Ecological Requirements for Abundance and Dispersion of Brazilian Yellow Fever Vectors in Tropical Areas.

In the Americas, wild yellow fever (WYF) is an infectious disease that is highly lethal for some non-human primate species and non-vaccinated people. Specifically, in the Brazilian Atlantic Forest, Haemagogus leucocelaenus and Haemagogus janthinomys mosquitoes act as the major vectors. Despite transmission risk being related to vector densities, little is known about how landscape structure affects vector abundance and movement. To fill these gaps, we used vector abundance data and a model-selection approach to assess how landscape structure affects vector abundance, aiming to identify connecting elements for virus dispersion in the state of São Paulo, Brazil. Our findings show that Hg. leucocelaenus and Hg. janthinomys abundances, in highly degraded and fragmented landscapes, are mainly affected by increases in forest cover at scales of 2.0 and 2.5 km, respectively. Fragmented landscapes provide ecological corridors for vector dispersion, which, along with high vector abundance, promotes the creation of risk areas for WYF virus spread, especially along the border with Minas Gerais state, the upper edges of the Serra do Mar, in the Serra da Cantareira, and in areas of the metropolitan regions of São Paulo and Campinas.

The role of forest fragmentation in yellow fever virus dispersal.

The intense process of deforestation in tropical forests poses serious challenges for the survival of biodiversity, as well as for the human species itself. This scenario is supported by the increase in the incidence of epidemics of zoonotic origin observed over the last few decades. In the specific case of sylvatic yellow fever (YF), it has already been shown that an increase in the transmission risk of the causative agent (yellow fever virus - YFV) is associated with areas with a high degree of forest fragmentation, which can facilitate the spread of the virus. In this study we tested the hypothesis that areas with more fragmented landscapes and a higher edge density (ED) but a high degree of connectivity between forest patches favor YFV spread. To this end, we used YF epizootics in non-human primates (NHPs) in the state of São Paulo to build direct networks, and used a multi-selection approach to analyze which landscape features could facilitate YFV spread. Our results showed that municipalities with the potential to spread the virus exhibited a higher amount of forest edge. Additionally, the models with greater empirical support showed a strong association between forest edge density and the risk of occurrence of epizootic diseases, as well as the need for a minimum threshold of native vegetation cover to restrict their transmission. These findings corroborate our hypothesis that more fragmented landscapes with a higher degree of connectivity favor the spread of YFV, while landscapes with fewer connections tend to act as dead zones for the circulation of the virus.

The influence of landscape structure on the dispersal pattern of yellow fever virus in the state of São Paulo.

Man-made changes to the landscape play a crucial role in altering the epidemiologic patterns of infectious diseases, mainly as a result of pathogen spillover. Sylvatic yellow fever is ideally suited to modeling of this phenomenon as the risk of transmission of the disease as well as its circulation and dispersal are associated with forest fragmentation. In this study we investigated the temporal dispersal pattern of yellow fever virus (YFV) by means of confirmed cases of epizootics in non-human primates in municipalities in the state of São Paulo where there was no recommendation for vaccination in 2017. We analyzed the resistance to dispersal associated with different classes of land use and the geographic distances between the different locations where epizootics were recorded. The model that best explained the temporal dispersal pattern of YFV in the study area indicated that this was influenced by the geographic distance between collection locations and by the permeability of the forest edges (150 m) at the interface with the following core areas: Water, Agricultural, Non-Forest Formation and Forestry. Water, Agricultural, Urban and Forest core areas and the interfaces between the latter two formed important barriers to circulation of the virus. These findings indicate that fragmentation of vegetation tends to decrease the time taken for pathogens to spread, while conservation of forest areas has the opposite effect.

Biodiversity and public health interface / Biodiversidade e a interface com a saúde pública

