More people, more cats, more parasites: Human population density and temperature variation predict the prevalence of Toxoplasma gondii oocyst shedding in free-ranging domestic and wild felids

Aim: Toxoplasma gondii is a ubiquitous zoonotic parasite that can infect warm-blooded vertebrates, including humans. Felids, the definitive hosts, drive T. gondii infections by shedding the environmentally resistant stage of the parasite (oocysts) in their feces. Risk factors for oocyst shedding are well-documented in domestic cats under controlled settings, but few studies characterize the role of climate and anthropogenic factors in oocyst shedding among free-ranging felids, which are responsible for the majority of environmental contamination. We aimed to determine how climate and anthropogenic factors influence the level of oocyst shedding in free-ranging domestic cats and wild felids. Location: Global Time period: 1973-2021 Major taxa studied: Felidae, Toxoplasma gondii Methods: We used generalized linear mixed models to determine the association between climatic, ecological, and anthropogenic factors and T. gondii oocyst shedding in free-ranging felids. T. gondii oocyst shedding data from 47 studies were compiled for domestic cats and 6 wild felid species, encompassing 256 positive samples out of 9,635 total fecal samples. Results: T. gondii shedding prevalence in domestic cats and wild felids was positively associated with human population density at the sampling location. Average annual temperature and total precipitation were not associated with increased shedding, however, temperature variables that reflected fluctuation on a smaller timescale were associated with oocyst shedding. Larger mean diurnal range was associated with higher T. gondii oocyst shedding prevalence in domestic cats, while higher temperatures in the driest quarter were associated with lower oocyst shedding in wild felids. Main conclusions: Anthropogenic factors associated with increasing human population density and climate change in the form of temperature fluctuation can exacerbate environmental contamination with the protozoan parasite T. gondii. Direct or indirect management of free-ranging domestic cats could lower the burden of environmental oocysts due to their large population sizes and close affinity with human settlements.【研究目的】刚地弓形虫（Toxoplasma gondii）是一种广泛分布的人畜共患寄生虫，可感染包括人类在内的所有温血脊椎动物。猫科动物作为其终末宿主，会通过粪便排出该寄生虫具有环境抗性的发育阶段——卵囊（oocysts），从而介导刚地弓形虫的传播。目前，受控实验环境下家猫的卵囊排出风险因子已有充分研究，但针对自由栖息猫科动物的气候与人为因素对卵囊排出影响的相关研究仍较为匮乏，而这类猫科动物正是造成绝大多数环境污染的源头。本研究旨在明确气候与人为因素如何影响自由栖息家猫及野生猫科动物的卵囊排出水平。 【研究范围】全球 【时间跨度】1973年—2021年 【研究类群】猫科（Felidae）、刚地弓形虫（Toxoplasma gondii） 【研究方法】本研究采用广义线性混合模型（generalized linear mixed models），探究气候、生态与人为因素与自由栖息猫科动物刚地弓形虫卵囊排出之间的关联。我们整合了47项研究的刚地弓形虫卵囊排出数据，涵盖家猫与6种野生猫科动物，总计9635份粪便样本中检出256份阳性样本。 【研究结果】家猫与野生猫科动物的刚地弓形虫卵囊排出阳性率，与采样点的人口密度呈正相关。年平均气温与总降水量与卵囊排出率升高无显著关联，但反映较短时间尺度波动的温度变量则与卵囊排出存在关联。家猫的平均昼夜温差越大，其刚地弓形虫卵囊排出阳性率越高；而野生猫科动物在最干旱季度的气温越高，其卵囊排出率则越低。 【主要结论】与人口密度升高相关的人为因素，以及以温度波动形式体现的气候变化，可能会加剧这种原生动物寄生虫刚地弓形虫造成的环境污染。由于自由栖息家猫种群规模庞大且与人类居住区毗邻，对其进行直接或间接管理，可有效降低环境中卵囊的负载量。