J. Parasitol., 92(2), 2006, pp. 346–349 q American Society of Parasitologists 2006
A NEW NEMATODE (NEMATODA: COSMOCERCIDAE) FROM THE LIZARD, CHAMAELEO INTURENSIS (SQUAMATA: CHAMAELEONIDAE) FROM THE DEMOCRATIC REPUBLIC OF CONGO Salah Bouamer and Serge Morand Centre de Biologie et de Gestion des Populations (CBGP), Campus International de Baillarguet, CS 30 016, 34988 Montferrier sur Lez Ce´dex, France. e-mail:
[email protected] ABSTRACT:
Maracaya africana n. sp. (Nematoda: Cosmocercidae) from the large intestine of the lizard Chamaeleo inturensis collected in Democratic Republic of Congo is described and illustrated. This is the first record of a species of Maracaya DiazUngria (1963) for Africa. Light microscopy and scanning electron microscopy (SEM) studies revealed morphological differences in the structure of the male caudal end and cephalic end, which enabled us to differentiate these new species from the others. A key for determination of all species in the genus is provided.
Maracaya was proposed by Diaz-Ungria (1963) for M. graciai from Amphisbaena sp. (dawn blind snakes) in Venezuela. Adamson and Baccam (1988) described M. belemensis from Amphisbaena alba Linnaeus, 1758, and retransferred Aplectana pusilla Miranda, 1924, from Amphisbaena sp. in Brazil to Maracaya. On the basis of the disposition of the caudal papillae in the males and the shape of the excretory pore in both sexes, Adamson and Baccam (1988) transferred Maracaya, Schrankiana Strand, 1942, Sckrankianella Freitas, 1959, Labeonema Puylaert, 1970, and Ibrahima Khalil, 1932, from the Atractidae to the Cosmocercidae. The present study gives the first record of a species of Maracaya out of the Neotropical region. Before the present, Maracaya contained 4 species parasites restricted to Squamata. MATERIALS AND METHODS Nematode parasites were recovered from the cecum of Chamaeleo inturensis Schmidt, 1919, from the Democratic Republic of Congo, No. 35019 from Museum Central Africa (Belgium), collected by R. P. Lejeune (17 January 1968). The worms were preserved in 70% ethanol before being cleared with lactophenol for study. Illustrations were made with the aid of a drawing tube. Nematodes were prepared for scanning electron microscopy (SEM) by being dehydrated in an alcoholic series, followed by critical point drying (M scope 500); they were then examined using a Hitachi S 520 SEM at 20 kv. Measurements are given in micrometers unless otherwise stated. DESCRIPTION
Maracaya africana n. sp. (Figs. 1–12) General: Small, thin body; cuticle thick. Large, traverse slit and prominent excretory pore, situated in anterior half, at level 3/4 posterior portion of corpus (fringed border not observed). Mouth triangular, with 2 rings of lips: external ring formed by 3 prominent and robust lips about 9 mm long, inside lateral surface of each lip with 2 bilobed cuticular transparent projection; internal ring formed by 3 short, transparent, and relatively large lips. Cephalic sense organs with inner circle of 6 terminal papillae, 2 pair on each lip; outer circle not observed. Two lateral amphids. Body cuticle bearing fine traverse striations about 30 apart, beginning just posterior to lips and continuing to end of tail. Lateral alae present, beginning 150 posterior to cephalic extremity and ending 100–200 anterior to anus. Buccal cavity without teeth, consisting of long lip cavity and shorter posterior region surrounded by esophageal tissue. Long esophagus, divided into 3 parts. Short pharynx, long corpus, short isthmus, wide and spherical-shaped bulb. Corpus poorly demarcated from isthmus and bulb. Received 18 July 2005; revised 20 September 2005; revised 26 September 2005; accepted 26 September 2005. 346
