Growth of Mantled Howler Groups in a Regenerating Costa Rican Dry Forest

We examined population dynamics in mantled howlers (Alouatta palliata palliata) in a regenerating tropical dry forest in Santa Rosa National Park (SRNP), Costa Rica. The population has grown at a rate of about 7% per annum during the past decade. The growth in numbers from 342 in 1984 to 554 in 1992 reflects an increase in the number of groups (from 25 to 34) and a slight increase in their average size (from 13.6 to 16.3). Population density has increased from 4.9 to 7.9 individuals per km ². Santa Rosa's population density and group compositions are similar to those at several other mantled howler sites, but densities of mantled howlers are much higher at two other well-studied sites: La Pacifica and Barro Colorado Island (BCI). We relate the low density of howlers at Santa Rosa to local historical and ecological factors. Howler populations at high and low densities differ in average group size and sex ratio. At high population densities, groups are larger and include more adult females. The number of male howlers per group appears to be more strictly limited and less variable than the number of females is. However, there is greater variation in male group membership at Santa Rosa than at La Pacifica or BCI, and at Santa Rosa there are more generating forests available into which males and females can disperse and form new groups. We present case studies describing two ways in which new howler groups are formed, and we suggest that, compared to females and compared to males at high density sites, males are relatively advantaged in the uncrowded habitats at Santa Rosa and other low density sites.     

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.     

Locomotor and postural behavior in Alouatta palliata and Cebus capucinus

Positional behavior of two platyrrhine monkeys, Alouatta palliata and Cebus capucinus, was observed at La Pacifica and Santa Rosa National Park, Costa Rica. Frequency data for locomotion, postures, support diameters, orientation of supports, and use of canopy were recorded on focal males and females. Alouatta palliata is a frequent user of arboreal quadrupedalism (47%) and climbing (37%), with bridging (10%) representing the next most frequent type of locomotion. Intraspecific comparisons show the smaller-sized females of Alouatta to prefer very small diameter supports, the lower canopy, and to climb more frequently than the larger males—a pattern opposite to that which has been documented to occur with increasing body size across species. A more limited study on Cebus capucinus shows this species to be highly quadrupedal (54%) with moderately high locomotor frequencies for climbing (26%) and leaping (15%).     

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.     

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.     

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.     

Habitat selection and seasonal patterns of activity and foraging of mantled howling monkeys(Alouatta Palliata) in Northeastern Costa Rica

I conducted a 15- month ecological study of habitat preferences and activity and foraging patterns of two troops of mantled howling monkeys, Alouatta palliata,in a lowland rain forest at La Selva Biological Reserve in northeastern Costa Rica. The two troops specialized on different habitats in spite of the fact that both of them had all habitats available and were not constrained by neighboring troops since the population density of howlers is low (7- 15 howlers/km ² ).Troop 1 spent the majority of time in primary forest (80%) followed by secondary forest (10%), while troop 2 spent the majority of time in undisturbed riparian habitat (60%) followed by primary forest (30%). Habitat sampling indicates that neither the total number of stems, species, or families nor the diversity (Shannon index) or evenness is a good indicator for howler habitat selection. Instead the density of trees from the 12 species most commonly consumed by each troop is the most important factor. Activity and foraging patterns were not dependent upon the season as has been described for howling monkeys in forests with a more pronounced dry season at Barro Colorado Island, Panama, and La Pacifica in northwestern Costa Rica. This is likely a result of the more constant food supply at La Selva, combined with less intraspecific competition due to the low howler density. The intraspecific variability of foraging patterns and troop- specific habitat specialization observed in Alouatta palliatashould be considered in the conservation biology of primates. Primate relocation programs should include not only an ecological assessment of the release site but also a comparison of the release site with the habitat that the groups currently occupy.     

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.     

Behavioural development of howling monkey twins (Alouatta palliata) in Santa Rosa National Park,Costa Rica

Twins born to a young female howling monkey in Santa Rosa National Park, Costa Rica were observed during the first 96 days of their life. The comparison of their development to that of single infants and the comparison of the behaviour of the mother of the twins to that of mothers of single infants revealed few differences. However, qualitative observations suggests that high costs are associated with maternal care of infant twins. The mother had difficulty carrying both infants and was the only female observed to become sick during the study. Increased costs of lactation were not compensated for by an increase in foraging time. It would seem that howling monkey mothers possess a maternal care system which is capable of providing suitable care to twins. However, the costs on the mother of raising twins is suggested as a factor selecting for a litter size of one.     

