Massey Aimee L, Ferreira da Silva David José, Vieira Carla Julia da Silva Pessoa, Allen Jennifer M, Canale Gustavo Rodrigues, Bernardo Christine Steiner São, de Morais Bronzoni Roberta Vieira, Peres Carlos A, Levi Taal
Department of Fisheries, Wildlife, and Conservation Sciences, Oregon State University, Corvallis, Oregon, United States of America.
Instituto de Ciências da Saúde, Universidade Federal de Mato Grosso, Sinop, Mato Grosso, Brazil.
PLoS Negl Trop Dis. 2025 Mar 27;19(3):e0012925. doi: 10.1371/journal.pntd.0012925. eCollection 2025 Mar.
There is debate concerning whether there exists a generalizable effect of land-use change on zoonotic disease risk. Strong data informing this debate are sparse because it is challenging to establish direct links between hosts, vectors, and pathogens. However, molecular methods using invertebrate-derived DNA (iDNA) can now measure species composition and interactions from vector samples at landscape scales, which has the potential to improve mechanistic understanding of the effects of land-use change on zoonotic disease risk.
METHODOLOGY/PRINCIPAL FINDINGS: We used iDNA metabarcoding of sandflies to disentangle the relationships between Leishmania parasites, sandfly vectors, and vertebrate hosts. We paired these samples with iDNA metabarcoding of carrion flies to survey vertebrates independent of sandfly feeding preferences. We collected sandflies and carrion flies at forest sites across a deforestation gradient in the southern Amazon 'Arc of Deforestation', which exemplifies global patterns of deforestation due to agricultural expansion. We used a series of models to test whether sandflies and the vertebrate they feed upon were influenced by deforestation, which we measured using percent forest cover, percent pasture cover, and distance to the major urban center. We found that vectors were encountered less frequently in forests surrounded by pasture. We also found that the probability of a Leishmania host/reservoir being detected in sandfly bloodmeals was quadratically related to local forest cover, with the highest probability found at sites with intermediate levels of deforestation. Hosts were also detected most often with carrion flies at sites with intermediate forest cover, suggesting that increased host availability rather than feeding preferences was responsible for this result. Domestic dogs and the nine-banded armadillo, Dasypus novemcinctus, were the most prevalent hosts found in the sandfly iDNA data.
CONCLUSIONS/SIGNIFICANCE: Our results did not support the generality of the 'dilution effect' hypothesis. However, important vectors and hosts showed consistent responses to deforestation and our findings suggest that interactions between domestic dogs and sylvatic hosts are a pathway for zoonotic disease transmission in human impacted tropical forests.
关于土地利用变化对人畜共患病风险是否存在可推广的影响存在争议。由于难以在宿主、媒介和病原体之间建立直接联系，为这场辩论提供有力依据的数据较为稀少。然而，利用无脊椎动物衍生DNA（iDNA）的分子方法现在可以在景观尺度上测量媒介样本中的物种组成和相互作用，这有可能改善对土地利用变化对人畜共患病风险影响的机制理解。
方法/主要发现：我们使用白蛉的iDNA元条形码技术来理清利什曼原虫寄生虫、白蛉媒介和脊椎动物宿主之间的关系。我们将这些样本与腐食性苍蝇的iDNA元条形码技术相结合，以调查独立于白蛉取食偏好的脊椎动物。我们在亚马逊南部“森林砍伐弧”的森林砍伐梯度上的森林地点收集白蛉和腐食性苍蝇，该地区体现了因农业扩张导致的全球森林砍伐模式。我们使用一系列模型来测试白蛉及其取食的脊椎动物是否受到森林砍伐的影响，我们用森林覆盖率、牧场覆盖率百分比以及到主要城市中心的距离来衡量森林砍伐情况。我们发现，在被牧场环绕的森林中，媒介的出现频率较低。我们还发现，在白蛉血餐中检测到利什曼原虫宿主/储存宿主的概率与当地森林覆盖率呈二次相关，在森林砍伐程度中等的地点概率最高。在森林覆盖率中等的地点，腐食性苍蝇也最常检测到宿主，这表明宿主可利用性增加而非取食偏好是导致这一结果的原因。家犬和九带犰狳（Dasypus novemcinctus）是在白蛉iDNA数据中发现的最常见宿主。
结论/意义：我们的结果不支持“稀释效应”假说的普遍性。然而，重要的媒介和宿主对森林砍伐表现出一致的反应，我们的研究结果表明，家犬与野生宿主之间的相互作用是人类影响的热带森林中人畜共患病传播的一条途径。
