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.

1. Introduction

In this review, updates were made on the current knowledge of endoparasites in non-domesticated animals with the potential for domestication. These animals have the potential to be meat protein sources for rural communities. Former reviews on endoparasites in the neotropics summarized the information on cattle (Bos indicus and Bos taurus), sheep (Ovis averies), goats (Capri hircus), horses, (Equus caballi), pigs (Sus sucrofa), and chickens (Gallus domesticus) [1]. Endoparasites mainly found in these domesticated animals were Strongylus vulgaris in horses, Hyostrongylus rubidis in pigs, Haemonchus contortus in ruminants, and Heterakis gallinarum in chickens. Some endoparasites of ducks (Anas platyrhynchos and Cairina moschata), turkeys (Melaegradis gallopavo), chinchillas (Chinchillas lanigera), guinea pigs (Cavia porcelleus), and south american camelids (Lama glama, Lama pacos, Lama gunacoa, and Vicuna vicuna) were Nematodirus spp., Trichostrongylus spp., Giardia duodenalis, Cryptosporidium spp., and Ascaridia gallinarum [2].

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.

2. 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 presumed healthy wild agoutis from Trinidad, Trichuris gracilis var. trintatae (in cecum and large intestines), Strongyloides agouti, Helminthoxys urichi, Eimeria spp., ascarid-like ova (unidentified species), trematode (unidentified species), and an unidentified cestode were detected [22] and more recently in intensively reared agouti (D. leporina), Strongyloides spp. was found in 36.9%, Trichuris spp. in 4.62%, and Paraspidodera uncinata in 15.4% of the agoutis sampled (n = 65). Despite the presence of these parasites, the animals were in good body condition (average body condition score of 3 out of 5) and had no history of gastrointestinal illness [23]. Using fecal floatation techniques, Trichuris spp. were found at a concentration of 2.2 × 102 eggs/gram, Strongyloides spp. at 4.28 × 102 eggs/gram, and Eimeria spp. at 2.15 × 103 oocysts/gram, all with no signs of gastrointestinal illness and a body condition score of 3 out of 5 [24].

In Paraguay, wild agoutis (D. azarae) were positive for Pudica pudica, Pudica gonosoma, Durettestrongylus baudi, Fuellebornema granulosa, and Fuellebornema demarsae [25]. In several studies in Brazil, agouti parasites that were found included Trichuris spp. (cecum), Eucyathostomum copulatum, Helminthoxys urichi (cecum and intestines), Physocephalus meridionalis (large intestine) and Dipetalonema spp. (body cavity), Eucyathostomum copulatum (large intestine), Heligmostrongylus agouti, H. almeidai, Heligmostrongylus sedecimradiatus, Monodontus aguiari, Pudica pudica, Pereiraia spp., Physocephalus meridionalis, Trichuris gracilis (cecum), Raillietina trinitae (small intestine), Physaloptera toressi, P. mediospiralis (stomach), Freitastrongylus angelae (stomach), Vianella trichospicula, and Avellaria intermedia were found [26,27,28,29,30,31,32,33,34,35]. The Eimeria spp. identified were E. aguti, E. cotiae, and E. paraensis. The predilection site of these protozoan parasites was the small intestines, but none of the infected animals showed signs of illness and the fecal pellets found were of normal consistency [31]. Reported prevalences were 45.3% (24/53) for protozoan oocysts, 10.8% (7/53) for Trichuris spp. eggs, and 18.8% (10/53) for Strongyloides spp. [29].

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.

Table 1

Endoparasites found in the agouti (Dasypocta spp.) at different locations and points in time.

