Climate determines transmission hotspots of Polycystic Echinococcosis, a life-threatening zoonotic disease, across Pan-Amazonia.

Polycystic Echinococcosis (PE), a neglected life-threatening zoonotic disease caused by the cestode Echinococcus vogeli, is endemic in the Amazon. Despite being treatable, PE reaches a case fatality rate of around 29% due to late or missed diagnosis. PE is sustained in Pan-Amazonia by a complex sylvatic cycle. The hunting of its infected intermediate hosts (especially the lowland paca Cuniculus paca) enables the disease to further transmit to humans, when their viscera are improperly handled. In this study, we compiled a unique dataset of host occurrences (~86000 records) and disease infections (~400 cases) covering the entire Pan-Amazonia and employed different modeling and statistical tools to unveil the spatial distribution of PE's key animal hosts. Subsequently, we derived a set of ecological, environmental, climatic, and hunting covariates that potentially act as transmission risk factors and used them as predictors of two independent Maximum Entropy models, one for animal infections and one for human infections. Our findings indicate that temperature stability promotes the sylvatic circulation of the disease. Additionally, we show how El Niño-Southern Oscillation (ENSO) extreme events disrupt hunting patterns throughout Pan-Amazonia, ultimately affecting the probability of spillover. In a scenario where climate extremes are projected to intensify, climate change at regional level appears to be indirectly driving the spillover of E. vogeli. These results hold substantial implications for a wide range of zoonoses acquired at the wildlife-human interface for which transmission is related to the manipulation and consumption of wild meat, underscoring the pressing need for enhanced awareness and intervention strategies.

Comparative gastrointestinal organ lengths among Amazonian primates (Primates: Platyrrhini).

OBJECTIVES: The morphological features of the gastrointestinal tract (GIT) in mammals reflect a species' food niche breadth and dietary adaptations. For many wild mammals, the relationship between the structure of the GIT and diet is still poorly understood, for example, the GIT for frugivorous primates is usually classified as unspecialized and homogeneous. Here, we compare the GIT structure of 13 primate species from the three families of extant platyrrhines (Atelidae, Pitheciidae, and Cebidae) in Amazonia, and discuss possible evolutionary adaptations to different diets and trophic niches. METHODS: We measured the length of the esophagus, stomach, small intestine, large intestine, cecum, colon, and rectum of the digestive tracts of 289 primate specimens. We determined the allometric relationships of the different tubular organs with the total length of the GIT as a proxy of specimen body size. Allometric parameters were used to establish the quotients of differentiation of every organ for each primate specimen. RESULTS: There was a high differentiation in structure of the digestive organs among genera. Alouatta specimens clearly separated from the other genera based on dissimilarities in gastric, colonic, and rectal quotients, likely linked to the fermentation of plant contents. In contrast, all cebines (Sapajus, Cebus, and Saimiri) and Cacajao species had similar small intestine quotients, which is expected due to their high rates of animal matter consumed. CONCLUSIONS: We show that diverse adaptations in digestive structure exist among frugivorous primates, which in turn reflect different dietary patterns within this group that may enable the geographic coexistence of different primate species.

Environmental predictors of filarial infection in Amazonian primates: Ecological factors and primate filarial infection.

Filarial nematode infections are common in primates, but have received little attention in the Neotropics. Epidemiological data on filarial infections in primates are still too sparse to fully understand the complex of this parasitism, especially because of the difficulty in studying the ecology and epidemiology of wild primates.. We describe natural infections by Dipetalonema parasitizing 211 primates belonging to eight free-living primate genera in Amazonia, and assess the relationships between parasitic indicators and climatic (rainfall and river level), ecological (fruiting periods of plants) and biological (sex, species' body mass, group size and density) factors. The overall prevalence was 64.4% (95% CI: 64.0 - 64.9); parasitic mean abundance (N filariae per individual) and parasitic mean intensity (N filariae per infected host) of infection were 11.9 (95% CI: 8.3 - 15.6) and 18.4 (95% CI: 13.4 - 23.4) filariae/individual, respectively. Although we observed differences in parasitic parameters among primate genera, there was no correlation between parasitic parameters with density, body mass or group size. Sapajus, Cebus and Lagothrix had the highest prevalence and parasitic mean intensity. Using Lagothrix lagotricha poeppigii, the most sampled species (n = 92), as a model, we found that the number of filariae per infected host was associated with fruit production in swamp forests during the dry season, the time of food scarcity. The long periods of food shortage may cause environmental stress on primates, impairing their immune defenses and leading to increased parasite load but not affecting infection prevalence. However, the lack of information on vector ecology, key to understand risk factors associated to infection rate, prevents confirming the existence of an infection pattern dependent on food availability.

