J. Parasitol., 99(6), 2013, pp. 1040–1044 Ó American Society of Parasitologists 2013
A NEW SPECIES OF SPIRURA BLANCHARD, 1849 (NEMATODA: SPIRURIDAE) PARASITE OF HELIOSCIURUS GAMBIANUS AND XERUS ERYTHROPUS (RODENTIA: SCIURIDAE) IN SENEGAL ˆ Yann Quilichini*, and Bernard Marchand* Malick Diouf, Cheikh Ahmadou Bamba Seck, Cheikh Tidiane Ba, Laboratory and Evolutionary, Ecology and Management of Ecosystems, Faculty of Sciences and Techniques, Cheikh Anta Diop University of Dakar, BP 5055, Dakar, Senegal. Correspondence should be sent to:
[email protected] ABSTRACT: A new species of Spirura is described from the stomach of Heliosciurus gambianus and Xerus erythropus (Sciuridae). Considering the number of preanal papillae of males, Babero (1973) and Giannetto and Canestri Trotti (1995) proposed the subdivision of the genus into 2 groups; those with 4 pairs of preanal papillae (25 species) and with more than 4 pairs of preanal papillae (4 species). Spirura mounporti n. sp. belongs to the second, with 5 pairs of preanal papillae, and differs from Spirura infundibuliformis (McLeod, 1933) Anderson et al., 1993, Spirura zapi (Erickson, 1938) Chabaud et al., 1965, Spirura leiperi Gupta and Trivedi, 1985, and Spirura michiganensis Sandground, 1935 in the number of pairs of pre-cloacal papillae. The new species further differs from other species of the genus in having 21 caudal papillae, in the ratio of spicules:body length, and in its morphoanatomical characters.
Parasitic nematodes of vertebrates in Africa have been the subject of various studies. From the former scientific expeditions to North Africa (Seurat, 1911, 1913, 1915), Sub-Saharan Africa (Gedoelst, 1916; Ortlepp, 1922; Baylis, 1928; Joyeux et al., 1928; Monnig, 1938; Campana and Chabaud, 1950; Vuylsteke, 1956; ¨ Morel, 1959; Quentin and Krishnasamy, 1975) until recent years (Vassiliades, 1980, 1992; Diouf et al., 1998, 2000, 2005; Diagne et al., 2000; Diouf and Durette-Desset, 2002; Durette-Desset et al., 2008; Smales et al., 2009), knowledge about the African nematofauna, unlike in other continents, is still scarce. From 1800 to 1967, 691 species of nematodes had been reported in African vertebrates (amphibians, reptiles, aves, and mammals) (Canaris and Gardner, 2003). For the reported species, West Africa is not well represented. In decreasing order, majority of knowledge comes from South, then East, and finally North Africa. Investigations of squirrel nematodes in Africa report 5 genera and 7 species: Dermatoxys getula Seurat, 1915, Dermatoxys polyoon Linstow, 1909, Dermatoxys probscidiphora Biocca and Chabaud, 1955, Oesophagostomum xeri Ortlepp, 1922, Syphacia pallaryi Seurat, 1915, Syphacia africana Chabaud and Biocca, 1955, and Spirura portesiana Campana and Chabaud, 1950. In this work, we add to the list of helminths encountered in mammals of the Ethiopian zone, a new nematode species of the genus Spirura Blanchard, 1849, a parasite of the Gambian sun squirrel H. gambianus and striped ground squirrel Xerus erythropus (rodents Sciuridae). To our knowledge, apart from S. portesiana Campana and Chabaud, 1950, all valid species known in Africa (Spirura gastrophila [Seurat, 1913], Spirura rothschildi [Seurat, 1915], Spirura dentata [Monnig, 1938], ¨ Spirura rytipleurites seurati [Chabaud, 1954], Spirura diplocyphos [Chabaud et al., 1965], Spirura spinicaudata [Chabaud et al., 1965], Spirura nycterisi [Quentin and Krishnasamy, 1975]) have been described in bats, carnivores, or primates (Monnig, 1938; ¨ Vuylsteke, 1956; Chabaud et al., 1965).
