Ischilinema baldoi, Serrano, Paula Carolina & Digiani, María Celina, 2016

Serrano, Paula Carolina & Digiani, María Celina, 2016, First record of Viannaiidae (Nematoda: Trichostrongylina) in fossorial rodents (Ctenomys spp.) from Central Argentina, with description of a new genus and species, Zootaxa 4168 (1), pp. 151-160 : 152-157

Ischilinema baldoi gen. n. sp. n.

( Figs. 1–14 )

Description. General: Small nematodes, mostly uncoiled. Excretory pore situated slightly before or behind oesophago-intestinal junction in males (84–106% of oesophagus length), more proximally in females (mostly within 71–93% of oesophagus length). Deirids minute, hardly visible, situated at level of excretory pore ( Fig. 1 ).

Head: Cephalic vesicle present. In apical view, triangular buccal opening with rounded corners, surrounded by thick ring. Six externo-labial and four submedian cephalic papillae visible ( Fig. 2 ).

Synlophe: (studied in 2 males and 2 females). In both sexes cuticle bearing longitudinal, uninterrupted ridges appearing posterior to cephalic vesicle. Number of ridges at oesophago-intestinal junction: 14 in male, 15 in female ( Figs. 3, 4 ); at mid-body and posterior third of body: 14–15 in male, 15 in female ( Figs. 5, 6 ). Size of ridges: at mid-body, ridges small, subequal, with those on left-ventral quadrant slightly larger, gradient in ridge size absent. Ridges with cuticular struts, oriented from right-ventral to left-dorsal quadrant. Axis of orientation of ridges single, inclined at about 65–70° in both sexes, determining two groups of 7–8 dorsal ridges and 7 ventral ones. On left side, presence of a cuticular dilatation supported by 3–4 ridges, cuticle between ridges 1’ and 2’ reinforced. Ridges almost equidistant, except distance between ridges 1’ and 2’, larger ( Figs. 5, 6 ). Within distal third of body: ridges small and subequal in size, mostly perpendicular to body surface; left dilatation supported by 5 ridges. Ridges supporting dilatation more spaced to each other than the other ridges ( Figs. 7, 8, 9 ). Disappearance of ridges at about 100 mm before caudal bursa in males ( Fig. 10 ), at ovejector level in females.

Males (n= 19 except where indicated) (syntypes from Ctenomys bergi ): 2.00–2.95 (2.54) mm long and 50–90 (66) wide at mid-body. Cephalic vesicle 28–45 (36) long and 18–28 (22) wide. Nerve ring, excretory pore and deirids situated at 100–150 (128) (n=11), 215–260 (234) (n=5) and 240–255 (248) (n=2) from apex, respectively. Oesophagus 220–260 (238) long.

Caudal bursa asymmetrical. Right lobe more developed than left one ( Fig. 11 ). Right lobe with pattern of type 1–4, with right ray 2 arising first from the common trunk of rays 2–6. Ray 3 thicker and longer than ray 2, both supporting ventral margin of lobe. Common trunk of rays 4–6 long, rays 6 diverging first, rays 4 and 5 apposed up to extremities ( Figs. 11, 12 ). Left lobe with atypical pattern of type 1-1-3, with rays 2 and 3 of similar size, short and arising separately on the common trunk of rays 2–6. Thick common trunk of rays 4–6, supporting left-dorsal angle of the bursa. Left rays 4–6 small, diverging distally from common trunk ( Figs. 11, 12 ). Dorsal lobe short. Dorsal ray thick and displaced towards right lobe. Branches of dorsal ray dissymmetrical, well separated, arising just posterior to arising of rays 8, left branch arising proximally. Each branch divided into two sub-branches, bearing papillae 9 (external) and 10 (internal). Rays 8 of similar length, arising dissymmetrically from dorsal ray, left ray 8 arising proximally. Both rays 8 reaching bursal margin ( Fig. 11 ). Spicules subequal, alate, not twisted, 215–320 (268) long, ending each in a rounded tip, enclosed in a membrane. SpL/BL 9.2–12.2 (10.6)%. Spicular alae visible ( Fig. 13 ). Gubernaculum not observed. Genital cone inconspicuous, not measured, papillae on genital cone not observed.

Females (n= 10 except where indicated) (syntypes from Ctenomys bergi ): 2.66–4.15 (3.59) mm long and 70– 100 (84) wide at mid-body. Cephalic vesicle 22–46 (38) long and 20–40 (24) wide. Nerve ring, excretory pore and deirids situated at 100–140 (118), 200–266 (219) (n=4) and 243 (n=1) from apex, respectively. Oesophagus 200– 275 (234) long. Monodelphic. Vulva situated at 58–80 (66) from caudal extremity (n=8). Vagina vera 9–12 (11) long (n=7), vestibule 50–85 (67) (n=8), sphincter 20–27 (24) long and 23–37 (30) wide, infundibulum 75–120 (92). Uterus 650–1240 (965) long, containing 10–16 (14) eggs, 55–75 long and 32–42 wide. UtL/BL 20.2–31.6% (26.5%). Tail conical, 25–45 (33) long ( Fig. 14 ).

