Effects of Ecology on the Gastrointestinal Parasites of Alouatta pigra

We examined the effects of demographic and ecological variables on the prevalence of intestinal parasites in free-ranging black howlers, Alouatta pigra, from Belize and Mexico. We collected 253 fecal samples from 50 individually identified monkeys during 2003. We processed all samples via standard centrifugation concentration techniques with sugar and zinc sulfate as flotation media. We used antigen capture enzyme-linked immunosorbent assays to detect protozoa. We analyzed data for each season separately. The most important factor in predicting whether an Alouatta pigra would be infected with a parasite was its membership in a particular social troop. It was not possible to isolate the effects of human presence, forest fragmentation, primate density, and the absence of Ateles geoffroyi on the prevalence of parasites in Alouatta pigra because the factors covaried. We detected few species of gastrointestinal parasites, possibly due to Alouatta pigra’s arboreal and herbivorous lifestyle and small geographic range. The prevalence of each parasite had a different pattern, with Controrchis sp. (presumed to be C. biliophilus), a fluke, tending to be more prevalent in Alouatta pigra that inhabited disturbed habitats, and Trypanoxyuris minutus, a pinworm, tending to be more prevalent in primates from undisturbed habitats. Giardia sp. tended to be more prevalent in primates at high densities. These results indicated that it is important to examine each parasite’s infection pattern separately to obtain a more accurate representation of the dynamics among the host, parasites, and ecology.     

Survey of Helminth Parasites in Populations of <Emphasis Type="Italic">Alouatta palliata mexicana</Emphasis> and <Emphasis Type="Italic">A. pigra</Emphasis> in Continuous and in Fragmented Habitat in Southern Mexico

The 2 howler species that occur in southern Mexico, Alouatta palliata mexicana and Alouatta pigra are endangered, mainly as a result of habitat loss and fragmentation from human activity. Little is known about the gastrointestinal parasite communities affecting their populations, and lack of baseline information for populations of howler species in continuous forest habitats, makes evaluations of gastrointestinal parasite prevalence in populations in fragmented landscapes difficult. We report the results of a one-time broad survey of gastrointestinal parasites in fecal samples of individuals from several demographically stable populations of Alouatta palliata mexicana and A. pigra existing in continuous and/or protected forests. We further report similar data for populations of both species in human-fragmented landscapes. We detected 6 parasites for each howler monkey species, but only 3 of them (Trematode I, Controrchis biliophilus, Trypanoxyuris sp.) were common to both species. While parasitic prevalence in populations of both howler species was, in general, higher in the fragmented habitat than in continuous and/or protected forests. The difference is only marginally significant in Alouatta pigra. Some parasites (Coccidia and Strongylid) only appeared in populations in fragmented landscapes. Preliminary data suggest that adult males tended to have higher parasite prevalence values than those of adult females in both howler species. Parasite prevalence is associated to average group size, but not to population density in Alouatta pigra.     

Determination of Fecal Glucocorticoid Metabolites to Evaluate Stress Response in <Emphasis Type="Italic">Alouatta pigra</Emphasis>

Measuring fecal glucocorticoid metabolites is now a common practice to assess the stress response in primates. Nevertheless, it is important to validate the utilized immunoassay for each primate species before the technique is applied to populations in the wild. We determined the stress response of black howlers (Alouatta pigra) via 2 different group-specific enzyme immunoassays (EIAs). 11-oxoetiocholanolone EIAs are suited to assess the stress response of black howlers via fecal glucocorticoid metabolites. Levels of fecal glucocorticoid metabolites increased after we applied a stressor, i.e. anesthesia, reaching peak concentrations 24–96 h poststressor. Both basal and stress-induced fecal glucocorticoid metabolite levels showed individual variations. The increase of fecal glucocorticoid metabolites after the stressor (paralleling increases in serum) indicates that one can effectively measure adrenocortical activity in Alouatta pigra via these 2 enzyme immunoassays. However, it is important to consider individual variations in the excretion of fecal glucocorticoid metabolites when planning field endocrinological research on Alouatta pigra. Fecal glucocorticoid metabolite excretion takes 1–3 d poststressor depending on the individual. Further, there is an important individual variability in the concentrations of glucocorticoid metabolites, which might reflect differences in stress reactivity or fecal glucocorticoid metabolite metabolism and excretion.     

