual support in times of conflict with non-family members. Because kinship bonds persist across the lifecourse, old females do not become socially isolated, nor experience a decrease in social power, nor engage in behavior patterns distinct from those of middleaged or young adults. Changes in female social networks occur within this strong intergenerational female kinship structure: in youth, a female's primary social bond is with her mother; in old age, it is with her daughter.

Cross-site comparison studies of behavioral variation can provide evidence for traditions in wild species once ecological and genetic factors are excluded as causes for cross-site differences. These studies ensure behavior variants are considered within the context of a species' ecology and evolutionary adaptations. We examined wide-scale geographic variation in the behavior of spider monkeys (Ateles geoffroyi) across five long-term field sites in Central America using a well established ethnographic cross-site survey method. Spider monkeys possess a relatively rare social system with a high degree of fission-fusion dynamics, also typical of chimpanzees (Pan troglodytes) and humans (Homo sapiens). From the initial 62 behaviors surveyed 65% failed to meet the necessary criteria for traditions. The remaining 22 behaviors showed cross-site variation in occurrence ranging from absent through to customary, representing to our knowledge, the first documented cases of traditions in this taxon and only the second case of multiple traditions in a New World monkey species. Of the 22 behavioral variants recorded across all sites, on average 57% occurred in the social domain, 19% in food-related domains and 24% in other domains. This social bias contrasts with the food-related bias reported in great ape cross-site comparison studies and has implications for the evolution of human culture. No pattern of geographical radiation was found in relation to distance across sites. Our findings promote A. geoffroyi as a model species to investigate traditions with field and captive based experiments and emphasize the importance of the social domain for the study of animal traditions.

All diurnal primates live in social groups but with a great range of variation in the types of groups they form. Primate societies vary in group size, composition, dispersal patterns, levels of cohesion, and the extent of overt social interaction or differentiation of relationships within the group. They also vary in the flexibility seen in these aspects of social organization. For example, cross-population studies as well as diachronic studies suggest that black howlers are constrained to live in highly cohesive groups of no more than 10 individuals, despite considerable variation in group composition (Pavelka and Chapman, 2006; Van Belle and Estrada, 2006). Other species, such as Muriquis, reveal considerable flexibility in group size and cohesion; an increase in population size over a 25-year period produced significantly larger social groups and a shift from cohesive to flexible fission–fusion grouping pattern in which members regularly fission and fuse into parties of ever-changing size and composition (Dias and Strier, 2003).

The purpose of this study was to investigate the prevalence, intensity, and possible transmission routes of the trematode, Controrchis spp. (Dicrocoeliidae), in a population of black howler monkeys (Alouatta pigra) near Monkey River, Belize. Alouatta pigra are arboreal primates that are typically folivorous and frugivorous. Controrchis is a dicrocoeliid trematode and, as such, should require a gastropod and an ant (Formicidae) intermediate host for transmission. From January to July 2005 and February 2006 to June 2007, we collected fecal samples and focal animal data from 18 individual primates in four social groups. Feces were stored in either 10% buffered formalin or 95% ethanol and examined using a double-centrifugation sugar-flotation technique. The prevalence of Controrchis spp. was 89%, and the mean intensity was 2.29 eggs per gram (epg), with a range of 1.00-6.57 epg. A general linear mixed model to examine the effect of sex, rainfall, and time spent feeding on various plant species, while controlling for individual and group identity, revealed that both group and the amount of time spent feeding on trumpet trees (Cecropia peltata) by individuals predicted the prevalence and intensity of Controrchis spp. infestation. Cecropia peltata has a mutualistic relationship with Azteca spp. ants and constitutes an important food source for A. pigra. Our findings provide strong, circumstantial evidence that A. pigra are infected with Controrchis spp. through the ingestion of metacercariae in Azteca spp. when feeding on C. peltata. Because C. peltata is a pioneer tree species and typically occurs in disturbed forests, results from this study suggest an important link between habitat disturbance and parasitism in a wild mammal.

High cortisol levels are known to cause low fecundity and increased mortality; thus, the prospect of using cortisol as a measure of population health is an exciting one. However, because so many factors can interact to influence cortisol release, it can be difficult to interpret what exactly is creating changes to cortisol levels. This study investigates variation in fecal cortisol levels in a population of black howlers (Alouatta pigra) from 350 fecal samples collected from 33 individuals in more than 4 years. A general linear mixed model revealed that cortisol varied significantly with fruit availability and contact with tourists. When fruit availability was low, cortisol increased, likely because when fruit availability is low monkeys eat less fruit, thus obtaining less sugar. This result may simply reflect cortisol's metabolic function of mobilizing glucose. It also indicates that these monkeys may be experiencing periods of food stress throughout the year, which was earlier thought to be minimal for a primarily folivorous species. Presence of tourists was the only other factor found to lead to high cortisol; with exposure to tourists increasing stress levels. These results highlight the importance of understanding how physiological factors can influence cortisol, making it easier to interpret results and determine the external social or ecological stressors that may increase cortisol.