Parasites	Location	Effect on Animal or Pathological Lesion	Diagnostic	Year	Ref.
Strongyloides spp.	Trinidad	Not recorded	Necropsy and microscopy	1940	[20]
Stichorchis giganteus, Raillietina demerariensis var. trinitatae, Strongyloides agouti, Trichuris gracilis var. trinitatae, Acanthocheilonema spp., Fuellebornema agoutii, Pudica pudica, Aspidodera binansata var. agoutiae, Helminthoxys urichi	Trinidad	Not recorded	Necropsy and microscopy	1951	[21]
Pudica pudica, Pudica gonosoma, Durettestrongylus baudi, Fuellebornema granulosa, Fuellebornema demarsae	Paraguay	Not recorded	Necropsy and microscopy	1991	[25]
Trichuris spp., Eucyathostomum copulatum, Helminthoxys urichi, Physocephalus meridionalis, Dipetalonema spp.	Brazil	Not recorded	Necropsy and microscopy	2002	[26]
Vianella trichospicula, Avellaria intermedia	Brazil	Not recorded	Necropsy and microscopy	2006	[28]
Protozoan oocysts, Trichuris spp., Strongyloides spp.	Brazil	Not recorded	Coproscopy	2006	[29]
Trichuris gracilis, Helminthoxys urichi, Physaloptera torresi, P. mediospiralis, Raillietina trinitatae	Brazil	Not recorded	Necropsy, fecal floatation and microscopy	2006	[30]
E. aguti, E. cotiae, E. paraensis	Brazil	None of the infected animals showed signs of illness and faecal pellets were of normal consistency	Fecal floatation	2007	[31]
Freitastrongylus angelae	Brazil	Not recorded	Necropsy and microscopy	2007	[32]
Strongyloides agouti, Paraspidodera uncinata, Helminthoxys urichi, Pudicinae, Trichuris gracilis	Brazil	Not recorded	Necropsy and microscopy	2008	[33]
Strongylida, Rhabditidia, Giardia spp., Eimeria spp.	Brazil	Not recorded	Fecal floatation	2008	[34]
Echinococcus oligarthrus (hydatid cyst), strongyles, Strongyloides spp.	Guyana	Clinically healthy with no significant findings on bloodwork	Necropsy and microscopy	2009	[36]
Trichuris gracilis var. trintatae, Strongyloides agouti, Helminthoxys urichi, Eimeria spp., ascarid-like ova (unidentified species), trematode (unidentified species), cestode (unidentified species)	Trinidad	Presumed to the healthy animals	Necropsy, fecal floatation and microscopy	2016	[22]
Eucyathostomum copulatum	Brazil	Not recorded	Necropsy and microscopy	2016	[35]
Strongyloides spp., Trichuris spp., Paraspidodera uncinata	Trinidad	All animals were in good body condition (average score of 3 out of 5) and no history of gastrointestinal illness	Fecal floatation	2017	[23]
Trichuris spp. (2.2 × 102 eggs/gram), Strongyloides spp. (4.28 × 102 eggs/gram), Eimeria spp. (2.15 × 103 oocysts/gram)	Trinidad	No signs of gastrointestinal illness and animals having an average body condition score of 3 out of 5	Fecal floatation (Mc Master)	2018	[24]

3. Lappe (Agouti paca/Cuniculus paca)

Most of the studies on lappe were from Brazil and the following parasites were found: Heligmostrongylus sedecimradiatus, Longistriata breviscapula, Oswaldonema cruzi, Oswaldonema skrjabini, Paraspidodera uncinata, Paraspidodera spp., Pereiraia spp., Turgida torresi, Trichuris spp., and Vianella avellari. Physocephalus spp. was found in the stomach, and Strongyloides spp. and Strongylus spp. were found in the small intestine. Heligmostrongylus agouti and Physocephalus meridionalis were found in the stomach and Echinococcus vogeli and Calodium hepaticum were found in the liver [26,27,39].

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].

In a few other countries, the Strongyloides spp. were found [43]. In Costa Rica, Strongyloides spp., Strongylida, Eimeria agouti, Capillaria spp., Ascaroidea, Taenia spp., and Trichuris spp. were found in the gastrointestinal tracts [44]. In Mexico, Strongyloides spp., Strongylida, Trichuris spp., and Eucoccidia were found [45] and in Venezuela, Raillietina demerariensis (a cestode) was found [46].

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.

Table 2

Endoparasites found in the lappe (Cuniculus paca/Agouti paca) at different locations.

Parasites	Location	Effect on Animal or Pathological Lesion	Diagnosis	Year	References
Heligmostrongylus sedecimradiatus, Longistriata breviscapula, Oswaldonema cruzi, Oswaldonema skrjabini, Paraspidodera uncinata, Paraspidodera spp., Pereiraia spp., Turgida torresi, Trichuris spp., Vianella avellari	Brazil	Not recorded	Necropsy and microscopy	1997	[27]
Strongyloides spp., Strongylus spp., Heligmostrongylus agouti, Physocephalus meridionalis	Brazil	Not recorded	Necropsy and microscopy	2002	[26]
Echinococcus vogeli, Calodium hepaticum	Brazil	Liver fibrosis with an infiltrate of lymphocytes and macrophages	Necropsy and microscopy	2013	[39]
Physocephalus spp.	Brazil (Tocantins)	Congestion, interstitial hemorrhaging, and mononuclear infiltrates	Necropsy and microscopy	2012	[40]
Eimeria spp., Strongyloides spp., Trichuris spp., Hymenolepis diminuta	Brazil	Not recorded	Fecal floatation	2018	[41]
Strongyloides spp.	Brazil (Sao Luis)	Not recorded	Necropsy and microscopy	2018	[43]
Strongyloides spp., Strongyloidea, Eimeria agouti, Capillaria spp., Ascaroidea, Taenia spp., Trichuris spp.	Costa Rica	Not recorded	Necropsy and microscopy	1991	[44]
Strongyloides spp. Strongylida, Trichuris spp., Eucoccidia	Mexico	Not recorded	Coproscopy	2001	[45]
Raillietina demerariensis	Venezuela	Not recorded	Necropsy and microscopy	1988	[46]
Echinococcus spp.	Columbia	Cysts found in liver and peritoneum	Necropsy and microscopy	1979	[47]
Echinococcus vogeli	Bolivia	Not recorded	Necropsy and microscopy	1988, 2013	[48,49]

4. 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].