Male parental behavior in black howler monkeys (Alouatta palliata pigra) in Belize and Guatemala

Male parental behavior was observed in black howler monkeys (Alouatta palliata pigra) in Belize and Guatemala from December 1978 to March 1979, with the objective of relating parental behavior to the prevailing monogamous group structure. The results revealed that male parental behavior inAlouatta palliata pigra agrees in some respects with reports from the literature on polygamous and polygynous species ofAlouatta, while in other respects the situation more closely resembles that in monogamous species of non-human primates. Considerable inter-individual variability in male-infant interactions prevailed among the study groups. Male parental behavior in the Belize groups became more prominent with increasing age of an infant.     

Seroprevalence of Trypanosoma cruzi and Leishmania mexicana in Free‐Ranging Howler Monkeys in Southeastern Mexico

Natural infection of wild mammals by protozoa parasites is quite common in nature. For Neotropical Primates different infections of parasites that are etiological agent of disease in human have been identified. In particular, infections by Trypanosoma cruzi and Leishmania sp., have been reported for some New World primate species, but there are no reports of infection with these parasites in any primate species in Mexico. A serological study was conducted on two howler monkey species (Alouatta pigra and A. palliata) from the Mexican states of Campeche and Tabasco. A total of 55 serum samples (20 samples from A. pigra, 20 samples from A. palliata, and 15 samples from semifree ranging A. palliata of Los Tuxtlas, Veracruz as negative controls) were analyzed for the detection of immunoglobulin G antibodies against T. cruzi and Leishmania mexicana through enzyme linked immunosorbent assay test, indirect immunofluorescence assay and Western blot. The overall prevalence of antibodies in howler monkeys was 17.5% for T. cruzi and 30% for L. mexicana. Our results also indicate that A. pigra is more susceptible to develop leishmaniasis than A. palliata. Finally, the finding of positive serology in these primates should be given serious consideration for public health, given the potential role of these primate species as wild reservoirs for these diseases and the increasing contact of monkeys with human populations due to habitat loss and fragmentation. Am. J. Primatol. 75:161‐169, 2013. © 2012 Wiley Periodicals, Inc.     

Genetic Structure and Kinship Patterns in a Population of Black Howler Monkeys, Alouatta pigra, at Palenque National Park, Mexico

We investigated the genetic structure and kinship patterns of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico. Fecal samples from 49 individuals residing in eight social groups were successfully genotyped for 19 polymorphic microsatellite markers known to be variable in other ateline primates. Overall, genetic diversity was low (H_o = 0.588) with an average of 4.2 alleles per loci (range = 2–8). We found that intergroup genetic variation among adults was relatively high (mean between‐group F_ST = 0.119), largely due to the genetic divergence of one study group from the others. Intragroup kinship patterns showed that in most social groups, either adult males, adult females, or individuals of both sexes resided with same‐sexed adult kin, suggesting that some black howler males and females may not disperse from their natal group or may disperse with related individuals. Of the six sampled immigrant males, two males joined established groups by themselves, and four males formed two pairs that each took over the social group they joined after evicting the resident males. Males in both these coalitions were genetically closely related, while the two solitary immigrants were not closely related to any of the resident males present in the group they joined. Am. J. Primatol. 74:948‐957, 2012. © 2012 Wiley Periodicals, Inc.     

The Role of Minerals in Food Selection in a Black Howler Monkey (Alouatta Pigra) Population in Belize Following a Major Hurricane

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. Am. J. Primatol. 74:1054‐1063, 2012. © 2012 Wiley Periodicals, Inc.     