Wild meat trade over the last 45 years in the Peruvian Amazon.

The trade in wild meat is an important economic component of rural people's livelihoods, but it has been perceived to be among the main causes of the decline of wildlife species. Recently, the COVID-19 pandemic has brought to light an additional concern of wildlife markets as a major human-health challenge. We analyzed data from the largest longitudinal monitoring (1973-2018) of the most important urban wild-meat markets in Iquitos, Peru, to examine the trends in and impacts of these markets on people's livelihoods. Over the last 45 years, wild meat sales increased at a rate of 6.4 t/year (SD 2.17), paralleling urban population growth. Wild meat sales were highest in 2018 (442 t), contributing US$2.6 million (0.76%) to the regional gross domestic product. Five species of ungulates and rodents accounted for 88.5% of the amount of biomass traded. Vulnerable and Endangered species represented 7.0% and 0.4% of individuals sold, respectively. Despite growth in sales, the contribution of wild meat to overall urban diet was constant: 1-2%/year of total meat consumed. This result was due to greater availability and higher consumption of cheaper meats (e.g., in 2018, poultry was 45.8% cheaper and was the most consumed meat) coupled with the lack of economic incentives to harvest wild meat species in rural areas. Most wild meat was sold salted or smoked, reducing the likelihood of foodborne diseases. Community-based wildlife management plans and the continued trade bans on primates and threatened taxa may avoid biodiversity loss. Considering the recent COVID-19 pandemic, future management plans should include potential viral hosts and regulation and enforcement of hygiene practices in wild-meat markets.

Comercio de Carne de Monte en los Últimos 45 Años en la Amazonia Peruana Resumen El comercio de carne de monte es un componente económico importante del sustento de habitantes de zonas rurales, pero se ha percibido como una de las principales causas de la declinación de especies de vida silvestre. Recientemente, la pandemia de COVID-19 ha traído a la luz una preocupación adicional de los mercados de vida silvestre como un reto importante para la salud humana. Analizamos datos del monitoreo longitudinal más extenso (1973-2018) de los mercados urbanos de carne de monte más importantes en Iquitos, Perú, para examinar las tendencias y los impactos de estos mercados sobre el sustento de los habitantes. Las ventas de carne de monte incrementaron en los últimos 45 años a una tasa de 6.4 t/año (DS 2.17), en paralelo con el crecimiento de la población. Las ventas de carne de monte fueron más altas en 2018 (442 t), aportando U.S. $2.6 millones (0.76%) al producto interno bruto de la región. Cinco especies de ungulados y roedores comprendieron el 88.5% de la biomasa comercializada. Especies vulnerables y en peligro representaron 7.0% y 0.4% de los individuos vendidos, respectivamente. A pesar del incremento de las ventas, la contribución de la carne de monte al total de la dieta urbana fue constante: 1-2%/año del total de carne consumida. Este resultado se debió a una mayor disponibilidad y consumo de carnes más baratas (e. g., en 2018 la carne de pollo fue 45.8% más barata y fue la más consumida) aparejado con la falta de incentivos económicos para cosechar carne de especies silvestres en áreas rurales. La mayor parte de la carne de monte se vendía salada o ahumada, reduciendo con ello la probabilidad de enfermedades transmitidas por alimentos. Los planes de manejo de vida silvestre basados en comunidades y la prohibición continua del comercio de primates y taxa amenazados pueden evitar la pérdida de biodiversidad. Considerando la reciente pandemia de COVID-19, los planes de manejo futuros deben incluir potenciales huéspedes virales y la regulación y aplicación de prácticas de higiene en los mercados de carne de especies silvestres.