In Brazil, numerous studies have been conducted on the gastrointestinal parasites of capybaras. Taxorchis schistocotyle, Cruorifilaria tuberocauda, Eucoleus hydrochoeri, Echinocoleus hydrochaeri, Habronema clarki, Hydrochoerisnema anomalobursata, Protozoophaga obesa, Strongyloides chapini, Trichostrongylus axei, Vianella hydrochoeri, Yatesia hydrochoerus, Monecocestus hagmanni, M. hydrochoeri, M. macrobursatum, M. hagmani, and H. fuelleborni have been found in capybaras. Capillaria hydrochoeri, Philophthalmus lachrymosus, Hippocrepis hippocrepis, Neocotyle neocotyle, Fasciola hepatica, Nudacotyle tertius, Nudacotyle valdevaginatus, Taxorchis schistocotyle, Eimeria ichiloensis, Fasciola hepatica, Eimeria spp., cestodes, Trichostrongylidae, Capillaria spp., Anoplochephalidae, Ascaridae, and M. jacobi have also been found [27,35,61,62,63,64,65,66,67,68].

Three more detailed studies on both juvenile and adult capybaras located the helminths at their predilection sites: Trichostrongylus axei (stomach and small intestines), Vianella hydrochoeri (stomach and small intestines), Strongyloides chapini (stomach and small intestines), Yatesia hydrochoerus, Cruorifilaria tubercauda, and Capillaria hydrochoeri (stomach and small intestines), Protozoophaga obesa (pyloric region of the stomach, cecum, colon, and rectum), Taxorchis schistocotyle (small and large intestines including cecum), Hippocrepis hippocrepis (small intestine, colon, and rectum), Nudacotyle tertius and Monoecocestus hydrochoeri (small intestines), Hydrochoerisnema anomalobursata (stomach and small intestine), Monoecocestus hagmanni (small intestine), M. macrobursatum (small intestine), Monoecocestus hagmanni (small intestine), and Philophthalmus lachrymosus (vitreous humour). Stongyloides spp. (stomach), Habronema spp. (stomach), Vianella hydrochoeri (stomach and small intestine), Hydrochoeristrema cabrali (cecum) [66,69,70,71] and S. chapini had a higher prevalence in juvenile animals in comparison with adults, while for Y. hydrochoerus and C. hydrochoerid, the opposite was recorded [69].

A more epidemiology-based study on 45 samples showed that 5.52% of the samples were positive for C. parvum [72], while another study showed that, of the 250 samples tested, 52.4% were positive for Eimeria trinidadensis, Eimeria ichiloensis, Eimeria boliviensis, and Eimeria araside [73]. Nine percent of 134 capybaras were found positive for Fasciola hepatica [74]. In 31 free ranging capybaras, 58% were positive for Protozoophaga spp., 23% for Vianella spp., 10% for Strongyloides spp., and 10% for Ancylostomatidae [75]. In Argentina, about 70% of the capybaras were found positive for endparasites and infections with multiple parasites and protozoa were higher in young animals and in spring. Parasites found included: Eimeria spp., Blastocystis spp., Balantidium coli, Ascaridia, Trichostrongylidae, Protozoophaga obesa, Strongyloides spp., Capillaria hydrochoaeri, Monoecocestus hydrochoerid, and Taxorchis schistocotyle [76]. Other studies in Argentina found Fasciola hepatica, Echinocoleus hydrochoerid, and Taxorchis schistocotyle [77,78]. In 2019, a new species named Trichuris cutillasae was identified in the cecum of capybaras [79].

In Bolivia, in the mid 1990, helminths including Monoecocestus hagmanni, M. hydrochoeri, M. macrobursatum, Habronema clarki, Vianella hydochoeri, Protozoophaga obesa, Taxorchis schistocotyle, and Hippocrepis hippocrepis were found [80], while the protozoa found were Eimeria trinidadensis, E. ichiloensis, and E. boliviensis [81]. A more detailed study in Venezuela found a negative association between the body condition and helminth intensity for M. macrobursatum (found in the small intestine), V. hydrochoeri (small intestine), and H. hippocrepis (large intestine) [82]. Other parasites found were Monoecocestus hagmanni (small intestine), Protozoophaga obesa (cecum), Taxorchis schistocotyle (cecum), Hippocrepis hippocrepis, Eimeria trinidadensis, E. ichiloensis, and E. boliviensis [81,82]. In Columbia, the following protozoan parasites were identified: Sarcocystis spp., Eimeria spp., Giardia spp., Cycloposthium hydrochaeri, C. incurvum, C. minutum, C. lenticularis, and C. compressum [83].

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).

Table 3

Endoparasites found in the Capybara (Hydrochoeris hydrochaeris) at different locations.