Over a period of 20 months, 18 aged and 22 non-aged semi-free ranging female Japanese monkeys were observed, and a total of 440 hours of focal animal data were collected. The goal of the study was to investigate the reported pattern of disengagement in old female monkeys. For each subject female, two sociability scores were calculated: the total number of other animals with whom time was spent in affiliative social interaction, and the total amount of time spent in affiliative social interaction. These data were analyzed in order to determine any change in sociability based on age. No relationship was found between age and sociability. The absence of a pattern of decreased social interaction with advancing age in these monkeys is discussed in terms of the methodological differences with earlier studies. It is suggested that the life of nonhuman primates may be essentially continuous from the attainment of adulthood to death, with no recognizable social stage for the elderly, at least in terms of sociability and isolation. Menopause, awareness of mortality, and interindividual dependence are three elements of the human life course that appear to be absent in this troop of Japanese monkeys, and these are discussed as key elements that may render the later portion of the human life course to be very different from that of monkeys, and possibly from that of all other primates.

As a life history characteristic of human females, menopause is universal, it occurs halfway through the maximum lifespan of the species, and it consistently occurs at approximately age 50 in different populations. Menopause is fundamentally distinct from the reproductive senescence that has been described for a very small number of very old individual alloprimates. Menopause is not a recent historical artifact. As a species universal showing little variation in occurrence across contemporary populations, it must be understood in evolutionary terms. Supporters of the “grandmother hypothesis” explain menopause as an adaptive feature in itself. Others see menopause as a byproduct of the increased lifespan of Homo sapiens. Plieotropy theory may help to explain menopause in broader mammalian terms.

The role of the aged in human society has received much attention from gerontologists, and the notion of a social role for aged monkeys is common in primatology. Four hundred and fifty hours of focal animal data were collected on a sample of 40 adult female Japanese monkeys. The animals are semi-free ranging and of known age. These data were analyzed in an attempt to determine whether old females constitute a behaviorally distinct subgroup. Very little behavioral variation based on age could be documented. Where age related variation occurs, it is better explained as a function of youth, rather than as a function of old age. The expectation that old monkeys will occupy a distinct social role because of their advanced age is discussed in terms of biological versus social aging, human versus non human aging, the evolution of behavioral change in old age, and the application of the social role concept to old female monkeys. It is concluded that there is little evidence that the behavior of the aged females differs significantly from that of the other adult females, and it does not appear that the fact of biological aging creates any radically different social situation which would cue the onset of specific role behavior for aged animals.

Alejandro Estrada Field Station Los Tuxtlas, Institute of Biology, National Autonomous University of Mexico, Apdo 176, San Andres Tuxtla, Veracruz, Mexico. Paul A. Garber Department of Anthropology, University of Illinois, Urbana, Illinois, USA. Mary S. M. Pavelka Department of Anthropology, University of Calgary, Calgary, Alberta, Canada. LeAndra Luecke Department of Anthropology, Washington University, St Louis, Missouri, USA.

A Central American black howler population in Monkey River, Belize, was monitored from May of 1999 to May of 2001 and was determined to have similar small group size with multi- and single-male groups. Fifty-three monkeys lived in 8 social groups in a 52-ha study area (population density 102 individuals/km2) that is part of the larger continuous forested area of the Monkey River watershed. On October 8, 2001, the study area was severely damaged by Hurricane Iris, a category four storm that resulted in complete defoliation of the forest along with severe structural damage to those trees not snapped or uprooted. When the area could be accessed again in February 2002, it was determined that the population had dropped by 42%, with 31 monkeys in 5 social groups inhabiting the study area. While initially it was hoped that the population would stabilize at this level, subsequent monitoring through May of 2004 (29 months post hurricane) has revealed a slow but steady decline in the population through the apparent dispersal of whole or parts of social groups, and poor infant survival. We hypothesize that a combination of nutritional and social stress interacting with increased parasite loads (and possibly increased predation) is leading groups and individuals to leave the area, moving west along the river in search of better habitat that is not available. The watershed forest fragment (approximately 100 km2) was equally damaged by the storm from the southern highway of Belize to the coast, leading us to believe that survival of the animals leaving the study site is unlikely. We are currently investigating phytochemical, hormonal, and parasite contributions to the continued decline of the Monkey River howler monkey population following hurricane Iris.

Natural catastrophic events such as hurricanes, floods, earthquakes, volcanic activity, and disease as well as extensive deforestation caused by humans have critical impacts on primate population viability. Natural and human-induced destruction results in habitat loss and fragmentation, population reduction, and in demographic, social, and reproductive disruption. Primate populations can persist in fragmented landscapes if remnant forest fragments are large enough to provide sufficient resources and expand in area through regeneration over time. The chapters in this section examine issues of primate behavior, ecology, diet, and mating strategies from different perspectives and offer important research methods for evaluating behavioral plasticity and the response of primate species to habitat contraction and fragmentation, resulting from natural or artificial causes. Demographic data on primate populations in continuous forests with minimal human disturbance provide needed baseline information about species’

Although infanticide has been witnessed in other species of howler monkey, and has been inferred for Alouatta pigra, an observed case of infanticide has not previously been recorded for this species. Here we describe the killing of a 2-week-old infant by the resident male of a small social group in southern Belize. The infanticide was witnessed as part of an intensive observational study that began in January 2003. The male was known to have resided in the group for at least 4 months, but it is not known whether he was the father of the infant. The literature proposes three main explanations for infanticide: two adaptive hypotheses (sexual selection and resource competition), and one nonadaptive hypothesis (social pathology). Individual cases of infanticide such as this one are important for comparative purposes, but when examined on their own they are difficult to interpret in relation to established theoretical frameworks. The data presented here show some consistency with the sexual-selection and resource-competition hypotheses, but the lack of critical information (i.e., as to paternity) makes it impossible to draw firm conclusions.

Comparative Primate Socioecology. P. C. Lee. ed. New York: Cambridge University Press, 1999. 412 pp.