Received 18 September 2012; revised 10 June 2013; accepted 21 June 2013. * CNRS UMR 6134 SPE, Parasites and Mediterranean Ecosystems Laboratory, University of Corsica Pascal Paoli, F20250 Corte, France. DOI: 10.1645/12-86.1
MATERIALS AND METHODS Rodents H. gambianus Ogilby, 1835 and X. erythropus Geoffrey, 1803 ´ were collected from 2 localities in Senegal: Kedougou (12833 0 N, 12810 0 W) and Fimela (1480 0 N, 16840 0 W). Prevalence and intensity of infections were determined from 30 animals (15 X. erythropus; 15 H. gambianus). Nematodes were recovered from stomachs and stored in 70% ethanol. For light microscopy studies, nematodes were cleared with lactophenol. Figures were made using a drawing tube. For scanning electron microscope studies, specimens were dehydrated in a graded ethanol series and dried with CO2 in an Emitech K850 (EM Technologies Ltd, Ashford, U.K.) critical point dryer. After being mounted, specimens were coated with gold–palladium in a Quorum Technologies SC7640 sputter coater (Quorum Technologies Ltd, Newhaven, U.K.) and examined with a Hitachi S-3400N scanning electron microscope (Hitachi High-Technologies Corporation, Tokyo, Japan) at acceleration voltages between 3 and 20 kV. Morphological studies were carried out on 5 males and 5 females collected from H. gambianus. The measurements are in micrometers unless otherwise stated and presented as types followed by extremes of paratypes in parentheses. The type material is deposited at the Museum National d’Histoire Naturelle de Paris (France).
DESCRIPTION Spirura mounporti n. sp. (Figs. 1–16) Whitish after fixation with a single ventral cuticular hump (Figs. 1, 8– 10) in the anterior part characteristic of the genus Spirura. Anterior body end tapered, widening gradually toward the hump. Wider, the posterior part is characterized by the presence of 2 longitudinal (1 dorsal and 1 ventral) alar formations, clearly visible only in scanning electron microscopy (Figs. 8–10). Each of these alae starts at 20 lm from the posterior edge of the hump in males. In females, they are further from the hump and appear at different levels (ventral: 4 mm; dorsal: 7 mm). The esophagus is very long with the muscular part representing about 1/10 of its entire length (Figs. 1, 2). In both sexes, the mouth opening is dorsoventral and bounded by 2 pseudolabia (Fig. 3). Each pseudolabium consists of 3 lobes, each bearing a medial bifid denticle (Figs. 3, 11, 12). In apical view there are 4 labial papillae, a buccal frame which is formed of a cuticular fold more or less chitinized, a single pair of amphids, and 4 submedian cephalic papillae more developed than the labial ones and posterior to amphids (Figs. 3, 11, 12). The deirids, equipped with a sensorial bristle (Figs. 1, 13), are anterior to the nerve ring, located itself in the third posterior part of the muscular esophagus (Fig. 1). The excretory pore (Fig. 1) is located just behind the nerve ring. The cuticle presents thin and homogeneous transverse striations (Fig. 13). Male: Body 22.4 (20.1–34.9) mm long, 610 (600–650) wide at the mid body. Deirids, nerve ring, and excretory pore at 120 (80–140), 400 (250– 450), 450 (400–550) from anterior extremity respectively. Esophagus, 4.6 (4.5–6.0) mm long with a muscular part of 380 (300–385). The ventral hump is located in the anterior part at 2.0 (2.5–1.51) mm of the apex with the ratio hump position:body length of 0.08 (0.07–0.09). In ventral view,
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FIGURES 1–7. Spirura mounporti n. sp. (1) Male, anterior extremity, right lateral view. The 2 faint regions correspond to an interruption of the diagram. (2) Male, anterior extremity, right lateral view. (3) Female, apical view. (4) Female, caudal extremity, left lateral view. (5) Male, caudal extremity, ventral view. (6) Female, vulvar region, right lateral view. (7) Eggs.