Abstract Alongside modernity, the human activity has been a key factor in global environmental risks, with worldwide anthropic modification being the cause of the emergence of diseases for wild and livestock animals, and even humans. In special, the increase in the spatial distribution and in the incidence of some emerging infectious diseases (EID) are directly associated to deforestation and global climate changes. Moreover, the arise of new EID agents, such as the SARS-COV-2 have been reported for the last 30 years. On the other hand, biodiversity has been shown to be a key indicator for ecosystem health, and to pose a role to increase the promotion of human public health. In neotropical regions, and in special, in Brazil, several infectious diseases have been demonstrated to be directly affected for the biodiversity loss, such as malaria, hantavirus pulmonary syndrome, yellow fever, urban arboviruses, spotted fever, amongst other. To better understand the ecosystem capacity of regulation of infectious diseases, FAPESP BIOTA program have supported researchers and research projects to increase knowledge about Brazilian biodiversity and the ecosystems, such as diversity of bird bioagents, venomous animals biodiversity, diversity of mosquitos species in forest patches inside urban areas, propagation of the yellow fever virus over fragmented forest territories, loss of ecological corridors and occurrence of spotted fever and malaria, amongst others. It is noteworthy that FAPESP BIOTA is a successful program and must be expanded as an important tool for present and future public health promotion.

Resumo Junto à modernidade, a atividade humana tem sido um fator chave ligada aos riscos ambientais globais, as modificações antrópicas em âmbito mundial têm sido causa do surgimento de doenças para os animais silvestres e domésticos, bem como para o ser humano. Em especial, o incremento na distribuição espacial e incidência de doenças infecciosas emergentes (DIE) estão diretamente associados ao desmatamento e às mudanças climáticas globais, além disso, o surgimento de novos agentes de DIE, como o SARS-COV-2, tem sido relatado nos últimos 30 anos. Por outro lado, a biodiversidade tem se mostrado um indicador chave para a saúde dos ecossistemas, além de representar um papel importante na promoção da saúde pública humana. Nas regiões neotropicais, e em especial, no Brasil, várias doenças infecciosas têm demonstrado ser diretamente afetadas pela perda de biodiversidade, como a malária, a síndrome pulmonar por hantavírus, a febre amarela, as arboviroses urbanas, a febre maculosa, entre outras. Para entender melhor a capacidade ecossistêmica de regulação de doenças infecciosas, o programa BIOTA FAPESP tem apoiado pesquisadores e projetos de pesquisa para aumentar o conhecimento sobre a biodiversidade e os ecossistemas brasileiros, como a diversidade de bioagentes de aves, a biodiversidade de animais peçonhentos, a diversidade de espécies de mosquitos em fragmentos florestais dentro de áreas urbanas, a propagação do vírus da febre amarela em território florestal fragmentado, perda e isolamento de remanescentes florestais e a ocorrência de febre maculosa e malária, entre outros. Ressalta-se que o BIOTA FAPESP é um programa de sucesso e deve ser ampliado como importante ferramenta de promoção da saúde pública presente e futura.

Anthropogenic landscape decreases mosquito biodiversity and drives malaria vector proliferation in the Amazon rainforest.

Inter-relationships among mosquito vectors, Plasmodium parasites, human ecology, and biotic and abiotic factors, drive malaria risk. Specifically, rural landscapes shaped by human activities have a great potential to increase the abundance of malaria vectors, putting many vulnerable people at risk. Understanding at which point the abundance of vectors increases in the landscape can help to design policies and interventions for effective and sustainable control. Using a dataset of adult female mosquitoes collected at 79 sites in malaria endemic areas in the Brazilian Amazon, this study aimed to (1) verify the association among forest cover percentage (PLAND), forest edge density (ED), and variation in mosquito diversity; and to (2) test the hypothesis of an association between landscape structure (i.e., PLAND and ED) and Nyssorhynchus darlingi (Root) dominance. Mosquito collections were performed employing human landing catch (HLC) (peridomestic habitat) and Shannon trap combined with HLC (forest fringe habitat). Nyssorhynchus darlingi abundance was used as the response variable in a generalized linear mixed model, and the Shannon diversity index (H') of the Culicidae community, PLAND, and the distance house-water drainage were used as predictors. Three ED categories were also used as random effects. A path analysis was used to understand comparative strengths of direct and indirect relationships among Amazon vegetation classes, Culicidae community, and Ny. darlingi abundance. Our results demonstrate that Ny. darlingi is negatively affected by H´ and PLAND of peridomestic habitat, and that increasing these variables (one-unit value at ß0 = 768) leads to a decrease of 226 (P < 0.001) and 533 (P = 0.003) individuals, respectively. At the forest fringe, a similar result was found for H' (ß1 = -218; P < 0.001) and PLAND (ß1 = -337; P = 0.04). Anthropogenic changes in the Amazon vegetation classes decreased mosquito biodiversity, leading to increased Ny. darlingi abundance. Changes in landscape structure, specifically decreases in PLAND and increases in ED, led to Ny. darlingi becoming the dominant species, increasing malaria risk. Ecological mechanisms involving changes in landscape and mosquito species composition can help to understand changes in the epidemiology of malaria.

