Description of Eimeria Arabukosokokensis Sp. N
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FOLIA PARASITOLOGICA 50: 23–30, 2003 Description of Eimeria arabukosokokensis sp. n. (Apicomplexa: Eimeriidae) from Telescopus semiannulatus (Serpentes: Colubridae) with notes on eimerian coccidia from snakes of Eastern Kenya Jan R. Šlapeta1, David Modrý1,2, James Ashe3 and Břetislav Koudela1,2 1Department of Parasitology, University of Veterinary and Pharmaceutical Sciences Brno, Palackého 1–3, 612 42 Brno, Czech Republic; 2Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic; 3Bio-Ken Snake Farm, P.O. BOX 3, Watamu, Kenya Key words: Coccidia, Apicomplexa, Caryospora, Eimeria, morphology, taxonomy, Reptilia, Serpentes Abstract. Parasitological examination of faeces of 26 snakes kept in Bio-Ken Snake Farm, Watamu, Kenya revealed new species of Eimeria Schneider, 1875 in Telescopus semiannulatus Smith, 1849. Oocysts of Eimeria arabukosokokensis sp. n. are cylindrical 26.8 (25–29) × 15.1 (14–16) µm with smooth, bilayered oocyst wall and a single polar granule. The broadly ellipsoidal sporocysts average 9.3 (8.5–10) × 7.1 (6.5–7.5) µm and possess single-layered wall composed of two plates joined by longitudinal suture. Caryospora cf. regentensis Daszak et Ball, 2001 is reported from Dendroaspis angusticeps (Smith, 1849) and two additional forms of Caryospora Léger, 1904 are reported and morphologically characterised from a single specimen of Psammophis orientalis Broadley, 1977. Systematic status of Caryospora spp. in sub-Saharan Psammophis Boie, 1827 is discusses and all species reported by various authors to date are suggested to be treated as species inquirendae until more detailed data on these parasites and their hosts are available. Coccidia of the family Eimeriidae parasitizing Dasypeltis medici (Bianconi, 1859) (1), Rhamphiophis reptilian hosts comprise predominantly members of the rubropunctatus (Fischer, 1884) (2), Scaphiophis genera Caryospora Léger, 1904, Eimeria Schneider, albopunctatus Peters, 1870 (1), Psammophis orientalis 1875 and Isospora Schneider, 1881 (e.g., Upton et al. Broadley, 1977 (1), Dispholidus typus (Smith, 1829) (1); 1986, McAllister et al. 1995, Modrý 1999). In contrast Boidae: Eryx colubrinus (Linnaeus, 1758) (1). Examined to the large diversity of African snakes, only a limited animals were kept in Bio-Ken Snake Farm, Watamu, Kenya. knowledge exists about the coccidian species para- Animals originated mostly from the localities in coastal Kenya; in described cases the locality is given in a species sitizing these hosts. In an attempt to shed more light on account. All samples were stored in individual tubes with the parasitofauna of East African snakes, we have per- 2.5% potassium dichromate, transported to laboratory and formed a coprological examination of several snake examined for the presence of parasites using flotation species kept in Bio-Ken Snake Farm in Eastern Kenya. technique. Morphological examinations and photo-graphy was These examinations revealed a diverse spectrum of performed using an Olympus Provis microscope equipped for coccidia which are reported below, together with a Nomarski interference contrast (NIC) micro-scopy. All description of one new species. measurements are given in µm as means followed by ranges in parentheses. The snake taxonomy used throughout this paper MATERIALS AND METHODS reflects the most recent opinion by Spawls et al. (2002). Faecal samples were collected from 26 snakes, representing 18 species in five families: (numbers of RESULTS examined specimens are noted in parentheses) Elapidae: Naja Nine of 26 samples examined (35%) contained nigricollis Reinhardt, 1843 (2), Naja pallida Boulenger, 1896 coccidian oocysts. Sporocysts of Sarcocystis spp., found (1), Dendroaspis angusticeps (Smith, 1849) (1); Viperidae: Bitis arietans (Merrem, 1820) (2), Bitis gabonica (Duméril, in four snakes (Lamprophis fuliginosus, Mehelya Bibron et Duméril, 1854) (1), Causus resimus (Peters, 1862) capensis, Rhamphiophis rubropunctatus, Psammophis (2), Echis pyramidum (Geoffroy Saint-Hilaire, 1827) (1); orientalis), were the most prevalent. Oocysts of Atractaspid-idae: Atractaspis microlepidota Günther, 1866 Caryospora were observed in three snakes (Telescopus (2); Colubri-dae: Lamprophis fuliginosus (Boie, 1827) (2), semiannulatus, Psammophis orientalis, Dendroaspis Philothamnus punctatus Peters, 1867 (1), Mehelya capensis angusticeps), and oocysts of Eimeria s.l. in three (Smith, 1847) (1), Telescopus semiannulatus Smith, 1849 (3), Telescopus semiannulatus and one Lamprophis Address for correspondence: J.R. Šlapeta, Wadsworth Center, New York State Department of Health, P.O. Box 22002, Albany, New York 12201-2002, USA. Phone: ++1 518 474 2187; Fax: ++1 518 473 6150; E-mail: [email protected] 23 Figs. 1–7. Nomarski interference contrast photographs of sporulated oocysts of found coccidia, all in the same scale. Figs. 1–2. Eimeria arabukosokokensis sp. n. from