Habitat fragmentation and population size of the black and gold howler monkey (Alouatta caraya) in a semideciduous forest in Northern Argentina

A population of black and gold howler monkeys (Alouatta caraya) living near the southern limit of its distribution in a semideciduous forest located in northern Argentina was studied in 2003 to evaluate the possible effects of habitat fragmentation - owing to logging - on its density and social organization within it. Aerial photographs taken in 1982, 1992, and 2001 were used to compare maps of vegetation. These maps were used to evaluate changes in the area covered by forest fragments. From March to June 2003, 10-day monthly surveys of howlers were made in each fragment. A total of 232 individual howlers were counted, belonging to 34 groups plus a solitary adult female. Groups ranged from 2 to 19 individuals (mean = 6.82, SD = 4.23), and 21% of the groups contained more than one adult male. Adults accounted for 55% of the individuals, immatures for 45%, and infants represented 13% of the total. Data obtained were compared with information available for the same population for 1982 and 1995. Results revealed no significant changes in the area of fragments, the crude and ecological density of howlers, and group composition. Group sizes and group composition of howlers suggest that the population remained stable over the past 22 years. The density, number of groups, and individuals appears not to be affected by fragmentation and logging, but crude density was low compared with other less-disturbed habitats. The status of the population remains uncertain owing to isolation, and because there are no protected areas to ensure its stability for the future.     

Fecundity in the captive howler monkey,Alouatta caraya

Seven female Black howler monkeys, Alouatta caraya, from both wild- and captive-born origins have reproduced at Riverbanks Zoological Park. Three of the five wild-born females arrived as juveniles and grew to maturity; the other two were already mature upon arrival and reproduced shortly therafter. Two females which were born within the park's collection have since reached maturity and also reproduced. The interval between the first and second young of wild-born howlers is longer than between subsequent birth intervals. Subsequent young are also more precocious than their preceding siblings. In at least one case, a socially inferior female did not reproduce until placed within a different troop situation which elevated her social status. Females born in captivity conceived when 42 and 35 months old, the former situation being linked to low social status. Young born to females housed under both seasonal and regulated conditions of photoperiod demonstrated no difference in breeding intervals and seasonality of birth does not appear to be a factor in howler monkey reproduction.     

Seed predation ofCariniana estrellensis (Lecythidaceae) by black howler monkeys,Alouatta caraya

Seed predation by howler monkeys is poorly documented. Here we report the seed predation onCariniana estrellensis (Lecythidaceae) fruits by the black howler monkeyAlouatta caraya in south-east Brazil during an intense dry season. This observation suggests that even non-specialized seed predators such as howlers can use seeds in critical periods of dry season.     

A new southern limit for the distribution ofAlouatta caraya in Rio Grande do Sul State,Brazil

The discovery of two groups of the black howler monkey,Alouatta caraya, inhabiting two orchards on a cattle farm, Fazenda Casa Branca (29°56′S, 55°59′W), Rio Grande do Sul State, Brazil, represents a new southern limit for the geographic distribution of this species.     

Effects of black howler monkey (Alouatta caraya) seed ingestion on insect larvae

Fig (Ficus monckii) and laurel (Ocotea puberula) seeds were obtained from Alouatta caraya feces (ingested seeds) and from trees (noningested) in northeastern Argentina. Seeds were examined to detect the presence (infested) or absence (noninfested) of larvae. Sixty percent (N = 315) of noningested fig seeds were galls with insect larvae inside, while 23% (N = 331) were encountered in the ingested group. Eighty-two percent (N = 28) of noningested laurel seeds were infested, and only 19% (N = 63) of ingested seeds were infested. According to the present data, the insects' larvae are digested by howlers intaking animal protein, but the laurel seeds were not destroyed. Am. J. Primatol. 45:411–415, 1998. © 1998 Wiley-Liss, Inc.     

