Gone With the Water: The Loss of Genetic Variability in Black and Gold Howler Monkeys (Alouatta caraya) Due to Dam Construction

Black and gold howler monkeys (Alouatta caraya) inhabit several eco-regions in South America with the highest population densities in riverine forests. Dam construction for electricity production represents a severe human alteration of ecosystems with consequences for primate conservation. To evaluate the possible loss of genetic diversity in A. caraya, we analysed and compared the genetic structure of the species across 22 study sites in Argentina (14), Paraguay (1), and Brazil (7). Four of these study sites (referred to as flooded) were sampled before dam-linked flooding which most likely caused a drastic decline or functional extinction of these populations. The genetic variability of 256 individuals was evaluated using 10 autosomal microsatellites (STRs) and 112 individuals by sequencing a fragment of 507 bp of mtDNA. DNA was extracted from tissue, blood, and faecal samples. Significantly higher values of genetic variability were observed for the flooded populations both in mtDNA and STRs. Population genetic structure showed a K = 1, 2, or 5 depending on the method, separating Argentinian and Paraguayan sites from Brazilian sites and, in the case of K = 5, two clusters were mostly represented by flooded populations. Isolation-by-distance analyses showed that geographic distances influence gene flow. Analytical methods, such as Pairwise Fst’s and Nei’s and regression model of Harpending and Ward, were concordant in detecting significant genetic structuring between flooded and remaining sites examined. Although some sites have very low sample sizes, these samples are of great importance since these sampling sites are currently flooded. Our results show that the study sites where dams were built had the greatest genetic diversity. As A. caraya is currently severely threatened by yellow fever outbreaks, the remaining populations may be more vulnerable to disease outbreaks due to impoverished genetic variability. Accordingly, it is essential to implement management actions to conserve the remaining populations. Our results underline the importance for Environmental Impact Assessments (EIA) to include data on the genetic structure of species in the affected sites prior to their alteration or destruction. These genetic data are also remarkably important for determining where to relocate specific individuals to help avoid biodiversity loss.Fil: Oklander, Luciana Inés. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas | Universidad Nacional de Misiones. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas; ArgentinaFil: Caputo, Mariela. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Departamento de Microbiología, Inmunología y Biotecnología. Cátedra de Genética y Biología Molecular; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay; ArgentinaFil: Fernández, Gabriela Paula. Universidad Nacional del Noroeste de la Provincia de Buenos Aires. Centro de Bioinvestigaciones (Sede Pergamino); Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro de Investigaciones y Transferencia del Noroeste de la Provincia de Buenos Aires. Universidad Nacional del Noroeste de la Provincia de Buenos Aires. Centro de Investigaciones y Transferencia del Noroeste de la Provincia de Buenos Aires; ArgentinaFil: Jerusalinsky, Leandro. Centro Nacional de Pesquisa e Conservação de Primatas Brazileiros; BrasilFil: de Oliveira, Silviene F.. Universidade do Brasília; BrasilFil: Bonatto, Sandro Luis. Pontificia Universidade Católica do Rio Grande do Sul; BrasilFil: Corach, Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay; Argentina. Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. Departamento de Microbiología, Inmunología y Biotecnología. Cátedra de Genética y Biología Molecular; Argentin

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Brown howler monkey: alouatta guariba Humboldt, 1812

Alouatta guariba is endemic to the Atlantic Forest in eastern Brazil and northeast Argentina. In the south, its distribution is limited by the Camaquã river basin (Printes et al. 2001) and to the north by the Paraguaçu river in the state of Bahia (Gregorin 2006; Neves et al. 2018). The western boundary is marked by the limits of the Atlantic Forest. It occurs in the Brazilian states of Bahia, Espírito Santo, Rio de Janeiro, Minas Gerais, São Paulo, Paraná, Santa Catarina and Rio Grande do Sul (Mendes et al. 2008, Bicca-Marques et al. 2018). In Argentina the species is limited to the province of Misiones (Agostini et al. 2017).Fil: Buss, Gerson. Centro Nacional de Pesquisa e Conservação dos Primatas; BrasilFil: Oklander, Luciana Inés. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas | Universidad Nacional de Misiones. Instituto de Biología Subtropical. Instituto de Biología Subtropical - Nodo Posadas; ArgentinaFil: Bicca Marques, Júlio César. Pontificia Universidad Catolica de Parana. Escola de Ciencias Da Vida.; BrasilFil: Hirano, Zelinda B.. Universidade Regional de Blumenau; BrasilFil: Chaves, Oscar M.. Pontificia Universidad Catolica de Parana. Escola de Ciencias Da Vida.; BrasilFil: Mendes, Sergio L.. Instituto Nacional da Mata Atlântica; BrasilFil: Neves, Leonardo G.. Universidade Estadual de Santa Cruz; BrasilFil: Melo, Fabiano R.. Universidade Federal de Viçosa.; BrasilFil: Rylands, Anthony B.. Wildlife Conservation Society; Estados UnidosFil: Jerusalinsky, Leandro. Centro Nacional de Pesquisa e Conservação dos Primatas Brasileiros; Brasi

