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.
Human-induced habitat fragmentation might seriously affect behavioural patterns and the survival of species whose ecological requirements strongly depend on specific environmental conditions. We compared the genetic structure and dispersal patterns of 2 populations of Alouatta caraya (Plathyrrhini, Atelidae) to understand how habitat reduction and fragmentation affect gene flow in this species. We sampled individuals from 7 groups living in continuous forest (CF, n=46, 22 males and 24 females), and 11 groups that inhabit a fragmented forest (FF, n=50, 24 males and 26 females). FST values based on 11 microsatellite loci showed a recent genetic differentiation among groups in the FF. In contrast, the CF showed no differentiation among groups. Further, FST values between sexes, as well as kinship relationships, also exhibited differences between habitats. In the CF, both males and females disperse, leading to nondifferentiated groups composed of adults that are not close relatives. Conversely, in the FF, some groups are differentiated, males disperse more than females, and groups are composed of closely related adult females. Our results suggest that habitat fragmentation modifies the dispersal patterns of black-and-gold howlers. These differences between habitats may reflect a reduced gene flow, providing genetic evidence that suggests that habitat fragmentation severely limits the howler's ability to disperse. An increasing level of isolation due to uncontrolled deforestation may cause similar loss of genetic diversity on other arboreal primates, and nonprimates that depend on Int J Primatol (2010) 31:813-832
In South America, yellow fever (YF) is an established infectious disease that has been identified outside of its traditional endemic areas, affecting human and nonhuman primate (NHP) populations. In the epidemics that occurred in Argentina between 2007-2009, several outbreaks affecting humans and howler monkeys (Alouatta spp) were reported, highlighting the importance of this disease in the context of conservation medicine and public health policies. Considering the lack of information about YF dynamics in New World NHP, our main goal was to apply modelling tools to better understand YF transmission dynamics among endangered brown howler monkey (Alouatta guariba clamitans) populations in northeastern Argentina. Two complementary modelling tools were used to evaluate brown howler population dynamics in the presence of the disease: Vortex, a stochastic demographic simulation model, and Outbreak, a stochastic disease epidemiology simulation. The baseline model of YF disease epidemiology predicted a very high probability of population decline over the next 100 years. We believe the modelling approach discussed here is a reasonable description of the disease and its effects on the howler monkey population and can be useful to support evidence-based decision-making to guide actions at a regional level.
Black-and-gold howler monkeys Alouatta caraya, are arboreal primates, inhabitants of Neotropical forests, highly susceptible to the yellow fever virus, considered early 'sentinels' of outbreaks, and thus, of major epidemiological importance. Currently, anthropogenic habitat loss and modifications threatens their survival. Habitat modification can prevent, reduce or change dispersal behavior, which, in turn, may influence patterns of gene flow. We explored past and contemporary levels of genetic diversity, elucidated genetic structure and identified its possible drivers, in ten populations (n = 138) located in the southernmost distribution range of the species in South America, in Argentina and Paraguay. Overall, genetic variability was moderate (ten microsatellites: 3.16 ± 0.18 alleles per locus, allelic richness of 2.93 ± 0.81, 0.443±0.025 unbiased expected heterozygosity; 22 haplotypes of 491-bp mitochondrial Control Region, haplotypic diversity of 0.930 ± 0.11, and nucleotide diversity of0.01± 0.007). Significant evidence of inbreeding was found in a population that was, later, decimated by yellow fever. Population-based gene flow measures (FST = 0.13; θST = 018), hierarchical analysis of molecular variance and Bayesian clustering methods revealed significant genetic structure, grouping individuals into four clusters. Shared haplotypes and lack of mitochondrial differentiation (non-significant θST) among some populations seem to support the hypothesis of historical dispersal via riparian forests. Current resistance analyses revealed a significant role of landscape features in modeling contemporary gene flow: continuous forest and riparian forests could promote genetic exchange, whereas disturbed forests or crop/grassland fields may restrict it. Estimates of effective population size allow anticipating that the studied populations will lose 75% of heterozygosity in less than 50 generations. Our findings suggest that anthropogenic modifications on native forests, increasingly ongoing in Northeastern Argentina, Southern Paraguay and Southeastern Brazil, might prevent the dispersal of howlers, leading to population isolation. To ensure long-term viability and maintain genetic connectivity of A. caraya remnant populations, we recommend preserving and restoring habitat continuity. To conserve the species genetic pool, as well, the four genetic clusters identified here should be considered separate Management Units and given high conservation priority. In light of our findings and considering complementary non-genetic information, we suggest upgrading the international conservation status of A. caraya to “Vulnerable”.
