Coprological Surveys of Alouatta pigra at Two Sites in Belize

Fecal samples were collected from black howler monkeys (Alouatta pigra) in north central Belize and analyzed for evidence of endoparasite life stages. At least six types of endoparasites were found in Alouatta pigra fecal samples collected in the Lamanai Archaeological Reserve and the Community Baboon Sanctuary in 1999. These include a digenean trematode, an oxyurid nematode, a strongyle-type nematode, an ascarid presumed to be Ascaris sp., Entamoeba coli and Iodamoeba bütschlii. Higher trematode prevalence was found in adult Alouatta pigra compared to juveniles and higher prevalence of nematode larvae in all animals was found in the wet season compared to the dry season.     

Parasites of free-ranging black howler monkeys (Alouatta pigra) from Belize and Mexico

Parasites are important members of the ecological web within which an animal lives, and can be used as indicators of ecosystem health. However, few baseline parasitological data are available for free-ranging animals, particularly for the black howler monkey (Alouatta pigra). In this study a total of 283 fecal samples were collected from 50 individually identified A. pigra during 2003 and 2004 and examined for parasites. The samples were processed using standard quantitative centrifugation concentration techniques, with sugar and zinc sulfate used as flotation media. The slides were examined using bright-field and phase microscopy. Antigen capture enzyme-linked immunosorbent assays (ELISAs) were used to detect protozoa. Four parasites were detected: 1) Controrchis biliophilus (Dicrocoeliidae), 2) Trypanoxyuris minutus (Oxyuridae), 3) Giardia sp. (Hexamitidae), and 4) Entamoeba sp. (Endamoebidae). Controrchis biliophilus was detected in 80% (wet season) and 81% (dry season) of the A. pigra samples; Trypanoxyuris minutus was detected in 8% (wet season) and 27% (dry season) of samples; and Giardia sp. was detected in 40% (wet season) and 27% (dry season) of samples. For the first time, DNA from Giardia sp.-positive fecal samples was extracted from A. pigra. Alouatta pigra individuals that lived near human settlements in Belize were infected with Giardia duodenalis (syn. G. lamblia, G. intestinalis) Assemblages A and B. These results suggest that G. duodenalis is transmitted from people and/or domestic animals to A. pigra.     

Feeding Competition and Group Size in Alouatta pigra

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.     

Feeding ecology of the black howler monkey (Alouatta pigra) in Northern Belize

We studied the feeding ecology of the black howler monkey (Alouatta pigra) from March 1994 to April 1995 in the Community Baboon Sanctuary in northern Belize, Central America. Activity and diet composition were recorded using continuous focal animal sampling. Diet composition was compared with the relative abundance of plant parts eaten by the howlers within the study site. The study animals spent an average of 24.4% of their time feeding, 61.9% resting, and approximately 9.8% traveling. In contrast to previously published reports on A. pigra, we found the diet composition to be similar to that of other Alouatta species (conforming to the folivore/frugivore profile), with 41% of feeding time spent eating fruit, 45% foliage, and 11% flowers. This contrast may indicate a wide degree of dietary flexibility that allows A. pigra to inhabit a variety of habitat types. We suggest that a high level of resource abundance throughout the year makes the Community Baboon Sanctuary excellent habitat for Alouatta pigra. Am. J. Primatol. 45:263–279, 1998. © 1998 Wiley-Liss, Inc.     

Epidemiology of intestinal helminth parasites in stray dogs from markets in south-eastern Nigeria

A survey of gastrointestinal helminth parasites of stray dogs (Canis familiaris) was conducted at Obollo-Afor and Ekwulobia markets, in Enugu and Anambra States, south-eastern Nigeria, respectively, to determine the patterns of infection among dogs in different parts of south-eastern Nigeria. Faecal samples collected, using long forceps, from every dog encountered in the markets between June 2007 and December 2008 were analysed by the Kato-Katz technique. Out of 413 dogs examined in both markets, 217 (52.6%) were infected with at least one of five parasites (Toxocara spp., Dipylidium caninum, Ancylostoma caninum, Taenia spp. and Trichuris vulpis). Overall faecal egg intensity of infection was 49.9?±?58.7 eggs/g (epg). The prevalence of infection was comparable between the markets and between the male and female dogs, but varied significantly (P?相似文献   

Cascading Effects of Climate Change: Do Hurricane‐damaged Forests Increase Risk of Exposure to Parasites?