Parasite	Location	Effect on Animal Health or Pathological Lesion	Diagnosis	Year	Ref.
Taxorchis schistocotyle	Panama	No lesions were observed in the intestinal tract	Necropsy and microscopy	1935	[57]
Balantidium coli	Florida	Ulceration on colon with infiltration of plasma cells, eosinophils and macrophages	Necropsy and histology	1961	[58]
Taxorchis schostocotyle, Protozoophaga obesa	Brazil	Not recorded	Necropsy and microscopy	2016	[35]
Cruorifilaria tuberocauda, Eucoleus hydrochoeri, Echinocoleus hydrochaeri, Habronema clarki, Hydrochoerisnema anomalobursata, Protozoophaga obesa, Strongyloides chapini, Trichostrongylus axei, Vianella hydrochoeri, Yatesia hydrochoerus	Brazil	Not recorded	Necropsy and microscopy	1997	[27]
Trichostrongylus axei, Vianella hydrochoeri, Strongyloides chapini, Yatesia hydrochoerus, Cruorifilaria tubercauda, Capillaria hydrochoeri, Protozoophaga obesa, Taxorchis schistocotyle, Hippocrepis hippocrepis, Nudacotyle tertius, Monoecocestus hydrochoeri, Monoecocestus hagmanni	Brazil	Not recorded	Necropsy and microscopy	1994	[69]
Monoecocestus hagmanni, M. hydrochoeri, M. macrobursatum, Habronema clarki, Vianella hydochoeri, Protozoophaga obesa, Taxorchis schistocotyle, Hippocrepis hippocrepis	Bolivia	Not recorded	Necropsy and microscopy	1995	[80]
Eimeria trinidadensis, E. ichiloensis, E. boliviensis	Bolivia and Venezuela	Not recorded	Necropsy and microscopy	1995	[81]
Protozoophaga obesa, Viannella hydrochoeri, Hydrochoerisnema anomalobursata, Taxorchis schistocotyle, Hippocrepis hippocrepis, Capillaria hydrochoeri, Strongyloides chapini, Monoecocestus macrobursatum, M. hydrochoeri, M. hagmani, Trichostrongylus axei, Neocotyle neocotyle, Nudacotyle valdevaginatus, N. tertius	Brazil	Not recorded	Necropsy and microscopy	2002	[62]
Stongyloides spp., Habronema spp., Capillaria hysrochoeri, Vianella hydrochoeri, Protozoophaga obesa, Taxorchis schistocotyle, Hydrochoeristrema cabrali, Monoecocestus hydrochoeris, Monoecocestus hagmani	Brazil	Not recorded	Necropsy and microscopy	2004	[70]
Eimeria spp., Blastocystis spp., Balantidium coli, Ascaridia, Trichostrongylidae, Protozoophaga obesa, Strongyloides spp., Capillaria hydrochoaeri, Monoecocestus hydrochoeri, Taxorchis schistocotyle	Argentina	Not recorded	Fecal floatation and sedimentation	2011	[76]
Echinocoleus hydrochoeri	Argentina	Not recorded	Necropsy and microscopy	2013	[78]
Protozoophaga spp., Vianella spp., Strongyloides spp., Ancylostomatidae	Brazil	Haematology and serum biochemistry showed a mild mal-nutrition and parasitism but no overt clinical signs were seen	Fecal floatation	2014	[75]
Sarcocystis spp., Eimeria spp., Giardia spp., Cycloposthium hydrochaeri, C. incurvum, C. minutum, C. lenticularis, C. compressum	Columbia	Not recorded	Fecal floatation, fecal sedimentation	2015	[83]
Hippocrepis hippocrepis, H. fuelleborni, Philophthalmus lachrymosus, Taxorchis schistocotyle, Monoecocestus macrobursatus, M. hydrochaeri, Monoecocustus spp., Anoplochephalidae, Protozoophaga obesa, Strongyloides spp.	Brazil	Not recorded	Necropsy and microscopy	2015	[66]
Capillaria hydrochoeri, Hydrochoerisnema anomalobursata, Monoecocestus hagmanni, M. macrobursatum, Protozoophaga obesa	Brazil	Not recorded	Necropsy and microscopy	2016	[71]
Fasciola hepatica, Capillaria spp.	Brazil	Not recorded	Coproscopy	2018	[68]
Trichuris cutillasae	Argentina	Not recorded	Molecular and Morphological techniques	2019	[79]

5. Manicou (Didelphis marsupialis insularis/Didelphis marsupialis)

The earliest data on endoparasites of the manicou (D. marsupialis insularis) were recorded in the early 1950s in Trinidad. In the large intestine, Aspidodera raillieti, Sublura trinitatis, Trichuris reesali, Trichuris minuta Trichuris urichi, Cruzia cameroni, Longistriata didelphis, and Viannnaia hamata were identified. In the small intestine, Fuellebornema agouti, Delicata spp., Camerostrongylus didelphis, and Capillaria spp. were recorded. Physaloptera turgida and Spirocerca cylicola (later found to be Didelphonema longispiculata [87]) were found in the stomach and small intestine. While, Helminthoxys urichi was found in the stomach [88]. The trematodes Achillurabainia recondita and Rhopalias coronatus were found in the intestines and Metadelphis evandroi was found in the bile duct [89].

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 Brazil, two hundred and twenty-four D. marsupialis were examined and fifteen animals were found with Besnoitia spp. in cystic leasions in the muscles and viscera [93]. Other parasites detected in Brazil were Capillaria spp. (palate), Eucoleus fluminensis (mouth), Trichuris minuta (large intestine), Heterostrongylus spp. (lungs), Mammomonogamus laryngeus (nostrils), and Aspidodera raillieti (large intestine). Aspidodera spp., Cruzia tentaculata, Turgida turgida (stomach), Thelazia iheringi, Dipetalonema spp. (liver cysts, peritoneum, skin), Litomosoides spp. (skin), Lagochilascaris turgida, Viannaia hamata, and Sarcocystis neurona [26,27]. S. neurona caused neurological diseases in different animal species and is also zoonotic [94]. Similar endoparasites that were found in D. marsupialis in Brazil were also found in Peru [95].