Environmental Determinants of Birth Seasonality in Night Monkeys (Aotus azarai) of the Argentinean Chaco

The night monkeys (Aotus azarai) of Formosa, Argentina provide an opportunity to investigate the influences of ambient temperature and photoperiod on reproduction in a highly seasonal environment: the Chaco. Between 1997 and 2000, we collected data to evaluate the relationship between rainfall, ambient temperature, photoperiod and food availability and the annual distribution of mating behavior and births in 15 groups of monkeys in the forests of the Eastern Argentinean Chaco. Our data show that the area is highly seasonal, characterized by significant fluctuations in rainfall, temperature, photoperiod and food availability. There are two rain peaks in April and November and a dry season lasting from June to August. Monthly mean temperatures were on average 11°C lower during winter months than they were during summer months. Temperatures <10°C and >33°C were also frequent through the year. Days are 3 h longer during the summer than during the winter months. Insect abundance and the percentage of tree species producing fruits, flowers or new leaves reached a low in the coldest winter months. Mating was infrequent, and we only observed it between May and September. Half the births (n = 13) occurred during a 2-week period in October. Infant survival during the first 6 mo of life was high (96%). Our findings suggest an environmental control of reproduction. Changes in photoperiod and temperature may promote reproductive activity in females that might conceive and begin pregnancy at a time void of high temperatures that could be metabolically challenging.     

Phlebotominae in peri‐domestic and forest environments inhabited by Alouatta caraya in northeastern Argentina

Multiple species of Phlebotominae are vectors of Leishmania (Protozoa: Trypanosomatidae), which causes visceral leishmaniasis (VL) and cutaneous leishmaniasis (CL). To describe the Phlebotominae (Diptera: Psychodidae) related to the environments of black and gold howler monkeys Alouatta caraya (Humbodlt, 1812) (Primates: Atelidae), potential vectors were sampled in different landscapes and vertical strata of sleeping trees. Phlebotomine captured between December 2011 and March 2012 (2365 individuals) belonged to eight species, of which Nyssomyia neivai (Pinto, 1926) (61.4%) and Migonemyia migonei (França, 1920) (18.73%) were the most abundant, and Ny. withmani was recorded for the first time in the Chaco province. In the ‘peri‐domestic’ landscape, the phlebotomine were mainly captured in henhouses (78.7%), whereas the tree canopy in ‘rural’ and ‘wild’ landscapes yielded 31.2% and 29.1% of the phlebotomine, respectively. A significant association between the type of landscape and the species of phlebotomine was observed by multivariate analysis. Lutzomyia longipalpis (Lutz & Neiva, 1912) and Mg. migonei were associated with ‘peri‐domestic’ landscape, and Ny. neivai was associated with the ‘wild’ landscape. The results of this prospective study suggest that the interaction between phlebotomine and A. caraya could be a key factor with respect to understanding the epidemiology of leishmaniasis.     

Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus).

We monitored the birth patterns of sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus) during a 4‐yr period from October 1996 to August 2000 at the Estação Biológica de Caratinga, Minas Gerais, Brazil. Brown howler monkey births (n = 34) occurred throughout the year, and birth frequencies did not differ between rainy and dry season months. The aseasonal birth patterns of the howler monkeys differed significantly from the dry season concentration and dry month peak in muriqui births (n = 23). We found no effects of infant sex or the number of females on interbirth intervals (IBIs) in our 10 howler monkey study troops. IBIs of brown howler monkeys averaged 21.2 ± 2.5 mo (n = 8, median = 21.0 mo), and were significantly shorter following dry season births than rainy season births. Their IBIs and yearling survivorship (74%) were similar to those reported for other species of howler monkeys, but yearling survivorship was much lower than that of muriquis (94%), whose IBIs were more than 12 mo longer than those of the howler monkeys. Our study extends comparative knowledge of birth patterns in Alouatta to a poorly known species, and provides insights into the different ways in which diet and life history may affect the timing of births in large‐bodied platyrrhines under the same seasonal ecological conditions. Am. J. Primatol. 55:87–100, 2001. © 2001 Wiley‐Liss, Inc.     

