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A Review of Trypanosoma Species Known from Malagasy Vertebrates

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A Review of Trypanosoma Species Known from Malagasy Vertebrates A review of Trypanosoma species known from Malagasy vertebrates Mercia Rasoanoro1,2, Beza Ramasindrazana1,2, les études ultérieures sur leur implication potentielle Steven M. Goodman3,4, Minoarisoa Rajerison1 & dans la santé publique. En outre, des données sur Milijaona Randrianarivelojosia1,5 les groupes de vecteurs connus dans le monde ont 1 Institut Pasteur de Madagascar, BP 1274, été documentées afin de déterminer si ces taxa Ambatofotsikely, Antananarivo 101, Madagascar sont présents à Madagascar et pourraient assurer la E-mail: [email protected], [email protected], transmission de Trypanosoma. Si aucune information [email protected],[email protected] n’est disponible sur la présence de Trypanosoma 2 Faculté des Sciences, Université d’Antananarivo, BP chez les poissons malgaches, des recherches 706, Antananarivo 101, Madagascar microscopiques antérieurs ont permis d’identifier huit 3 Association Vahatra, BP 3972, Antananarivo 101, espèces de Trypanosoma dont cinq espèces chez Madagascar les reptiles, à savoir : T. therezieni chez Calumma 4 Field Museum of Natural History, 1400 South Lake brevicorne, T. haranti chez Liopholidophis lateralis, Shore Drive, Chicago, IL 60605, USA T. petteri chez Phelsuma lineatum, T. betschi chez E-mail: [email protected] 5 Faculté des Sciences, Université de Toliara, Toliara Zonosaurus madagascariensis et T. domerguei chez 601, Madagascar Oplurus cuvieri. Deux espèces de trypanosomes ont été décrits chez les oiseaux : T. avium chez Falco newtoni, Atelornis pittoides, Acridotheres tristis, Abstract Cyanolanius madagascarinus, Schetba rufa et Tylas eduardi et T. everetti chez Ploceus sakalava. We report on the different species of trypanosomes Trypanosoma lewisi, un parasite cosmopolite a été known from Malagasy vertebrates based on trouvé chez le rongeur introduit Rattus rattus. Par published literature; this review provides baseline ailleurs, des taxa de Trypanosoma non identifiés et information for future public health research. Further, encore non décrits ont été également trouvés chez we provide data at a worldwide scale of invertebrate différent groupes de vertébrés comme les reptiles groups known to be Trypanosoma vectors and tels Calumma nasutum, Furcifer willsii et Pelomedusa their presence or absence on Madagascar, as subrufa, les oiseaux tels Atelornis crossleyi, Motacilla further insight into the potential vectors on the flaviventris, Hypsipetes madagascariensis, Berniera island. Different microscopic studies highlighted the madagascariensis, Xanthomixis zosterops et presence of eight described species of Trypanosoma Zosterops maderaspatana, les chauves-souris tels in Malagasy vertebrates, including five species Miniopterus mahafaliensis et M. brachytragos, un known from reptiles: T. therezieni, T. domerguei, rongeur endémique Nesomys rufus (Nesomyidae : T. haranti, T. petteri, and T. betschi; two species in Nesomyinae) et chez un lémurien, Indri indri, mais birds: T. everetti and T. avium; and one species in faute de données disponibles sur leur caractérisation rodents, T. lewisi. In addition, other unidentified taxa morphologique et moléculaire, l’identité taxonomique have been reported in reptiles, birds, bats, rodents, de ces parasites restent à élucider. Une récente and lemurs based on microscopic techniques or étude moléculaire sur Hoplobatrachus tigerinus a molecular screening. montré l’absence du genre Trypanosoma chez cette espèce introduite. Key words: Trypanosoma, reptiles, birds, bats, mammals, Madagascar Mots clés : Trypanosoma, reptiles, oiseaux, chauves-souris, mammifères, Madagascar Résumé détaillé La présente revue résume les informations Introduction disponibles sur les différentes espèces de Protozoan parasites of the genus Trypanosoma trypanosomes infectant les vertébrés malgaches (Kinetoplastida: Trypanosomatidae) are dans le but d’établir une base de recherche pour taxonomically diverse, geographically widespread, Rasoanoro, M., Ramasindrazana, B., Goodman, S. M., Rajerison, M. & Randrianarivelojosia, M. 2019. A review of Trypanosoma species known from Malagasy vertebrates. Malagasy Nature, 13: 65-75. 