Community-based environmental protection in the Brazilian Amazon: Recent history, legal landmarks and expansion across protected areas.

Globally, community-based initiatives are effective in protecting ecosystems and the species within them. In this paper, we analyze the emergence and large-scale expansion of a community-based environmental protection system (the Voluntary Environmental Agents Program - VEA Program) in the Brazilian Amazon and identify factors that have determined its success since its inception, 25 years ago. Collective actions to protect the environment in the region have been undertaken by local people for at least 40 years, before their legal regulation in 2001 by the federal government of Brazil, and by the Amazonas state in 2007. The system is based on territorial surveillance and monitoring, and on guidelines for the better use of the territory and its natural resources. Between 1995 and 2020, the VEA Program expanded into the two protected areas where it was first implemented reaching approximately 9 thousand km2 of area protected by the system. The number of people participating also grew in this period by around 2050%, as did the participation of women, which grew by 5600%. The system was replicated in 37 protected areas in central Amazonia, and currently covers almost 200 thousand km2 of Amazon rainforest. From our analyses we unveil four main factors that may have allowed the VEA Program to expand and flourish: (a) the communities' previous demand for an effective control system, (b) its legal formalization and regulation, (c) the support from external institutions, and (d) the consolidation of community-based management programs to fund actions. These factors shall be further investigated as to confirm their critical role in the success of the VEA Program. We demonstrate that this community-based environmental protection system has established itself as a legitimate form of social control, and as a mechanism of socio-environmental governance in the areas in which it operates. By allowing more effective protection of territories, it generates consensus amongst users for the adequate management of natural resources, especially in contexts where government's actions are absent or inefficient. We claim that this system can be replicated in various parts of the world.

Urban wild meat consumption and trade in central Amazonia.

The switch from hunting wild meat for home consumption to supplying more lucrative city markets in Amazonia can adversely affect some game species. Despite this, information on the amounts of wild meat eaten in Amazonian cities is still limited. We estimated wild meat consumption rates in 5 cities in the State of Amazonas in Brazil through 1046 door-to-door household interviews conducted from 2004 to 2012. With these data, we modeled the relationship between wild meat use and a selection of socioeconomic indices. We then scaled up our model to determine the amounts of wild meat likely to be consumed annually in the 62 urban centers in central Amazonia. A total of 80.3% of all interviewees reported consuming wild meat during an average of 29.3 (CI 11.6) days per year. Most wild meat was reported as bought in local markets (80.1%) or hunted by a family member (14.9%). Twenty-one taxa were cited as consumed, mostly mammals (71.6%), followed by reptiles (23.2%) and then birds (5.2%). The declared frequency of wild meat consumption was positively correlated with the proportion of rural population as well as with the per capita gross domestic product of the municipality (administrative divisions) where the cities were seated. We estimated that as much as 10,691 t of wild meat might be consumed annually in the 62 urban centers within central Amazonia, the equivalent of 6.49 kg per person per year. In monetary terms, this amounts to US$21.72 per person per year or US$35.1 million overall, the latter figure is comparable to fish and timber production in the region. Given this magnitude of wild meat trade in central Amazonia, it is fundamental to integrate this activity into the formal economy and actively develop policies that allow the trade of more resilient taxa and restrict trade in species sensitive to hunting.