Moving to healthier landscapes: Forest restoration decreases the abundance of Hantavirus reservoir rodents in tropical forests.

Hantavirus Cardiopulmonary Syndrome (HCPS) is a disease with high human lethality rates, whose transmission risk is directly related to the abundance of reservoir rodents. In the Brazilian Atlantic forest, the main reservoirs species, Oligoryzomys nigripes and Necromys lasiurus, are thought to increase in abundance with deforestation. Therefore, forest restoration may contribute to decrease HCPS transmission risk, a topic still unexplored, especially in tropical regions. Aiming at filling this research gap, we quantified the potential of forest restoration, as required by the current environmental legislation, to reduce the abundance of Hantavirus reservoir rodents in the Brazilian Atlantic Forest. Using a dataset on small mammal communities sampled at 104 sites, we modeled how the abundance of these two rodent species change with the percentage of forest cover and forest edge density. From the best model, we extrapolated rodent abundance to the entire Atlantic Forest, considering two scenarios: current and restored forest cover. Comparing the estimated abundance between these two scenarios, we show that forest restoration can reduce the abundance of O. nigripes up to 89.29% in 43.43% of Atlantic forest territory. For N. lasiurus, abundance decreased up to 46% in 44% of the Atlantic forest. To our knowledge, this is the first study linking forest restoration and zoonotic diseases. Our results indicate that forest restoration would decrease the chance of HCPS transmission in ~45% of the Atlantic forest, making the landscape healthier to ~2,8 million people living within this area. This positive effect of restoration on disease regulation should be considered as an additional argument to encourage and promote forest restoration in tropical areas around the world.

Use of highway culverts by the water opossum (Chironectes minimus) in southeastern Brazil / Uso de drenagens fluviais sob rodovias pela cuíca dagua (Chironectes minimus) no sudeste do Brasil

Abstract The water opossum (Chironectes minimus) is a semi-aquatic mammal that is infrequently sampled in Atlantic rainforest areas in Brazil. Here we report on new records of C. minimus in the state of São Paulo, southeastern Brazil, and comment on its behavior and ecology. We placed nine camera traps in culverts and cattle boxes under a highway, between 2017 and 2019. From a total of 6,750 camera-trap-days, we obtained 16 records of C. minimus (0.24 records/100 camera-trap-days) in two cameras placed in culverts over streams. Most of the records were made between May and August, in the dry season and in the first six hours after sunset. The new records are from a highly degraded area with some riparian forests. The records lie approximately 30 km away from the nearest protected area where the species is known to occur. We suggest that C. minimus has some tolerance to degraded habitats, as long as the water bodies and riparian forests are minimally preserved. The new records presented here also fill a distribution gap in western São Paulo state.

Resumo A cuíca d'agua (Chironectes minimus) é um mamífero semiaquático pouco amostrado em áreas de Mata Atlântica do Brasil. Neste estudo apresentamos novos registros de C. minimus no estado de São Paulo, sudeste do Brasil, e comentamos sobre seu comportamento e ecologia. Nós instalamos nove armadilhas fotográficas em drenagens fluviais e passagens de gado sob uma rodovia, entre 2017 e 2019. De um total de 6.750 armadilhas-fotográficas-dia, obtivemos 16 registros de C. minimus (0,24 registros/100 armadilhas-fotográficas-dia) em duas armadilhas fotográficas instaladas em drenagens fluviais. A maioria dos registros foram feitos entre maio e agosto, na estação seca, e nas seis primeiras horas da noite. Os novos registros são de uma área altamente degradada que possui algumas matas ciliares. Os registros estão a aproximadamente 30 km da área protegida mais próxima onde a espécie já foi registrada. Nós sugerimos que C. minimus possui certa tolerância a hábitats degradados, contanto que os corpos d'agua e as matas ciliares estejam minimamente preservados. Os novos registros aqui apresentados também preenchem uma lacuna amostral no oeste de São Paulo.

Climate change and sugarcane expansion increase Hantavirus infection risk.

