Nippostrongylus smalesae, Asakawa, 2017

Asakawa, Mitsuhiko, 2017, Nippostrongylus smalesae sp. nov. (Nematoda: Heligmonellidae) collected from Maxomys whiteheadi (Rodentia: Muridae) of Sumatra, Indoneisa, Zootaxa 4323 (4), pp. 579-585 : 580-583

Nippostrongylus smalesae sp. nov.

( Figs. 1–11 )

General: Trichostrongyloidea: Heligmonellidae : Nippostrongylinae . Small worms often forming sinistral coils with ventral side located inside. Cephalic vesicle present ( Fig. 1 ). Mouth triangular, surrounded by 4 cephalic papillae and amphidial pores ( Fig. 2 ). Cuticle finely striated; synlophe well developed with pointed ridges, commencing just posterior to cephalic vesicle and ending anterior to bursa in male and at vulval level in female ( Figs. 1, 5 , 10, 11 ). In midbody of both sexes 14 ridges present ( Figs. 3 , 8 ); carene of type A supported by hypertrophied left lateral ridge 1’ present; axis of orientation of ridges passing through ventral-right and dorsal left sides, inclined ca. 45° from sagittal axis; ridges 2’ to 4’ well developed; ridges 5 and 6 larger than other ridges in dorsal side of axis of orientation; ventral right and dorsal ridges less developed. Esophagus club-shaped. Nerve ring slightly posterior to midlevel of esophagus; excretory pore and deirids at midlevel between nerve ring and esophago-intestinal junction.

Male (holotype and 9 paratypes): Length 2.61–3.36 (2.94) mm; width at midbody 59–67 (63). Cephalic vesicle 44–54 (51) long by 24–30 (25) wide. Nerve ring 152–183 (170), excretory pore 228–285 (252) and deirids 233– 278 (251) (n=8) from cephalic end. Esophagus 270–320 (295) long and 20–24 (23) wide near posterior end. Body ridges becoming smaller in posterior body and restricting to left ventral side at prebursal level ( Fig. 4 ). Bursa markedly asymmetrical with larger right lobe folding over dorsal lobe partly ( Figs. 5, 6 ). Bursal rays of right lobe thicker than those of left lobe except rays 6 and 8. Right lobe: ray 2 much shorter and thinner than and distally divergent from ray 3; ray 3 shorter than ray 4; rays 4 and 5 thick, long and distally divergent; distance between papillae 3 and 4 nearly shorter than distance between papillae 4 and 5; ray 6 much thinner and shorter than other laterals ( Figs. 5, 6 ). Left lobe: rays 2, 3, 4 and 5 divergent distally; distance between papillae 3 and 4 wider than that between papillae 2 and 3, and papillae 4 and 5; rays 3 and 4 nearly same in length; ray 6 much thicker, widely divergent from other laterals; distance between papillae 5 and 6 more than four times larger than distance between papillae 4 and 5; papilla 6 close to papilla 8 ( Figs. 5, 6 ). Ray 8 of both sides diverged at same level from common trunk with dorsal ray; right ray 8 thinner than left ray 8; dorsal ray divided into 2 asymmetrical branches: right branch longer and re-divided into 2 offshoots at middle of its length; left branch divided into 2 offshoots immediately after primary branching of dorsal ray; each of both inner offshoots giving rise of minute protuberance directing laterally near distal end ( Figs. 5, 6 ). Spicules alate, similar in length, distally united, not strongly twisted, to form pointed end, 285–355 (324) long ( Figs. 5–7 ). Gubernaculum small, 25–35 (28) long ( Figs. 5–7 ).

Female (allotype and 9 paratypes): Length 2.79–5.56 (3.77) mm; 61–75 (69) wide at midbody. Cephalic vesicle 40–61 (51) long by 24–38 (29) wide. Nerve ring 108–175 (133), excretory pore 143–255 (196) and deirids 165–260 (203) from cephalic end. Esophagus 250–330 (283) long and 24–28 (26) wide near posterior end. In prevulval portion, ridges becoming fewer in number but with stout support ( Fig. 9 ); body distended at dorsal right side lacking prominent ridges. Anus 23–30 (27) and vulva 83–148 (111) from caudal apex ( Figs. 10, 11 ). Vagina vera 20–40 (31) long, vestibule 38–73 (51) long, sphincter 20–33 (26) long and infundibulum 38–88 (63) long ( Fig. 10 ). Cuticle distended at prevulval level forming small prepuce in some worms. Tail conical with blunt end. Eggs ellipsoidal, thin-shelled, containing early cleavage stage embryo at deposition, 54–65 by 26–34.