Red howler monkey birth data I: Seasonal variation

A large set of birth data from a population of red howler monkeys (Alouatta seniculus) in two habitats found a consistent birth “dip,” with births occurring less frequently in early wet season (May–July) than during the remaining months. In one of two habitats, births were negatively correlated with rainfall, and viable conceptions were positively correlated with rainfall. The observed degree of within-troop birth synchrony appeared to reflect populational synchrony with environmental factors. Correlations between births and the phenology of plant foods were not striking, but there was weak support for the hypothesis that births are timed to maximize the availability of weaning foods. Reduced births in early wet season also minimize the number of Infants who would experience the transition to independent locomotion and feeding during the peak of the dry season when probable low moisture content of foods and high daytime temperatures might be disadvantageous. However, there was no relationship between season of birth and infant mortality.     

Serum Nutritional Profiles of Free-Ranging <Emphasis Type="Italic">Alouatta Caraya</Emphasis> in Northern Argentina: Lipoproteins; Amino Acids; Vitamins A,D, and E; Carotenoids; and Minerals

Quantifying circulating nutrient concentrations in sera of free-ranging subjects will help to establish a basis from which we can evaluate the nutritional status and needs of the captive population. We collected serum samples from 26 free-ranging black-and-gold howlers (Alouatta caraya) in San Cayetano forest in northern Argentina. We analyzed them for concentrations of lipoproteins; amino acids; vitamins A, D, and E; carotenoids; and minerals. There are a few significant differences between sexes in concentrations of high-density lipoprotein cholesterol, certain amino acids, vitamin E, lutein + zeaxanthin, and copper. Most nutritional parameters are similar to the ones measured in free-ranging Mexican mantled howlers (Alouatta palliata mexicana) and in captive New World primates (NWPs). Carotenoid, vitamin D, and phosphorus concentrations are the exceptions. Carotenoid concentrations are higher in free-ranging Alouatta caraya than reported for other free-ranging and captive species. Vitamin D concentrations are 14 times greater in the free-ranging black-and-gold howlers than in captive NWPs. Phosphorus concentrations are also higher than expected and higher than typically occur in captive primates, leading to a 1:1.6 calcium:phosphorus ratio. Because we based our study on a small number of free-ranging howlers, additional samples from different regions and throughout the year would better define desirable nutritional parameters for captive howlers.     

Grooming in brown howler monkeys,Alouatta fusca

The grooming behavior of a group of brown howler monkeys was studied for one year in an Atlantic forest reserve of southeastern Brazil. A total of 290 grooming bouts were recorded and analyzed. The two adult females directed most of the grooming (91%), while the adult male was the major recipient (37%). Grooming between females, and between them and their siblings, also occurred quite often. On average, the group spent 2% of its daily time grooming, with a higher frequency around noon. There were significant differences, however, in time spent grooming between seasons; grooming was more abundant during the coldest seasons (autumn–winter) and rarer in hotter ones (spring–summer). A significant negative correlation was found between grooming time and temperature, but contrary to expectations, grooming time failed to correlate with both the group' diet and the demands of food-gathering, as measured by travelling time and day range length. A comparison of grooming behavior with other species of the genus suggests that brown, red (A. seniculus), and black howler monkeys (A. caraya) are more similar to each other than to mantled howlers (A. palliata), a result that probably is linked with the differing social structure and group size of the latter species. © 1995 Wiley-Liss, Inc.     

