Forbidden fruits? Ecosystem services from seed dispersal by fruit bats in the context of latent zoonotic risk

Old world fruit bats are important seed dispersers of forest plants as
well as of commercial fruit crops. Bats scatter seeds across landscapes
and also aggregate (clump) seeds under feeding and roosting trees. In
agroforestry landscapes, bat frugivory and seed dispersal can result in
simultaneous accrual of socio-economic benefits and costs to humans, which
may be further affected by human health risks from zoonotic spillover
through human-bat interactions. In our study, we used an integrated
approach to assess socio-economic benefits (from seed dispersal) and costs
(from frugivory) from bats, in relation to latent zoonotic risk. We
carried out the study in five agroforestry landscapes along India’s
Western Ghats, for selected commercial fruit crops (cashew, areca, banana,
and other pulpy/fleshy fruits). Specifically, we hypothesized that
people’s perceptions of benefits from fruit bats would be correlated with
measured extents of clumped seed dispersal in fruit plantations. We
conducted ecological studies to investigate the effects of fruit crop type
and plantation attributes on clump-dispersal, and in turn, on perceived
“net benefits” assessed from interviews with plantation-associated people.
We then explored associations between perceived socio-economic net
benefits and spatial data on disease risk factors for fruit-bat-linked
henipavirus transmission. We found that the extent of bat-mediated
clump-dispersal was highest for cashew, especially in isolated
plantations. People’s perceptions of benefits from fruit bats matched the
measured extents of clump-dispersal of cashew and areca. These benefits
came with some costs from scatter-dispersal and damage to other fleshy
fruits from frugivory by bats. Interestingly, we did not detect tradeoffs
between perceived net benefits from bats and disease risk, which is of
significance for bat conservation and its implications for human
well-being. Overall, our results highlight that bat-mediated seed
dispersal needs to be sustained as an important ecosystem service, despite
some latent zoonotic risk, in the Anthropocene.

旧大陆果蝠（Old World fruit bats）是森林植物与经济果树作物的重要种子传播者。蝙蝠可将种子扩散至整片景观区域，同时在取食与栖息的树木下将种子聚集成团。在农林复合景观（agroforestry landscapes）中，蝙蝠的食果行为与种子传播过程会同时为人类带来社会经济收益与成本，而人类与蝙蝠互动引发的人畜共患病溢出（zoonotic spillover）风险，可能进一步影响这一收益与成本的平衡。本研究采用整合研究方法，针对潜在人畜共患病风险，评估蝙蝠介导的种子传播所带来的社会经济收益，以及蝙蝠食果行为造成的经济成本。研究在印度西高止山脉（Western Ghats）沿线的5处农林复合景观中开展，选取腰果、槟榔、香蕉及其他肉质果作为目标经济果树作物。我们提出具体研究假说：人们对果蝠带来收益的感知，与果树种植园中实测的集群种子传播程度呈显著相关。本研究通过生态学调查，探究果树作物类型与种植园属性对集群种子传播的影响，并通过对种植园相关从业者的访谈，评估其感知的"净收益"。随后，我们分析了感知到的社会经济净收益，与果蝠相关亨尼帕病毒（henipavirus）传播的疾病风险因子空间数据之间的关联。研究结果显示，蝙蝠介导的集群种子传播程度在腰果种植园中最高，尤其是在孤立式种植园中。人们对果蝠收益的感知，与腰果和槟榔的实测集群种子传播程度相匹配。这类收益同时伴随一定成本，包括扩散式种子传播以及蝙蝠食果对其他肉质果造成的损害。值得注意的是，我们未发现人们感知的蝙蝠净收益与疾病风险之间存在权衡关系，这一发现对蝙蝠保护及其对人类福祉的影响具有重要参考价值。总体而言，本研究结果表明，尽管存在潜在的人畜共患病风险，但在人类世（Anthropocene）背景下，蝙蝠介导的种子传播作为一项关键的生态系统服务，仍需得到持续维持与保护。