Endoparasites of capybaras (Hydrochoerus hydrochaeris) from anthropized and natural areas of Brazil

Braz J Vet Parasitol 2021; 30(2): e027420 | https://doi.org/10.1590/S1984-29612021049 This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Endoparasites of capybaras (Hydrochoerus hydrochaeris) from anthropized and natural areas of Brazil


Introduction
The capybara (Hydrochoerus hydrochaeris) is considered the largest rodent in the world. It is native to Brazil and is widely distributed in South America (Alho, 1986;Vargas et al., 2007) and prefers warm environments with water bodies, areas for grazing and forest fragments, which provide refuges as well as shelters for parturition and protection against predators (Alho, 1986;Rodrigues et al., 2013).
Anthropic factors include the expansion of human activities over habitats originally occupied by native fauna, such as capybaras. The cutting of native forest for the formation of pastures or crops promotes the growth of capybara populations because natural predators are free from such habitats and capybaras have a high reproductive potential (Vargas et al., 2007;Rodrigues et al., 2013). Anthropized areas often feature large numbers of capybaras that cause agricultural damage; consequently, capybaras are often considered pests and pose public health and safety risks (Vargas et al., 2007;Rodrigues et al., 2013). The increase in capybara populations in anthropized areas results in the increased contact of these animals with the human population and domestic livestock (Ribeiro et al., 2010).
For epidemiological studies and routine laboratory diagnosis of endoparasites in populations of wild animals, mainly rare and endangered species, there is a growing demand to encourage the use of noninvasive methods (Solórzano-García & Pérez-Ponce de León, 2017). Parasitological analyses of feces might provide an important methodological alternative (Vieira et al., 2006), as such analyses permit rapid diagnoses and allow a large number of samples to be easily assessed (Brandão et al., 2009).
Most epidemiological studies using parasitological analyses of feces to study endoparasites are based on samples from a single location or population of capybaras in public parks (El-Kouba et al., 2008;Truppel, 2009;Gioia-Di Chiacchio et al., 2014) or captive animals (Gurgel et al., 2007;Santos et al., 2011;Reginatto et al., 2008). These studies thus do not capture the effect of different environments on the parasitic diversity in animals.
Given the lack of comprehensive epidemiological studies, the aim of this study was to evaluate and to compare the occurrence of endoparasites in the fecal samples of capybaras from anthropized areas in seven cities in the state of São Paulo, southeastern Brazil, and natural areas in two locations in the Pantanal biome.

Materials and Methods
The capybaras sampled in this study were from anthropized areas in the state of São Paulo and from natural areas of the Pantanal biome, as described by Luz et al. (2019). Anthropized areas sampled were environments modified by human activities and were located in the municipalities of Americana, Araras, Avaré, Piracicaba, Pirassununga, Ribeirão Preto and Tatuí in the state of São Paulo. The natural areas were environments that have not been altered by human activities and consisted of two locations in the Pantanal biome: Poconé in the state of Mato Grosso and Corumbá in the state of Mato Grosso do Sul.
Animals were collected between 2015 and 2018 following the methods of Luz et al. (2019). Fecal samples were collected directly from the rectum of captured capybaras, packed in plastic containers, and kept refrigerated at 4 ºC until they were brought to the laboratory. Centrifugal sedimentation in water-ether (Ferreira et al., 1962) and centrifugal flotation in sucrose solution (Ogassawara & Benassi, 1980) were used for parasitological evaluations. The eggs and oocysts of the parasites in capybara feces were identified morphologically based on Faust (1935), Casas et al. (1995), Thienpont et al. (2003), Monteiro (2011), andDracz et al. (2016). In some cases, the structures were measured using Image-Pro Plus 5.1 for the analysis of images and morphometry fitted to an Olympus microscope.
The proportions of capybaras containing eggs or oocysts of each of the identified parasites were compared between anthropic and natural areas by chi-square tests. Analyses were performed using the program Minitab® Release 18; differences were considered significant when P < 0.05. This study was approved by the Institutional Animal Care and Use Committee (IACUC) of the Faculty of Veterinary Medicine of the University of São Paulo (approval number 5948070314) and was carried out in accordance with the regulations/guidelines of the Brazilian National Council of Animal Experimentation (CONCEA). Field captures of capybaras were authorized by the Brazilian Ministry of the Environment (permit SISBIO Nos. 43259-6) and by the São Paulo Forestry Institute (Cotec permit 260108-000.409/2015).