Phytochemical and mineral components of foods consumed by black howler monkeys (Alouatta pigra) at two sites in Belize

We analyzed the chemical composition of the diets of eight groups of free‐ranging black howler monkeys (Alouatta pigra) in Belize, Central America. The study groups were located in two different forests: the Community Baboon Sanctuary (CBS) and the Cockscomb Basin Wildlife Sanctuary (CBWS). Two of the study groups were translocated from the CBS to CBWS 3 months into the study, and we compared the diets of groups in the two forests. Young and mature leaves, fruits, flowers, and fig samples (n = 144) were analyzed for water content, crude and available protein, fiber, simple sugars, and minerals. Statistically significant differences were found among the plant parts in all measures except acid‐detergent fiber. Dietary foliage in CBS was higher in water content and protein but lower in simple sugars than dietary foliage in CBWS. We suggest that changes in the selection of plant parts by primates may be related to differences in the nutritional content of those parts. These data may be useful in developing optimal diets for captive howler monkeys. Zoo Biol 19:95–109, 2000. © 2000 Wiley‐Liss, Inc.     

Observed case of infanticide committed by a resident male central American black howler monkey (Alouatta pigra)

Although infanticide has been witnessed in other species of howler monkey, and has been inferred for Alouatta pigra, an observed case of infanticide has not previously been recorded for this species. Here we describe the killing of a 2-week-old infant by the resident male of a small social group in southern Belize. The infanticide was witnessed as part of an intensive observational study that began in January 2003. The male was known to have resided in the group for at least 4 months, but it is not known whether he was the father of the infant. The literature proposes three main explanations for infanticide: two adaptive hypotheses (sexual selection and resource competition), and one nonadaptive hypothesis (social pathology). Individual cases of infanticide such as this one are important for comparative purposes, but when examined on their own they are difficult to interpret in relation to established theoretical frameworks. The data presented here show some consistency with the sexual-selection and resource-competition hypotheses, but the lack of critical information (i.e., as to paternity) makes it impossible to draw firm conclusions.     

Population genetic studies of Alouatta caraya (Alouattinae, Primates): inferences on geographic distribution and ecology

Cytochrome b DNA sequence data (ca. 1,140 bp) of 44 Alouatta caraya, including 42 specimens from three localities of Brazil and two from Bolivia, were used for phylogenetic reconstructions and population studies. Seventeen haplotypes were identified, eight of which were present in more than one individual. Seven of these eight haplotypes were shared by individuals from a same locality and one by individuals from two localities. We found 26 variable sites along the entire gene, consisting of 18 transitions and eight transversions; most replacements occurring at the third codon position (65.39%) in contrast to first and second positions (26.92 and 7.69%, respectively). In the sample collected at Chapada dos Guimarães (Brazil), nucleotide and haplotype diversity estimates were π=0.002325 and h=0.8772, respectively. Maximum parsimony analysis grouped all haplotypes in two clades, separating Bolivian haplotypes from Brazilian haplotypes, the grouping of which did not show a straightforward correspondence with geographic distribution. Median‐joining and TCS network pointed to haplotypes 11 or 12 as the most likely ancestral ones. Mismatch distribution and the goodness‐of‐fit test (SSD estimate=0.0027; P=0.6999) indicated that the population from Chapada dos Guimarães experienced a demographic expansion, in agreement with the median‐joining star‐like pattern, although this finding could not be confirmed by Fu's F_s test. Am. J. Primatol. 69:1093–1104, 2007. © 2007 Wiley‐Liss, Inc.     

Geographic Distribution of Red Howlers (Alouatta seniculus) in Southwestern Brazilian Amazonia, with Notes on Alouatta caraya

We surveyed howler (Alouatta) populations at 36 sites throughout the Brazilian state of Rondônia, in southwestern Amazonia, using quantitative (line transect surveys) and qualitative (interviews) methods. We recorded the red howler (Alouatta seniculus) at only one- third of the sites, and the species was relatively rare at most of them, especially in comparison with sympatric atelids (Ateles chamek and Lagothrix cana). In addition to local discontinuities, Alouatta was absent from a wide area (possibly as much as 100,000 km²) of northern Rondônia, south of the upper Madeira river. This lacuna apparently contradicts the typical association of the species with flooded forest ecosystems, but the ecological factors that may underlie it remain unclear. Competition with sympatric atelids does not appear to be a significant factor anywhere within the study area. Also, there is no evidence to suggest that the distribution patterns are related to recent human colonization of the state. We collected indirect evidence of the presence of a second howler species – Alouatta caraya – at two sites in southern Rondônia, where they are associated with highland savanna habitats and gallery forests in the Guaporé grasslands.     

