Didelphimorphia, Gill, 1872

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 : 253-255

4.1. Order Didelphimorphia

The autochthonous American order Didelphimorphia is the only marsupial order recognized in the Americas. Mammals from this order have a wide distribution, mainly due to their remarkable adaptability to different ecological niches, particularly to environments with a high degree of human activity. The genus Didelphis is the most widely dispersed on the continent, occurring from southeastern Canada to southern Argentina ( Austad, 1988). Didelphis spp. are nomadic, solitary (mainly males), and excellent climbers that are mainly found in holes in trees and foliage. These animals can colonize ceilings of houses and other shelters in domestic and peridomestic areas, where they feed on human food garbage ( Austad, 1988; Olifiers et al., 2005). Most likely due to its synanthropic character, this species is one of most studied regarding infection by Leishmania spp. , although only a few of these studies included follow up on the natural or experimental infection ( Travi et al., 1994, 1998b).

Didelphis marsupialis , a species distributed from Mexico to the Amazon region has been found to be infected with at least four Leishmania species ( Arias et al., 1981; Corredor et al., 1989; Grimaldi et al., 1991) ( Table 1). Its importance as a potential reservoir for L. infantum was demonstrated in a rural community from Colombia, where these animals were abundant, and displayed a high prevalence of positive cultures and high parasite loads (as observed in slide imprints), in the spleen ( Corredor et al., 1989). Later studies also confirmed their importance elsewhere in Colombia and Venezuela ( Quinnell and Courtenay, 2009; Travi et al., 1998a). Additionally, its importance as a reservoir was confirmed by the experimental infection by L. infantum of five specimens, which resulted in clinical signs suggestive of visceral leishmaniasis in one young female that presented amastigote parasites in the spleen, liver and lymph nodes. Parasites were re-isolated from all of these specimens, and three were also infective for Lu. longipalpis ( Travi et al., 1998b) .

Didelphis albiventris is abundant in central South America, from Colombia to northern Argentina, and is quite abundant in northeastern, central and southern Brazil. L. infantum isolation from this marsupial species was first described in Bahia, Brazil ( Sherlock et al., 1984). Later, the same authors demonstrated its infectivity to vectors by xenodiagnosis ( Sherlock, 1996), and others reported their natural

Mammal host species described infected by different Leishmania species in the Americas.

Order Host species Leishmania species Infection pattern Country References

Didelphimorphia Didelphis marsupialis L. infantum Potential reservoir CO, VE Corredor et al., 1989; apud Quinnell and Courtenay, 2009

L. amazonensis Parasite host BR Grimaldi et al., 1991

L. guyanensis Potential reservoir BR; FG Arias et al., 1981; Dedet et al., 1989

L. forattinii Parasite host BR IOCL 0067

D. albiventris L. infantum Potential reservoir BR Sherlock et al., 1984; Sherlock, 1996

L. braziliensis Parasite host BR Quaresma et al., 2011

L. peruviana Potential reservoir PE Llanos-Cuentas et al., 1999

D. aurita L. infantum Parasite host BR Carreira et al., 2012

Philander opossum L. amazonensis Parasite host BR Lainson et al., 1981a

Marmosa cinerea L. amazonensis Parasite host BR Arias et al., 1981

Marmosa sp L. (Viannia) sp. Parasite host BR Brandão-Filho et al., 2003

Micoreus paraguayanus L. amazoensis Parasite host BR Quintal et al., 2011

L. braziliensis Parasite host BR Quintal et al., 2011

Gracilinanus agilis L. braziliensis Parasite host BR Quaresma et al., 2011

Marmosops incanus L. guyanensis Parasite host BR Quaresma et al., 2011

Metachirus nudicaudatus L. amazonensis Parasite host BR Lainson et al., 1981a

Monodelphis domestica L. (Viannia) sp. Parasite host BR Lima et al., 2013

Pilosa Choloepus didactylus L. guyanensis Potential reservoir FG; BR Gentile et al., 1981; Lainson et al., 1981a

L. shawi Parasite host BR Lainson et al., 1989

C. hoffmanni L. colombiensis Parasite host PN Kreutzer et al., 1991

L. equatoriensis Parasite host EC Grimaldi et al., 1992

L. panamensis Parasite host PN apud Ashford, 2000

Bradypus tridactylus L. shawi Parasite host BR Lainson et al., 1989

Tamandua tetradactyla L. guyanensis Parasite host BR Lainson et al., 1981a

L. amazonensis Parasite host EC Mimori et al., 1989

L. infantum Parasite host BR Araújo et al., 2013

Cingulata Dasypus novemcinctus L. naiffi Potential reservoir BR Lainson and Shaw, 1989; Naiff et al., 1991

L. guyanensis Parasite host BR Lainson et al., 1979

Rodentia Proechimys species L. amazonensis Potential reservoir BR; FG Arias et al., 1981; Dedet et al., 1989