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).

Table 4

Endoparasites found in the Manicou (Didelphis marsupialis insularis/D. marsupialis) at different locations.

Parasite	Location	Effect on Animal Health or Pathological Lesion	Diagnosis	Year	Ref.
Aspidodera raillieti, Sublura trinitatis, Trichuris reesali, Trichuris minuta Trichuris urichi, Cruzia cameroni, Longistriata didelphis, Viannnaia hamata, Fuellebornema agouti, Delicata spp., Camerostrongylus didelphis, Capillaria spp., Physaloptera turgida, Spirocerca cylicola, Helminthoxys urichi	Trinidad	Not recorded	Necropsy and microscopy	1951	[88]
Didelphonema longispiculata (syn. Spirocerca cylicola)	Trinidad	Not recorded	Necropsy and microscopy	1953	[87]
Achillurabainia recondita, Rhopalias coronatus, Metadelphis evandroi	Trinidad	Not recorded	Necropsy and microscopy	1958	[89]
Isospora boughtoni, Isospora spp.	Alabama	Not recorded	Sedimentation techniques	1969	[90]
Phyaloptera turgida, Brachylaima virginianum, Cruzia americana, Capillaria aerophilia, Perostrongylus spp.	Georgia	Weak, emaciated, circling and uncoordinated	Necropsy and microscopy	1975	[91]
Didelphostrongylus hayesi	Georgia	Not recorded	Necropsy and microscopy	1976	[92]
Besnoitia spp.	Brazil	Not recorded	Necropsy and Histology	1983	[93]
Aspidodera raillieti, Cruzia tentaculata, Lagochilascaris turgida, Viannaia hamata	Brazil	Not recorded	Microscopy	1997	[27]
Capillaria spp., Eucoleus fluminensis, Trichuris minuta, Heterostrongylus spp., Mammomonogamus laryngeus, Aspidodera raillieti, Aspidodera spp., Cruzia tentaculata, Turgida turgida, Thelazia iheringi, Dipetalonema spp., Litomosoides spp.	Brazil	Not recorded	Necropsy and Microscopy	2002	[26]
Eimeria marmosopos	Costa Rica	Not recorded	Fecal floatation and microscopy	2015	[96]
E. marmosopos (1 × 105 oocyst/gram)	Costa Rica	Necrosis of cells of the small intestine	Histology	2015	[97]
Amphimerus caudaletestis, Philandrophilus magnacirrus, Rhopalias coronatus, R. macracanthus, Thaumasioscolex didelphidis, Viannaia viannai, Travassostrongylus spp., Onicola luehei, Cruzia tentaculata, Trichuris didelphis, Turgida turgida, Capillaria spp.	Mexico	Not recorded	Necropsy and Microscopy	2015	[98]
Aspidodera spp., Cruzia tentaculata	Brazil	Not recorded	Necropsy and microscopy	2016	[35]

6. Collared Peccary (Pecari tajucu/Tayassu tajacu)

The earliest study on parasites in peccaries was done in the 1930s in Texas and Moneizia bendeni and Parostertagia heterospiculum was found in the small intestine [99]. In the stomach, Physocephalus sexalatus was found and in the oesophagus, Parabronema spp. [99,100]. Much later and in the same region, Eimeria chaparralensis, Eimeria dicotylensis, Eimeria pecari, Eimeria spp., Klossia spp., Balantidium spp., Dirofilaria acutiuscula, Gongylonema baylisi, Gongylonema pulchrum, Physocephalus sexalatus, Parabronema pecariae (Stomach), Parostertagia heterospiculum, Physocephalus spp., Texicospirura turki, Moniezia benedeni, and Fascioloides magna were found [101,102,103,104,105], while another study failed to recover endoparasites [106]

In Brazil, in the late 1930s, Gonglyonema baylisi was found in the oesophagus [107] and later on Texicospiruria turki, Parabronema pecariae, Physocephalus sexalatus, Gongylonema spp., and Gongylonema baylisi detected in the stomach. Monodontus semicircularis and Moniezia benedeni in the small intestine; Eucyathostomum dentatum, Trichuris spp., and Balantidium coli in the large intestine; and Dirofilaria acutiuscula, Molineus semicircularis, Nematodirus molina, and Oesophagostomumdentatum [27,108,109]. In Peru, eggs of Ascaris spp., ancylostomatids, spirurids, Paragonimus spp., Giardia spp., Cryptosporidium spp., Balantidium spp., and Eimeria spp. were identified in the fecal samples [110,111]. It should be noted that Cryptosporidium spp. and Giardia spp. are of zoonotic importance (Table 5).

Table 5

Endoparasites found in the collared peccary (Tayassu tajacu) at different locations.