Hantavirus Cardiopulmonary Syndrome (HCPS) is a disease caused by Hantavirus, which is highly virulent for humans. High temperatures and conversion of native vegetation to agriculture, particularly sugarcane cultivation can alter abundance of rodent generalist species that serve as the principal reservoir host for HCPS, but our understanding of the compound effects of land use and climate on HCPS incidence remains limited, particularly in tropical regions. Here we rely on a Bayesian model to fill this research gap and to predict the effects of sugarcane expansion and expected changes in temperature on Hantavirus infection risk in the state of São Paulo, Brazil. The sugarcane expansion scenario was based on historical data between 2000 and 2010 combined with an agro-environment zoning guideline for the sugar and ethanol industry. Future evolution of temperature anomalies was derived using 32 general circulation models from scenarios RCP4.5 and RCP8.5 (Representative greenhouse gases Concentration Pathways adopted by IPCC). Currently, the state of São Paulo has an average Hantavirus risk of 1.3%, with 6% of the 645 municipalities of the state being classified as high risk (HCPS risk ≥ 5%). Our results indicate that sugarcane expansion alone will increase average HCPS risk to 1.5%, placing 20% more people at HCPS risk. Temperature anomalies alone increase HCPS risk even more (1.6% for RCP4.5 and 1.7%, for RCP8.5), and place 31% and 34% more people at risk. Combined sugarcane and temperature increases led to the same predictions as scenarios that only included temperature. Our results demonstrate that climate change effects are likely to be more severe than those from sugarcane expansion. Forecasting disease is critical for the timely and efficient planning of operational control programs that can address the expected effects of sugarcane expansion and climate change on HCPS infection risk. The predicted spatial location of HCPS infection risks obtained here can be used to prioritize management actions and develop educational campaigns.

Landscape, Climate and Hantavirus Cardiopulmonary Syndrome Outbreaks.

We performed a literature review in order to improve our understanding of how landscape and climate drivers affect HCPS outbreaks. Anthropogenic landscape changes such as forest loss, fragmentation and agricultural land uses are related with a boost in hantavirus reservoir species abundance and hantavirus prevalence in tropical areas, increasing HCPS risk. Additionally, higher precipitation, especially in arid regions, favors an increase in vegetational biomass, which augments the resources for reservoir rodents, also increasing HCPS risk. Although these relationships were observed, few studies described it so far, and the ones that did it are concentrated in few places. To guide future research on this issue, we build a conceptual model relating landscape and climate variables with HCPS outbreaks and identified research opportunities. We point out the need for studies addressing the effects of landscape configuration, temperature and the interaction between climate and landscape variables. Critical landscape thresholds are also highly relevant, once HCPS risk transmission can increase rapidly above a certain degree of landscape degradation. These studies could be relevant to implement preventive measures, creating landscapes that can mitigate disease spread risk.

Landscape, Environmental and Social Predictors of Hantavirus Risk in São Paulo, Brazil.

Hantavirus Pulmonary Syndrome (HPS) is a disease caused by Hantavirus, which are negative-sense RNA viruses in the family Bunyaviridae that are highly virulent to humans. Numerous factors modify risk of Hantavirus transmission and consequent HPS risk. Human-driven landscape change can foster transmission risk by increasing numbers of habitat generalist rodent species that serve as the principal reservoir host. Climate can also affect rodent population dynamics and Hantavirus survival, and a number of social factors can influence probability of HPS transmission to humans. Evaluating contributions of these factors to HPS risk may enable predictions of future outbreaks, and is critical to development of effective public health strategies. Here we rely on a Bayesian model to quantify associations between annual HPS incidence across the state of São Paulo, Brazil (1993-2012) and climate variables (annual precipitation, annual mean temperature), landscape structure metrics (proportion of native habitat cover, number of forest fragments, proportion of area planted with sugarcane), and social factors (number of men older than 14 years and Human Development Index). We built separate models for the main two biomes of the state (cerrado and Atlantic forest). In both biomes Hantavirus risk increased with proportion of land cultivated for sugarcane and HDI, but proportion of forest cover, annual mean temperature, and population at risk also showed positive relationships in the Atlantic forest. Our analysis provides the first evidence that social, landscape, and climate factors are associated with HPS incidence in the Neotropics. Our risk map can be used to support the adoption of preventive measures and optimize the allocation of resources to avoid disease propagation, especially in municipalities that show medium to high HPS risk (> 5% of risk), and aimed at sugarcane workers, minimizing the risk of future HPS outbreaks.