Endoparasites of Selected Native Non-Domesticated Mammals in the Neotropics (New World Tropics)

In this review, information was summarized on endoparasites found in six non-domesticated neotropical animals. These mammals have the potential to be domesticated. The animals included three rodents, agouti (Dasyprocta leporina), lappe (Agouti paca), and capybara (Hydrochoerus hydrochaeris); a marsupial, manicou (Didelphis marsupialis insularis); and an artiodactyl, the collared peccary (Tayassu tajacu/Peccari tajacu) and a ruminant (the red brocket deer, Mazama americana). While there are many descriptions of the parasites present, the majority of publications failed to note the effect of them on the animals. Most information is available on endoparasites of capybara, while the endoparasites of the red brocket deer were the least reported. The manicou was reported to have had the most number of endoparasites, 44 species of parasites were reported, while there were only 24 endoparasites reported in the lappe. The most common parasites found in these neotropical animals were Paraspidodera uncinata, Strongyloides spp., Eimeria spp., Moniezia benedeni, Trichuris spp., Physocephalus spp., and Giardia spp. A large majority of the studies concluded that these animals were reservoirs for parasites that could affect domesticated livestock. Endoparasites of zoonotic significance were Echinoccocus spp., Trichuris spp., Giardia spp., and Cryptosporidium spp.

Since these six native neotropical animals have potential for domestication [3], it is required to focus on factors which affect animal production. These factors are (i) feeding and nutrition, (ii) reproduction and breeding, (iii) health and disease, (iv) housing and environement, (v) economic and socioeconomic factors, and (vi) animal behavior and psycology [3,4]. Recently, the agouti, D. leporina, has been studied in more detail, with focus on the anatomy of the male and female reproductive system, oestrus cycle in the female (28-31 days) as well as semen analysis using electroejaculation [5][6][7][8] Further anatomical investigations of the digestive system of the agoutis revealed that the majority of the gastrointestinal tract was small intestine in conjunction with a large cecum [9]. The agoutis mainly are frugivorous with the majority of the diet consisting of nuts and fruits, with potentially a preferential particle size [10][11][12][13]. Earlier it was found that these animals were rather omnivorous and would consume eggs and chicks [14]. It is clear that there is a need for more investigation on their feeding habits. Several studies have reported on the blood values of captive reared animals, and differences in diets and environments did not affect those values [15]. As such, blood values are a good basis for determination of the health status of neotropical mammals.
The lappe was decribed as a frugivore, the manicou as an omnivore, the collared peccary as a pseudo-ruminant herbivore, and the red brocket deer was grouped with ruminants [12][13][14][15][16][17][18][19]. The manicou has a gestation period of three weeks [17,18]. Other information on these species is lacking. The objective of this review was to summarize the knowledge of endoparasites found in six native non-domestic neotropical animal species. These neotropical animals are potential sources of meat protein which can be utilized by rural communities.

Agouti (Dasyprocta spp.)
The earliest work on the gastrointestinal parasites of the agouti, D. leporina, was done in the mid 1930s. Strongyloides agoutii was described in the feces of the agouti. This parasite has a similar life cycle as the other species of the Strongyloides genus [20]. Similar work was done on agoutis found in Trinidad, but the entrails of the animals were analyzed for gastrointestinal parasites. In the early 1950s, the amphistome, Stichorchis giganteus; the tapeworm, Raillietina demerariensis var. trinitatae; and seven roundworms including Strongyloides agouti, Trichuris gracilis var. trinitatae, Acanthocheilonema spp., Fuellebornema agoutii, Pudica pudica, Aspidodera binansata var. agoutiae, and Helminthoxys urichi were detected in the agouti [21].
In a zoo in Mephis Tennessee, Echinococcus oligarthrus hydatid cysts and Strongyloides spp. were found in healthy Brazilian agoutis from Guyana. These animals were treated with ivermectin (0.7 mg subcutaneously, twice daily for 14 days), praziquantel (28.4 mg intramuscularly, twice daily for 30 days), and albendazole (65 mg per os, once a day for 30 days) and some of the subcutaneous cysts were removed surgically [36]. In the studies performed in Argentina, similar parasites as to those mentioned above were found [37].
Other treatments that were reported included fenbendazole (5 mg/kg/day for 5 days) and piperazine citrate (180 mg/kg/day for 5 days), and the efficacy reported with these treatments were poor [38]. Most authors identified various parasites in captive-reared and wild agoutis in the neotropical region; however, only a few made reference to the effect these parasitic organisms had on the animals' health and body condition. A summary of the endoparasites found in the agouti at different locations and the effects on the animals (host) can be seen in Table 1.
Few studies reported the pathology casued on internal organs by the endoparasites. The liver pathology potentially caused by Echinococcus vogeli and Calodium hepaticum was characterized by fibrosis with a scanty infiltrate of lymphocytes and macrophages [39] and the histopathological lesions of Physocephalus spp. in the stomach showed congestion, interstitial hemorrhaging, and mononuclear inflammatory infiltrates [40]. In a breeding farm in Brazil, Eimeria spp., Strongyloides spp., Trichuris spp., and Hymenolepis diminuta were found and managed by anthelmintics and sanitation [41]. Quick lime was also used as an anthelmintic treatment for the larval stages of the parasites in the soil [42].
Echinococcus spp. take a special place in the list of parasites found in the lappe as they are zoonotic. They have been found in Columbia where approximately 47% (44/93) of the lappe were found to be infected [47]. In Bolivia as well as Peru, Echinococcus vogeli was found but there were no relyable prevalence figures available [48][49][50]. A later study in Peru demonstrated larval cysts of E. vogeli in 12% of the lappe (15/120) [51].
Echinococcosis has been reported as being zoonotic and the agouti (D. leporina) and the lappe (A. paca) are the intermediate hosts of E. vogeli and E. oligarthrus. However, humans become infected via the ingestion of eggs that come from the adult parasites present in dogs [51][52][53][54][55][56]. All data on endoparasites in the lappe are summarized in Table 2.