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FIGURES 8–16. Spirura mounporti n. sp. scanning electron microscopy. (8) Male, lateral view. (9) Male, anterior extremity, left lateral view. (10) Female, anterior extremity, right lateral view. (11) Male, anterior extremity, lateral view. (12) Female, cephalic portion, apical view. (13) Dierids. (14) Male, caudal extremity, lateral view. (15) Male, caudal extremity, ventral view. (16) Male, caudal extremity, pedunculate papillae. Abbreviations: A ¼ alae, B ¼ boss or hump, D ¼ denticle, Di ¼ dierids, PAP ¼ papillae, S ¼ bristle. Arrow heads ¼ labial and cephalic papillae. Scale bars 8 ¼ 1 mm; 9–10 ¼ 500 lm; 11 ¼ 20 lm; 12–13 ¼ 10 lm; 14 ¼ 200 lm; 15 ¼ 50 lm; 16 ¼ 5 lm.
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the caudal end exhibits 21 papillae (5 pre-cloacal pairs, 5 post-cloacal pairs, and a median cloacal papillae) (Fig. 5). The 10 pairs of papillae are pedunculate, each of them formed of 2 nested spherical elements at its apex (Figs. 14–16). Spicules, unequal lengths: the right 700 (600–750); the left, 200 (200–250). Gubernaculum ‘‘U’’ shaped, 100 (95–100) long, and 50 (45–50) wide at its base. Female: Body 33.3 (44–27) mm long, 650 (950–430) wide in the middle of the body. Deirids, nerve ring, and excretory pore at 300 (270–340), 340 (340–410), 440 (400–550) from anterior extremity, respectively. The ventral hump is located at 2.8 (2.1–3.1) mm of the apex. The esophagus is 6.3 (5.2–7.6) mm long with a muscular part of 580 (580–400) in length. Amphidelphic (Fig. 6), the vulva opens in the middle region at 18.15 (17.3– 19.7) mm from anterior extremity of the body, Vagina-vera 150 (150–170) long. Eggs ovoid (Fig. 7), 55 (50–60) long, 35 (30–40) wide. The tail (Fig. 4) measures 410 (600–400). Position of the hump:body length: 0.08 (0.07– 0.08). Taxonomic summary Type host: Heliosciurus gambianus Ogilby, 1835 (Musser and Carleton, 2005). Other host: Xerus erythropus Geoffrey, 1803 (Musser and Carleton, 2005). Site of infection: Stomach. ´ ´ egal. ´ Type locality: Kedougou (12833 0 N, 12810 0 W), Sen ´ egal. ´ Other locality: Fimela (1480 0 N, 16840 0 W), Sen Prevalence and intensity: H. gambianus 66.6% (15 examined, 10 infected); 2 (1–5) worms per infected host; X. erythropus 40% (15 examined, 6 infected), 2 (1–10) worms per infected host. Deposition of types: Museum National d’Histoire Naturelle de Paris under numbers: Holotype and allotype, MNHN HEL251; paratypes, MNHN HEL252. Etymology: The species is named in memoriam of Professor Danamou Mounport (1956–2012). Remarks To our knowledge, 30 valid species and subspecies (29 species and 1 subspecies) have been identified successively in this genus (HeringHagenbeck et al., 2001; Peralta-Rodriguez et al., 2012). All species of the genus have been divided into 2 groups (Babero, 1973; Giannetto and Canestri-Trotti, 1995) depending on the number of pre-cloacal papillae. The first group, found in Europe, Asia, Africa, and South America, comprises species with 4 pairs of pre-cloacal papillae. It is widely the most important group with about 20 species (Anderson et al., 1993). The second group of species, which have more than 4 pairs of papillae, is usually encountered in North America and India (Babero, 1973; Giannetto and Canestri Trotti, 1995). According to this subdivision, our specimens belong to the second group. In addition to our specimens, Spirura narayani of Indian origin, with 4 pre-cloacal papillae, belongs to the first group. This undermines the geographic distribution reported by Babero (1973). Compared to species from North America (S. infundibuliformis, S. michiganensis, S. zapi) and India (S. leiperi), the specimens reported in the present study differ in the number of pairs of pre-cloacal papillae. The number of pre-cloacal papillae varies from 9 to 13 pairs and in the right spicule length of 800 lm or less in S. infundibuliformis (Anderson et al., 1993). The right spicule length of S. michiganensis is more than 800 lm and the number of pre-cloacal papillae usually less than 10 pairs (Babero, 1973). Spirura zapi usually has 10 pairs of pre-cloacal papillae and a right spicule length of 768 to 800 lm (Erickson, 1938). Spirura leiperi differs from our specimens by its 9 pairs of caudal papillae (5 pre-cloacal and 4 post-cloacal), right spicule length (310 lm), caudal alae length, the position of vulva, and egg size.
