Dental topography and molar wear in Alouatta palliata from Costa Rica.

Paleoprimatologists depend on relationships between form and function of teeth to reconstruct the diets of fossil species. Most of this work has been limited to studies of unworn teeth. A new approach, dental topographic analysis, allows the characterization and comparison of worn primate teeth. Variably worn museum specimens have been used to construct species-specific wear sequences so that measurements can be compared by wear stage among taxa with known differences in diet. This assumes that individuals in a species tend to wear their molar teeth in similar ways, a supposition that has yet to be tested. Here we evaluate this assumption with a longitudinal study of changes in tooth form over time in primates. Fourteen individual mantled howling monkeys (Alouatta palliata) were captured and then recaptured after 2, 4, and 7 years when possible at Hacienda La Pacifica in Costa Rica between 1989-1999. Dental impressions were taken each time, and molar casts were produced and analyzed using dental topographic analysis. Results showed consistent decreases in crown slope and occlusal relief. In contrast, crown angularity, a measure of surface jaggedness, remained fairly constant except with extreme wear. There were no evident differences between specimens collected in different microhabitats. These results suggest that different individual mantled howling monkeys wear their teeth down in similar ways, evidently following a species-specific wear sequence. Dental topographic analysis may therefore be used to compare morphology among similarly worn individuals from different species.

Drinking from arboreal water sources by mantled howling monkeys (Alouatta palliata Gray).

Despite occasional trips to the ground and feeding in trees whose canopies touched the river, mantled howling monkeys were never seen to drink from any ground water. Drinking from arboreal cisterns was observed, but only during the wet season (meteorologically the less stressful season but phenologically the more stressful season). The lack of sufficient new leaves during the wet season forced the howlers to ingest more mature leaves which contained significantly less water. To compensate for the lowered amount of water in their food, the monkeys utilized arboreal water cisterns. The cisterns dried up during the dry season, but the howlers maintained their water balance by altering their time of actiivity and selecting a diet comprised largely of succulent new leaves. The effect of plant-produced secondary compounds on drinking also was discussed.

Plasma lipoproteins of free-ranging howling monkeys (Alouatta palliata).

1. Plasma lipids and lipoproteins of free-ranging howling monkeys from Costa Rica (Alouatta palliata), aged 5 months to 23 years, were characterized. 2. High density lipoproteins were lipid-rich, similar to HDL2 of human plasma. 3. Fatty acid compositions of major lipid classes of very low, low and high density lipoproteins differed among social groups, possibly due to both dietary and genetic factors. 4. Low and high density lipoprotein phospholipids were enriched in phosphatidylethanolamine. 5. Howler plasma cross reacted with antihuman apoA-I antibodies but not with antihuman LDL antibodies. 6. No dimeric form of apoA-II was present, unlike human apoA-II.

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.

Mechanical defenses in leaves eaten by Costa Rican howling monkeys (Alouatta palliata).

Primate species often eat foods of different physical properties. This may have implications for tooth structure and wear in those species. The purpose of this study was to examine the mechanical defenses of leaves eaten by Alouatta palliata from different social groups at Hacienda La Pacifica in Costa Rica. Leaves were sampled from the home-ranges of groups living in different microhabitats. Specimens were collected during the wet and dry seasons from the same tree, same plant part, and same degree of development as those eaten by the monkeys. The toughness of over 300 leaves was estimated using a scissors test on a Darvell mechanical tester. Toughness values were compared between social groups, seasons, and locations on the leaves using ANOVA. Representative samples of leaves were also sun-dried for subsequent scanning electron microscopy and energy dispersive x-ray (EDX) analyses in an attempt to locate silica on the leaves. Both forms of mechanical defense (toughness and silica) were found to be at work in the plants at La Pacifica. Fracture toughness varied significantly by location within single leaves, indicating that measures of fracture toughness must be standardized by location on food items. Monkeys made some food choices based on fracture toughness by avoiding the toughest parts of leaves and consuming the least tough portions. Intergroup and seasonal differences in the toughness of foods suggest that subtle differences in resource availability can have a significant impact on diet and feeding in Alouatta palliata. Intergroup differences in the incidence of silica on leaves raise the possibility of matching differences in the rates and patterns of tooth wear.

