Vertical foraging shifts in Hawaiian forest birds in response to invasive rat removal

Worldwide, native species increasingly contend with the interacting stressors of habitat fragmentation and invasive species, yet their combined effects have rarely been examined. Direct negative effects of invasive omnivores are well documented, but the indirect effects of resource competition or those caused by predator avoidance are unknown. Here we isolated and examined the independent and interactive effects of invasive omnivorous Black rats (Rattus rattus) and forest fragment size on the interactions between avian predators and their arthropod prey. Our study examines whether invasive omnivores and ecosystem fragment size impact: 1) the vertical distribution of arthropod species composition and abundance, and 2) the vertical profile of foraging behaviors of five native and two non-native bird species found in our study system. We predicted that the reduced edge effects and greater structural complexity and canopy height of larger fragments would limit the total and proportional habitat space frequented by rats and thus limit their impact on both arthropod biomass and birds’ foraging behavior. We experimentally removed invasive omnivorous Black rats across a 100-fold (0.1 to 12 ha) size gradient of forest fragments on Hawai‘i Island, and paired foraging observations of forest passerines with arthropod sampling in the 16 rat-removed and 18 control fragments. Rat removal was associated with shifts in the vertical distribution of arthropod biomass, irrespective of fragment size. Bird foraging behavior mirrored this shift, and the impact of rat removal was greater for birds that primarily eat fruit and insects compared with those that consume nectar. Evidence from this model study system indicates that invasive rats indirectly alter the feeding behavior of native birds, and consequently impact multiple trophic levels. This study suggests that native species can modify their foraging behavior in response to invasive species removal and presumably arrival through behavioral plasticity.

全球范围内，本土物种正日益面临栖息地破碎化与外来物种入侵两类交互胁迫因子的叠加威胁，然而二者的联合效应却极少得到系统研究。入侵性杂食动物的直接负面影响已有大量文献佐证，但由资源竞争引发的间接效应，或是因捕食者规避产生的间接效应，目前仍不明晰。
本研究分离并检验了入侵杂食性黑家鼠（Rattus rattus）与森林片段面积，对鸟类捕食者及其节肢动物猎物之间相互作用的独立效应与交互效应。
本研究旨在探讨两大科学问题：1）入侵杂食动物与生态系统片段面积是否会影响节肢动物群落组成与丰度的垂直分布；2）本研究样地系统内的5种本土鸟类与2种非本土鸟类，其觅食行为的垂直特征是否受上述因子调控。
我们提出如下假说：面积更大的森林片段具有更弱的边缘效应、更高的结构复杂度与林冠高度，这将限制黑家鼠活动的总栖息地空间与占比，进而削弱其对节肢动物生物量以及鸟类觅食行为的影响。
我们在夏威夷岛设置了跨度达100倍（0.1至12公顷）的森林片段面积梯度，开展入侵性杂食黑家鼠的移除实验，并在16个鼠移除样地与18个对照样地中，同步开展森林雀形目鸟类的觅食行为观测与节肢动物采样。
研究结果显示，无论森林片段面积大小，移除黑家鼠均会引发节肢动物生物量的垂直分布发生显著改变。
鸟类的觅食行为也随之出现对应变化，且相较于专性取食花蜜的鸟类，主要以果实与昆虫为食的鸟类对黑家鼠移除的响应更为显著。
本基于模型系统的研究结果表明，入侵黑家鼠可通过间接途径改变本土鸟类的觅食行为，进而对多个营养级产生影响。
本研究提示，本土物种可通过行为可塑性响应外来物种的入侵与移除，调整自身的觅食策略。