Shifts in Social Structure of Black Howler (Alouatta pigra) Groups Associated with Natural and Experimental Variation in Population Density

We examined variation in the group structure of black howlers (Alouatta pigra) using the adult composition of 48 social groups. We compared the structure of groups at 5 sites with different population densities and variation in group structure over time with rising population density. In addition, we examined changes in the group structure of monkeys that were translocated from an area of high population density to an area with a much lower population density. We found at low population densities, groups comprised either heterosexual pairs or a single male with two females. At high population densities groups tended to be multimale and often contained >2 adult females. We suggest the relative costs and benefits of dispersal by maturing adults varies with population density, and in Alouatta pigra results in a shift from single to multimale groups of larger size with increasing population density.     

Potential distribution of Mexican primates: modeling the ecological niche with the maximum entropy algorithm

We developed a potential distribution model for the tropical rain forest species of primates of southern Mexico: the black howler monkey (Alouatta pigra), the mantled howler monkey (Alouatta palliata), and the spider monkey (Ateles geoffroyi). To do so, we applied the maximum entropy algorithm from the ecological niche modeling program MaxEnt. For each species, we used occurrence records from scientific collections, and published and unpublished sources, and we also used the 19 environmental coverage variables related to precipitation and temperature from WorldClim to develop the models. The predicted distribution of A. pigra was strongly associated with the mean temperature of the warmest quarter (23.6%), whereas the potential distributions of A. palliata and A. geoffroyi were strongly associated with precipitation during the coldest quarter (52.2 and 34.3% respectively). The potential distribution of A. geoffroyi is broader than that of the Alouatta spp. The areas with the greatest probability of presence of A. pigra and A. palliata are strongly associated with riparian vegetation, whereas the presence of A. geoffroyi is more strongly associated with the presence of rain forest. Our most significant contribution is the identification of areas with a high probability of the presence of these primate species, which is information that can be applied to planning future studies and then establishing criteria for the creation of areas to primate conservation in Mexico.     

Geographic Microsatellite Variability in Central American Howling Monkeys

In 1997, we began to assess the genetic variability and the potential conservation risk of the increasing human impact on the howling monkeys of Ometepe Island in southern Nicaragua. We captured and collected blood from 29 howling monkeys (Alouatta palliata) at two geographically separated localities in a single area (San Ramon) on Ometepe Island, Nicaragua, during two field seasons. We also collected blood from a community of 10 Alouatta pigra in the Scotland Half Moon region in Belize. We extracted DNA from the blood and analyzed 12 microsatellite loci. The number of alleles per locus (allele variability) is less for most (but not all) loci in the Ometepe versus the Belize sample and less than earlier published reports of mixed geographic samples from Central America. The results are noteworthy in that both the Ometepe Island sample and the Belize sample possess greater allelic heterozygosity for most loci than reported in other Central American howling monkey populations. The Ometepe and Belize groups also demonstrated differences in allele frequencies at each geographic location. There appeared to be adequate gene flow in both locations despite extensive fragmentation due to agriculture and other human land usage.     

Interferon‐Gamma test for the detection of Mycobacterium tuberculosis complex infection in Macaca mulatta and other non‐human primates

We have formatted an assay to detect Mycobacterium tuberculosis complex infections of non‐human primates. Commercially available reagents were used to elicit a specific immune response that was measured by interferon‐gamma release. Initial evaluation using blood samples from Rhesus macaques experimentally infected with M tuberculosis distinguished infected versus uninfected animals.     