Increased parasitism in animals in disturbed habitats is often understood to be the result of increased disease susceptibility due to low food availability resulting in nutritionally stressed and immunocompromised individuals. Such habitat change, however, might also lead to increased exposure to disease. In this article, we test measures of susceptibility and exposure to explain the prevalence and intensity of directly and indirectly transmitted helminths in black howler monkeys (Alouatta pigra) following a hurricane in Belize. None of these parasites were predicted by direct measures of susceptibility (as measured by fruit consumption and fecal cortisol levels). Rather, directly transmitted parasites (Trichuris sp. and strongylid type eggs.) were predicted by host density and group size, both measures of exposure. Similarly, only the consumption of Cecropia peltata, a fast growing pioneer that has a mutualistic relationship with ants predicted levels of the indirectly transmitted trematode Controrchis spp., also suggesting exposure. Cecropia peltata also increased in density post‐hurricane, was high in digestible protein, sugar, and salt and eaten by monkeys more frequently than predicted based on distribution. These data suggest that in this hurricane‐damaged forest the ingestion of this abundant and nutritious pioneer species increased exposure of the monkeys to Controrchis through ingestion of ant intermediate hosts. These results may point to a pattern true of pioneer species in general, leaving animals in disturbed forests with higher levels of parasitism as a result of changes to forest structure. As severe weather events are expected to increase, this suggests a cascading effect of climate change on ecosystem interactions and disease ecology.     

Blood parameters are little affected by time of sampling after the application of ketamine in black howler monkeys (Alouatta pigra)

Background Ketamine hydrochloride is an anesthetic commonly utilized to obtain biological samples in various non‐human primates. Its application alters individual hematologic and biochemical values. The aim of this study was to analyze its effect on blood parameters of Alouatta pigra. Method We collected blood samples at 10 and 40 minutes after the application of ketamine in 12 adult female A. pigra living in free‐ranging conditions. Results The analysis showed that 40 minutes after application of ketamine, the number of platelets, lymphocytes and concentration of phosphorus decreased; however, creatinine, cholesterol, triglycerides, and potassium values increased. Conclusions Our results suggest that ketamine appears to have little effect on the hematology and blood biochemistry of Alouatta pigra females with respect to those reported for other non‐human primates. It is also important to consider the elapsed time after their application when taking blood samples for proper interpretation of the hemogram of Alouatta pigra females.     

Botfly parasitism and tourism on the endangered black howler monkey of Belize

Tourism imposes costs and benefits on wild primates. Endangered black howler monkey (Alouatta pigra) troops with high exposure to tourism had higher levels of botfly (Alouattamyia baeri) parasitism. Edge habitat and juvenile numbers did not seem to confound the observed relationship. To improve the cost/benefit ratio of tourism, we recommend further investigation.     

Epidemiology of Ancylostoma spp. in the endangered Iberian lynx (Lynx pardinus) in the Doñana National Park, south-west Spain

The epidemiology of Ancylostoma spp. was studied in the endangered Iberian lynx (Lynx pardinus) in the Do?ana National Park, south-west Spain. Faecal samples were collected throughout a complete annual cycle (August 1997 to September 1998). The overall egg prevalence of Ancylostoma spp. was 57.8%. The pattern of abundance of Ancylostoma spp. eggs in faeces was overdispersed. Juvenile lynx demonstrated a statistically higher prevalence and abundance of Ancylostoma spp. than in adults. These levels of egg output (maximum 21195 epg), as previously reported in free ranging large felid cubs, could be close to disease involvement. The potential pathogenicity of hookworms and the influence of individual and ecological factors on hookworm transmission in the Iberian lynx from the Do?ana National Park population are discussed.     