Impact of the COVID-19 Pandemic on Primate Research and Conservation

There is evidence to suggest that the Coronavirus Disease 2019 (COVID-19) pandemic may hamper our achievement of the Sustainable Development Goals (SDGs). Here, we use non-human primates as a case study to examine the impacts of COVID-19 on the ability to achieve biodiversity conservation and management sustainability targets. We collected data through a survey of members of the IUCN SSC Primate Specialist Group from January to March 2022. Of the 93 experts that responded to our survey, we found that 39% had not been able to visit any of their field sites since March 2020, 54% said they had less funding available for their primate-related work, and only one out of ten said they had managed to achieve at least 76–100% of their planned primate-related work since March 2020. Six out of 10 respondents (61%) felt that primate conservation efforts in protected areas were worse than before the onset of the COVID-19 pandemic and one-third (33%) felt hunting was happening more frequently than before. This study provides evidence of the impacts of COVID-19 on progress towards achieving the SDGs, and provides practical lessons learned for biodiversity conservation efforts moving forward

Primates in peril: the significance of Brazil, Madagascar, Indonesia and the Democratic Republic of the Congo for global primate conservation

Primates occur in 90 countries, but four—Brazil, Madagascar, Indonesia, and the Democratic Republic of the Congo (DRC)—harbor 65% of the world’s primate species (439) and 60% of these primates are Threatened, Endangered, or Critically Endangered (IUCN Red List of Threatened Species 2017-3). Considering their importance for global primate conservation, we examine the anthropogenic pressures each country is facing that place their primate populations at risk. Habitat loss and fragmentation are main threats to primates in Brazil, Madagascar, and Indonesia. However, in DRC hunting for the commercial bushmeat trade is the primary threat. Encroachment on primate habitats driven by local and global market demands for food and non-food commodities hunting, illegal trade, the proliferation of invasive species, and human and domestic-animal borne infectious diseases cause habitat loss, population declines, and extirpation. Modeling agricultural expansion in the 21st century for the four countries under a worst-case-scenario, showed a primate range contraction of 78% for Brazil, 72% for Indonesia, 62% for Madagascar, and 32% for DRC. These pressures unfold in the context of expanding human populations with low levels of development. Weak governance across these four countries may limit effective primate conservation planning. We examine landscape and local approaches to effective primate conservation policies and assess the distribution of protected areas and primates in each country. Primates in Brazil and Madagascar have 38% of their range inside protected areas, 17% in Indonesia and 14% in DRC, suggesting that the great majority of primate populations remain vulnerable. We list the key challenges faced by the four countries to avert primate extinctions now and in the future. In the short term, effective law enforcement to stop illegal hunting and illegal forest destruction is absolutely key. Long-term success can only be achieved by focusing local and global public awareness, and actively engaging with international organizations, multinational businesses and consumer nations to reduce unsustainable demands on the environment. Finally, the four primate range countries need to ensure that integrated, sustainable land-use planning for economic development includes the maintenance of biodiversity and intact, functional natural ecosystems

ATLANTIC-PRIMATES: a dataset of communities and occurrences of primates in the Atlantic Forests of South America

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/km 2 (Alouatta guariba at Fragmento do Bugre, Paraná, Brazil) to 400 individuals/km 2 (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. © 2018 by the The Authors. Ecology © 2018 The Ecological Society of Americ

Terrestrial behavior in titi monkeys (Callicebus, Cheracebus, and Plecturocebus) : potential correlates, patterns, and differences between genera

