The application of community ecology theory to co-infections in wildlife hosts

Priority effect theory, a foundational concept from community ecology, states that the order and timing of species arrival during species assembly can affect species composition. Although this theory has been applied to co-infecting parasite species, it has almost always been with a single time lag between co-infecting parasites. Thus, how the timing of parasite species arrival affects co-infections and disease remains poorly understood. To address this gap in the literature, we exposed post-metamorphic Cuban tree frogs (Osteopilus septentrionalis) to Ranavirus, the fungus Batrachochytrium dendrobatidis (Bd), a nematode Aplectana hamatospicula, or pairs of these parasites either simultaneously or sequentially at a range of time lags and quantified load of the secondary parasite and host growth, survival and parasite tolerance. Prior exposure to Bd or A. hamatospicula significantly increased viral loads relative to hosts singly infected with Ranavirus, whereas A. hamatospicula loads in hosts were higher when co-exposed to Bd than when co-exposed to Ranavirus. There was a significant positive relationship between time since Ranavirus infection and Bd load, and prior exposure to A. hamatospicula decreased Bd loads compared to simultaneous co-infection with these parasites. Infections with Bd and Ranavirus either singly or in co-infections decreased host growth and survival. This research reveals that time lags between co-infections can affect parasite loads, in line with priority effects theory. As co-infections in the field are unlikely to be simultaneous, an understanding of when co-infections are impacted by time lags between parasite exposures may play a major role in controlling problematic co-infections.

优先效应理论（Priority effect theory）是群落生态学（community ecology）的核心概念，其指出物种组装过程中物种抵达的时序与时机可影响群落的物种组成。尽管该理论已被应用于共感染寄生虫类群的研究，但既往相关研究几乎均仅设置了共感染寄生虫间的单一时间滞后（time lag）。因此，寄生虫物种的感染时机如何影响共感染态势与疾病进程，目前仍不甚明晰。

为填补这一研究空白，本研究将变态后的古巴树蛙（Osteopilus septentrionalis）分别暴露于蛙虹彩病毒（Ranavirus）、蛙壶菌（Batrachochytrium dendrobatidis，简称Bd）、线虫Aplectana hamatospicula，以及上述三类寄生虫的两两组合；暴露模式设置为同时感染，或在一系列时间滞后梯度下的先后感染。本研究随后量化了次级寄生虫的载量，以及宿主的生长、存活与寄生虫耐受能力。

实验结果表明：相较于仅感染蛙虹彩病毒的宿主，预先暴露于Bd或A. hamatospicula可显著提升病毒载量；当宿主与Bd共感染时，A. hamatospicula的载量显著高于其与蛙虹彩病毒共感染的组别。宿主感染蛙虹彩病毒后的时间间隔与Bd载量之间存在显著正相关关系；且相较于同时感染A. hamatospicula与Bd的宿主，预先暴露于A. hamatospicula可降低Bd的载量。无论是单一感染还是共感染模式，Bd与蛙虹彩病毒均可抑制宿主生长并降低其存活率。

本研究证实，共感染间的时间滞后可显著影响寄生虫载量，这与优先效应理论的预测相符。由于野外自然环境中的共感染几乎不可能为同时发生，明确感染时间滞后对共感染态势的影响机制，或将为管控有害共感染发挥关键作用。