Resource Use in a Landscape Matrix by an Arboreal Primate: Evidence of Supplementation in Black howlers (Alouatta pigra)

Across the tropics, landscapes of continuous rain forest are being replaced by forest fragments embedded in a matrix of pastures and farmlands. This conversion has endangered many species, including arboreal primates. Species vary, however, in how they are able to supplement their diets from the matrix, although this is rarely studied in primates. We studied two groups of black howlers (Alouatta pigra) for a total of 1156 h, one inhabiting a smaller fragment (0.4 ha) and the other a larger fragment (20 ha). monkeys inhabiting the smaller fragment spent more time in the matrix than in the habitat fragment, spending 50 % of their time (335 of 667 h) in an abandoned mango (Mangifera indica) plantation, 8.8 % in scattered trees, and 0.2 % in pastures. In contrast, monkeys in the larger fragment spent 75 % of their time (368 of 489 h) in the forest fragment and only 25 % of their time in the matrix. Feeding in the matrix accounted for 53 % and 12 % of the foraging time for groups in the smaller and larger fragments respectively. We suggest that Alouatta pigra can use resources in the matrix to supplement their diet by means of crop raiding or taking other resources in many fragmented landscapes and that this may be true also for many fragment-dwelling primates. It is important to include a consideration of the matrix in conservation planning, considering both the total resources available to primates and the consequences of crop raiding for farmers.     

Color Vision Variation as Evidenced by Hybrid L/M Opsin Genes in Wild Populations of Trichromatic Alouatta New World Monkeys

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 λ_max) for 8 and 18 X chromosomes from Alouatta palliata and A. pigra, respectively. The wavelengths of maximal absorption (λ_max) 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 λ_max 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.     

Sex differences in total body water in adolescent rhesus macaques estimated by ethanol dilution

Abstract: Non‐human primates are widely used in research, yet relatively few studies have addressed potential pharmacokinetic differences between males and females. The present study examined the relationship between total body water, sex, age, and weight in the rhesus macaque (Macaca mulatta). Ethanol‐naïve, adolescent rhesus macaques (n = 119) were administered ethanol (males, 2.1 g/kg; females, 2.0 g/kg) intravenously, and blood samples for blood ethanol concentration obtained at 5, 10, and 60 minutes following the end of the infusion. Non‐linear regression was used to compare and contrast a series of pharmacokinetic models examining the relationship between weight, sex, age, V_d and zero‐order elimination rate. V_d (mean ± SEM) for male rhesus was 0.771 ± 0.008 l/kg and for females was 0.730 ± 0.008 l/kg, different at P < 0.00001. There were no sex differences in the rate of zero‐order ethanol elimination, estimated to be 0.0032 ± 0.0004 g/kg/minute. The data reported here may be useful in designing and interpreting pharmacokinetic studies using rhesus monkeys.     

The effect of captivity on the primate gut microbiome varies with host dietary niche

Despite careful attention to animal nutrition and wellbeing, gastrointestinal distress remains relatively common in captive non‐human primates (NHPs), particularly dietary specialists such as folivores. These patterns may be a result of marked dietary differences between captive and wild settings and associated impacts on the gut microbiome. However, given that most existing studies target NHP dietary specialists, it is unclear if captive environments have distinct impacts on the gut microbiome of NHPs with different dietary niches. To begin to examine this question, we used 16S ribosomal RNA gene amplicon sequences to compare the gut microbiomes of five NHP genera categorized either as folivores (Alouatta, Colobus) or non‐folivores (Cercopithecus, Gorilla, Pan) sampled both in captivity and in the wild. Though captivity affected the gut microbiomes of all NHPs in this study, the effects were largest in folivorous NHPs. Shifts in gut microbial diversity and in the relative abundances of fiber‐degrading microbial taxa suggest that these findings are driven by marked dietary shifts for folivorous NHPs in captive settings. We propose that zoos and other captive care institutions consider including more natural browse in folivorous NHP diets and regularly bank fecal samples to further explore the relationship between NHP diet, the gut microbiome, and health outcomes.     

