Margaret R. Clarke

Parasites of Wild Howlers (Alouatta spp.)

A literature review of howler parasites provides the basis for an overview of the ecological significance of parasite surveys in primates. Within this framework, we have added insights into the interactions between primate hosts and their parasites from a long-term study in Costa Rica. We collected fecal samples from mantled howlers (Alouatta palliata) over a 9-year period (1986–1994 inclusive) and analyzed them for parasite eggs, larvae, cysts, and oocysts. We found many misperceptions inherent in the typical methodology of primate parasite surveys and in the reporting of the findings. Our work in Costa Rica suggests that a snapshot effect occurs with most surveys. A static view does not reflect the dynamic and changing ecological interaction between host and parasite. We describe some problems with parasite data analyses that emphasize the need for long-term longitudinal surveys in wild primate groups.

A coprological survey of parasites of wild mantled howling monkeys, Alouatta palliata palliata.

Fecal samples from 155 mantled howling monkeys (Alouatta palliata palliata) examined at Centro Ecologico La Pacifica, Guanacaste Province, Costa Rica, revealed 75 (48%) had parasitic infections. A sampling of nine howling monkeys from Santa Rosa National Park, Costa Rica indicated only one infected animal (11%). Only three of 19 (16%) spider monkeys (Ateles geoffroyi) also from Santa Rosa were infected. Controrchis biliophilus, Trypanoxyuris minutus, unidentified strongylid eggs and Isospora sp. oocysts were found. Three monkeys from La Pacifica died and were examined for adult helminths. They were infected with Ascaris lumbricoides, C. biliophilus and T. minutus.

Responses to Deforestation in a Group of Mantled Howlers (Alouatta palliata) in Costa Rica

To evaluate the effects of partial deforestation of the home range of a group of free-ranging howlers on Hacienda La Pacifica, Costa Rica, we compared activity patterns, social interactions, daily travel lengths, group sizes and migration patterns before, during, and after habitat destruction. Immediate responses were a decrease in social interactions and increase in start to travel. Long-term responses included an increase in feeding time and longer daily path length. The long-term responses were associated with the adjustment to a new home range which was longer and narrower, with the patchiest resources at the furthest end points. Group size decreased due to a significant decrease in adult males and females and a significant increase in infant deaths between the predeforestation period and the deforestation/postdeforestation periods. Significant increase in adult female deaths/emigration continues, though emigration of immatures remains unchanged. Reduced group size could be due to reduced resources or disturbed migration routes throughout the farm due to the construction of a major canal system.

Morphometric comparison of Chinese-origin and Indian-derived rhesus monkeys (Macaca mulatta).

Chinese‐origin and Indian‐derived rhesus monkeys (Macaca mulatta), ranging in age from 6 months to 15 years, were weighed and measured during the 1995 inventory of the SAIDS breeding colony at the Tulane Regional Primate Research Center. Data were analyzed separately for males (n=279) and females (n=554), and an analysis of variance was done for five measurements and two indices, with age and country of origin as independent variables. All measurements increased significantly with age, but Chinese‐origin males were heavier, longer, and taller than Indian‐derived males. Chinese‐origin juvenile females were heavier and longer than Indian‐derived juvenile females, but this pattern was reversed for adults. Chinese‐origin rhesus monkeys exhibited more adult sexual dimorphism than did Indian‐derived rhesus monkeys. An analysis of Chinese‐origin adults that were Louisiana‐born vs. China‐born indicated that Louisiana‐born adults were lighter, longer, and taller than their China‐born parental generation. These differences were statistically significant for adult females and descriptively suggestive for adult males, and both suggest body and appendage adaptation to a warmer, wetter climate. Am. J. Primatol. 47:335–346, 1999.

Agonistic and Affiliative Relationships of Adult Female Howlers (Alouatta palliata) in Costa Rica Over a 4-Year Period

We observed 12 adult female mantled howlers (Alouatta palliata), which have been part of Group 2 at Hacienda La Pacifica, Guanacaste Province, Costa Rica, via focal animal sampling during portions of July and August of 1988 and 1990–1992 (7–9 females/year, 955.3 hr of observation). We used agonistic interactions and time in proximity (<1 m) as indices of social relationships. The rate of female–female agonistic interactions was 0.38/hr (yearly range: 0.24 to 0.51/hr). Yearly dominance hierarchies, based on outcomes of dyadic agonistic interactions, varied in linearity between 60.7 and 94.6%. Adult females spent 7.10% of their time in proximity to another adult female (yearly range: 1.04–15.64%) and 4.95% of their time in proximity to an adult male (yearly range: 2.27–7.51%). Using yearly dominance ranks, we tested proximity patterns for differences based on rank and presence of dependent offspring. In 3 of the 4 years, high-ranking females spent significantly greater proportions of their time in proximity with other females than did low-ranking females. Time in proximity with the 3 or 4 adult males was not associated with rank. Having a dependent infant was not related to the proportion of time in proximity to females or males, and females, especially top-ranking ones, spent more time in proximity to females with dependent infants than to females without infants. These results show that social relationships in mantled howler groups are dynamic and generally support predictions made by von Schaik (1989) regarding scramble-type, female competitors. We also discuss the roles of immigrations, infants, and male relationships in the patterning of social relationships.

