Taxonomic summary

Trypanoxyuris (Paraoxyuronema)lagothricis (^{Buckley, 1931}) ^{Hugot et al., 1999} (Figure 1, Table 1).

Figure 1.  Trypanoxyuris (Paraoxyuronema)lagothricis found in Lagothrix cana from Brazil. (a-f) female: (a) total view, (b) anterior region, lateral view, (c) apical end, en faceview, (d) anterior region, detail of extremity, ventral view, (e) tail, lateral view; (f) detail of ovejector, lateral view. (g) Egg found in the feces. (h-l) male: (h) total view, (i) posterior region, lateral view, (j) anterior region, ventral view, (k) apical end, en face view, (l) tail, ventral view. 

(Syn.: Enterobius lagothricis ^{Buckley, 1931}, Trypanoxyuris(Trypanoxyuris) lagothricis (^{Buckley, 1931}) Inglis &Cosgrove, 1965)

Host: Lagothrix cana (É. Geoffroy, 1812) (Primates, Atelidae), Gray Woolly Monkey.

Locality: Brazilian Amazon, undetermined locality.

Site of infection: large intestine.

Intensity of infection: 64 parasites (17 males, 47 females).

Specimens deposited: DPIC 2467.

Remarks: Trypanoxyuris(Paraoxyuronema) lagothricis was described from a single infected specimen of Lagothrix lagotricha (Humboldt, 1812) (= Lagothrix humboldtii É. Geoffroy, 1812) originated from South America and taken to a London zoo (^{BUCKLEY, 1931}). Later, the species was reported in L. lagotrichain Venezuela and Peru, and in L. cana, also in Peru (^{INGLIS; Dí AZ-UNGRIA, 1960}; ^{INGLIS; DUNN, 1964}; ^{HUGOT, 1985}; ^{TANTALEAN et al., 1990}). This is the first report on the occurrence of this parasite in Brazil. The measures (Table 1) and morphological features of the specimens studied, as well as the structural arrangement of the buccal cavity, the presence of ventral esophageal teeth with a small apical end, and the shape of male bursa and female ovejector are in agreement with those reported for T. (P.)lagothricis by ^{Buckley (1931)} and ^{Hugot (1985)}. In relation to other species of Trypanoxyuris reported in Brazilian primates, T. (P.) lagothricisdiffers from the species belonging to subgenera Hapaloxyuris andTrypanoxyuris by presenting two lips instead of three. Moreover, T. (P.) lagothricispresents measures of both males and females significantly smaller than the five other species from other subgenera previously reported in Brazil. In relation toT. (P.) brachytelesi, a species described based only on female parasites and with buccal structure not studied, T. (P.) lagothricispresents structures also significantly smaller. Regarding other species of the subgenus Paraoxyuronema not yet reported in Brazil,T. (P.) lagothricis can be easily distinguished from T. (P.)duplicidens which presents several larger measures, mainly the length of esophagus, teeth subdivided by a deep groove, and lacks a terminal spine in the male; the species reported in the present study also differ fromT. (P.) atelis in which presents greater total length, and ventral esophageal teeth with a verrucose ornamentation instead a small apical point (^{HUGOT, 1985}).

The clinical manifestations verified in the infection withTrypanoxyuris as well as other pinworm infections are not significant in most cases. Anal itching and irritation, irritability, agitation, and aggressiveness of the host are the clinical signs usually verified during the course of the disease (^{TOFT II, 1982}). However, the occurrence of high parasitic burden and erratic parasitism has been observed and, in some cases, it may be associated with the death of the host (^{MURATA et al., 2002}; ^{AMATO et al., 2002}; ^{FOX et al., 2002}). In the present study, there was no evidence that infection with T.(P.) lagothricis was associated with the death of the specimen studied. In fact, during the necropsy of the primate, there were no gross changes such as edema, hyperemia, or mucosal lesions of the caecum, colon and rectum of the animal, at least in part, due to low intensity of infection.

Considering the biology of these oxyurids, conditions of captivity and close contact between primates may favor the transmission and maintenance of the parasite (^{FELT; WHITE, 2005}; ^{BARROS MONTEIRO et al., 2009}). Indeed,T. (P.) lagothricis was first described and found in animals from zoos (^{BUCKLEY, 1931}; ^{HUGOT, 1985}). Similarly, the specimen of L. cana studied was kept for an unknown period of time under illegal captivity before being confiscated.

Under an evolutionary approach, studies of primate oxyurids have provided evidence of the process of coevolution between these parasites and their hosts.^{Cameron (1929)} was the first to find high host specificity in this group of nematodes, suggesting that each species of these parasites would occur in specific groups of primates. Evidence for this phenomenon was subsequently obtained for genera belonging to the subfamily Enterobiinae, including Trypanoxyuris (^{BROOKS; GLEN, 1982}; ^{HUGOT et al., 1996};^{HUGOT, 1998}, ¹⁹⁹⁹).

Given the close evolutionary relationship betweenTrypanoxyuris and their platyrrhine hosts, as well as reports of infection of these primates in other South American countries with species not yet recorded in Brazil, it is possible that the diversity of these oxyurids occurring in the country could be underestimated. In this regard, at least nine other species of Trypanoxyuris, which have already been reported in South American primates, may still be found in Brazil: T.(T.) trypanuris Vevers, 1923 inPithecia spp. (Primates: Pitheciidae); T.(H.) goldii (Inglis &Coosgrove, 1965) inCallimico spp. (Primates: Cebidae); T.(H.) tamarini (^{Inglis &Dunn, 1964}) and T. (H.)oedipi in Saguinus spp. (Primates: Cebidae);T. (P.) atelis (^{Cameron, 1929}) in Ateles spp. (Primates: Atelidae); T. (P.)duplicidens (^{Buckley, 1931}) in Lagothrix spp.; T.(T.) satanas ^{Hugot, 1985} in Chiropotesspp. (Primates: Pitheciidae); T. (T.)croizati Hugot, Morand &Guerrero, 1994 andT. (T.) callicebi Hugot &Vaucher, 1985 in Callicebus spp. (Primates: Cebidae). Moreover, primates belonging to the genera Leontopithecus Lesson, 1840, Cebuella Gray, 1866 (Primates: Cebidae) andCacajao Lesson, 1840 (Primates: Pitheciidae) have not yet been reported infected with Trypanoxyuris (^{HUGOT, 1999}), and they may be hosts of unknown species.

Overall, the study of helminth parasites from primates in Brazil is fragmented. Although the Brazilian primate fauna currently comprises 118 species (^{PAGLIA et al., 2012}), most primate species have not yet been evaluated for infection by parasites. So far, only 27 species of nematodes have been reported in 36 species of primates in the country, and only four nematodes species in primates of the genus Lagothrix(revised by ^{VICENTE et al., 1997}; ^{PINTO et al., 2011}). On the other hand, the reduction of natural habitats and illegal hunting have contributed to a substantial number of endangered primate species (26) in Brazil (^{CHIARELLO et al., 2008}). In fact, the reduction of populations, and even extinction of hosts, can also be related to the co-extinction of parasite species (^{WHITEMAN; PARKER, 2005}; ^{DOBSON et al., 2008}; ^{MUNIZ-PEREIRA et al., 2009}). Thus, it is possible that other species of Trypanoxyuris and several other parasitic interactions be eliminated before they become known. In this way, conservation of primate species is important for the maintenance of these parasite species. Furthermore, the scientific interaction between primatologists and helminthologists should be encouraged to maximize achievement on parasitological information, thereby contributing to increase the knowledge on the biodiversity of helminths from primates in Brazil.