Hantavirus host assemblages and human disease in the Atlantic Forest

Several viruses from the genus Orthohantavirus are known to cause lethal disease in humans. Sigmodontinae rodents are the main hosts responsible for hantavirus transmission in the tropical forests, savannas, and wetlands of South America. These rodents can shed different hantaviruses, such as the lethal and emerging Araraquara orthohantavirus. Factors that drive variation in host populations may influence hantavirus transmission dynamics within and between populations. Landscape structure, and particularly areas with a predominance of agricultural land and forest remnants, is expected to influence the proportion of hantavirus rodent hosts in the Atlantic Forest rodent community. Here, we tested this using 283 Atlantic Forest rodent capture records and geographically weighted models that allow us to test if predictors vary spatially. We also assessed the correspondence between proportions of hantavirus hosts in rodent communities and a human vulnerability to hantavirus infection index across the entire Atlantic Forest biome. We found that hantavirus host proportions were more positively influenced by landscape diversity than by a particular habitat or agricultural matrix type. Local small mammal diversity also positively influenced known pathogenic hantavirus host proportions, indicating that a plasticity to habitat quality may be more important for these hosts than competition with native forest dwelling species. We found a consistent positive effect of sugarcane and tree plantation on the proportion of rodent hosts, whereas defaunation intensity did not correlate with the proportion of hosts of potentially pathogenic hantavirus genotypes in the community, indicating that non-defaunated areas can also be hotspots for hantavirus disease outbreaks. The spatial match between host hotspots and human disease vulnerability was 17%, while coldspots matched 20%. Overall, we discovered strong spatial and land use change influences on hantavirus hosts at the landscape level across the Atlantic Forest. Our findings suggest disease surveillance must be reinforced in the southern and southeastern regions of the biome where the highest predicted hantavirus host proportion and levels of vulnerability spatially match. Importantly, our analyses suggest there may be more complex rodent community dynamics and interactions with human disease than currently hypothesized.

数种属于正汉塔病毒属的病毒已知可致人类死亡。 Sigmodontinae啮齿类动物是南美洲热带森林、草原和湿地中汉塔病毒传播的主要宿主。这些啮齿类动物可排放多种汉塔病毒，如致命且新兴的阿拉拉夸拉正汉塔病毒。驱动宿主种群变异的因素可能影响汉塔病毒在种群内部及种群间的传播动力学。景观结构，尤其是农业用地和森林残存地占主导地位的区域，预计将影响大西洋森林啮齿类社区中汉塔病毒宿主的比率。在此，我们利用283份大西洋森林啮齿类捕获记录和地理加权模型来检验预测因子是否随空间变化。我们还评估了啮齿类社区中汉塔病毒宿主比率与整个大西洋森林生物群落人类汉塔病毒感染易感指数之间的对应关系。我们发现，汉塔病毒宿主比率受景观多样性影响较特定栖息地或农业基质类型更为显著。地方小型哺乳动物多样性也正面向地影响了已知致病汉塔病毒宿主的比率，表明对这些宿主而言，栖息地质量的适应性可能比与本土森林栖息物种的竞争更为重要。我们发现甘蔗和树木种植园对啮齿类宿主比率具有一致的正面影响，而物种灭绝的强度与社区中潜在致病汉塔病毒基因型宿主的比率无关，这表明未灭绝地区也可能成为汉塔病毒疾病爆发的热点。宿主热点与人类疾病易感区的空间匹配率为17%，而冷点匹配率为20%。总体而言，我们发现在大西洋森林景观层面，汉塔病毒宿主受到强烈的空间和土地利用变化的影响。我们的研究结果表明，在生物群落中预测的汉塔病毒宿主比例和易感水平最高的南部和东南部地区，疾病监测必须得到加强。重要的是，我们的分析表明，啮齿类社区动态与人类疾病之间的相互作用可能比目前假设的更为复杂。