Results
Results of the evaluation of fecal samples from capybaras from the anthropized areas of the state of São Paulo and from natural areas of the Pantanal biome are detailed in Table 1.
The only statistical difference observed in the occurrence of an endoparasite between natural and anthropized areas was for S. chapini, which was identified only in capybaras from anthropized areas ( Table 1).
The oocysts of Eimeria spp. were detected in 76.1% (86/113) of the samples and were found in all locations in the natural and anthropized areas of the study. Cryptosporidium spp. was detected in a single sample from the anthropized area (Ribeirão Preto).
Capybaras from anthropized areas had a greater species richness of endoparasites, especially F. hepatica and Cryptosporidium spp., which may have zoonotic potential. Some of the eggs and oocysts in capybara fecal samples are shown in Figure 1.

Discussion
In this study, 113 fecal samples from capybaras were evaluated. To our knowledge, this is the first study to compare the species richness of gastrointestinal endoparasites in a population of capybaras in anthropized and natural areas with samples from more than 100 wild animals.
We detected the presence of helminths and coccidian protozoa in 97.3% of the sampled capybaras. This high prevalence and diversity of endoparasites might stem from the gregarious, amphibious and territorial behavior of these mammals; in addition, their habit of grazing close to the ground might facilitate the ingestion of eggs and larvae (Truppel, 2009;Gioia-Di Chiacchio et al., 2014).
Eggs from nematodes belonging to the superfamily Trichostrongyloidea were detected in capybaras from both areas. The parasites (Trichostrongyloidea, Viannaiidae) V. hydrochoeri and H. anomalobursata are specific to capybaras. The nematode V. hydrochoeri might be particularly widespread given that it is commonly reported in necropsy studies that have been conducted in various regions of Brazil and in other South American countries, reaching as high as 100% of capybara samples (Costa & Catto, 1994;Bonuti et al., 2002;Salas & Herrera, 2004;Sinkoc et al., 2004).
Although H. anomalobursata was identified in 90% of capybaras evaluated by necropsy in the Pantanal (Bonuti et al., 2002) and in 58.3% in a study of the Taim Ecological Reserve in southern Brazil (Sinkoc et al., 2009), several studies based on necropsy did not detect it, indicating that this nematode does not have a wide distribution across all regions (Costa & Catto, 1994;Salas & Herrera, 2004;Sinkoc et al., 2004).
Although the eggs of parasites belonging to the superfamily Trichostrongyloidea have similar morphological characteristics, which make accurate identification to genus or species of the agents involved in the infection impossible, necropsy studies point out that V. hydrochoeri is the most likely Trichostrongyloidea parasite affecting capybaras in both natural and anthropized areas (Costa & Catto, 1994;Bonuti et al., 2002;Salas & Herrera, 2004;Sinkoc et al., 2004).
The occurrence of other nematodes (Trichostrongyloidea, Trychostrongylidae), such as Trichostrongylus axei, Haemonchus sp. and Cooperia spp., is rare and often considered accidental (Sinkoc et al., 2009). Infection of capybaras by these parasites usually occurs in anthropized areas and requires interaction with other livestock species, such as cattle, goats, sheep and horses.
Ellipsoid larvated eggs were detected in this study and were consistent with the morphological and biometric description of Vieira et al. (2006) for S. chapini, the only species of this genus that is known to parasitize capybaras. Young animals are more susceptible to parasitism (Costa & Catto, 1994), and severe clinical manifestations have been observed in individuals bred in captivity (Pinheiro et al., 2006;Santos et al., 2011). Eggs of S. chapini were only detected in stool samples of capybaras from anthropized areas. Other studies that have collected stool samples of capybaras from anthropized areas such as public parks reported occurrences of this parasite ranging from 0 to 56% (El-Kouba et al., 2008;Truppel, 2009;Gioia-Di Chiacchio et al., 2014); results from this study were similar to those obtained from captive samples (Santos et al., 2011). The high variation observed for capybaras sampled from anthropized areas may stem from the large number of samples from pups collected in these areas; in contrast, a smaller number of samples from pups was collected from natural areas.
