Introduction
Toxoplasma gondii is an obligate intracellular parasite that can infect more than 350 species of mammals and birds worldwide (Dubey, 2010; Lindsay & Dubey, 2007; Tenter et al., 2000). It is the single species within its genus, in the phylum Apicomplexa (Roberts & Janovy Jr. 2000). The parasite (Dubey et al., 1970) undergoes sexual reproduction to produce oocysts in most domestic and wild felids, which function as definitive hosts (DH) and excrete oocysts in their feces. Oocysts are the infective stage for intermediate hosts (IH), and thus, felid latrines are a source of contamination for IH (VanWormer et al., 2013). T. gondii can also spread asexually, often via ingestion of encysted organisms in tissue (Su et al., 2003), allowing the parasite to bio-accumulate in IH such as carnivores and scavengers. In addition, several species of cockroaches, earthworms, and beetles function as mechanical hosts (Dubey, 2010; Chinchilla et al., 1994).
Seroprevalence of antibodies against T. gondii in hosts varies spatially (Afonso et al 2010) and temporally, and is influenced by climate (Salant & Spira, 2004; Afonso et al., 2010). For example, higher seroprevalence has been observed during years with high temperatures or high rainfall in humans (Hubálek, 2005), rabbits (Almeria et al., 2004), wild ruminants (Gamarra et al., 2008), and domestic cats (Afonso et al., 2006; 2010; 2013). Risk is often moderated through impacts on the distribution of domestic and wild cats, which are influenced by human factors such as the presence of prey, intra or inter-specific territorial interactions, environmental stress, vegetation, and topography (Horn et al., 2011).
Host-specific factors also influence susceptibility to T. gondii,with higher prevalence sometimes detected in larger rodents and lagomorphs than smaller ones (Afonso et al., 2007), and in species with a longer life expectancy (De Thoisy et al., 2003). This may be due to greater exposure to oocysts in species with larger home ranges, longer life expectancies, and higher energy requirements, which are related to body size (Ottaviani et al., 2006). Male cats have a five times greater chance of having antibodies than females (Afonso et al., 2007), possibly due to having larger body sizes and greater need to consume more and larger prey than females (Niewold, 1986). In French Guiana, burrowing, granivorous, and insectivorous mammals had much higher prevalences than arboreal ones (Carme et al., 2002). Mammals in terrestrial or mixed terrestrial / arboreal habits were more exposed to oocysts than strictly arboreal ones (Thoisy et al., 2003; Nardoni et al., 2011).
Among Neotropical primates (NP), the intensity of T. gondiipathology varies among infected species: such differences could be due in part to differences in ecology and behavior (Catão-Dias et al., 2013). Toxoplasmosis in the Callitrichinae NP subfamily (Saguinus, Leontopithecus, Callithrix ) may cause almost 100% mortality, resulting in very low seroprevalence and contributing to difficulty in making ante-mortem diagnosis, particularly in free-ranging populations. NP in the Saimiri and Aotus genera of Cebidae and Atelesand Alouatta in Atelidae may experience acute and severe signs including prostration, anorexia, hypothermia, dyspnea, and vomiting, with mortality from 20-80%, allowing for seroprevalence of 15-66% (Catão-Dias et al., 2013). In contrast, signs among Cebus sp. NP are usually subacute and moderate, with a very low mortality rate that generates high and persistent IgG titers (Bouer et al 2010). Reports in captivity range from 28-79% of infected Cebus sp. monkeys, compared with 30.2% of animals in the wild (Garcia et al., 2005; Leite et al., 2008; Bouer et al., 2010). Cebus sp. NP may have evolved greater resistance than other NP species after frequent exposure toT. gondii (Catão-Dias et al., 2013). Cebus sp. NP commonly forage for insects on the ground and drink water from puddles and water holes, where they may encounter oocysts (Fragaszy et al., 2004). In addition, although most of the Cebus diet protein comes from invertebrates, they may consume a variety of vertebrates weighing up to 1/3 of their body weight and constituting up to 3% of their feeding time (Fragaszy et al., 2004).
In Costa Rica there are four species of NPs. While the Central American white-faced capuchin (Cebus imitator ) and the Mantled howler monkey (Alouatta palliata ) are considered at low risk (least concern) according to IUCN Red List, Geoffroy’s spider monkey (Ateles geoffroyi ) and both subspecies of the Central American squirrel monkey (Saimiri oerstedii oerstedii and S. o. citrinellus ) are endangered mainly due to habitat loss and fragmentation (Cuarón et al., 2008a-e). Some species still are captured for the illegal pet trade, and are thus protected from international trade under Appendix I of the Convention on International Trade in Endangered Species (CITES, 2020). Although Costa Rica has protected areas that cover 25% of the country (González & Lobo, 1999), other conservation actions include a system of incentives to farmers known as payments of environmental services (PEP) since 1997 (Pagiola, 2008), and a national program of biological corridors (PNCB) to increase connectivity between forest patches, species migration and genetic flow (La Gaceta, 2006, SINAC, 2008). Ex situ actions include keeping some NP in zoos for education purposes and rescue centers across the country focus on rehabilitation and reintroduction of individuals back to protected areas.
The high mortality rates observed in some NP can imperil already at-risk populations, but the causes of mortality and high rates of exposure are poorly understood (Bouer et al., 2010; Catão-Dias et al., 2013), so it is important to assess the infection status in captive NP. Living in altered environments or in contact with humans (where domestic cats are present) can affect NP behavior (McKinney, 2011) and exposure to infectious agents (Wolfe et al., 1998, Ekanayake et al 2004). Thus, it is important to evaluate impacts of T. gondii infection in NP in different areas that experience differential contact with human-altered habitat and have differing behaviors and diet (Fragaszy et al., 2004; Catão-Dias et al., 2013). Here we analyzed exposure to T. gondiiin A. geoffroyi, A. palliata, C. imitator and S. oerstedii and the influences of environmental, anthropogenic, and biological variables in wild A. palliata and C. imitator in Costa Rica.