Primata

Roque, André Luiz R. & Jansen, Ana Maria, 2014, Wild and synanthropic reservoirs of Leishmania species in the Americas, International Journal for Parasitology: Parasites and Wildlife 3 (3), pp. 251-262 : 258

4.6. Order Primata

Nonhuman primates can be divided in two groups: the catarrhines (infraorder Catarrhini ), from Africa, Europe and Asia (Old World Primates) and the platyrrhines ( Platyrrhini ) from the Americas (New World or Neotropical Primates). The main difference between them is that the catarrhines have upside-down nostrils on a long snout, while platyrrhines have laterally-faced nostrils on a shorter snout ( Verona and Pissinatti, 2007). The different species of neotropical primates are included in the families Cebidae (tamarins) and Callitrichidae (marmosets), although some classifications also recognize three other families: Aotidae , Pithecidae and Atelidae . The neotropical primates occupy distinct arboreal strata and consume diverse diets, including species that feed on fruits, invertebrates and even small mammals ( Verona and Pissinatti, 2007).

To date, few studies have described natural infection by Leishmania parasites in neotropical primates. Infection by L. shawi was described in the tufted capuchin monkey Cebus apella and the bearded saki Chiropotes satanas (Lainson et al., 1989) , while infection by Leishmania (Viannia) sp. was recently demonstrated in four Argentinean owl monkeys Aotus azarai ( Acardi et al., 2013) . In Panamá, Geoffroy’s tamarin Saguinus geoffroyi and the owl monkey Aotus trivirgatus were found to be infected with L. amazonensis and L. braziliensis , respectively ( Herrer and Christensen, 1976; Herrer et al., 1973). In a Brazilian zoo, one black-fronted titi Callicebus nigrifrons from Belo Horizonte/MG presented with a fatal disease that resembled visceral leishmaniasis. Histological and immunohistochemical examinations, as well as a PCR specific for parasites from the L. donovani complex, confirmed infection with L. infantum ( Malta et al., 2010). The other primate species that had PCR-positive blood samples in the same study were Alouatta guariba , Cebus xanthosternos, Leonthopitecus crysomelas, Aotus nigriceps , Pithecia irrorata and Saguinus imperator ( Malta et al., 2010). In the zoo in Bauru/SP, Leishmania amazonensis was detected by PCR-RFLP in a spider monkey Ateles paniscus from the endemic Amazon region ( Lima et al., 2012b) ( Table 1).

Leishmania species that circulate in the Americas have been demonstrated to infect other neotropical primates, but only under experimental conditions. Most of these studies focused on the immune response to different drug treatments or on vaccine development. For many years, black-tufted marmosets Callithrix penicillata were used in experimental studies with L. braziliensis and L. amazonensis ( Cuba et al., 1990; Cuba-Cuba and Marsden, 1993). Experimental infection of the common squirrel monkey Saimiri sciureus resulted in non-ulcerated skin lesions from which L. braziliensis and/or L. panamensis could be re-isolated ( Pung et al., 1988). Owl monkeys Aotus trivirgatus developed localized cutaneous lesions after experimental infection with L. braziliensis , L. mexicana and L. panamensis ( Christensen and de Vasquez, 1981; Lujan et al., 1986). Cebus apella developed skin lesions after experimental infection with L. lainsoni , L. amazonensis , L. braziliensis , L. mexicana and L. guyanensis ( Garcez et al., 2002; Grimaldi, 2008). Conversely, Cebus nigrivittatus developed fatal disease when experimentally infected with L. infantum ( Vouldoukis et al., 1986) .

All neotropical primates are included in the list of the “Convention on International Trade in Endangered Species of Wild Fauna and Flora” (CITES), indicating that all are vulnerable to some degree ( Verona and Pissinatti, 2007). For this reason, many species such as the golden lion tamarin Leonthopitecus rosalia are included in conservation programs. These programs often include exchange, translocation and re-introduction of animals without consideration of their parasite fauna, here including Leishmania and other trypanosomatids. Data from naturally infected primates demonstrate that these mammals may be involved in the maintenance of Leishmania in the wild, especially considering their ecology, species transmitted in the canopy. Taking into account the transmission cycle of these parasites, a lack of knowledge regarding the health status of the relocated primates may result in the introduction of infected mammals into a given area, promoting the establishment of new transmission cycles ( Lisboa et al., 2006).