Infant-Nonmother Interactions of Free-Ranging Mantled Howlers (Alouatta palliata) in Costa Rica

Proximate and ultimate explanations of interactions between infants and nonmothers vary depending upon the relatedness of the interactors. We investigated interactions of infants and nonmothers from a 22-month continuous study and from the long-term monitoring of the mantled howler population of La Pacifica, Guanacaste Province, Costa Rica. Relatedness is low or absent in these mantled howler groups. Juvenile females appeared to practice care skills with older infants, but as most first infants died, they failed to benefit. Infant positive interactions with adults occurred with the mother and probable father. Other adult females behaved aggressively toward the youngest infants. Mothers were retentive of infants and responded negatively to these interactions, suggesting that they perceived them as threatening. Interactions with infants appear to reflect competition in groups of unrelated adults. A review of other populations of Alouatta palliata and other species of howlers indicate variability in social group size and suggest variability in intragroup relatedness. We suggest that further study will confirm that social behavior (including interactions with infants) will vary by resource availability (group size) and associated demographic patterns (male and female migration) that affect relatedness in howler social groups.

Behavioral, immunological, and hormonal responses associated with social change in rhesus monkeys (Macaca mulatta)

Twelve animals to be socially reorganized in a group of 49 animals were compared with ten animals in a socially stable group (n = 51) for reproductive hormones, cortisol concentrations, immune function, and behavioral patterns for a 6 week baseline and 16 week postreorganization period. Cortisol values, mitogen‐induced lymphocyte blastogenesis, and rates of behavior reflected social events. Increased cortisols, increased noncontact aggression, and decreased mitogen response were associated with animal introductions. Increased cortisol concentration and decreased mitogen response correlated significantly only in animals removed from the group for trauma, and females successful at group membership exhibited lower cortisol concentrations. High‐ranking animals in small stable groups exhibited significantly higher lymphocyte proliferation than middle‐ or low‐ranking animals. While relative ranks established in small groups were maintained following reorganization, baseline cortisol values, immune measures, or male testosterone values did not predict success at group membership.

Group takeover by a natal male howling monkey (Alouatta palliata) and associated disappearance and injuries of immatures

As part of a long-term study on howling monkey behavior and social dynamics, a known natal male was observed taking over his group from his putative sire. Due to the accidental death of one of the adult males, this natal male had matured in a one-male group and had never observed juvenile male emigration nor adult male immigration and associated behaviors. Nevertheless, the behaviors associated with the takeover were indistinguishable from those of an immigrant male, including disappearance of immatures, one of whom was found with extensive injuries. While it cannot be said that the natal male inherited these behaviors from his presumed father, it can be said that he exhibited species-typical behaviors associated with male takeover in the absence of observational learning.

Survey of the howling monkey population at La Pacifica: A seven-year follow-up

We surveyed the howling monkey population at La Pacifica in Costa Rica over a 1-month period in July and August 1991. The survey method consisted of an initial 6-day survey, directly comparable to a 1984 survey, and at least two repeat surveys of all areas to locate all groups and to identify all animals. The initial survey indicated an increase in the number of groups and a decrease in the size of groups from earlier surveys, though the group composition was unchanged. We used the results of initial and repeat surveys to determine population size and composition. We located 30 groups with a total of 370 animals. Twenty-one groups contained animals marked with collars and/or legbands, and four additional groups contained animals with clearly identifiable white markings. Although the population structure has changed over 7 years, it is still within the species-typical range for Alouatta palliata.

Longitudinal Assessment of Immature-to-Adult Ratios in Two Groups of Costa Rican Alouatta palliata

We used immature-to-adult female ratios (IFR), which indicate replacement rates, to assess changes in and viabilities of nonhuman primate groups and populations. Heltne et al. (1975) concluded that the howling monkey (Alouatta palliata) population at La Pacifica (Guanacaste, Costa Rica) was declining, as the IFR was <1.5, the ratio thought needed for a sustainable population. Our population surveys of 1984, 1991, and 1998 revealed that the number of monkeys in the population was stable, but the number of groups had increased and mean group size decreased. To examine these group-level changes, we present the IFR and immature-to-adult (IAR) ratios for La Pacifica Groups 2 and 18, which we have studied longitudinally for 18 and 10 years, respectively. Group 2 was larger than Group 18, but both groups showed similar mean IFRs for the study periods. The mean IFR for each group exceeded the population IFR. The annual IFRs varied more in the smaller group than in the larger group, and the IARs for these groups varied more than the IFRs did. All annual IFRs in the groups were below the hypothesized critical value of 1.5. Given these group and population values, we examined this critical IFR value with respect to mantled howler life history characteristics, particularly interbirth intervals and juvenile emigration, both of which preclude ratios ≥1.5, and compared the La Pacifica mantled howler population ratios with those of other populations. Group size, in conjunction with these ratios, might be more predictive of sustainable groups and populations.