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The Hemoflagellates of Sloths Vermilinguas (Anteaters)

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The Hemoflagellates of Sloths Vermilinguas (Anteaters) THE HEMOFLAGELLATES OF SLOTHS, VERMILINGUAS (ANTEATERS), AND ARMADILLOS Jeffrey J. Shaw ' The Wellcome Parasitology Unit, Instituto Evandro Chagas, Fundação Serviços de Sáude PúbUca, 66.00 Belém, Para, Brazil Abstract Hemoflagellates found in sloths, vermUinguas (neotropical anteaters), and armadillos are listed and their taxonomic status, vectors, distribution and importance to man are discussed. Sloths, particularly two-toed sloths Choloepus, harbor the greatest variety of hemo• flagellates and in Panamá the two-toed sloth is the major vertebrate host of Leishmania braziliensis panamensis which causes cutaneous leishmaniasis in man. In the Amazon region the common long-nosed armadillo Dasypus novemcinctus is infected with a Leishmania not yet isolated from man. Two-toed sloths appear to be the major reservoir of L. b. guyanensis in northern Pará, Brazil, and in French Guiana. In an endemic "pian-bois" region of Pará, Tamanduá anteaters are important secondary reservoirs. Ali the Leishmania of sloths, anteaters and armadillos that have been studied in sandflies are peripylarians, a type of Leishmania found in New World mammals, and it is suggested that this group may have evolved in xenarthrans. The genus Endotrypanum is intermediate between Leishmania and Trypanosoma and has retained certain features of its leishmanial ancestors in the vector, but in its vertebrate host it develops in the epimastigotic form and in rare situations the trypanomorphic form. Phlebotomine sandflies are the most probable vectors of xenarthran Leishmania and Endotrypanum. In drier, more open, áreas of Panamá, sloths are commonly infected with Trypanosoma leuwenhoeki, which may be responsible for some of the ran^e/í-like infections in man. Common long-nosed armadillos are commonly infected with T. cruzi, but Brazilian stocks of this parasite belong to a zymodeme that is only rarely found in man. Separate lines of T. cruzi may have evolved in xenarthrans and marsupials from a New World insect leptomonad stock. There are enormous gaps in our knowledge of xenarthran hemoflagellates but it is recommended that particular priority be given to the isolation and characterization of stocks from the numerous hosts found in different geographical regions. Abstracto Se han enumerado los hemoflagelados que se encuentran en monos perezosos, osos hormigueros neotropicales, y armadillos y se explica su status taxonómico, presencia de vectores, distribución y importância para el hombre. Monos perezosos, particularmente el mono perezoso de dos dedos Choloepus, albergan la mayor variedad de hemoflagelados y en Panamá Choloepus es el mayor hospedero entre los vertebrados de Leishmania brasiliensis panamensis el cual es la cuasa de leishmaniasis cutânea en el hombre. Choloepus es el que Ueva la mayor cantidad de L. b. guyanensis en el norte de Pará, Brasil y en la Guyana Francesa. En una región endémica "pian bois" de Pará, los osos hormigueros Tamanduá son un importante hospedero secundário. Todas las Leishmania de monos perezosos, osos hormigueros, y armadillos que han sido estudiadas en flebótomus son peripilarios, un tipo de Leishmania que se encuentra en mamíferos dei Nuevo Mundo, y se sugiere que este grupo ha podido evolutionar en xenartranos. El género Endotripanum es intermédio entre Leishmania y Tripanosoma y ha conservado ciertas características de sus antecesores leishmanianos en el vector, sin embargo en su hospedero verte• brado se desarroUa en la forma epimastigótica y raras veces en la forma tripanomórfica. Flebótomus son los vectores mas probables de Leishmania y Endotripanum en los xenartranos. En las áreas más secas y abiertas de Panamá, los monos perezosos están infectados por Tripanosoma leuwenhoeki, el cual puede ser la causa algunas de las infecciones tipo rangeli en el hombre. Los armadillos comunes de trompa larga son usualmente infectados por T. cruzi; sin embargo las cepas brasUeiias de este parasito pertenecen a un cimodema que solo en raras ocasiones se encuentra en el hombre. Líneas separadas de T. cruzi han podido evolocionar en los xenartranos y en mar- supiales a partir de un cepa leptomonade de un insecto dei Nuevo Mundo. Hay enormes brechas en nuestro conicimiento de los hemo• flagelados de xenartranos pero se recomienda que se le dé prioridad particular al aislamiento y caracterización de cepas de los abundantes huéspeded que se encuentran en las diferentes regiones geográficas. Resumo No presente trabalho todos os hemoflagelados de preguiças, tamanduás e tatus, são citados com suas posições taxonômicas, vetores, distribuições geográficas e suas importâncias como fontes de infecção ao homem. Preguiças, especialmente as do género Choloepus, têm