Parasite	Location	Effect on Animal Health or Pathological Lesion	Diagnostics	Year	Ref.
Moneizia bendeni	Texas	Not recorded	Necropsy	1931	[99]
Physocephalus sexalatus, Moniezia benedeni, Parostertagia heterospiculum	Texas	Not recorded	Necropsy	1933	[100]
Texicospirura turki	Texas and New Mexico	Not recorded	Necropsy	1966	[110]
Balantidium spp., Dirofilaria acutiuscula, Gongylonema baylisi, Parabronema pecariae, Parostertagia heterospiculum, Physocephalus spp., Texicospirura turki, Moniezia benedeni, Fascioloides magna	Texas	Not recorded	Necropsy	1970	[101]
Gongylonema pulchrum, Parabronema pecariae, Texicospirura turki, Physocephalus sexalatus and Moniezia benedeni	Texas	No evidence of disease or loss of body condition	Necropsy	1985	[102]
Eimeria chaparralensis, Eimeria dicotylensis, Eimeria pecari, Eimeria spp., Klossia spp.	Texas	Not recorded	Fecal floatation	1996	[103]
Ascarid suum	Texas	Respiratory distress and coughing	Necropsy	1984	[117]
Parabronema peccariae, Trichostrongylus columbiformis	Mexico	Not recorded	Necropsy	1968	[105]
Globocephalus urosubulatus, Parabronema pecariae, Parostertagia spp., Texicospiruria turki, Paramphistomum spp., Oesophagostomum spp., Moniezia benedeni	Mexico	Not recorded	Fecal floatation, sedimentation and necropsy	2008	[113]
Gonglyonema baylisi	Brazil	Not recorded	Necropsy	1937	[107]
Dirofilaria acutiuscula, Eucyathostomum dentatum, Gongylonema baylisi, Molineus semicircularis, Nematodirus molina, Oesophagostomum dentatum	Brazil	Not recorded	Necropsy	1997	[27]
Parabronema pecariae	Brazil	Not recorded	Necropsy	2000	[109]
Strongyloides spp., Eimeria spp., Isospora spp., Oesophagostomum spp.	Brazil	Not recorded	Fecal centrifugation floatation and Mc Master Technique	2014	[114]
Texicospiruria turki, Monodontus angulari, Eucyathostomum spp., Stichorchis giganteus, Moniezia benedeni, Ascaris spp., Eimeria spp.	Bolivia	Not recorded	Fecal floatation and sedimentation	2014	[116]
Entamoeba coli, Entamoeba spp., Cryptosporidium spp., Endolimax nana, Strongyloides spp.	Panama	Not recorded	Fecal centrifugation floatation	2010	[115]
Ascaris spp., ancylostomatids, spirurid, Paragonimus spp.	Peru	Not recorded	Fecal floatational and sedimentation	2008	[110]
Texicospiruria turki, Parabronema pecariae, Physocephalus sexalatus and Gongylonema spp., Monodontus semicircularis, Moniezia benedeni, Eucyathostomum dentatum, Trichuris spp., Balantidium coli	Central Amazon	Not recorded	Necropsy	1986	[108]
Toxocara alienate	Surinam	Not recorded	Necropsy	1982	[112]
Giardia spp., Cryptosporidium spp., Balantidium spp., Eimeria spp.	Brazil	Not recorded	Fecal floatation	2010	[111]

In Surinam, Toxocara alienata were found but was not associated with poor body condition [112]. In Mexico, Globocephalus urosubulatus, Parabronema pecariae, Parostertagia spp., Texicospiruria turki, and Paramphistomum spp. were detected in the stomach and Oesophagostomum spp. Strongyloides spp., Eimeria spp., Isospora spp., Oesophagostomum spp., and Moniezia benedeni inhabited the intestines [113,114]. In Panama, Entamoeba coli, Entamoeba spp., Cryptosporidium spp., Endolimax nana, and Strongyloides spp. were detected [115]. In Bolivia, Texicospiruria turki, Monodontus angulari, Eucyathostomum spp., Stichorchis giganteus, Moniezia benedeni, Ascaris spp., and Eimeria spp. were detected [116]. In the work done in mid 1980s by Hellgren et al. [117] on collared peccaries with signs of respiratory distress and coughing, Ascaris suum was found in the bile duct and the same parasite was found in South America [117,118,119].

7. Red Brocket Deer (Mazama americana)

In Trinidad, in the 1930s, Mazama simplicicornis was found to have the following parasites; Mazamanema longibursatum, Ierestrongylus filiformis, Mazamastrongylus trinitatis, Paramphistomum cotylophorum, Moniezia benedeni, Setaria bidentata, Eucyathostomum longesubulatum, Strongyloides papillosus, and Nematodirus urichi. Setaria bidentate was found in the omentum, and Eucyathostomum longesubulatum and an oxyurid-type worm was found in the large intestine [120,121,122]. In Brazil, parasites found in Mazama americana were Dictyocaulus spp., Eucyathostomum spp., Eucyathostomum longibursatum, Seteria bidentate, Seteria spp. Haemonchus contortus, Haemonchus similis, Trichostrongylus axei, Trichostrongylus colubriformis, Physocephalus sexulatus, P. lassencei, Pygarginema verrucosa, Paramphistomum spp., Eimeria spp., and Cooperia punctata [27,61,123,124] (Table 6). Lux Hoppe et al. [125] found Trichostrongylus axei, Haemonchus contortus, H. similis, Physocephalus lassancei, and Pygarginema verrucosa in the abomasum. Capillaria bovis, Bunostomum phlebotomum, and Cooperia punctata inhabited the small intestine.