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.     

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.     

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.     

Intragroup Social Relationships of Male Alouatta palliata on Barro Colorado Island,Republic of Panama

We examined social and spatial relations of adult males in one group of mantled howling monkeys (Alouatta palliata) on Barro Colorado Island (BCI) in central Panama to document patterns of association. Beyond the existence of an alpha male, we could not distinguish any linear dominance hierarchy among the 6 study males. All males copulated with estrous females. Our findings contrast with reports of intragroup male behavior in Costa Rican howlers. Study males engaged in little or no affiliative or agonistic behavior with one another, but engaged in significantly more such interactions with females. The alpha male, the oldest male and a younger male were most frequently in association with females. Of group males, the oldest male associated significantly more with other males. Overall, male behavior in mantled howling monkeys on BCI generally followed the van Hooff and van Schaik (1994) model of male relationships. The low incidence of intragroup social interactions of any type in the focal males may reflect the energetic costs of social behavior. We suggest that intragroup social relationships among mantled howler males are structured by more subtle means than overt physical interactions, possibly including vocal communication, relationships with individual group females, and kinship.     

Population trends of the mantled howler groups of La Pacifica,Guanacaste, Costa Rica

A complete survey of La Pacifica in Guanacaste Province, Costa Rica was conducted in July 1984 in order to determine whether the howler (Alouatta palliata) population had declined since 1972 as a result of deforestation. During the 6-day survey, 257 howlers were located, representing 16 different social groupings and nine solitary animals. The total number of howlers, the number and location of groups, and the age-sex composition were very similar to a 1972–1976 survey of the same population. Age-sex composition of La Pacifica howler groups was similar to those of another population of mantled howlers in Costa Rica and of populations in Mexico and in Panama, although La Pacifica had a higher mean number of adult females per group. There was no evidence to support the hypothesis that the La Pacifica howler population has declined in recent times.     

Howling on the edge: Mantled howler monkey (Alouatta palliata) howling behaviour and anthropogenic edge effects in a fragmented tropical rainforest in Costa Rica

The function of long calling is a subject of interest across animal behaviour study, particularly within primatology. Many primate species have male‐specific long‐distance calls, including platyrrhines like the folivorous howler monkey (Alouatta spp.). Howler monkeys may howl to defend resources such as feeding trees or areas of rich vegetation from other monkey groups. This study tests the ecological resource defence hypothesis for howling behaviour in the mantled howler monkey (Alouatta palliata) and investigates how anthropogenic forest fragmentation may influence howling behaviour. More specifically, this study examines how howling bout rate, duration, precursors and tree species richness, DBH, and canopy cover vary in 100 m anthropogenic edge and interior forest zones at La Suerte Biological Research Station (LSBRS), a fragmented tropical rainforest in Costa Rica. Results show that tree species richness and canopy cover are higher in forest interior at this site, suggesting that monkeys should howl at greater rates in the interior to defend access to these higher‐quality vegetation resources. Overall, our results supported the ecological resource defence hypothesis. The main howl precursor was howling from neighbouring groups. Although howling rate did not differ between forest zones, howling bouts from forest interior were longer, had a greater number of howls per bout and were preceded by different precursors than howls from anthropogenic edge zones, including more howls from neighbouring groups. Our findings provide some of the first evidence for behavioural edge effects in primate vocal communication behaviour.     

Intestinal parasites in howler monkeys Alouatta palliata (Primates: Cebidae) of Costa Rica

Fecal samples of 102 howler monkeys (Alouatta palliata) from several sites of Costa Rica were studied for intestinal parasites. The zones studied were: Central Valley (San Ramón, Alajuela), Central Pacific (Chomes and Manuel Antonio National Park. Puntarenas), North Pacific (Palo Verde Park and Playa Potrero, Guanacaste). Chira Island in the Nicoya Gulf and Caribean area (Cahuita. Limón). Animals were anesthetized with dards containing Telazol in order to collect the fecal material; some monkeys defecated spontaneously and others by direct stimulation. Samples were studied in saline solution (0.85%) and a Iodine solution, or stained with Haematoxylin. The material was also cultured in Dobell culture medium to determine the presence of amoeba and flagellates. Strongvloides. Controrchis. Trypanoxyuris genera were found in 3.4% of the samples. In addition 16.7% to 80% of the animals showed protozoa infection with Endolimax, Entamoeba, Trichomonas and Giardia. It is discussed the relationships of parasite infection with environmental conditions, animal population and human presence, specially in the monkey conservation programs point of view.     