Comparative use of color vision for frugivory by sympatric species of platyrrhines

Ateles spp. and Alouatta spp. are often sympatric, and although they are mainly frugivorous and folivorous, respectively, they consume some of the same fruit species. However, they differ in terms of color vision, which is thought to be important for fruit detection. Alouatta spp. have routine trichromatic color vision, while Ateles spp. presents the classic polymorphism of platyrrhines: heterozygous females have trichromatic color vision, and males and homozygous females have dichromatic vision. Given these perceptual differences, one might expect Alouatta spp. to consume more reddish fruits than Ateles spp., since trichromats have an advantage for detecting fruits of that hue. Furthermore, since Ateles spp. have up to six different color vision phenotypes, as do most other platyrrhines, they might be expected to include fruits with a wider variety of hues in their diet than Alouatta spp. To test these hypotheses we studied the fruit foraging behavior of sympatric Alouatta palliata and Ateles geoffroyi in Costa Rica, and modeled the detectability of fruit via the various color vision phenotypes in these primates. We found little similarity in fruit diet between these two species (Morisita = 0.086). Furthermore, despite its polymorphism, A. geoffroyi consumed more reddish fruits than A. palliata, which consumed more greenish fruits. Our modeling results suggest that most fruit species included in the diet of A. geoffroyi can be discriminated by most color vision phenotypes present in the population. These findings show that the effect of polymorphism in platyrrhines on fruit detection may not be a disadvantage for frugivory. We suggest that routine trichromacy may be advantageous for other foraging tasks, such as feeding on young leaves.     

Seasonal Variations in the Diet and Feeding Effort of Two Groups of Howlers in Different Sized Forest Fragments

Little is known about how resource limitation affects the feeding ecology of primates in forest fragments. Here, we describe seasonal variation in the diet and feeding effort of 2 groups (RH and RC3) of howlers (Alouatta palliata mexicana) living in different sized forest fragments in Los Tuxtlas, Mexico. The RH group, which lived in a larger and more preserved forest fragment, with a higher availability of fruit and Ficus trees, had a higher and more constant consumption of fruit throughout the study year. Moreover, this group fed from larger food sources, i.e., trees, lianas, and shrubs, and spent more time feeding from each food source. The feeding effort, defined as the time spent feeding and traveling divided by time spent resting, of the RH group was also significantly lower and more stable than that of the RC3 group throughout the study year. As feeding effort has been positively related to stress in primates, such increases in feeding effort could have negative consequences for howlers in small or degraded forest fragments. Our study suggests that habitat characteristics interact with plant seasonality to determine the diet and feeding effort of howlers in forest fragments and that groups living in small and degraded forest fragments may be particularly vulnerable to years of low fruit production.     

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.     

Molecular systematics and biogeography of the Neotropical monkey genus,Alouatta

We take advantage of the broad distribution of howler monkeys from Mexico to Argentina to provide a historical biogeographical analysis on a regional scale that encompasses the entire Neotropics. The phylogenetic relationships among 9 of the 10 recognized Alouatta species were inferred using three mitochondrial and two nuclear genes. The nuclear gene regions provided no phylogenetic resolution among howler monkey species, and were characterized by very low levels of sequence divergence between Alouatta and the Ateles outgroup. The mtDNA genes, on the other hand, produced a well-resolved phylogeny, which indicated that the earliest split among howler monkeys separated cis- and trans-Andean clades. Eight monophyletic mtDNA haplotype clades were identified, representing six named species in South America, including Alouatta seniculus, Alouatta sara, Alouatta macconelli, Alouatta caraya, Alouatta belzebul, and Alouatta guariba, and two in Mesoamerica, Alouatta pigra and Alouatta palliata. Molecular clock-based estimates of branching times indicated that contemporary howler monkey species originated in the late Miocene and Pliocene, not the Pleistocene. The causes of Alouatta diversification were more difficult to pin down, although we posit that the initial cis-, trans-Andean split in the genus was caused by the late Miocene completion of the northern Andes. Riverine barriers to dispersal and putative forest refuges can neither be discounted nor distinguished as causes of speciation in many cases, and one, the other or both have likely played a role in the diversification of South American howler monkeys. Finally, we estimated the separation of Mesoamerican A. pigra and A. palliata at 3Ma, which corresponds to the completion date of the Panama Isthmus promoting a role for this earth history event in the speciation of Central American howler monkeys.     