Male (based on 10 specimens): Testis beginning just posterior to midbody, running anteriorly and flexing posteriorly 630–649 posterior to base of esophagus, leading to seminal vesicle filled with round-spherical spermatids with central-located chromatin. Wide and elevated anal region, forming a prominent genital cone. Slender, short, and pointed tail. Spicules similar, equal, short, and slightly arcuate. Gubernaculum short than spicules. Fourteen paired and 1 unpaired caudal papillae distributed as follows: 5 medium-sized pairs pre-anal, with 4 slightly subventral and 1 lateral, anterior lip of anus with 3 ventral small-sized pair papillae and 1 large and mushroom shaped papilla; 1 medium-sized pair adanal and sublateral; 2 pairs postanal closed together and sublateral; 1 small-sized pair ventral near of the tail end. Dorsal papilla and Phasmids not observed. Body length (holotype) 2.485 mm, with maximum body width 88. Head width 22. Nerve ring 182 and excretory pore 313 from anterior end. Total esophagus length 503 mm, with pharynx and isthmus length, respectively 28 and 39, bulb length 83 and bulb width 62. Testes length 1.3 mm. Tail length 116, width 82. Spicules length 66. Gubernaculum length 38. Body length (2 paratypes) 2.389 (2.246–2.5) mm, with maximum body width 79 (66–88). Head width 23 (19–26). Nerve ring 200 (182–240), and excretory pore 346 (313–385) from anterior end. Total esophagus length 483 (437–203), with pharynx and isthmus length, respectively, 37 (25–31) and 36 (32–45), bulb length 77 (72– 83), and bulb width 56 (53–62). Testes length 1.214 (1.145–1.385) mm. Tail length 122 (108–137), width 80 (75–92). Spicules lengths 63 (54– 68). Gubernaculum length 40 (30–46). Female (based on 10 specimens): Monodelphic. Ovary coiled on dorsal side just posterior to base of esophagus. Oviduct flexing anteriorly, then posteriorly before passing via prominent sphincter to uterus containing 1 to 4 eggs. Uterus extending posteriorly, and flexing anteriorly to join vagina; vagina running posteriorly to vulva near midbody. Eggs large, thin shelled; those nearest vagina containing larvae. Tail conical. Body length (allotype) 2.381 mm, with maximum body width 81. Head width 22. Nerve ring 213 and excretory pore 344 from anterior end. Total esophagus length 522 mm, with pharynx and isthmus length, respectively, 31 and 42; bulb length 73, and bulb width 58. Vulva 1.59 mm from anterior end. Tail length 138. Eggs 89 3 53. Body length (2 paratypes) 2.41 (2.12–2.78) mm, with maximum body width 84 (79– 90). Head width 22 (20–24). Nerve ring 217 (199–245) and excretory pore 349 (338–356) from anterior end. Total esophagus length 528 (512–539) with pharynx and isthmus length, respectively, 33 (29–38) and 45 (39–48), bulb length 72 (69–78), and bulb width 56 (51–59). Vulva 1.579 (1.56–1.61) mm from anterior end. Tail length 141 (121– 149). Eggs 87 3 49 (88–50 3 91–57). Taxonomic summary Type host: Chamaeleo inturensis Schmidt, 1919, Royal Museum for Central Africa, Belgium, No. 35019. Type locality: Biombrue, Democratic Republic of Congo, 008109S; 0298149E. Site of infection: Large intestine. Type specimens: Royal Museum for Central Africa, Brussels, Belgium; Holotype No. MRAC 37465; Allotype No. MRAC 35019; 2 males paratype No. MRAC 37466; 2 females paratype No. MRAC 37467. Etymology: The name refers to the type locality.