Necropsy studies have revealed that the oxyurid P. obesa had a high occurrence and intensity of infection and affected approximately 100% of capybaras (Bonuti et al., 2002;Salas & Herrera, 2004;Sinkoc et al., 2009); it can be easily detected in wild populations of capybaras in natural areas (Costa & Catto, 1994;Bonuti et al., 2002), anthropized areas (Truppel, 2009;Gioia-Di Chiacchio et al., 2014) and in captive-bred individuals (Sinkoc et al., 2004). Because female parasites are eliminated in feces along with a large number of eggs, they clump externally in the form of a cluster (Ribeiro & Amato, 2003), permitting many eggs to be simultaneously ingested (Sinkoc et al., 2004).
Helminthological surveys conducted during the previous decades using animal necropsies have shown that the nematode Capillaria hydrochoeri is the only species of this genus that parasitizes capybaras (Costa & Catto, 1994;Bonuti et al., 2002;Sinkoc et al., 2004;2009) and can be found in natural (Costa & Catto, 1994;Bonuti et al., 2002) and anthropized areas (El-Kouba et al., 2008;Truppel, 2009). The ability of the eggs of this nematode to persist in the environment for several months may lead to gradual infections of capybaras that progress with age, resulting in a greater occurrence in adult animals. The tendency of capybaras to feed close to the ground and their coprophagic habits facilitate the ingestion of eggs and infectious parasites (Alho, 1986;Ribeiro & Amato, 2003).
Capybaras can be specifically affected by cestodes belonging to the family Anoplocephalidae, especially the genus Monoecocestus. Previous necropsies of capybaras identified the following species: M. hydrochoeri, M. hagmanni, M. macrobursatum, and M. jacobi (Rego, 1961;Sinkoc et al., 2009). The cestodes of the family Anoplocephalidae use oribatid mites as intermediate hosts for the development of cysticercoid larvae. As these mites are found in superficial layers of the soil in vegetation and pastures (Monteiro, 2011), several environments are conducive to the development of the biological cycle of these cestodes in wild capybaras in natural areas (Costa & Catto, 1994;Bonuti et al., 2002), anthropized areas (Truppel, 2009) or in captive capybaras (Sinkoc et al., 2004).
Parasites belonging to the Paramphistomoidea superfamily documented in studies based on necropsies of capybara populations were Taxorchis schistocotyle and Hydrochoeristrema cabrali, both of which were considered specific to capybaras (Sinkoc et al., 1998;Avelar et al., 2015); furthermore, their occurrence was directly related to the presence of mollusks that act as intermediate hosts for the development of immature stages (Avelar et al., 2015).
Hydrochoeristrema cabrali is thought to be a parasite of the cecum of capybaras (Sinkoc et al., 1998) and was verified through necropsy studies in areas with livestock exploration in the ecological reserve of Taim in Rio Grande do Sul (Sinkoc et al., 2009) and in areas with captive-bred capybaras in the State of São Paulo (Sinkoc et al., 2004), where its occurrence and distribution are restricted.
Although the eggs of parasites belonging to the superfamily Paramphistomoidea have similar morphological characteristics that hinder the identification of the genus of the agents involved in the infection, the digenetic T. schistocotyle is considered the parasite (Paramphistomoidea) most likely to affect capybaras in natural and anthropized areas. The common detection of T. schistocotyle in necropsy studies may favor the denomination of this species for eggs with morphological characteristics of the superfamily Paramphistomoidea, which have often been identified in parasitological analyses of feces (Corriale et al., 2011;. The digenetic F. hepatica is not specific to capybaras and can affect several species of domestic and wild animals, including humans, causing great economic losses to livestock (Dracz et al., 2016).
The origin of F. hepatica lies in the Old World. This parasite was introduced in America by European colonists through the transport of infected farm animals (Bargues et al., 2017). As capybaras are native to South America, F. hepatica is not considered a natural parasite of capybaras and can establish a nonharmonious parasitic host relationship with acute pathogenicity promoting necro-hemorrhagic cholangiohepatitis, which can cause the death of animals and devastate the group of capybaras in an area .
Accidental parasitism appears to be a common occurrence; F. hepatica only occurs in capybaras from anthropized areas, such as public parks (Santarém et al., 2006;El-Kouba et al., 2008;Truppel, 2009;Labruna et al., 2018), or rural areas (Bellato et al., 2009;Dracz et al., 2016) shared with livestock, primarily ruminants. The maintenance of the population of capybaras in isolated natural areas where there is no interaction with the breeding sites of ruminants or access to collections of water contaminated by the waste of these animals could hinder infection.
