Research Article: Toxoplasma gondii infection in wild mustelids and cats across an urban-rural gradient

Date Published: June 20, 2018

Publisher: Public Library of Science

Author(s): Macarena Barros, Oscar Cabezón, Jitender P. Dubey, Sonia Almería, María P. Ribas, Luis E. Escobar, Barbara Ramos, Gonzalo Medina-Vogel, Michael E. Grigg.

http://doi.org/10.1371/journal.pone.0199085

Abstract

The increase in human population and domestic pets, such as cats, are generating important consequences in terms of habitat loss and pathogen pollution of coastal ecosystems with potential to generate negative impacts in marine biodiversity. Toxoplasma gondii is the etiological agent of zoonotic disease toxoplasmosis, and is associated with cat abundance and anthropogenic disturbance. The presence of T. gondii oocysts in the ocean has negatively affected the health status of the threatened Southern sea otter (Enhydra lutris nereis) populations. The present study analyzed seroprevalence and presence of T. gondii DNA in American mink (Neovison vison), Southern river otters (Lontra provocax) and domestic cats (Felis silvestris catus) in four different areas in Southern Chile comprising studies in rivers and lakes in Andean foothills and mountains, marine habitat and island coastal ecosystems. Mean seroprevalence of T. gondii in the study was 64% of 151 total animals sampled: 59% of 73 American mink, 77% of 13 Southern river otters, 68% of 65 domestic cats and in two of two kodkods (Leopardus guigna). Toxoplasma gondii DNA was detected in tissues from one American mink and one Southern river otter. The present study confirms the widespread distribution of T. gondii in Southern Chile, and shows a high exposure of semiaquatic mustelids and domestic cats to the parasite. Cats and anthropogenic disturbance have a role in the maintenance of T. gondii infection in ecosystems of southern Chile.

Partial Text

Contamination of the aquatic environment derived from human activities is a concern worldwide, and the study of the biological effects of these activities in the marine ecosystem has been declared a goal for future research by the scientific community [1]. The effect of human settlement in coastal areas causes significant negative impacts on coastal marine habitats and their wildlife species, including the flow of human/terrestrial pathogens [2, 3, 4]. Toxoplasma gondii, a worldwide distributed zoonotic protozoan parasite, presents an indirect cycle with domestic and wild felines as definitive hosts. Oocysts are eliminated to the environment through feces where they can remain infective for months or years. Warm-blooded species can become infected by ingesting the sporulated oocysts and infection can persist in infected hosts for the life of the host [5]. Although better studied in terrestrial landscapes, T. gondii has also emerged as a significant aquatic pathogen linked to marine mammal infection and water-borne outbreaks of disease in humans worldwide [6]. The presence of T. gondii in the marine and freshwater ecosystems has been confirmed by the exposure of several aquatic species to this parasite [7, 8, 9, 10], with clinical disease observed in seals, dolphins, whales, sea otters, and manatees [7, 11, 12]. Animals living in freshwater systems are also at risk. As many as 85% (82 of 95) of free-ranging Amazon river dolphins had antibodies to T. gondii [13]. In this respect, T. gondii has been used as a model for the study of land-to-sea pathogen contamination [14, 15, 16]. Higher flow of T. gondii oocysts to the marine ecosystem has been related to the high coastal human densities and estuarine wetland degradation due to human activities [14, 17]. The effect of this higher T. gondii presence in the ocean has negatively affected the health status of the threatened Southern sea otter (Enhydra lutris nereis) populations, increasing its mortality related to the parasite [18, 19], and supporting the hypothesis of land to sea transmission of this parasite through contaminated freshwater runoff [20]. Widespread T. gondii infection in aquatic mammals suggests that contamination of terrestrial watersheds with T. gondii is prevalent, and that sufficient numbers of oocysts are distributed in freshwater and marine ecosystems to infect and cause disease in both near-shore and pelagic mammals [10].