Capybara (Hydrochoerus hydrochaeris)
The first reports that were made in Panama on endoparasites was in the 1930s and amphistomate flukes (Taxorchis schistocotyle) were detected in a dead animal. However, no lesions were found in the intestinal tract. [57]. Another case report came from the San Diego Zoo, where Balantidium coli was associated with mortality as well as mucoid diarrhea. Histological findings of the colon found ulceration and cellular infiltrates that consisted of eosinophils, macrophages, and plasma cells [58]. In Brazil, the death of a capybara was associated with four specimens of trematodes, Trichostrongylidae, Eimeria, and Strongyloides spp. There was multifocal fibrosis with marked thickening of the liver capsule and granulomatous thickening of the bile ducts [59]. Eimeria ichiloensis and Eimeria trinidadensis have been associated with diarrhoea in the capybara [60].
Stress by feed restriction and physical restraint had a negative effect on growth and body condition and induced a significantly higher coccidia infestation, and a lower helminth burden showing that the living conditions may have an influence on parasitic infestation [84]. Environmental conditions such as season, age, and sex of the animals have also been associated with different parasitic infestations. This shows that the interactions amongst gastrointestinal parasites are complex and further research is needed [85].
Capybaras have been shown to have a wide range of endoparasites, but they appear largely resistant to their effects and show only a few signs of ill health [86]. The capybaras, being the largest rodents on earth, have been given a lot of attention. However, the majority of investigations only noted the presence or absence of endoparasites without making observations on the effects these organisms had on the animals (Table 3).
In the US (Alabama and Georgia), Isospora boughtoni and Isospora spp. oocysts, Brachylaima virginianum, and Cruzia americana were found in the intestines of opossum (D. marsupialis) [90]. Phyaloptera turgida was found in the stomach and ulcerations penetrated from the glandular mucosa to the submucosal level [91]. In the lung, Capillaria aerophila and metastrongyloid nematodes which resembled Perostrongylus and Didelphostrongylus hayesi were found [91,92]. The lungs infested with Perostrongylus showed a diffuse interstitial pneumonia pattern [91].
In Costa Rica, the coccidian, Eimeria marmosopos, was found [96], and this coccidial species was located in the epithelial cell of the small intestines and caused cellular necrosis [97]. Recently in Mexico, the gall bladder was found to be the site of infection for Amphimerus caudaletestis and Philandrophilus magnacirrus. In the intestines, Rhopalias coronatus, R. macracanthus, Thaumasioscolex didelphidis, Viannaia viannai, Travassostrongylus spp., and Onicola luehei were found and the cecum was the predilection site for Cruzia tentaculata and Trichuris didelphis. Turgida turgida was found in the stomach and Capillaria spp. was found in the lungs [98]. Aspidodera spp. and C. tentaculata were found in the small intestines of D. marsupialis in Pocone, Brazil [35] (Table 4).

Conclusions
Most endoparasites were detected (clinical or subclinical) in the agouti, while for the red brocket deer (Mazama americana) few endoparasites were found (Table 7). This was in relation to the number of studies performed on these animals. A large majority of the authors viewed these neotropical non-domesticated animals as parasitic reservoirs that could affect domesticated introducted livestock species. The endoparasites of zoonotic significance found in the non-domesticatic neotropical animals were Echinoccocus spp., Trichuris spp., Giardia spp., and Cryptosporidium spp. There were a few reports of parasites showing negative effects on neotropical non-domesticated animals. Further studies on the effect of parasitism on these six neotropical species should elucidate their importance as pathogens, and their effect on the growth and performance of animals. Furthermore, the relation between the infestation grade and clinical manifestation should be deteremined.