Taxonomic summary.

Type host: Maxomys whiteheadi (Thomas, 1894) (Whitehead’s spiny rat) ( Muridae : Murinae ). Type locality: Bukit Batu, Bengkalis, Riau, Sumatra, Indonesia. Site in host: Small intestine.

Date of collection: 6 April 2011.

Coparasites: Syphacia maxomyos Dewi et al., 2015 and Sabanema cf. montana.

Specimens deposited: Holotype male and allotype female (MZBNa 735), 9 male and 9 female paratypes (MZBNa 736).

Etymology. The species epithet is dedicated to Dr. Lesley R. Smales, an outstanding parasitologist contributing to the zoogeography of murine helminths in Sahul region.

Remarks. The present species possesses every feature characteristic of the genus Nippostrongylus Lane, 1923 ( Durette-Desset, 1970, 1983). Nine named species have been known in Nippostrongylus , i.e., N. brasiliensis (Travassos, 1914) , N. djumachani (Tenora, 1969) , N. magnus ( Mawson, 1961) , N. marhaeniae Hasegawa & Syafruddin, 1995 , N. rauschi Chabaud & Desset, 1966 , N. rysavyi (Erhardová, 1959) , N. sembeli Hasegawa & Tarore, 1995 , N. typicus ( Mawson, 1961) , and N. witenbergi Greenberg, 1972 ( Durette-Desset, 1970; Hasegawa, 1999). By having widely diverged rays 3 and 4 in the left lobe of the bursa copulatrix, the present species is readily distinguished from all of these congeners ( Mawson, 1961; Beveridge & Durette-Desset, 1992; Chabaud & Desset, 1966; Durette-Desset, 1970; Greenberg, 1972; Hasegawa, 1999; Hasegawa & Tarore, 1995; Hasegawa & Syafruddin, 1995). Two unnamed species, Nippostrongylus sp. ‘Taiwan’ from Niviventer culturatus (recorded as N. confucianus ) of Taiwan and Nippostrongylus sp. ‘Kalimantan’ from N. cremoriventer of Kalimantan, Indonesia, were also known ( Hasegawa, 1990, 1999). The former species possesses rays 3 and 4 of the left lobe close together, differing from the present species ( Hasegawa, 1990). Meanwhile, in the latter species, the rays 3 and 4 are divergent in the left lobe of the bursa copulatrix resembling the present one ( Hasegawa, 1999). The worms collected from M. whiteheadi in Kalimantan are presumably conspecific with Nippostrongylus sp. ‘Kalimantan’ although the body length was generally shorter ( Table 1). Although those from Kalimantan showed less prominent divergence of the rays 3 and 4 in the left lobe (see Fig. 3C of Hasegawa, 1999) and shorter spicules ( Table 1), they are surmised to be the same species with the present worms.

* Distance from cephalic apex. ** Distance from caudal apex.

Figures

FIGURES 1 – 7. Male of Nippostrongylus smalesae sp. nov. collected from Maxomys whiteheadi in Riau, Sumatra, Indonesia. 1. Anterior end of holotype, left lateral view. 2. Cephalic end, apical view. 3. Cross section through midbody. Arrow indicating axis of orientation of synlophe. 4. Cross section through prebursal level. 5. Posterior end of holotype, left lateral view. 6. Bursa copulatrix, severed, ventral view. 7. Distal ends of spicules and gubernaculum. Abbreviations: D. dorsal; Dl. dorsal lobe; L. left; Ll. left lobe; R. right; Rl. right lobe; V. ventral.

FIGURES 8 – 11. Female of Nippostrongylus smalesae sp. nov. collected from Maxomys whiteheadi in Riau, Sumatra, Indonesia. 8. Cross section through midbody. Arrow indicating axis of orientation of synlophe. 9. Cross section through vestibule. 10 and 11. Posterior end of allotype showing ovejector (10), right lateral view and body ridges (11), left lateral view. Abbreviations: D. dorsal; L. left; R. right; V. ventral.