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Natural infection of Evandromyia lenti (Mangabeira) (Diptera: Psychodidae) by Psychodiella chagasi (Adler & Mayrink) (Apicomplexa: Lecudinidae)

2015; Wiley; Volume: 40; Issue: 2 Linguagem: Inglês

10.1111/jvec.12184

1948-7134

Leonardo de Souza Rocha, Claudiney Biral dos Santos, Aloísio Falqueto, Reginaldo Peçanha Brazil,

Research on Leishmaniasis Studies

Phlebotomine sand flies (Diptera: Psychodidae) are vectors of several important pathogens including Bartonella bacilliformis, arboviruses, and Leishmania spp. These flies have a worldwide distribution, particularly in tropical countries (Warburg 1991). In addition, neotropical sand flies harbor other protozoans, including Trypanosoma, Endotrypanum, microsporidians (McConnell and Correa 1964, Lainson et al. 1977 Plasmodium spp. (Klein et al. 1987 and gregarines (Adler and Mayrink 1961, Ayala 1971, Lewis et al. 1970 The genus Ascogregarina comprises several species, among which are three sand fly gregarine species that have been placed with mosquito gregarines for a long time based on their morphological characters. Phylogenetic analyses by Votypca et al. (2009) clearly demonstrated paraphyly of the current genus, Ascogregarina. The authors revealed disparate phylogenetic positions of gregarines parasitizing mosquitoes and gregarines retrieved from sand flies, reclassifying the genus Ascogregarina and creating a new genus Psychodiella. This accommodated the three gregarines from sand flies, Ascogregarina mackiei a parasite of the Old World sand flies, Ascogregarina chagasi (Adler and Mayrink 1961), and Ascogregarina saraviae (Ostrovska et al. 1990 parasites of neotropic sand flies. Recently, two new gregarines were described in the genus Psychodiella (formerly Ascogregarina), Psychodiella sergenti n. sp. and Psychodiella tobbi n. sp. (Lantová et al. 2010 Their description was based on morphology and life cycle observations conducted on larvae and adults of their natural hosts, the Old World sand fly species Phlebotomus sergenti (Parrot 1917) and Phlebotomus tobbi, respectively (Lantová et al. 2010 Neotropic gregarines have been reported infecting several sand fly species, including Bichromomyia flaviscutellata (Mangabeira 1942), Evandromyia evandroi (Costa Lima and Antunes 1936), Evandromyia edwardsi (Mangabeira 1941), Evandromyia sallesi (Galvão and Coutinho 1939), Expapillata firmatoi (Barretto, Martins and Pellegrino, 1956), Lutzomyia amarali (Barretto and Coutinho 1940), Lutzomyia cruzi (Mangabeira 1938), Lutzomyia cruciata (Coquillett 1907), Lutzomyia gomezi (Nitzulescu 1939), Lutzomyia hartmanni (Fairchild and Hertig 1957), Lutzomyia longipalpis (Lutz and Neiva 1912), Lutzomyia sanguinaria (Fairchild and Hertig 1957), Micropygomyia trinidadensis (Newstead 1922), Nyssomyia trapidoi (Fairchild and Hertig 1952), Nyssomyia whitmani (Antunes and Coutinho 1939), Nyssomyia ylephiletor (Fairchild and Hertig 1952), Pintomyia fischeri (Pinto 1926), Pintomyia townsendi (Ortíz, Ortíz 1960), Pressatia camposi (Rodríguez 1950), Psathyromyia shannoni (Dyar 1929) and Psychodopygus panamensis (Shannon 1926) (Adler and Mayrink 1961, McConnell and Correa 1964, Lewis et al. 1970 Brazil and Ryan 1984, Brazil et al. 2002 However, it has been suggested that, P. chagasi (Adler and Mayrink 1961) only complete its life cycle in L. longipalpis (Wu and Tesh 1989). The life cycle of P. chagasi was originally described in the hemocele and accessory glands of infected L. longipalpis females (Adler and Mayrink 1961, Coelho and Falcão 1967). Two morphologically similar trophozoites are confined in a cyst. They become gamonts that grow and divide to produce gametocysts. These fuse to form a zygote wall, which thickens to give origin to sporocysts that attach themselves to the surface of the egg. Therefore, the larvae become infected after hatching (Adler and Mayrink 1961). In this study, we report for the first time the infection of Evandromyia lenti (Mangabeira 1938) by P. chagasi, in the municipality of Pancas, during a study of natural infection of phlebotomine sand flies by Leishmania spp. conducted in six municipalities of the Espírito Santo, a