Table 6

Endoparasites found in the Red Brocket deer (Mazama americana) at different locations.

Parasites	Location	Effect on Animal Health or Pathological Lesion	Diagnostic	Year	Ref.
Mazamanema longibursatum, Ierestrongylus filiformis, Mazamastrongylus trinitatis, Nematodirus urichi	Trinidad	Not recorded	Necropsy	1935	[120]
Eucyathostomum longesubulatum, Setaria bidentata, Oxyurid	Trinidad	Not recorded	Necropsy	1936	[121]
Paramphistomum cotylophorum, Moniezia benedeni, Setaria bidentata, Eucyathostomum longesubulatum, Nematodirus urichi, Mazamastrongylus trinitatis, Strongyloides papillosus	Trinidad	Not recorded	Necropsy	1936	[122]
Dictyocaulus spp., Eucyathostomum spp., Eucyathostomum longibursatum, Seteria bidentata, Seteria spp.	Brazil	Not recorded	Necropsy	1997	[27]
Haemonchus contortus, Haemonchus similis, Trichostrongylus axei, Trichostrongylus colubriformis, Cooperia punctata	Brazil	Not recorded	Necropsy	2000	[123]
Paramphistomum spp., Eimeria spp.	Brazil	Not recorded	Fecal floatation and sedimentation	2007	[124]
Trichostrongylus axei, Haemonchus contortus, H. similis, Physocephalus lassancei, Pygarginema verrucosa, Capillaria bovis, Bunostomum phlebotomum, Cooperia punctata	Brazil	Not recorded	Necropsy	2010	[125]
Cooperia punctata, Eucyathostomum spp., Haemonchus contortus, H. similis, Physocephalus sexulatus, P. lassencei, Setaria bedentata, Trichostrongylus axei, T. colubriformis, Pygarginema verrucosa	Brazil	Not recorded	Necropsy	2017	[61]
Paramphistomum cervi	Mexico	Not recorded	Necropsy	2008	[115]
Eimeria spp. and Trichuris spp., Strongyloides spp., Mammomonogamus spp.	Mexico	Not recorded	Fecal floatation and Necropsy	2014	[116]
Taeinia hydatigena	Peru	Not recorded	Necropsy	2015	[126]

In Mexico, Paramphistomum cervi was found in the rumen and abomasum as well as Eimeria spp., Trichuris spp., Strongyloides spp., and Mammomonogamus spp. [115,116] (Table 6). In Peru, the cysticercus of Taenia hydatigena was found in the omentum of M. americana as an intermediate host, while the definitive hosts were identified as carnivores [126]. A summary of endoparasites found in specific neo-tropical host species was provided (Table 7). Endoparasites that were common to different animal (host) was also listed (Table 7).

Table 7

Endoparasites found in selected non-domesticated neotropical animals.