Type-host. Ctenomys bergi Thomas, 1902 ( Rodentia, Hystricomorpha , Ctenomyidae ), MZUC I00 436.

Type-locality. Las Toscas , Salinas Grandes, Departamento Ischilín, Córdoba, Argentina (30°09'23.75"S – 64°55'36.24"W).

Prevalence and intensity of infection. 2 out of 3 hosts examined (P=66.6%) were parasitized with 218 and 8 worms, respectively.

Type material. 29 syntypes (19 males, 10 females) MLP-He 3504-1.

Other material studied. 1 male, 1 female MLP-He 3503-1 (same host species and locality, host not deposited).

Etymology. the species is dedicated to Mgr. Jorge Baldo (VICAM -CONICET) who captured and identified the hosts.

Other hosts and or localities. Ctenomys rosendopascuali Contreras, 1995 ( Rodentia , Ctenomyidae ). Xanaes River mouth, Mar Chiquita (30°57'15.91"S – 62°43'44.60"W), and lands of Milanesio family, Miramar (30°55'51.34"S – 62°41'53.42"W), both in Departamento San Justo, Córdoba, Argentina .

Site. Small intestine, secondarily in large intestine.

Prevalence and intensity of infection. 3 out of 7 C. rosendopascuali examined (P=42.8%) were parasitized with 3–65 (MI=26.6) worms, respectively.

Material deposited. 1 male, 2 females MLP-He 3498-1 (host MZUC I00430 ), 1 male, 11 females MLP-He 3501 (host MZUC I00434), 18 males, 47 females MLP-He 3505 (host not deposited).

Measurements of 10 (except where indicated) males from C. rosendopascuali . 1.80–2.50 (2.16) mm long and 55–70 (59) wide at mid-body. Cephalic vesicle 26–45 (36) long and 20–35 (26) wide. Nerve ring, excretory pore and deirids situated at 100–140 (124), 170–250 (206) (n=7) and 210–250 (229) (n=4) from apex, respectively.

Oesophagus 200–240 (218) long. Spicules 230–262 (248) long, SpL/BL 10.4–13.9 (11.5)%. Gubernaculum not observed. Genital cone inconspicuous, not measured, papillae on genital cone not observed.

Measurements of 18 (except where indicated) females from C. rosendopascuali . 2.35–3.35 (2.79) mm long and 60–80 (68) wide at mid-body. Cephalic vesicle 30–40 (37) long and 20–33 (26) wide. Nerve ring, excretory pore and deirids situated at 90–145 (114) (n=11), 163–200 (178) (n=7) and 166–200 (180) (n=4) from apex, respectively. Oesophagus 210–240 (226) long (n=11). Vulva situated at 48–57 (54) from caudal extremity (n=10). Vagina vera 7–12 (9) long (n=8), vestibule 50–80 (61) (n=8), sphincter 20–30 (26) long and 25–40 (30) wide (n=9), infundibulum 70–110 (84) (n=7). Uterus 540–860 (689) long, containing 7–17 (13) eggs, 60–85 long and 30–45 wide. UtL/BL 18.3–31.6% (24.5%).Tail 20–30 (24) long.

Differential diagnosis. The presence of a cephalic vesicle and a synlophe with an axis of orientation not bilaterally symmetrical, places these specimens into the superfamily Heligmosomoidea, as redefined by Durette- Desset (1983) and Durette-Desset & Chabaud (1993), which is composed of six families. Among these, the Herpetostrongylidae and the Nicollinidae are readily excluded: both families are characterized morphologically by having well developed buccal capsules and lips; in addition both have fairly restricted host and geographical distributions: saurians, monotremes and marsupials in the Australasian region ( Durette-Desset 1985, Beveridge et al. 2013). The lack of a spine on the female tail, and the axis of orientation of the ridges oblique and directed from the right-ventral to the left-dorsal quadrant, allow readily excluding the families Heligmosomidae and Ornithostrongylidae , respectively (see Beveridge et al. 2013).

The other two families of Heligmosomoidea, i.e. Heligmonellidae and Viannaiidae , are both well represented in South American Hystricognathi rodents (or Caviomorpha). The Heligmonellidae parasitic in caviomorphs belong to two subfamilies, the Heligmonellinae and the Pudicinae. The Heligmonellinae are characterized by synlophes with the left ridge and the right ridge (the single ridges situated just opposite to the lateral cords) distinct and well developed, whereas the Pudicinae possess either a well developed careen (left cuticular dilatation supported by two hypertrophied ridges) or comaretes (large ridges derived from the fusion of two or more ridges) ( Beveridge et al. 2013). The specimens studied here clearly lack these characters and show ridges which are subequal in size, preventing their inclusion in the Heligmonellidae .