Hunting restraint by Creoles at the Community Baboon Sanctuary, Belize: a preliminary survey

This study surveyed 33 male hunters between the ages of 17 and 54 at the Community Baboon Sanctuary (CBS), Belize, to evaluate attitudes and behaviors in relation to hunting black howler monkeys (Alouatta pigra). The study defined hunting restraint as a learned predisposition not to hunt 1 or more species of nonhuman animal. Consistent with Belizean folklore, Creoles at the CBS exhibited hunting restraint with respect to black howlers, preferring to kill bushmeat other than monkeys. The most cited reasons for the observed hunting restraint were utilitarian. Historical and cultural factors also appeared significant. The study results are interpreted in terms of economic theory and suggest that disinhibition of hunting restraint might depend on changes in opportunity costs of hunting these primates. Nonetheless, a change in hunting attitudes and behaviors by Belizean Creoles seems unlikely in the near future because the local and national government and the benefits of ecotourism economically and legally protect howlers. The Creoles' culturally transmitted hunting restraint also culturally protects A. pigra, and the species is not a preferred source of food.     

Bigger ant colonies reduce herbivory and herbivore residence time on leaves of an ant-plant: Azteca muelleri vs. Coelomera ruficornis on Cecropia pachystachya

Summary The effect of defence force size in colonies of the ant Azteca muelleri on the time spent to localize, attack and expel the specialized herbivorous beetle Coelomera ruficornis from Cecropia pachystachya bushes was studied in an area of Atlantic forest in northeastern Brazil. Our results show that Azteca muelleri expel Coelomera ruficornis from Cecropia pachystachya and that the number of ants leaving a colony (defence force size) is negatively correlated with the residence time of an adult beetle on the plant. Colonies with larger defence forces recruited larger numbers of ants, resulting in faster herbivore discovery (r ²=0.80; n=17; P<0.001) and reduced herbivore residence time on a leaf (r ²=0.79 n=23; P<0.001) before being driven off by the ants. We also found a negative and significant relationship between herbivore damage on leaves and ant colony size (r ²=0.28; n=17; P<0.05). We conclude that larger colonies have more individuals available to patrol a plant and recruit defenders toward herbivores. This reduces the time spent to locate and expel susceptible herbivores from the plant. Since the plant probably benefits from reduced herbivory and the plant provides food for the ants, the association between Azteca muelleri and Cecropia pachystachya appears mutualistic.     

Demographic survey of black howler monkey (Alouatta pigra) in the Lachuá Eco-region in Alta Verapaz, Guatemala

Guatemala harbors three species of primates (Alouatta palliata, Alouatta pigra and Ateles geoffroyi), but the distribution and state of conservation of populations of these species are poorly documented. In the case of A. pigra, populations have been studied recently and documented in several sites in Mexico and Belize, and only in one site in Guatemala (Tikal National Park). In this study, we report first-time population data for A. pigra existing in the Lachuá Eco-region in northwestern Guatemala. Surveys were conducted between September 2002 and April 2003 in the northern portion (32 km2) of the Lachuá National Park (LLNP; 145 km2) and in a fragmented landscape north of the protected area. In this latter area we surveyed a large forest fragment (17.14 km2), "Nueve Cerros", and 26 small forest fragments that ranged in size from 0.01 to 3.9 km2. Surveys resulted in a total count of 414 howler monkeys of which 403 belonged to 80 mixed-sex groups, four were solitary males, two were solitary females and five were found in two male groups. Standardized sampling effort among sites indicated 16.7 monkeys/100 survey hours at LLNP, 35.8 individuals/100 survey hours at "Nueve Cerros" and 71.0+/-62.2 individuals/100 survey hours in the forest fragments. Mean group size varied from 4.07 individuals at LLNP to 5.19 individuals in the forest fragments. Conservation problems for the black howler population surveyed are discussed, along with possible conservation scenarios.     

Artificial nest predation by brown howler monkeys (Alouatta guariba clamitans)

Howler monkeys (Alouatta spp.) have long been considered strongly vegetarian primates. Their occasional ingestion of invertebrates has largely been interpreted as unintentional. Recent observations of the consumption of bird eggs by Alouatta caraya living in small and resource-impoverished habitat patches in the state of Rio Grande do Sul (RS), Brazil help to confirm that such behavior by howler monkeys is at times intentional. We report the findings of an experimental study on artificial nest predation by free-ranging Alouatta guariba clamitans in RS and third-party unpublished observations of intentional feeding on animal matter by Alouatta arctoidea in Venezuela and Alouatta palliata in Mexico. A nest station composed of ten artificial nests baited daily with two quail eggs each was placed at six study sites. Each site was monitored from dawn to dusk during 10–12 consecutive days. Individuals (juvenile males and an adult female) from two of the six study groups inspected the nests and ate eggs once. Study subjects from these two groups were the only ones to be supplemented with food (basically fruit) by local inhabitants, a habit that may have decreased their level of neophobia and facilitated their visit to the artificial nests. We suggest that faunivory is an opportunistic and infrequent, but intentional howler monkey feeding behavior.     