The overall T. gondii seroprevalence, according to the MAT analysis, was 64% (97/151), with 68% (44/65) in domestic cats, 59% (43/73) American mink, and 77% (10/13) in otter (Table 1). The two kodkods were also seropositive. With GLM and Kruskal-Wallis test, seroprevalence for T. gondii among study sites showed no statistical differences (Fig 2A). However, there were differences between study areas (F3,147 = 9.7; P<0.01) because the significantly lower prevalence in area 4 (Magdalena Island), there were not significantly difference between the other areas (F2,120 = 1.12; P = 0.33). Analysis by species showed a consistent prevalence in cats among all of the analyzed study sites, areas and habitats, but not in Magdalena island. No differences were found between T. gondii seroprevalences of mink and otter, or between animal sex or age, although a tendency towards higher prevalence was observed in older animals. Mink had significantly higher seroprevalences in the study sites associated to medium and high presence of domestic cats (H2 = 22.0; P<0.01) (Fig 2B), and significantly less observed seroprevalences in marine habitats (H2 = 28.9; P<0.01) (Fig 2C). In fact, the only study site with significantly less observed seroprevalence was Magdalena Island (Fig 2A). Otter seropositivity had no relationship with cat presence, but was also significantly lower in marine habitats (H1 = 31.5; P = 0.04) (Fig 2C). Indeed, the differences of seroprevalences between study sites for otters were close to significant (F5,7 = 3.5; P = 0.07). Our random forest analysis revealed that seropositivity to Toxoplasma gondii was mainly explained by presence of humans and density of cats (Fig 3). Toxoplasma gondii DNA was detected in the liver of one American mink in Choshuenco (Area 1), and in the lung of the otter found dead in Valdivia (outside of the study areas). The analysis of the vegetation structure revealed considerable variation in the vegetation biomass in the ten-year period assessed (Fig 4). At province level, areas of dramatic vegetation loss were identified in central western Valdivia, eastern Ranco, dispersed areas across Llanquihue, central west Palena, and across the southern sampled areas in Aysen. A significant association was found between the T. gondii seropositivity and the level of vegetation loss of the study sites (COR = 0.65; df = 85; P<0.001) with habitat loss being associated with increase of T. gondii seroprevalence. Results obtained by Toxo-Screen DA fast kit were similar to those obtained with MAT. Of the 40 samples, 27 were equally positive and 9 equally negative, with 2 “false positives” and 2 “false negatives”. The Cohen’s kappa analysis shows a good agreement between the two tests (Kappa = 0.75; 95% confidence interval = 0.52–0.98; P<0.001). The present study confirms the widespread distribution of T. gondii in Southern Chile, and shows a high exposure of semiaquatic mustelids and domestic cats to the parasite. The high explanatory power of human presence followed of cat density in our machine learning analysis (Fig 3), suggests the role of domestic cats as a form of anthropogenic disturbance for the maintenance of T. gondii infections in Southern Chilean ecosystems. The mean prevalences observed in the study, 59% in mink, 77% in otters, and 68% in domestic cats are consistent with those observed in previous studies. A 70% prevalence of T. gondii in American mink has been reported in the Maullín River [32]. We observed similarly high seroprevalence level at the same site in mink in the current study (83%). Our findings also agree with recent reports of T. gondii seroprevalences of 77% in American mink in the USA [54]. Seroprevalence of T. gondii revealed the lowest values (25%) in Magdalena Island. These results were expected considering that there are no reports of the presence of domestic cats in this island due to its geographic isolation (five km distant from the continent). Our results also agree with another study in USA which suggests that prevalence of T. gondii antibodies below 40% indicates low exposure to the parasite [55]. However, the prevalence on this island may support the idea of horizontal transmission of T. gondii. Mink and otters from Magdalena Island may have become infected while feeding on other intermediate hosts.   Source: http://doi.org/10.1371/journal.pone.0199085

 

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