Mercado y Consumo Urbano de Carne Silvestre en la Amazonia Central Resumen El cambio de la caza de animales silvestres para consumo del hogar a caza para surtir mercados urbanos más lucrativos en la Amazonia puede afectar negativamente a algunas especies de caza. A pesar de esto, la información sobre la cantidad de carne silvestre que se consume en las ciudades de la Amazonia todavía es limitada. Estimamos las tasas de consumo de carne silvestre en cinco ciudades del Estado de Amazonas, Brasil, por medio de 1046 entrevistas presenciales a hogares realizadas entre 2004 y 2012. Con estos datos modelamos la relación entre el uso de la carne silvestre y una selección de índices socioeconómicos. Después aumentamos nuestro modelo para determinar la cantidad de carne silvestre que tal vez se consume anualmente en los 62 centros urbanos de la Amazonia central. Un total de 80.3% de todos los entrevistados reportaron el consumo de carne silvestre durante un promedio de 29.3 (CI 11.6) días por año. La mayoría de la carne silvestre fue reportada como comprada en mercados locales (80.1%) o cazada por algún integrante de la familia (14.9%). Se citaron 21 taxones como parte del consumo, principalmente mamíferos (71.6%), seguidos por reptiles (23.2%) y aves (5.2%). La frecuencia declarada de consumo de carne silvestre estuvo correlacionada positivamente con la proporción de población rural, así como con el producto doméstico bruto per cápita de la municipalidad (divisiones administrativas) en donde se encuentran las ciudades. Estimamos que un máximo de 10,691 toneladas de carne silvestre podrían ser consumidas anualmente en los 62 centros urbanos de la Amazonia central, el equivalente a 6.49 kg/persona/año. En términos monetarios, esto equivale a US$21.72/persona/año o US$35.1 millones en general. Esta última cifra es comparable con la producción de madera y de peces en la región. Dada esta magnitud del mercado de carne silvestre en la Amazonia central, es fundamental la integración de esta actividad en la economía formal y el desarrollo activo de políticas que permitan el mercado de taxones más resilientes y que restrinjan el mercado para las especies sensibles a la caza.

Long-term population monitoring of the threatened and endemic black-headed squirrel monkey (Saimiri vanzolinii) shows the importance of protected areas for primate conservation in Amazonia.

Population monitoring of endangered species is essential to the improvement of their management and conservation plans. The black-headed squirrel monkey (Saimiri vanzolinii) is a vulnerable species on the IUCN Red List and has extreme geographical endemism, exhibiting the smallest known distribution among Neotropical primates (ca. 870 km2 ), over 90% of which occurs in white-water flooded forests within the Mamirauá Sustainable Development Reserve (MSDR), Brazilian Amazonia. To assess the effectiveness of this protected area in conserving the species, we conducted population monitoring of black-headed squirrel monkeys across five consecutive years (2009-2013) on nine trails 2 km each. Each year samples included both low and high river water periods. We used the distance sampling method, recording the distance to each observed social group as well as counting component individuals. We also calculated annual encounter rates based on the number of individuals sighted every 10 km traveled. Densities ranged from 256 individuals/km2 (2011) to 453 individuals/km2 (2013), and no seasonal differences were detected. Population size was estimated to be 147,848 mature individuals. Encounter rates ranged from 100 individuals/10 km (2010) to 179 individuals/10 km (2013); no significant difference among years was found. We found that S. vanzolinii populations remained stable throughout the years, which indicates that the MSDR has been playing an essential role on protecting this species. Due to difficulties of fulfilling assumptions of the distance sampling method, we consider the encounter rate analysis to be more effective for monitoring this and other Saimiri species. Given the critical endemism and worrying conservation status of S. vanzolinii, we suggest that monitoring of the species population should be carried out regularly.

Menstrual cycle in four New World primates: Poeppig's woolly monkey (Lagothrix poeppigii), red uakari (Cacajao calvus), large-headed capuchin (Sapajus macrocephalus) and nocturnal monkey (Aotus nancymaae).

Genital organs from 33 nocturnal monkeys Aotus namcymaae, 29 Poeppig's woolly monkeys (Lagothrix poeppigii), 21 red uakaris (Cacajao calvus) and 11 large-headed capuchins (Sapajus macrocephalus) were histologically analyzed in order to describe the endometrial changes related to the ovarian cycle. A. nancymaae and S. macrocephalus showed histological evidence of menstrual cycle with the detachment of the most superficial endometrium and the subepithelial reabsorption of the endometrial functional layer, explaining the extensive presence of both hemosiderin and fibrin clusters in the early follicular stages. In L. poeppigii, despite the presence of fibrin clusters promoting the remodeling of the endometrium, we did not observe the detachment of the functional layer of the endometrium, suggesting that this species presents a non-menstruating cycle. Finally, C. calvus showed no histological sign of menstrual phase. This reproductive information is useful to improve assisted reproductive techniques in non-human primates, and give us opportunity for comparative studies on the evolution of animal reproductive biology, including humans.