southeastern state in Brazilian (Rocha et al. 2010 Female sand flies were captured with a CDC light trap and manual aspirator. The females were dissected in sterile saline (0,9%); the head and terminal parts of the abdomen were assembled for specific identification according to Galati (2003). The insects were collected periodically between 2004 and 2008 in the peridomiciliary dependencies of six endemic areas of cutaneous leishmaniasis located in some municipalities of the state of Espírito Santo: Afonso Cláudio, Água Doce do Norte, Iconha, Itaguaçú, Viana, and Pancas, an endemic area of cutaneous and visceral leishmaniasis (Figure 1). From a total of 1,689 female sand flies, 18 species were identified (Rocha et al 2010). After the removal of the last three abdominal segments of one E. lenti from Pancas municipality, it was observed that oocysts of P. chagasi were escaping from the hemocele (Figure 2). The ratio of natural infection by gregarines generally does not exceed 1% (McConnell and Correa 1964). In our study, the ratio of infection by P. chagasi presented by E. lenti was 0.23% (one in 431 E. lenti) and 2.56% in L. longipalpis (two in 78 L. longipalpis) in the same locality. In contrast, Adler and Mayrink (1961) observed a high ratio of infection in wild-caught Lutzomyia longipalpis (10%). The gregarines were identified as P. chagasi, taking into account the biological aspects of gregarina in its host and the morphological characteristics of oocysts. P. chagasi, despite other described Ascogregarina species, including A. mackiei, lacks intracellular development and completes its life cycle in the larval gut and/or the adult hemocele of L. longipalpis (Warburg and Ostrovska 1991). We did not observe intracellular development of the parasite in either of the infected species. Within the hemocele of two adults of L. longipalpis males, oocysts and mature gametocysts were observed. However, in E. lenti we did not observe any other life cycle stage of P. chagasi than oocysts, indicating that L. longipalpis is still the unique natural host of this gregarine species. P. chagasi oocysts are typically wide and spindle-shaped, measuring 12.7 × 7.5 μm (11.614.5 × 7.2–7.8 μm) (Adler and Mayrink 1961). In contrast, P. saraviae present an ellipsoidal oocysts 12.4 × 5.8 μm (11.6–13.1 × 5.6–5.9) μm (Ostrovska et al. 1990 In addition, the elongate form of A. saraviae oocysts, and their more delicate walls, clearly distinguishes them from oocysts of P. chagasi (Ostrovska et al. 1990 In our study, the natural observation of E. lenti infection by P. chagasi coincided with the presence of the gregarine natural host, L. longipalpis. In areas with an absence or low density of L. longipalpis, infection of E. lenti or any other sand fly species was not observed. It has been demonstrated that mosquito gregarines can cause damage to Aedes aegypti Malpighian tubules (Barret 1968) and can kill more than 80% of the larvae of unnatural host species (Walsh and Olson 1976). Wu and Tesh (1989) observed that P. chagasi could reduce the longevity of L. longipalpis in colony but, apparently, they do not reduce the egg production. In Panama, McConnell and Correa (1964) collected more than 6,000 female sand flies and only 18 were infected by gregarines. The infected sand flies apparently tolerated the infection by gregarines. Fifteen out of the 18 infected sand flies were captured when attempting to take a blood meal, an indication of normal physiology of infected sand flies (McConnell and Correa 1964). Thus, the capacity of this parasite to be employed in the field as a biological agent control of wild populations of sand flies, particularly L. longipalpis, could not be efficient. The parasite seems to have a limited range, a minimal effect on the sand fly biology under natural conditions, and a low rate of infection (Wu and Tesh 1989). Despite the potential of this parasite to be used as a biological control agent of phlebotomine sand flies, a better acknowledgement of the life cycle of this parasite is necessary to determine or understand the strict relationship between this parasite and L. longipalpis, the vector of Leishmania infantum in the Neotropics (Brazil 2013).