Begging and transfer of coati meat by white-faced capuchin monkeys,Cebus capucinus

White-faced capuchin monkeys were frequently observed to raid the nests and predate the pups of coatis at two study sites (Santa Rosa National Park and Lomas Barbudal Biological Reserve) in northwestern Costa Rica. Adult monkeys of both sexes were the primary participants in nest-raiding. At Santa Rosa, the original captor of the pup tended to eat the entire carcass, whereas at Lomas Barbudal, the monkeys rapidly became satiated and allowed another monkey to have the carcass. At Lomas Barbudal, there was a tendency for adult females to share preferentially with their own offspring, but only if the offspring were less than 1 year old. Dominance rank of the owner of the carcass relative to the rank of the beggar did not significantly affect the probability of willingly transferring meat to the beggar. In one of two years, carcass theft was more likely to occur when the thief was higher ranking than the carcass owner.     

Life history and locomotion in Cebus capucinus and Alouatta palliata

As an individual matures from birth to adulthood, many factors may influence the positional repertoire. The biological and behavioral changes that accompany a growing individual are expected to influence foraging strategy, social status and interaction, diet, predator avoidance strategies, and ultimately positional behavior as a behavioral link between anatomy and the environment. In this work, positional behavior is considered as an important feature of life history in juvenile and adult white‐faced capuchins (Cebus capucinus) and mantled howling monkeys (Alouatta palliata) inhabiting the same tropical forest in Costa Rica. During growth and development ontogenetic changes in body size, limb proportions, and motor skills are likely to influence locomotion and posture through the arboreal canopy. I collected data on positional behavior, activity, branch size, branch angle, and crown location during a 12‐month period at Estación Biológica La Suerte in northeastern Costa Rica. Life history timing and differences in rates of growth did not predictably influence the development of adultlike positional behaviors in Cebus and Alouatta. Young Cebus resembled the adult pattern of positional behavior by 6 months of age while howlers exhibited significant differences in several positional behavior categories through 24 months of age. The positional repertoire of both species revealed similarities in the types of modes used during feed/forage and travel in juveniles and adults. Data presented here suggest that the environment exerts different pressures on growing Cebus and Alouatta that may relate to diet, energy expenditure, foraging skill, and/or social learning. Am J Phys Anthropol, 2009 © 2009 Wiley‐Liss, Inc.     

Genetic Variation of Mantled Howler Monkeys (Alouatta palliata) from Costa Rica1

We examined genetic diversity of howler monkeys (Alouatta palliata) from Costa Rica. Blood samples of howler monkeys were collected at various locations in Costa Rica, and electrophoresis of total plasma proteins yielded no variation. We also conducted starch gel electrophoresis of red cell isozymes and did not find variation for any of the 14 loci analyzed (i.e., ACP, ADA, CA2, EST, GPI, IDH, LDH‐1, LDH‐2, MDH, PGD, PGM‐1, PGM‐2, SOD, and TPI). These findings were compared with the levels of genetic variation for A. seniculus and A. belzebul from one Brazilian population. Four of the 14 isozymes (ADA, GPI, PGD, and SOD) showed more than one allele for these species. Both A. seniculus and A. belzebul from Brazil showed similar levels of genetic variation. The potential causes of the low genetic variation in A. palliata from Costa Rica are discussed.     

Mantled howler population of Hacienda La Pacifica, Costa Rica, between 1991 and 1998: effects of deforestation

A survey of the mantled howler (Alouatta palliata) population on Hacienda La Pacifica, Guanacaste, Costa Rica, was done in July and August of 1998 to determine population parameters following deforestation due to major canal construction between 1990 and 1994. The survey was carried out in a manner identical to our 1991 survey and consisted of a single pass and two re-surveys of all forested areas of the farm. As canal construction effectively increased fragmentation of the habitat, we predicted decreased population and group size over this time. Results indicated that between the 1991 and 1998 survey, group size decreased but not significantly, and there were significantly fewer adult males and adult females per group. Population size, however, remained unchanged as there was an increase in animals in the immature age classes. An increase in the infant to adult female ratio suggests a stable or even expanding population, which could represent recovery from the initial disturbance of deforestation. Thus, despite changes in the forest and land use patterns, the area now appears to support the same number of howlers as found in previous surveys.