DISCUSSION Among 10 African species different from our specimens, S. portesiana is the only one described in a rodent, Scuiridae, of similar genus (Xerus rutilus) in the Ivory Coast. Its description, based on 3 immature females, cannot place it in a group, contrary to the proposition of Giannetto and Canestri Trotti, 1995. Compared to our specimens, the females of S. portesiana differ by
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the form of amphids, the presence of specific chitinous cephalic formations (not observed in all species of Spirura) (Campana and Chabaud, 1950), the vulva position, and the genital tractus form. In S. portesiana, ovojector and infandibulum are impair, directed posteriorly, before branching into the uteri, contrary to our specimens.Furthermore, X. rutilus, the type host, is not present in West Africa (Musser and Carleton, 2005; Granjon and Duplantier, 2009). Therefore, our specimens correspond to a new species. LITERATURE CITED ANDERSON, R. C., E. T. BARNES, AND C. M. BARTLETT. 1993. Restudy of Spirura infundibuliformis McLeod, 1933 (Nematoda: Spiruroidea) from Spermophilus richardsonii with observations on its development in insects. Canadian Journal of Zoology – Revue Canadienne de Zoologie 71: 1869–1873. BABERO, B. B. 1973. Nematodes of Nevada ground squirrel with description of two new species. Transactions of the American Microscopical Society 92: 265–272. BAYLIS, H. A. 1928. On a collection of nematodes from Nigerian mammals (chiefly rodents). Parasitology 20: 280–301. ´ CAMPANA, Y., AND A. G. CHABAUD. 1950. Note sur quelques nematodes africains de la collection Camille Desportes. Annales de Parasitologie ´ (Paris) 25: 308–324. Humaine et Comparee CANARIS, A. G., AND S. L. GARDNER. 2003. Bibliography of helminth species described from African vertebrates. Faculty publications from the Harold W. Manter Laboratory of Parasitology, University of Nebraska – Lincoln, Lincoln, Nebraska, 101 p. ´ CHABAUD, A. G., E. R. BRYGOO, AND A. J. PETTER. 1965. Les Nematodes ` parasites de Lemuriens malgaches. VI. Description de six especes ´ erales. ´ nouvelles et conclusions gen Annales de Parasitologie Humaine ´ 40: 181–214. et Comparee DIAGNE, M., M. DIOUF, L. LOCHOUARN, AND O. BAIN. 2000. Trichosomoides nasalis Biocca et Aurzi, 1961 et T. spratti n. sp. (Nematoda: ´ Parasite 7: Trichinelloidea) parasites de fosses nasales de murides. 215–220. DIOUF, M., C. T. BAˆ, AND B. MARCHAND. 2000. Pterygodermatites (Mesopectines) senegalensis n. sp. (Nematoda, Rictulariidae) parasite of Mastomys huberti (Rodentia, Muridae) in Senegal. Journal of Parasitology 86: 1313–1317. ———, ———, ———, AND O. FAYE. 1998. Subulura saloumensis n. sp. (Nematoda, Subuluridae) from four species of rodents in Senegal. Journal of Parasitology 84: 566–570. ———, I.-H. DAOUDA, AND M. C. DURETTE-DESSET. 