Telescopus semiannulatus. Note visible sutures of sporocyst wall plates (arrows). Figs. 3–4. Caryospora cf. regentensis from Dendroaspis angusticeps. Fig. 5. Caryospora sp. I from Psammophis orientalis. Fig. 6. Caryospora sp. II from P. orientalis, transversal view. Fig. 7. Caryospora sp. II from P. orientalis, longitudinal view. Scale bar = 10 µm. 24 Šlapeta et al.: Eimerian coccidia from snakes T y p e m a t e r i a l : Photosyntypes deposited under the original collection No. KA31/1999 at Department of Parasitology, University of Veterinary and Pharmaceutical Sciences Brno, Czech Republic. E t y m o l o g y : The name is derived from the local name of nearby situated Arabuko-Sokoke Forest in coastal East Africa, in honour of this unique and endangered place. Remarks: Based on the oocyst shape (cylindrical) and the absence of Stieda and substieda body, the studied isolate probably belongs to Choleoeimeria Paperna et Landsberg, 1989 as defined by Paperna and Landsberg (1989a, b) rather than to Eimeria. However, such classification has been questioned and not accepted or simply ignored by several authors (e.g., Asmundsson et al. 2001, Daszak and Ball 2001a). Therefore, we follow a recently used wider concept of Eimeria; for details see Discussion. The endogenous development of all histologically studied species of Eimeria with elongated cylindrical oocysts is confined to the gall bladder epithelium (e.g., Paperna and Landsberg 1989a, b, Paperna and Lainson 2000, Modrý Fig. 8. Composite line drawing of sporulated oocyst of et al. 2001). Thus, it is probable that E. Eimeria arabukosokokensis sp. n. Scale bar = 5 µm. arabukosokokensis also affects this organ. Caryospora cf. regentensis Daszak et Ball, 2001 fuliginosus. Only three Caryospora spp. and a single Figs. 3–4, 9 Eimeria sp. had sufficient number of sporulated oocysts Description: Oocysts spherical, 15.3 (14.5–16) × to be morphologically further characterised. 15.0 (14–16), SI = 1.0 (1.0–1.1) (n = 30). Oocyst wall smooth and bilayered, ~1 thick, inner layer thinner, APICOMPLEXA: E i m e r i i d a e outer layer yellowish. Micropyle and oocyst residuum absent. Spherical polar granule present in 60% of Eimeria arabukosokokensis sp. n. Figs. 1–2, 8 oocysts examined. Sporocysts ellipsoidal, 10.9 (10–12) Description: Oocysts cylindrical, long sides almost × 8.2 (6.5–9), SI = 1.3 (1.2–1.5) (n = 30). Sporozoites parallel to each other; 26.8 (25–29) × 15.1 (14–16), with one barely visible refractile body and almost shape index (length:width ratio, SI) = 1.8 (1.6–1.9) (n = invisible, centrally located nucleus. Surface of banana- 30). Oocyst wall smooth, bilayered, approximately 2 shaped sporozoites smooth. Sporocyst residuum usually thick, with inner layer being thinner. Single polar compact, spherical, 3–4 × 1.5–3.5 in diameter, often granule present. Sporocysts broadly ellipsoidal, broader accompanied by up to 5 globules scattered among toward one end, 9.3 (8.5–10) × 7.1 (6.5–7.5), SI = 1.3 sporozoites. Eight sporozoites, 1.5–2 in diameter, fill (1.2–1.5) (n = 30). Sporocyst wall thin, smooth, single- tightly sporocyst. Stieda body ellipsoidal, 1.5–2 × 0.5, layered, composed of two plates joined by longitudinal substieda body ellipsoidal, 2.5–3 × 1.5. suture. Sporozoites with one refractile body and barely H o s t : Dendroaspis angusticeps (Smith, 1849), the green visible nucleus located centrally. Surface of banana- mamba (Serpentes, Elapidae). shaped sporozoites appeared striated or finely granular. L o c a l i t y : Watamu near Malindi, coastal area of Kenya Sporocyst residuum consists of numerous globules 1– (ca. 03°21’S, 40°01’E). 1.5 in diameter, forming a spherical cluster 3–4 in S i t e o f i n f e c t i o n : Unknown, oocysts recovered from diameter or being scattered among sporozoites. faeces. P r e v a l e n c e : Single examined sample originated from a T y p e h o s t : Telescopus semiannulatus Smith, 1849 colony of dozens of green mambas in Bio-Ken, where the (Serpentes, Colubridae, Boiginae). snakes are used for venom milking. T y p e l o c a l i t y : Watamu near Malindi, coastal area of S i t e o f i n f e c t i o n : Unknown, oocysts recovered from Kenya (ca. 03°21’S, 40°01’E), Africa. faeces. S i t e o f i n f e c t i o n : Unknown, oocysts recovered from V o u c h e r m a t e r i a l : Oocyst microphotographs faeces; probably the gall bladder (see Remarks). deposited under the original collection No. KA26/1999 at P r e v a l e n c e: All 3 examined snakes expelled oocysts in Department of Parasitology, University of Veterinary and faeces. Pharmaceutical Sciences Brno, Czech Republic. 25 Remarks: The morphology of the found isolate colourless (Bray 1960). Caryospora weyerae Bray, matches the original description of Caryospora 1960, reported by the original author to resemble C. regentensis Daszak et Ball, 2001. Sporocysts of C. hermae in every way except the size, thus is smaller regentensis were originally described to be 13.0 (10.2– than our isolate too.