Fallow deer approaching humans are also more likely to be seropositive for Toxoplasma gondii

Andrew R. Ryan, Annetta Zintl, Laura L. Griffin, Matthew Quinn, Amy Haigh, Pietro Sabbatini, Bawan Amin, Simone Ciuti
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Abstract

Toxoplasma gondii (T. gondii) is a trophically-transmitted protozoan parasite that has been suggested to facilitate its transmission by altering intermediate hosts’ anti-predator behaviour, thus increasing the likelihood of completing the cycle inside its definitive host i.e. domestic and wild felines. T. gondii has been linked to reduced risk-aversion, slower reaction times, and more exploratory behaviours in intermediate hosts, including most famously weakened aversion to the scent of feline predators in mice. Studies examining this phenomenon, however, have almost exclusively been carried out in laboratory conditions with small mammals, whereas little is known about the role of T. gondii within more complex ecological contexts involving large mammals in the wild. Under such scenario, the goals of our study were three-fold. Firstly, to determine the prevalence of T. gondii infection in a population of free-living fallow deer (Dama dama) living in a park at the edge of a metropolis. Secondly, to find a link between deer seropositivity and space use in the park, namely proximity to buildings with domestic cats, where deer may have been more likely to contract the disease. Finally, to determine whether infection with T. gondii was linked to risk taking behaviour in these free ranging large mammals, namely likelihood to approach park visitors. To achieve our goals, we estimated seropositivity and combined it with spatial distribution and behavioural data of individually-recognizable deer ranging from those that avoid humans (risk-avoiders) to those who beg for food (risk-takers). We found T. gondii to be quite widespread in this population with a seropositive of 20% (24 out of 120 individuals). Contrary to our expectations, we found no correlation between T. gondii seropositivity and space use in the park, therefore not allowing us to engage with the dynamics of disease contraction. We did however find that fallow deer taking the risk of approaching humans were also more likely to be seropositive. Are risk taking individuals more likely to contract the disease? Or, alternatively, do they take more risk because they have contracted the disease? The causal mechanism behind our result has yet to be disentangled, opening new scenarios in research aimed at tackling host manipulation in this parasite. It is a fact, however, that those animals that were more likely to be in contact with the public were also those more likely to be seropositive, adding key empirical evidence to the study of zoonotic diseases. Our study is a significant contribution on the transmission and maintenance dynamics of T. gondii, offering new insights on the need to conduct longitudinal studies able to disentangle the causal mechanism and T. gondii’s ability to manipulate its intermediate host.
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接近人类的雌鹿也更有可能对弓形虫血清呈阳性反应
弓形虫(T. gondii)是一种滋养传播的原生动物寄生虫,有人认为它可以通过改变中间宿主的反捕食行为来促进其传播,从而增加在其最终宿主(即家猫和野生猫科动物)体内完成循环的可能性。淋病双球菌与中间宿主的风险规避能力下降、反应速度变慢和探索行为增多有关,其中最著名的是小鼠对猫科动物捕食者气味的厌恶感减弱。然而,对这一现象的研究几乎都是在实验室条件下对小型哺乳动物进行的,而对于淋球菌在野外大型哺乳动物的复杂生态环境中的作用却知之甚少。在这种情况下,我们的研究有三个目标。首先,确定生活在大都市边缘公园中的自由生活的秋鹿(Dama dama)群体中的淋病双球菌感染率。其次,寻找鹿血清阳性反应与公园空间使用之间的联系,即靠近养有家猫的建筑物,在那里鹿可能更容易感染疾病。最后,我们还想确定淋病双球菌感染是否与这些自由活动的大型哺乳动物的冒险行为(即接近公园游客的可能性)有关。为了实现我们的目标,我们估算了血清阳性率,并将其与可单独识别的鹿的空间分布和行为数据相结合,这些鹿既有躲避人类的(风险规避者),也有乞讨食物的(风险承担者)。我们发现,淋病双球菌在这个种群中相当普遍,血清阳性率为 20%(120 头鹿中有 24 头)。与我们的预期相反,我们没有发现淋病双球菌血清阳性反应与公园空间使用之间的相关性,因此我们无法对疾病感染的动态进行研究。不过,我们确实发现,冒险接近人类的秋鹿也更有可能血清呈阳性。冒险的个体更容易感染疾病吗?或者说,他们是否因为感染了疾病而冒了更大的风险?我们的研究结果背后的因果机制还有待厘清,这将为旨在解决寄生虫宿主操纵问题的研究提供新的思路。但事实是,那些更有可能与公众接触的动物也更有可能出现血清阳性,这为人畜共患病的研究增添了关键的实证证据。我们的研究是对淋球菌传播和维持动态的重大贡献,为开展纵向研究的必要性提供了新的见解,从而能够将致病机制与淋球菌操纵中间宿主的能力区分开来。
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