For arboreal primates, ground use may increase dispersal opportunities, tolerance to habitat change, access to ground-based resources, and resilience to human disturbances, and so has conservation implications. We collated published and unpublished data from 86 studies across 65 localities to assess titi monkey (Callicebinae) terrestriality. We examined whether the frequency of terrestrial activity correlated with study duration (a proxy for sampling effort), rainfall level (a proxy for food availability seasonality), and forest height (a proxy for vertical niche dimension). Terrestrial activity was recorded frequently for Callicebus and Plecturocebus spp., but rarely for Cheracebus spp. Terrestrial resting, anti-predator behavior, geophagy, and playing frequencies in Callicebus and Plecturocebus spp., but feeding and moving differed. Callicebus spp. often ate or searched for new leaves terrestrially. Plecturocebus spp. descended primarily to ingest terrestrial invertebrates and soil. Study duration correlated positively and rainfall level negatively with terrestrial activity. Though differences in sampling effort and methods limited comparisons and interpretation, overall, titi monkeys commonly engaged in a variety of terrestrial activities. Terrestrial behavior in Callicebus and Plecturocebus capacities may bolster resistance to habitat fragmentation. However, it is uncertain if the low frequency of terrestriality recorded for Cheracebus spp. is a genus-specific trait associated with a more basal phylogenetic position, or because studies of this genus occurred in pristine habitats. Observations of terrestrial behavior increased with increasing sampling effort and decreasing food availability. Overall, we found a high frequency of terrestrial behavior in titi monkeys, unlike that observed in other pitheciids

Variabilidad genética de Alouatta caraya en Sudamérica

El mono aullador negro y dorado (Alouatta caraya) habita en varias provincias Argentinas, estados Brasileños, nordeste de Bolivia y Paraguay. Esta especie posee la distribución más austral entre todos los primates neotropicales. A. caraya es una especie que soporta niveles moderados de deforestación y contribuye en la regeneración y modelación de los bosques por ser dispersor de semillas, jugando un papel fundamental en el mantenimiento de los ambientes en los que habita. A pesar de estar descripta como una especie con bajo riesgo de extinción (CITES: Apéndice II), los monos carayá se consideran amenazados por el actual desmonte indiscriminado en el límite del sur de su rango geográfico. La variabilidad genética de los individuos de una especie es esencial para su supervivencia a largo plazo. Cuando se reduce la diversidad genética de una población disminuye su potencial evolutivo disminuye, es decir, se reduce su capacidad de responder ante futuros retos ambientales. Por este motivo es importante estudiar los niveles de variabilidad genética tanto en especies en peligro como especies que enfrentan una intensa fragmentación del hábitat, como es el caso de los aulladores. Se analizaron muestras provenientes de 5 estados de Brasil (RS n=3, MGS n=30 PR n=20, MG n=5, GO n=2), 2 provincias de Argentina (Corrientes n=10, Chaco n=10), Bolivia (n=5) y Paraguay (n=5) utilizando la diversidad genética de secuencias de ADN mitocondrial y de microsatélites autosómicos mediante los programas ARLEQUIN 3.11, MEGA 4.0 y STUCTURE 2.2. Los resultados del AMOVA mostraron una diferenciación genética entre los sitios de muestreo (Fst=0,07, p=0,000). El análisis de distancia genética basada en una matriz pareada de Fst mostró diferencias significativas entre 4 grupos de sitios de muestreo. Estos 4 grupos serian: 1) Argentina-Paraguay-RS, 2) Bolívia-GO-MG 3) PR 4) MGS. Estos resultados fueron confirmados mediante el análisis de subestructuración genética llevados a cabo con STRUCTURE. Por otra parte el análisis de la Región Control del ADN mitocondrial permitió obtener resultados consistentes con la subestructuración geográfica obtenida mediante marcadores nucleares. Los resultados de este estudio aportan conocimientos sobre la filogeografía de Alouatta caraya, contribuyendo al esclarecimiento los procesos de radiación adaptativa en el continente Americano que determinan su actual distribución. Asimismo, contribuye al conocimiento de las características genéticas exclusivas de cada población, lo cual permitirá establecer zonas prioritarias para la conservación de esta especie.Simposio: Avances y proyecciones de primatología argentinaAsociación de Antropología Biológica de la República Argentin