Primates play an important role in ecosystem functioning and offer critical insights into human evolution, biology, behavior, and emerging infectious diseases. There are 26 primate species in the Atlantic Forests of South America, 19 of them endemic. We compiled a dataset of 5,472 georeferenced locations of 26 native and 1 introduced primate species, as hybrids in the genera Callithrix and Alouatta. The dataset includes 700 primate communities, 8,121 single species occurrences and 714 estimates of primate population sizes, covering most natural forest types of the tropical and subtropical Atlantic Forest of Brazil, Paraguay and Argentina and some other biomes. On average, primate communities of the Atlantic Forest harbor 2 ± 1 species (range = 1–6). However, about 40% of primate communities contain only one species. Alouatta guariba (N = 2,188 records) and Sapajus nigritus (N = 1,127) were the species with the most records. Callicebus barbarabrownae (N = 35), Leontopithecus caissara (N = 38), and Sapajus libidinosus (N = 41) were the species with the least records. Recorded primate densities varied from 0.004 individuals/km2 (Alouatta guariba at Fragmento do Bugre, Paraná, Brazil) to 400 individuals/km2 (Alouatta caraya in Santiago, Rio Grande do Sul, Brazil). Our dataset reflects disparity between the numerous primate census conducted in the Atlantic Forest, in contrast to the scarcity of estimates of population sizes and densities. With these data, researchers can develop different macroecological and regional level studies, focusing on communities, populations, species co‐occurrence and distribution patterns. Moreover, the data can also be used to assess the consequences of fragmentation, defaunation, and disease outbreaks on different ecological processes, such as trophic cascades, species invasion or extinction, and community dynamics. There are no copyright restrictions. Please cite this Data Paper when the data are used in publications. We also request that researchers and teachers inform us of how they are using the data.
We identified 11 polymorphic microsatellite markers for Alouatta caraya . Three markers were isolated from an enriched genomic library of A. caraya (AC14, AC17, AC45), five were previously described in Homo sapiens (TGMS1, TGMS2, D5S117, D8S165, D17S804), and three were identified for Lagothix lagotricha (1110, 1118, 157). Forty-eight individuals from one Argentinean population were genotyped, yielding heterozygosity values between 0.146 and 0.792. These markers provide an exclusion power of 0.922 when neither parent is known (0.992 when one parent is known) and are suitable for parentage analysis, population genetics and phylogeographical studies of A. caraya, the southernmost primate in the New World.
The black and gold howler monkey (Alouatta caraya) is a neotropical primate that faces the highest capture pressure for illegal trade in Argentina. We evaluate the applicability of genetic assignment tests based on microsatellite genotypic data to accurately assign individuals to their site of origin. The search was conducted on a genetic database to determine the nearest sampled population or to associate them to three clusters described here for the Argentinean populations of A. caraya. We correctly assign 73% of the individuals in the database to nearest population of origin, and 93.3% to their cluster of origin. With this database, we were able to determine the probable origin of 17 confiscated individuals, 12 of which were reintroduced in the province of Misiones and 5 confiscated individuals reintroduced in the province of Santa Fe. Moreover, we also determined the probable origin of 3 individuals found dead in cities in northern Argentina. This approach highlights the relevance of generating genotype indexing databases of species to assist with in-situ and exsitu conservation and management programs. Our results underscore the importance of knowing the origin of individuals for reintroduction and/or species recovery programs and to pinpoint the hotspots of illegal capture of various species.
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