Dental microwear in live, wild-trapped Alouatta palliata from Costa Rica.

One problem with dental microwear analyses of museum material is that investigators can never be sure of the diets of the animals in question. An obvious solution to this problem is to work with live animals. Recent work with laboratory primates has shown that high resolution dental impressions can be obtained from live animals. The purpose of this study was to use similar methods to begin to document rates and patterns of dental microwear for primates in the wild. Thirty-three Alouatta palliata were captured during the wet season at Hacienda La Pacifica near Canas, Costa Rica. Dental impressions were taken and epoxy casts of the teeth were prepared using the methods of Teaford and Oyen (1989a). Scanning electron micrographs were taken of the left mandibular second molars at magnifications of 200x and 500x. Lower magnification images were used to calculate rates of wear, and higher magnification images were used to measure the size and shape of microwear features. Results indicate that, while basic patterns of dental microwear are similar in museum samples and samples of live, wild-trapped animals of the same species, ecological differences between collection locales may lead to significant intraspecific differences in dental microwear. More importantly, rates of microwear provide the first direct evidence of differences in molar use between monkeys and humans.

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. © 1994 Japan Monkey Centre.

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.

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 (19861994 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.

Wear and its effects on dental topography measures in howling monkeys (Alouatta palliata).

OBJECTIVES: Three dental topography measurements: Dirichlet Normal Energy (DNE), Relief Index (RFI), and Orientation Patch Count Rotated (OPCR) are examined for their interaction with measures of wear, within and between upper and lower molars in Alouatta palliata. Potential inferences of the "dental sculpting" phenomenon are explored. MATERIALS AND METHODS: Fifteen occluding pairs of howling monkey first molars (15 upper, 15 lower) opportunistically collected from La Pacifica, Costa Rica, were selected to sample wear stages ranging from unworn to heavily worn as measured by the Dentine Exposure Ratio (DER). DNE, RFI, and OPCR were measured from three-dimensional surface reconstructions (PLY files) derived from high-resolution CT scans. Relationships among the variables were tested with regression analyses. RESULTS: Upper molars have more cutting edges, exhibiting significantly higher DNE, but have significantly lower RFI values. However, the relationships among the measures are concordant across both sets of molars. DER and EDJL are curvilinearly related. DER is positively correlated with DNE, negatively correlated with RFI, and uncorrelated with OPCR. EDJL is not correlated with DNE, or RFI, but is positively correlated with OPCR among lower molars only. DISCUSSION: The relationships among these metrics suggest that howling monkey teeth adaptively engage macrowear. DNE increases with wear in this sample presumably improving food breakdown. RFI is initially high but declines with wear, suggesting that the initially high RFI safeguards against dental senescence. OPCR values in howling monkey teeth do not show a clear relationship with wear changes.

Distribution, ecology, life history, genetic variation, and risk of extinction of nonhuman primates from Costa Rica

We examined the association between geographic distribution, ecological traits, life history, genetic diversity, and risk of extinction in nonhuman primate species from Costa Rica. All of the current nonhuman primate species from Costa Rica are included in the study; spider monkeys (Ateles geoffroyi), howling monkeys (Alouatta palliata), capuchins (Cebus capucinus), and squirrel monkeys (Saimiri oerstedii). Geographic distribution was characterized accessing existing databases. Data on ecology and life history traits were obtained through a literature review. Genetic diversity was characterized using isozyme electrophoresis. Risk of extinction was assessed from the literature. We found that species differed in all these traits. Using these data, we conducted a Pearson correlation between risk of extinction and ecological and life history traits, and genetic variation, for widely distributed species. We found a negative association between risk of extinction and population birth and growth rates; indicating that slower reproducing species had a greater risk of extinction. We found a positive association between genetic variation and risk of extinction; i.e., species showing higher genetic variation had a greater risk of extinction. The relevance of these traits for conservation efforts is discussed.