2005. Two new Nippostrongylinae (Nematoda, Trichostrongylina, Heligmonellidae), coparasites of Matomys natalensis (Muridae, Murinae) from Benin. Zoosystema 27: 27–35. ———, AND M. C. DURETTE-DESSET. 2002. Two new species of Nippostrongylinae (Nematoda, Trichostrongylina), parasites of Cricetomys gambianus and Arvicanthis niloticus (Muridae) from Senegal. Parassitologia 44: 97–101. DURETTE-DESSET, M. C., C. BROUAT, M. DIOUF, AND J. M. DUPLANTIER. 2008. Description of two new species of Nippostrongylinae (Nematoda: Heligmonellidae), coparasites in three sympatric species of Mastomys spp. (Rodentia: Muridae) from Senegal. Parasite 15: 539– 551. ERICKSON, A. B. 1938. Parasites of some Minnesota Cricetidae and Zapodidae and a host catalogue of helminth parasites of native American mice. American Midland Naturalist 20: 575–589. GEDOELST, L. 1916. La Faune Africaine du Congo Belge. Revue Zoologique Africaine 5: 1–90. GIANNETTO, S., AND G. CANESTRI-TROTTI. 1995. Light and scanning electron microscopy of Spirura rytipleurites seurati Chabaud, 1954 (Nematoda: Spiruridae) from Erinaceus europaeus in Sicily. Journal of Helminthology 69: 305–311. GRANJON, L., AND J. M. DUPLANTIER. 2009. Les rongeurs de l’Afrique ´ soudano-sahelienne. Faune et flore tropicale, Publication scientifique ´ du Museum National d’Histoire Naturelle (MNHN), Paris, 215 p. HERING-HAGENBECK, S., J. BOOMKER, AND O. BAIN. 2001. Paraspirura bettinae n. sp. from a South African skink with comments on spirurid
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´ QUENTIN, J. C., AND M. KRISHNASAMY. 1975. Nematodes Spirura parasites ` des Tupaia et du Nictycebe en Malaisie. Annales de Parasitologie ´ 50: 795–812. Humaine et Comparee SEURAT, L. G. 1911. Sur l’habitat et les migrations du Spirura talpae Gmel ´ (¼Spiroptera strumosa Rud.). Comptes Rendus des Seances de la ´ e´ de Biologie et de ses Filiales 71: 606–608. Societ ´ ———. 1913. Sur quelques nematodes du sud tunisien. Bulletin de la ´ e´ d’Histoire Naturelle de l’Afrique du Nord 5: 126–130. Societ ´ ´ ———. 1915. Nematodes parasites. Expedition de MM. Walter Roth´ child, E. Harbert et C. Hilgert dans le sud algerien (Mars-mai 1914) 22: 1–25. SMALES, L. R., P. D. HARRIS, AND J. M. BEHNKE. 2009. A redescription of Protospirura muricola Gedoelst, 1916 (Nematoda: Spiruridae), a parasite of murid rodents. Systematic Parasitology 72: 15–26. VASSILIADES, G. 1980. Inventaire des Helminthes parasites d’Oiseaux du ´ egal. ´ Sen Bulletin de l’Institut Fondamental d’Afrique Noire 42: 122– 134. ´ es ´ du Sen ´ egal. ´ ———. 1992. Inventaire des Helminthes de Vertebr Revue ´ egalaise ´ Sen de Recherches Agricoles et Halieutiques 4: 72–83. ´ parasites avec VUYLSTEKE, C. 1956. Note sur quelques Nematodes ` description de neuf especes nouvelles. Revue de Zoologie et de Botanique Africaines 53: 441–477.