BOUAMER AND MORAND—A NEW COSMOCERICID FROM AFRICA
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FIGURES 1–6. Maracaya africana n. sp. 1. Anterior end of female; 2. Cephalic end, en face of female; 3. Anterior end of the male; 4. Cephalic end, en face of male; 5. Caudal end of male, lateral view; 6. Caudal end of male, ventral view. Scale lines: 1. 100 mm, 2. 10 mm, 3. 100 mm, 4. 10 mm, 5. 30 mm, 6. 10 mm. Remarks Maracaya africana n. sp. was identified on the basis of the following criteria: shape of the oval opening, esophagus in both sexes, the size and similarity of the spicules, and the gubernaculum size. The new African species differs from other Neotropical species of the genus by the shape of the oral opening. In the new species, there are 2 rings of oral lips. In the other species, there is 1 ring. The shape of the cloacal region, the number and the disposition of the caudal papillae are also different; in the African species, the cloacal region is much wider than the rest of body. However, in the Neotropical species, this region is less wide than the rest of the body. The presence of 1 median and pre-anal mushroom-shaped papilla, and 2 sublateral, postanal, and close proximity of pairs of papillae in African species differentiate M. africana n. sp. from the Neotropical species. Finally, the
position of the excretory pore at the posterior end of the corpus in the new species differs from those in the Neotropical species, which are situated between the isthmus and the bulb.
DISCUSSION The Cretaceous was the most active period of Gondwanan fragmentation, with Indo-Madagascar separating from Antarctica by 130–125 myr, and South America separating from Africa around 100 myr (Scotese et al., 1988; Pitman et al., 1993; Smith et al., 1994), whereas Madagascar first broke away from Africa 165 myr ago, with movement ending by 121 myr ago (Rabinowitz et al., 1983).
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FIGURES 7–11. Maracaya africana n. sp. Scanning electron micrograph (SEM): 7. Anterior end of female; 8. Cephalic end, en face of female; 9. Cephalic end, en face of male; 10. Caudal end of male, lateral view; 11. Caudal end of male, ventral view. Scale lines: 7. 10 mm, 8. 10 mm, 9. 10 mm, 10. 30 mm, 11. 15 mm.
The Amphisbaenidae originated from Gondwana landmass; the divergence of this family occurred before 80 myr (Macey et al., 2004), with actual distribution in Neotropical and Ethiopian regions, except Madagascar. In contrast, the Chamaeleonidae originated from Madagascar, with multiple ‘out-ofMadagascar’ dispersal events to other Gondwanan landmasses (Raxworthy et al., 2002). There were no indications of Maracaya species in Chamaeleonidae or in other Squamata from Madagascar (Chabaud and Brygoo, 1960; Caballero, 1968; Petter, 1968), India (Deshmukh and Choudhari, 1980; Nagpur, 1981; Sood, 1999), or Australia
and New Guinea (Owen and Moorhouse, 1980; Moravec, 1990; Cameron and Cogger, 1992; Bursey and Goldberg, 1999, 2001). On the basis of the present knowledge, we hypothesize a South American origin for species of Maracaya, with dispersal events to Africa, which should have occurred before the separation between these 2 continents, i.e., from 110 to 100 myr (Scotese et al., 1988) until 95 myr ago (Raven and Axelrod, 1972). Chamaeleonidae may have been parasitized by species of Maracaya posterior to their ‘out-of-Madagascar’ dispersal events to Africa, according to the Madagascar origin of this family (Raxworthy et al., 2002).
BOUAMER AND MORAND—A NEW COSMOCERICID FROM AFRICA
Key to species of Maracaya 1 Oral opening with 1 row of lips, male anal region smaller than the rest of the body . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 1 Oral opening with 2 rings of lips, male anal region larger than the rest of the body . . . . . . . . . . . . . . . . . . . M. africana n. sp. 2 Bifid spicules . . . . . . . . . . . . . . . . . . . M. pusilla (Miranda, 1924) 2 Simple spicules . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 3 Pre-anal, sublateral, median papillae present; arcuate spicules; gubernaculum tapering more gradually . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .M. belemensis (Adamson & Baccam, 1988) 3 Pre-anal, sublateral, median papillae absent; straight spicules; large gubernaculum . . . . . . . . . . M. graciai (Diaz-Ungria, 1963)
ACKNOWLEDGMENTS We are indebted to Rudy Jocque´ (Royal Museum for Central Africa, Brussels, Belgium) for generously providing the Afrotropical nematodes.
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