Natal emigration by both sexes in the La Pacifica population of mantled howlers: when do some stay?

We have reported previously that all male and female mantled howlers emigrate from natal groups at Hacienda La Pacifica, Costa Rica. In the years since that report, a small number of juveniles have stayed in the natal group without experiencing a solitary phase. Here, we present a post hoc analysis on juvenile emigration in six groups of howlers under observation for varying amounts of time between 1972 and 2005. Our records revealed 139 juveniles for whom emigration status was certain, and 125 of these did emigrate. There was a significant association between presence of mother and emigration: juveniles without mothers were more likely to remain in their natal group (chi(1)(2) = 53.1, P<.0001). The mean age of emigration for all juveniles (n = 125) was 2.47 years (SD = 0.9, range = 1.5-6.5). There was no difference in age of emigration by adult male composition (one-male, multi-male, both), but juveniles of unknown sex emigrated younger than either known males or females (F(2,116) = 4.4, P<.02). For emigrating juveniles of known sex (n = 99), both males and females without mothers left at a later age than those with mothers (F(1,95) = 6.5, P<.02). Although philopatry or delayed emigration occurs in a few motherless animals, most males and females do emigrate from their natal groups at ages consistent with those reported for other species of howlers.

Fatty acid composition of wild anthropoid primate milks.

Fatty acids in milk reflect the interplay between species-specific physiological mechanisms and maternal diet. Anthropoid primates (apes, Old and New World monkeys) vary in patterns of growth and development and dietary strategies. Milk fatty acid profiles also are predicted to vary widely. This study investigates milk fatty acid composition of five wild anthropoids (Alouatta palliata, Callithrix jacchus, Gorilla beringei beringei, Leontopithecus rosalia, Macaca sinica) to test the null hypothesis of a generalized anthropoid milk fatty acid composition. Milk from New and Old World monkeys had significantly more 8:0 and 10:0 than milk from apes. The leaf eating species G. b. beringei and A. paliatta had a significantly higher proportion of milk 18:3n-3, a fatty acid found primarily in plant lipids. Mean percent composition of 22:6n-3 was significantly different among monkeys and apes, but was similar to the lowest reported values for human milk. Mountain gorillas were unique among anthropoids in the high proportion of milk 20:4n-6. This seems to be unrelated to requirements of a larger brain and may instead reflect species-specific metabolic processes or an unknown source of this fatty acid in the mountain gorilla diet.

Reproduction and population growth in free-ranging mantled howling monkeys.

Free-ranging mantled howling monkey (Alouatta palliata Gray) females experienced a regular estrus cycle averaging 16.3 days, demonstrated sexual skin changes, and participated in multiple matings before becoming pregnant. Gestation averaged 186 days. The average interval between births was 22.5 months. Sexual maturity occurred at approximately 36 and 42 months for females and males, respectively. Female age at first birth was about 3 1/2 years. Births were scattered during some years and clustered during others. The age, rank, and parity of the females affected infant survival. More female than male infants survived to one year of age. Increased population size was the result of immigration rather than births.

Field methods for capture and measurement of three monkey species in Costa Rica.

A total of 54 free-ranging monkeys were captured and marked in Santa Rosa National Park, Costa Rica, during May 1985, and an additional 17 were captured during March 1986. The animals were darted using a blowpipe or a CO2 gun. The drugs used were Ketaset, Sernylan and Telazol. Ketaset was effective for Cebus capucinus but unsuccessful for Alouatta palliata and Ateles geoffroyi. Sernylan was successful for A. geoffroyi and A. palliata but is no longer commercially available. Telazol proved to be an excellent alternative capture drug for both A. palliata and A. geoffroyi.