o maior niimero de hemoflagelados e, no Panamá, a preguiça real é um dos principais hospedeiros de Leishmania braziliensis pana• mensis, que é responsável pela leishmaniose cutânea no homem, neste país. Na região amazônica, o tatu galinha Dasypus novemcinctus, é comuraente infectado com uma espécie de Leishmania que, por enquanto, não tem sido encontrada no homem. A preguiça real é o mais importante reservatório silvestre de L. b. guyanensis no norte do estado do Pará, Brasil e na vizinha Guiana Francesa. Nas regiões endémicas de "pian bois" do Pará, tamanduás do género Tamanduá são importantes reservatórios secundários de L. b. guyanensis. Todas as leishraanias de preguiças, tamanduás e tatus, cujo desenvolvimento em flebótomos tem sido estudado, pertencem à peripilaria, que até agora só foi encontrado em mamíferos do novo mundo. O autor sugere que essas leishmanias provavelmente evolem em xenarthros. O género Endotrypanum é intermediáro entre a Leishmania e Trypanosoma e, no vetor, seu desenvolvimento é mais parecido com Leishmania mas, na preguiça, se aproxima aos membros do género Trypanosoma quanto à sua morfologia. É bem provável que os vetores de Leishmania e Endotrypanum de xenarthros sejam flebotomíneos. Nas regiões mais secas com menos árvores do Panamá, preguiças de vários géneros são infectadas com Trypanosoma leuwenhoeki, que pode ser responsável por algumas das infecções do tipo rangeli, encontrados no homem, naquele país. Infecções por T. cruzi são frequentement encontradas no tatu galinha nas Américas, mas as cepas desse parasito no Brasil, pertencem a um zimodema que raramente infecta o homem. É possível que linhagens diferentes de T. cruzi evoluam em xenarthros e marsupials, dos flagelados ancestrais. Nosso conhecimento sobre hemoflagelados dos xenarthros é extrem• amente escasso e o autor sugere que o isolamento e caracterização de amostras de vários hospedeiros de áreas geográficas diferentes seriam uma das linhas prioritárias de pesquisa. The modem xenarthra are ali that remains of a group reviews or illustrates a particularly important point, of mammals that appeared in the fóssil record some 60 the source is cited. million years ago during the Upper Paleocene period in North America (Herschkovitz, 1971), although the PARASITES AND THEIR HOSTS xenarthrans may have become genetically distinct as a lineage more than 80 million years ago (Sarich, 1985). The hemoflagellates are protozoa of the subphylum Ali living Xenarthra are, therefore, survivors of a mam- Sarcomastigophora (flagellar and/or pseudopodial loco- malian stock that is older than such groups as the motion); class Zoomastigophorea (no chlorophyll): rodents, that appeared in the fóssil record some 22 order Kinetoplastida (possessing a kinetoplast): family million years later in the early Ohgocene period. Their Trypanosomatidae (parasites with one flagellum). only rivais for being the oldest mammalian group in the Members of the genera Leishmania and Trypanosoma are New World are the marsupials that go back as far as the found in sloths, anteaters, and armadillos, while flag- Cretaceous period. Unlike the marsupials, who have ellates of the genus Endotrypanum occur in sloths. living members in both Austraha and the Américas, the These three genera are ali digenetic in that their life xenarthrans are, and apparently have always been, cycle involves both an invertebrate and a vertebrate host. limited to the New World. To parasitologists such mammals represent a fascinating group, for they are Genus Leishmania Ross 1903 hosts in which typically New World parasites may have evolved and survived. Members of this genus develop as amastigotes in cells of Protozoologists are presently studying interspecific and the reticuloendothelial system of their vertebrate host intraspecifíc variations of many groups in great depth and as promastigotes and paramastigotes in the intestine and in particular those economically important protozoa of their invertebrate host. The only known vectors are such as the leishmanias and trypansomes. New bio- phlebotomine sandflies (Diptera: Psychodidae). Based chemical methods are becoming available (see reviews by on their development in sandflies, Lainson and Shaw Newton and Burnett, 1972; Chance, 1979; Godfrey, (1979) divided the genus into the sections Hypopylaria, 1979) and such techniques in conjunction with studies Peripylaria and Suprapylaria. Until now the Leishmania on morphology, physiology and immunology and in vivo found in xenarthra ali belong to the section Peripylaria and in vitro behavior show a considerable degree of and no members of this section have so far been found diversity, even among organisms that are morpho- in mammals outside the neotropics. logically very similar. Godfrey (1979) drew attention to the stability that certain isoenzymes showed in different Leishmania
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