L. guyanensis Parasite host BR; FG Dedet et al., 1989; Lainson et al., 1981b

P. canicollis L. infantum Parasite host CO Travi et al., 1998a

P. semispinosus L. panamensis Potential reservoir CO Travi et al., 2002

L. infantum Parasite host CO Travi et al., 2002

Thrichomys apereoides L. braziliensis Parasite host BR Quaresma et al., 2011

L. guyanensis Parasite host BR Quaresma et al., 2011

L. infantum Parasite host BR Oliveira et al., 2005; Quaresma et al., 2011

L. amazonensis Parasite host BR Oliveira et al., 2005

T. laurentius L. infantum Potential reservoir BR Roque et al., 2010

L. braziliensis Potential reservoir BR Roque et al., 2010

L. naiffi Parasite host BR Cássia-Pires, unpublished data

L. shawi Parasite host BR Cássia-Pires, unpublished data

T. inermis L. shawi Parasite host BR Cássia-Pires, unpublished data

T. pachyurus L. naiffi Parasite host BR Cássia-Pires, unpublished data

Nectomys squamipes L. infantum Parasite host BR Dantas-Torres and Brandao-Filho, 2006

L. braziliensis Parasite host BR Peterson et al., 1988

Rattus rattus L. infantum Parasite host BR; VE apud Quinnell and Courtenay, 2009

L. braziliensis Potential reservoir BR; VE Vasconcelos et al., 1994; De Lima et al., 2002

L. mexicana Parasite host VE De Lima et al., 2002

Clyomys laticeps L. infantum Parasite host BR Cássia-Pires, unpublished data

Dasyprocta azarae L. infantum Parasite host BR Cássia-Pires, unpublished data

Dasyprocta sp. L. amazonensis Parasite host BR Lainson et al., 1981b

Rhipidomys mastacalis L. infantum Parasite host BR Quaresma et al., 2011

Coendu sp. L. lainsoni Parasite host BR IOCL 1058

L. hertigi / L. deanei Parasite host PN; BR Herrer, 1971; Silva et al., 2013

Coendu prehensilis L. infantum Parasite host BO Le Pont et al., 1989

Akodon arviculoides L. braziliensis Parasite host BR Forattini et al., 1972; Rocha et al., 1988

Akodon sp. L. amazonensis Parasite host BO Telleria et al., 1999

Necromys lasiurus L. braziliensis Potential reservoir BR Brandão-Filho et al., 2003; de Freitas et al., 2012 Sigmodon hispidus L. braziliensis Potential reservoir VE De Lima et al., 2002

L. mexicana Potential reservoir MX, VE Van Wynsberghe et al., 2000; De Lima et al., 2002 Holochilus scieurus L. infantum Parasite host BR Lima et al., 2013

H. scieurus L. (Viannia) sp. Parasite host BR Brandão-Filho et al., 2003

Cerradomys subflavus L. (Viannia) sp. Parasite host BR Lima et al., 2013

Mus musculus L. braziliensis Parasite host BR de Freitas et al., 2012

Oryzomys species L. amazonensis Parasite host BO Kerr et al., 2006

O. melanotis L. amazonensis Potential reservoir MX Van Wynsberghe et al., 2000

O. nigripes L. braziliensis Parasite host BR Forattini et al., 1972

Oligoryzomys sp. L. amazonensis Parasite host BO Telleria et al., 1999

Sciurus vulgaris L. amazonensis Parasite host EC Mimori et al., 1989

S. granatensis L. equatorensis Parasite host EC Grimaldi et al., 1992

Neotoma species L. mexicana Potential reservoir US Kerr et al., 1995; Raymond et al., 2003

Ototylomys phyllotis L. mexicana Potential reservoir BE; MX Ashford, 1996; Van Wynsberghe et al., 2000

Heteromys species L. mexicana Parasite host BE; MX Ashford, 1996; Van Wynsberghe et al., 2009 H. dermarestianus L. panamensis Parasite host CR Zeledon et al., 1977

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infection detected by PCR ( Humberg et al., 2012; Santiago et al., 2007). The other Leishmania species found infecting D. albiventris are L. braziliensis ( Quaresma et al., 2011) and L. peruviana ( Llanos-Cuentas et al., 1999) ( Table 1).

L. infantum has also been detected in D. aurita ( Carreira et al., 2012) , and another study also strongly suggests such infection in the periphery of urban areas ( Santiago et al., 2007). Although its role as a reservoir has not yet been demonstrated, it has strong potential to act as a reservoir due to the great phylogenetic proximity among the Didelphis species ( Jansa et al., 2014). A unique study on a marsupial species able to explore distinct forest strata, the opossum Philander opossum , described its infection by L. amazonensis ( Lainson et al., 1981a) . The Leishmania species found infecting other marsupial species are described in Table 1 ( Quintal et al., 2011).

Apart from the Didelphis species, which are proven as potential Leishmania reservoirs, other marsupial species are poorly studied. These ancient mammals are perhaps the very first Leishmania spp. hosts in the Americas, although their role in transmission net remains to be defined.