The biological cycle of F. hepatica likely takes place in wetlands, and mollusks of the genus Lymnaea are required as intermediate hosts for the development of immature stages (Dracz et al., 2016). The absence of these mollusks in most areas could inhibit the development of the biological cycle and the occurrence of F. hepatica in capybara populations.
The occurrence of the protozoa Eimeria spp. can vary widely in the capybara population and can be as high as 95 to 100% of infected animals, both in wild areas under natural circumstances where population densities are not high as well as in areas with higher population densities, such as areas with captive breeding (Casas et al., 1995;Silva et al., 2007;Reginatto et al., 2008). The constant and successive infections occurring throughout the 7/10 Endoparasites of capybaras life of the animals promote the development of an immune response that can make most adult animals capable of withstanding parasitic infections (Gurgel et al., 2007).
The protozoa Eimeria spp. are much more common in captive-bred individuals and can cause clinical manifestations and death, especially in young animals (Pinheiro et al., 2006). Stress and adverse conditions can decrease the immunity of capybaras and increase the intensity of infection (Pinheiro et al., 2006;Eberhardt et al., 2013).
Few studies have documented the occurrence of Cryptosporidium spp. in capybaras (Meireles et al., 2007;Meireles, 2010). These protozoa are not specific to capybaras and can affect a variety of hosts, including humans and domestic and wild animals (Meireles, 2010;Zahedi et al., 2016). In only one capybara sample from the anthropized area, oocysts with morphological characteristics consistent with Cryptosporidium spp. were observed. The occurrence of Cryptosporidium spp. appears to be related to capybaras coming from anthropized areas, such as places where cattle are reared (Meireles et al., 2007) or in captivity (Reginatto et al., 2008).
Although little is known about the role of capybaras as reservoirs, a molecular study based on the analysis and sequencing of the 18S rRNA and GP60 genes using samples of capybara feces collected on the banks of rivers in the State of São Paulo identified C. parvum zoonotic subtype, suggesting that water reservoirs might be contaminated (Meireles et al., 2007).
Although the high population density observed in groups of capybaras in some anthropized areas may contribute to the infection of these animals (Truppel, 2009), significant differences in the frequency of the occurrence of the majority of endoparasites detected in capybaras from natural and anthropized areas were not observed.
Capybaras are considered relatively long-lived animals, but variation in their generations is similar to that observed in small rodents. This property indicates that capybaras show high phenotypic plasticity and genetic variability, which permit them to rapidly respond to environmental changes and might be responsible for their success in anthropized areas (Bovo et al., 2016). This high capacity to adapt to the novel environmental conditions of anthropized areas (Bovo et al., 2016) and their ability to remain gregarious and territorial in anthropized areas as in natural areas (Rodrigues et al., 2013;Almeida et al., 2013) could explain the largely similar pattern of occurrence of capybara-specific endoparasites across the different study areas.
The helminths specific to capybaras appear to be characterized by a dynamic and delicate balance (Pino et al., 2009) that aids the ability of capybaras to withstand the effects of parasitism. Capybaras can develop stressdependent prophylaxis, in which components of their immunity are mobilized to help control the parasitic load of specific helminths (Eberhardt et al., 2013), favoring their adaptation regardless of the habitat in which they occur. In fact, capybaras are considered robust to parasitism, which increases the difficulty of measuring the effects of parasitism on the health of these animals (Salas & Herrera, 2004;Reginatto et al., 2008). In addition, this property of capybaras facilitates their captive breeding and makes them well adapted for breeding in limited areas (Nogueira-Filho & Nogueira, 2004).
In the capybaras of anthropized areas, a greater number of species of endoparasites was observed, emphasizing that F. hepatica and the protozoan Cryptosporidium spp. are not specific parasites of capybaras. Anthropized areas can greatly differ in their environmental conditions compared with natural areas, which could facilitate the contact of capybaras with other animal species, such as ruminants (Meireles et al., 2007;Bellato et al., 2009;Sinkoc et al., 2009) and with the human population (El-Kouba et al., 2008;Truppel, 2009;Labruna et al., 2018), and promote the occurrence of these accidental endoparasites. These parasites have zoonotic potential and can be transmitted through water and food, mainly Cryptosporidium spp. (Santarém et al., 2006;Zahedi et al., 2016). There is thus a need to monitor parasites through coproparasitological examinations of capybaras, that could act as sentinel animals, indicating the presence of these parasites, especially in public parks .