66 Rasoanoro et al.: A review of Malagasy Trypanosoma and known to infect different vertebrate groups, relationship, and potential implications for public including fish, amphibians, reptiles, birds, and health. mammals (Stevens, 2008; Noyes, 1998; Barret et al., 2003). In humans, Trypanosomiasis has specific Occurrence of trypanosomes in geographic range depending on availability of vectors Malagasy vertebrates (Noyes, 1998; Barret et al., 2003). Trypanosoma Trypanosoma in aquatic vertebrates is transmitted by a wide range of hematophagous Trypanosoma are common symbionts of freshwater arthropods (Stevens et al., 2001; Hamilton et al., and marine fishes throughout the world (Kreier & 2007) and based on the discovery of trypanosomes Baker, 1987). The trypanosomes of aquatic hosts in a female sand fly (Diptera: Ceratopogonidae) are transmitted by leeches, such as Hemiclepsis from Burmese Cretaceous amber deposits, it was marginata (family Glossiphoniidae) and Hirudo suggested that this group of parasites existed since nipponica (family Hirudinidae) (Molyneux, 1977; at least 380 million years (Haag et al., 1998; Poinar & Stevens et al., 2001; Hayes et al., 2014; Fermino Poinar, 2004). et al., 2015). Within non-terrestrial vertebrates, Within the Kinetoplastida, the family Trypanosoma are transmitted by blood-sucking Trypanosomatidae comprises a paraphyletic group leeches (Hamilton et al., 2005) and a variety of adapted to colonize a diverse range of eukaryotic arthropods (Johnson et al., 1993; Lehane, 2005; Pinto hosts (Hughes & Piontkivska, 2003; Piontkivska & et al., 2015). Within the fish fauna of Madagascar, Hughes, 2005; Simpson et al., 2006). Trypanosomes we are unaware of any published information on are traditionally divided into two groups based on the Trypanosoma parasites. transmission route of the insect vector: the Salivaria group, transmitted via the vector’s proboscis, and the Trypanosoma in reptiles Stercorcaria group, transmitted via the vector’s feces (Hoare, 1964). Based on blood smear screening, six families of Published phylogenies of Trypanosoma suggest reptiles are known to be infected by Trypanosoma that most clades are generally associated with (Table 1). Some taxa, such as T. therezieni, which particular vertebrate hosts (Sehgal et al., 2001; is apparently non pathogenic in its natural host Noyes et al., 2002; Hamilton et al., 2007; Ferreira et Calumma brevicorne (family Chamaeleonidae), al., 2008), with little or no apparent negative effects are host-specific. However, during an experimental on infected hosts (Smith et al., 2005). Nevertheless, study of other chameleon species (e.g., C. parsonii, some Trypanosoma species are harmful to other C. oustaleti, C. verrucosus, and Furcifer lateralis), host species following their introduction into a novel Brygoo (1963) demonstrated that inoculation of taxonomic group (Onyango et al., 1966; Maraghi & infected blood of T. therezieni in these taxa was fatal. Molyneux, 1989; Wyatt et al., 2008). Trypanosomes In other hosts, T. domerguei, T. haranti, T. have different complex life cycles; generally diphasic petteri, and T. betschi were found in Oplurus occurring between a vertebrate host, where they cuvieri (family Iguanidae), Liopholidophis lateralis are represented by a trypomastigote form in the (family Colubridae), Phelsuma lineatum (family bloodstream, and undergo development within the Gekkonidae), and Zonosaurus madagascariensis digestive tract of the invertebrate vector (Botero et (family Gerrhosauridae), respectively (Brygoo, 1965, 1966b). Further, three reptile species, al., 2016). Calumma nasutum, Furcifer willsii, and Pelomedusa On Madagascar, information concerning subrufa (family Pelomedusidae) are parasitized by trypanosomes in wild animals is poorly documented unidentified Trypanosoma (Brygoo, 1965). in the literature. Nevertheless, within the highly- endemic fauna of the island, trypanosomes have been reported from different vertebrate groups, Trypanosoma in amphibians generally based on blood smear screening and Amphibians are exposed to terrestrial and aquatic in certain cases molecular analysis. The aim of ectoparasites, such as arthropods and leeches, which this review is to compile published information on can serve as hosts and vectors for trypanosomes. Trypanosoma known from non-human vertebrates Recent laboratory analyses of 134 Hoplobatrachus on Madagascar, with the intent to provide a baseline tigerinus (family Dicroglossidae), a frog introduced for future research on their diversity, phylogenetic to Madagascar, found no evidence of Trypanosoma Rasoanoro et al.: A review of Malagasy Trypanosoma 67 infection based on either blood smear microscopy or between 1971 and 1973. Among those, two species, molecular techniques (Maeder et al., 2018). Falco newtoni (family Falconidae) and Acridotheres tristis (family Sturnidae, introduced), showed about Trypanosoma in birds 33% prevalence rates for T. avium. Subsequent Based on morphological techniques, nine families work by Savage et al. (2009) identified T. avium of birds on Madagascar are known to be infected by parasites in four endemic bird species, Atelornis Trypanosoma, which include the Brachypteraciidae, pittoides (family Brachypteraciidae), and Cyanolanius Bernieridae, Falconidae, Motacillidae, Ploceidae, madagascarinus, Schetba rufa, and Tylas eduardi Pycnonotidae, Sturnidae, Vangidae, and Zosteropidae (family
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