Chromosome painting in two genera of South American monkeys: species identification, conservation, and management

Cytogenetic studies showed that a number of New World primate taxa, particularly the genera Alouatta, Aotus, and Callicebus, have highly derived karyotypes. Cytogenetics in these primates, at every level of analysis, has contributed to the recognition of species and revealed that their number was certainly underestimated by researchers relying solely on traditional morphological data. Further attention was drawn to Alouatta and Aotus because they are characterized by translocations of the Y chromosome to autosomes, generating multiple sex chromosome systems. Here we present a report on the hybridization of human chromosome-specific paints on metaphases from 4 individuals originally assigned to Alouatta caraya and 1 individual of Aotuslemurinus. This is only the third karyotype studied with chromosome painting out of more than 10 known karyomorphs in Aotus. The banded chromosomes matched those of karyotype II as defined by Ma et al. [1976a], and we were able to more precisely assign the origin of the sample to A. l. griseimembra. Our results on the Argentinean Alouatta caraya samples were generally comparable to the banding and hybridization pattern of previous studies of A. caraya including the presence of an X(1)X(1)X(2)X(2)/X(1)X(2)Y(1)Y(2) sex chromosome system. The karyotype of the Brazilian Alouatta sample labeled as A. caraya differs from the 3 Argentinean samples by at least 10 chromosome rearrangements. The diploid number, G banding, and hybridization pattern of this female cell line was almost identical to previous painting results on Alouatta guariba guariba. Therefore we must conclude that this cell line is actually from an A. guariba guariba individual. The contribution of cytogenetic tools in identifying species or in this case assigning individuals or cell lines to their precise taxonomic allocation is stressed. Gathering further molecular cytogenetic data on New World primates should be conservation and management priorities.     

Genetic diversity in black howler monkeys (Alouatta pigra) from Belize

To assess the level of genetic variation in a threatened black howler monkey (Alouatta pigra) population, we examined 36 allozyme loci and restriction fragment profiles of mitochondrial DNA (mtDNA). Mean heterozygosity at allozyme loci was only 0.021 and 5.6 percent of the loci were polymorphic. Analyses of mtDNA also revealed low genetic diversity compared with other primates. F-statistics revealed no significant genetic heterogeneity among troops within the Bermudian Landing preserve, but did indicate a deficiency of heterozygotes at one of the two loci. We explore several explanations for this result, which is unexpected in a socially structured primate. Low genetic diversity in this population may reflect its history of demographic bottlenecks. Am. J. Phys. Anthropol. 102:329–336, 1997. © 1997 Wiley-Liss, Inc.     

Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. nodule bacteria on two Mimosa spp. in Costa Rica

rRNA gene sequencing and PCR assays indicated that 215 isolates of root nodule bacteria from two Mimosa species at three sites in Costa Rica belonged to the genera Burkholderia, Cupriavidus, and Rhizobium. This is the first report of Cupriavidus sp. nodule symbionts for Mimosa populations within their native geographic range in the neotropics. Burkholderia spp. predominated among samples from Mimosa pigra (86% of isolates), while there was a more even distribution of Cupriavidus, Burkholderia, and Rhizobium spp. on Mimosa pudica (38, 37, and 25% of isolates, respectively). All Cupriavidus and Burkholderia genotypes tested formed root nodules and fixed nitrogen on both M. pigra and M. pudica, and sequencing of rRNA genes in strains reisolated from nodules verified identity with inoculant strains. Inoculation tests further indicated that both Cupriavidus and Burkholderia spp. resulted in significantly higher plant growth and nodule nitrogenase activity (as measured by acetylene reduction assays) relative to plant performance with strains of Rhizobium. Given the prevalence of Burkholderia and Cupriavidus spp. on these Mimosa legumes and the widespread distribution of these plants both within and outside the neotropics, it is likely that both beta-proteobacterial genera are more ubiquitous as root nodule symbionts than previously believed.