Sexual behavior across ovarian cycles in wild black howler monkeys (Alouatta pigra): male mate guarding and female mate choice

We studied two multimale–multifemale groups of black howler monkeys (Alouatta pigra) during a 14‐month study (June 2006–July 2007) in Palenque National Park, Mexico to evaluate the ways in which their sexual behavior changes across ovarian cycles. We analyzed 231 fecal samples, collected every 2.2±1.4 days from five females. For four females, estradiol and progesterone profiles revealed an average (±SE) cycle length of 18.3±1.4 days. Copulations occurred significantly more frequently during the periovulatory period (POP), defined as the estimated day of ovulation ±3 days (N=18). This was largely the result of cycling females soliciting sexual interactions during their POPs. Females directed their solicitations significantly more often toward “central” males of their group, who had close spatial associations with females at other times, compared with “noncentral” males, who did not associate closely with females. Central males rarely solicited sexual interactions, but instead monitored the females' reproductive status by sniffing their genitals, and maintained significantly closer proximity to females during their POPs, suggesting male mate guarding when conceptions are most likely to occur. Our findings indicate that the reproductive strategies of black howler central males and females coincide, highly skewing mating opportunities toward central males. Black howler females, however, occasionally choose to copulate with noncentral resident males or extra‐group males during their POPs, undermining the ability of central males to monopolize all reproductive opportunities. Am. J. Primatol. 71:153–164, 2009. © 2008 Wiley‐Liss, Inc.     

Enzootic simian piroplasm (Entopolypoides macaci ) in wild-caught Kenyan non-human primates

Background Three species of non‐human primates comprising African green monkeys (AGMs), (Cercopithecus aethiops, n = 89), Syke’s monkeys (Cercopithecus mitis, n = 60) and olive baboons (Papio cynocephalus anubis, n = 30), were screened for Entopolypoides macaci. Methods Observation of blood smears prepared from these animals revealed E. macaci infection rate of 42.7% in AGMs, 35% in Syke’s monkeys and 33.3% in baboons. Results Gender infection rate was 38.2% in females and 29% in males. Statistically, there was no significant difference in infection rates between the monkey species and sexes (P > 0.05). Subsequent indirect immuno fluorescent antibody test supported the morphological appearance of E. macaci observed by microscopy. Sera from infected animals reacted positively (1:625) with E. macaci antigen, but not to Babesia bigemina or B. bovis antigen at 1:125 titer. Conclusion This study has revealed high prevalence of E. macaci infection in all three widely distributed Kenyan non‐human primates. With the continued use of these animals as models for human parasitic diseases, the presence of this highly enzootic parasite should be noted.     

Free-ranging black howler monkeys, Alouatta pigra, in southern Belize are not parasitized by Controrchis biliophilus

Several coprological studies of Alouatta pigra, the black howler monkey, inhabiting Belize and Mexico have been published in the past several years. Trematodes, specifically Controrchis biliophilus (Dicrocoeliidae), have been detected in A. pigra from all locations in Belize and Mexico examined in those studies. A routine coprological survey of A. pigra was conducted in May and June 2010 as part of baseline data collection for an A. pigra population in Punta Gorda, Toledo District, southern Belize. The 51 fecal samples collected in this area were all negative for C. biliophilus. Subsequently, two additional fecal samples were collected from another population of A. pigra in Toledo District and 25 additional fecal samples were collected from six other areas of Belize during December 2010 and January 2011 and were examined for parasites. To date, C. biliophilus eggs have been detected in fecal samples from A. pigra inhabiting every district of Belize except Toledo District in southern Belize. This finding is notable, for no other population of A. pigra completely free of C. biliophilus infection had been located prior to this study.     

The evolution of culture: New perspectives and evidence

This and the next issue of Evolutionary Anthropology are devoted to presenting the most recent advances in our understanding of the evolution of culture in non‐human primates and humans. This effort was stimulated in part by the recent explosion of comparative evidence for extensive communicative and material culture in two great apes, chimpanzees 1 and orangutans. 2 Before this evidence accumulated, it was easy for anthropologists to maintain that examples of non‐human primate culture were little more impressive than those put forward for many other non‐human species, and thus they could leave intact the seemingly huge gap between animal and human culture. The overall purpose of this special pair of issues of Evolutionary Anthropology is to ask how and why culture has changed over evolutionary time from non‐primates to non‐human primates to early hominins to modern humans.