Chromosome studies in Alouatta belzebul

The chromosome constitution of Alouatta belzebul was studied with G-, C-, and silver staining. In ten specimens identified as Alouatta belzebul, the chromosome constitution of males (2n = 49) differed from that of females (2n = 50) owing to a Y-autosome translocation. In another single female specimen, probably Alouatta belzebul nigerrima, the diploid chromosome number was also 50, though its karyotype was drastically different from that of Alouatta belzebul belzebul. Chromosome studies, taken together with phenotypic and field observations, suggest that Alouatta belzebul belzebul is phenotypically variable in respect to pelage coloration. This attribute is therefore unreliable for the precise identification of Alouatta belzebul subspecies. Conversely, relatively minor phenotypic differences, allowing for the characterization of subspecies within a same species, coexist with unparalleled, drastic karyotypic divergence. These findings clearly question gross morphological attributes as discriminative characteristics of Alouatta belzebul subspecies.     

Seismic activity response as observed in mantled howlers (Alouatta palliata), Cuero y Salado Wildlife Refuge, Honduras

This report documents the response of wild mantled howlers (Alouatta palliata) to coseismic activity (seismic activity at the time of an earthquake). During field work on the north coast of Honduras, data were collected on a habituated troop of mantled howlers as they responded to coseismic activity. The seismic event occurred on 13 February 2001 at 0822 hours local time with a magnitude of Richter scale 6.6, focus depth of approximately 15 km at a distance of 341 km from the epicentre to the field site, Cuero y Salado. At the field site, based upon Jeffreys and Bullen (1988), body waves, noted as P and S waves, arrived at 60 and 87 s, respectively, with surface waves arriving approximately 103 s post-origin time of the seismic event. While there are three reports on non-human primate response to coseismic activity in the literature, they report on captive non-human primates. This is the first documented response on a non-captive troop. In addition, this report compares the intensity measure encountered by a wild troop of howlers and one captive group of orangutans as set out by the Modified Mercalli Intensity scale. The Modified Mercalli measure of intensity is one of two standard measures of seismic activity and rates what a person sees and feels at their location (Wood and Neumann 1931; Richter 1958). Thus, arboreal nonhuman primates are found to respond to coseismic activity ranging from Level IV to Level VI as based upon the modified Mercalli intensity scale.     

Relation of Intergroup Variation in Allogrooming to Group Social Structure and Ectoparasite Loads in Red Howlers (Alouatta seniculus)

We compare the allogrooming behavior of 5 troops (average size = 8.2) of red howlers (Alouatta seniculus) from the Venezuelan Llanos with that of other A. seniculus and Alouatta spp. of the genus. In 126.9 observation hr, we recorded 118 allogrooming events, with an average bout length of 109 sec. Females groomed more frequently than males did, but as groomees there is no significant differences between sexes. Adult males groomed adult females mostly in a sexual context (before copulation). Allogrooming rates differ significantly among groups. There are also significant differences among members of the same troop both as groomers and groomees, which we explain in the context of the social behavior and history of each troop. There is no significant correlation between weight of the groomee and duration of the grooming bout. However, the examination of grooming rates and ectoparasite load suggests that allogrooming may have hygienic consequences. Differences in allogrooming rates among species of Alouatta are related to differences in group kin structure and patterns of female competition, in particular, coalition formation. We conclude that the social structure and the degree of relatedness among individuals within a group (or among individuals in a population in interpopulation comparisons) is a more important determinant of allogrooming rate than body size or group size. Our results emphasize the importance of considering intergroup and interpopulational variation in behavior.