Neotropical Animals Species (Hosts)	Total No. of Internal Parasites Reported	Endoparasites Found in the Six Selected Host Species	Similar Endoparasites Found in Various Neotropical Animal Host Species
Agouti (D. leporina)	29	Strongyloides spp., Stichorchis giganteus, Raillietina demerariensis var. trinitatae, Strongyloides agouti, Trichuris gracilis var. trinitatae, Trichuris spp., Acanthocheilonema spp., Fuellebornema agouti, Pudica pudica, Aspidodera binansata var. agouti, Helminthoxys urichi, Paraspidodera uncinata, Pudica gonosoma, Durettestrongylus baudi, Fuellebornema granulosa, Fuellebornema demarsae, Eucyathostomum copulatum, Physocephalus meridonalis, Physocephalus torresi, Physocephalus mediospiralis, Diptalonema spp., Vianella trichospicula, Avellaria intermedia, Eimeria aguti, Eimeria cotiae, Eimeria paraensis, Eimeria spp., Giardia spp., Echinococcus oligarthrus, Freitastrongylus angelae	Helminthoxys urichi (manicou and agouti)Paraspidodera uncinata, Trichuris spp., Strongyloides spp., Physocephalus meridonalis, Eimeria agouti, Raillietina demarariensis, Eimeria spp., (agouti and lappe)
Lappe (A. paca)	24	Heligmostrongylus sedecimradiatus, Heligmostrongylus agouti, Longistriata breviscapula, Oswaldonema cruzi, Oswaldonema skrjabini, Paraspidodera uncinata, Paraspidodera spp., Pereiraia spp., Turgida torresi, Trichuris spp., Vianella avellari, Strongyloides spp., Strongylus spp., Physocephalus meridonalis, Echinococcus vogeli, Coladium hepaticum, Physocephalus spp., Eimeria spp., Hymenolepis diminuta, Eimeria agouti, Capillaria spp., Taenia spp., Raillietina demarariensis, Echinococcus spp.	Strongyloides spp., Giardia spp., Eimeria spp. (agouti, lappe, capybara, and collared peccary)
Capybara (H. hydrochaeris)	42	Taxorchis schistocotyle, Balantidium coli, Protozoophaga obesa, Cruorifilaria tuberocauda, Eucoleus hydrochoeri, Echinocoleus hydrochaeri, Habronema clarki, Habronema spp., Hydrochoerisnema anomalobursata, Strongyloides chapini, Strongyloides spp., Trichostrongylus axei, Vianella hydrochoeri, Vianella spp., Yatesia hydrochoerus, Hippocrepis hippocrepis, Hippocrepis fuelleborni, Philophthalmus lachrymosus, Neocotyle neocotyle, Nudacotyle valdevaginatus, Nudacotyle tertius, Monoecocestus hydrochoeri, Monoecocestus hagmanni, Monoecocestus macrobursatum, Monoecocestus spp., Eimeria trinidadensis, Eimeria ichiloensis, Eimeria boliviensis, Eimeria spp., Blastocystis spp., Sarcocystis spp., Giardia spp., Cycloposthium hydrochaeri, Cycloposthium incurvum, Cycloposthium minutum, Cyclposthium lenticularis, Cycloposthium compressum, Fasciola hepatica, Capillaria spp., Trichuris cutillasae	Trichostongylus columbiformis, Strongyloides spp., Eimeria spp., Physocephalus sexulatus, Trichuris spp., Moniezia benedeni, Paramphisotmum spp. (capybara and red brocket deer)Capillaria spp. (capybara and manicou)Balantidium coli, Giardia spp., (common to capybara and collared peccary)
Manicou (D. marsupialis insularis)	44	Aspidodera raillieti, Aspidodera spp., Sublura trinitatis, Trichuris reesali, Trichuris minuta, Trichuris urichi, Trichuris didelphis, Cruzia cameroni, Cruzia americana, Cruzia tentaculata, Longistrata didelphis, Viannaia hamata, Viannaia viannai, Fuellebornema agouti, Delicata spp., Travassostrongylus spp., Camerostrongylus didelphis, Capillaria aerophilia, Capillaria spp., Physaleptera turgida, Spirocerca cylicola, Helminthoxys urichi, Achillurabainia recondite, Rhopalias coronatus, Metadelphis evandroi, Isospora boughtoni, Isospora spp., Brachylaima virginianum, Perostrongylus spp., Heterostrongylus spp., Didelphostrongylus hayesi, Besnoitia spp., Lagochilascaris turgida, Eucoleus fluminensis, Mammomonogamus laryngeus, Turgida turgida, Thelazia iheringi, Diptalonema spp., Litomosoides spp., Eimeria marmosopos, Amphimerus caudaletestis, Philandrophilus magnacirrus, Thaumasioscolex didelphidis, Onicola luehei	Trichostongylus columbiformis, Strongyloides spp., Eimeria spp., Physocephalus sexulatus, Trichuris spp., Moniezia benedeni, Paramphisotmum spp. (capybara and red brocket deer)Capillaria spp. (capybara and manicou)Balantidium coli, Giardia spp., (common to capybara and collared peccary)
Collared peccary (T. tajacu)	39	Moniezia benedeni, Physocephalus sexalatus, Physocephalus spp., Parostertagia heterospiculum, Texicospirura turki, Balantidium coli, Dirofilaria acutiuscula, Gongylonema baylisi, Gongylonema pulchrum, Parabronema pecariae, Fascioloides magna, Eimeria chaparrelensis, Eimeria dicotylensis, Eimeria pecari, Eimeria spp., Isospora spp., Klossia spp., Ascaris suum, Ascaris spp., Trichostrongylus columbiformis, Globocephalus urosubulatus, Paramphistomum spp., Oesophagostomum spp., Oesophagostomum dentatum, Nematodirus molina, Eucyathostomum dentatum, Eucyathostomum spp., Stichorchis giganteus, Molineus semicircularis, Strongyloides spp., Paragonimus spp., Monodontus angularis, Entamoeba coli, Entamoeba spp., Cryptosporidium spp., Endolimax nana, Trichuris spp., Toxocara alienata, Giardia spp.	Trichurs spp., Strongyloides spp., Eimeria spp., Giardia spp., Stichorchis giganteus (agouti and collared peccary)
Red Brocket deer (M. americana)	30	Mazamanema longibursatum, Ierestrongylus filiformis, Mazamastrongylus trinitatis, Nematodirus urichi, Eucyathostomum longesubulatum, Eucyathostomum spp., Setaria bidentata, Setaria spp., Paramphistomum cotylophorum, Paramphistomum cervi, Paramphistomum spp., Moniezia benedeni, Strongyloides papillosus, Strongyloides spp., Dictyocaulus spp., Haemonchus contortus, Haemonchus similis, Trichostrongylus axei, Trichostrongylus columbiformis, Cooperia punctata, Eimeria spp., Physocephalus lassancei, Physocephalus sexalatus, Pygarginema verrucosa, Capillaria bovis, Bunostomum phlebotomum, Trichuris spp., Taenia spp., Mammomonogamus spp.	Trichuris spp., Strongyloides spp., Eimeria spp. (agouti and red brocket deer)Strongyloides spp., Eimeria spp. (lappe and red brocket deer)

8. 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.