The last family of Heligmosomoidea, the Viannaiidae , is at present composed of seven genera, three of which are parasitic in marsupials and four in caviomorph rodents: Viannella Travassos, 1918 , Avellaria Freitas & Lent, 1934 , Hydrochoerisnema Arantes & Artigas, 1980 and Oswaldonema Travassos, 1927 . The main character grouping the Viannaiidae of caviomorphs is the synlophe, which combines ridges subequal in size, an oblique axis of orientation and ridges absent on the lateral sides ( Durette-Desset 1971, 1983, Beveridge et al. 2013). The synlophe of the present specimens partly conform to this pattern, by having at mid-body an axis of orientation inclined at about 65–70° to the sagittal axis, and a distinct gap free of ridges on the left side, between ridges 1’ and 2’. In view of this, we have opted to include these specimens in the family Viannaiidae , though some particular characters of the synlophe and caudal bursa do not allow their inclusion in any of the known genera.

The genus Viannella comprises eight species described from five families of caviomorphs and a primate from Brazil and Argentina : Viannella hydrochoeri (Travassos, 1914) (type species), Viannella argentina Freitas, Lent & Almeida, 1937 , Viannella brevispicula (Lent & Freitas, 1936) , Viannella dubia (Travassos, 1921) , Viannella lenti Durette-Desset, 1968 , Viannella travassossi Pinto, 1935 , Viannella trichospicula Durette-Desset, Gonçalves & Pinto, 2006 , and Viannella viscaciae Goodey, 1925 . All these species differ from our specimens mainly by having subsymmetrical bursae with well developed dorsal lobes, spicules short and twisted, and synlophes (known only in 5 species) with ridges in two distinct groups (dorsal and ventral or right-dorsal and left-ventral), more or less separated by left and right gaps ( Travassos 1937, Durette-Desset 1971, Durette-Desset et al. 2006).

The genus Avellaria is composed of two species described from Cuniculidae and Dasyproctidae in Brazil ( Freitas & Lent 1934, Durette-Desset et al. 2006). They share with our specimens relatively long spicules not twisted, but with synlophes with ridges separated into two distinct groups, like some species of Viannella , and subsymmetrical bursae with the dorsal lobe reduced. In addition, species of Avellaria are characterized by having didelphic females ( Durette-Desset et al. 2006), a character which separates them clearly from the specimens studied here.

The monotypic Hydrochoerisnema anomalobursata Arantes & Artigas, 1980 is a parasite of capybaras Hydrochoerus hydrochaeris (L.) ( Caviidae ). It is characterized by a bursa with the left lobe strongly chitinized, with rays 3 to 6 appearing as fused, and a synlophe with dorsal and ventral ridges in two distinct groups, separated in the female by two lateral cuticular thickenings without ridges, and in the male only by two lateral gaps ( Arantes & Artigas 1983). These differences in the bursa and the synlophe allow the differentiation of H. anomalobursata from the present specimens. The erection of the subfamily Hydrochoerisnematinae to accommodate this single taxon ( Arantes & Artigas 1983) seems poorly justified and was contested by Beveridge et al. (2013), who also questioned the taxonomic validity of the genus.

The genus Oswaldonema (= Heligmoskrjabinia Freitas & Lent, 1937 ) is at present composed of two closely related species, Oswaldonema cruzi Travassos, 1927 and Oswaldonema skrjabini ( Freitas & Lent, 1937) , both coparasitic in Cuniculus paca (L.) ( Cuniculidae ) from Brazil. Both species share a strong asymmetry of their caudal bursae, involving the lateral lobes, the rays 8 and the dorsal lobe. In both species the right ray 8 appears hypertrophied and displaced to the right whereas the left ray 8 is associated with the left trunk of rays 3–6 rather than with the dorsal lobe. The dorsal lobe, which emerges from the right ray 8, is atypically composed of three branches, all three forked at different levels and bearing papillae whose homologies with papillae 9, 10 and phasmids are not clear. In addition, in both species the pattern on the right lobe is of type 3–2; that on the left lobe being more variable, but with the characteristic of the left ray 8 incorporated into the common trunk of rays 3–6 ( Travassos 1937, Freitas & Lent 1937). The asymmetry of the bursa of our specimens, involving mainly the elements of the dorsal lobe, evokes the species of Oswaldonema , however in these latter the dissimilar development of both rays 8 and the arising and position of the dorsal ray are significant differences with respect to these specimens. The pattern of the lateral lobes is also different, with a predominant pattern of type 3–2 on the right lobe in Oswaldonema spp. versus a pattern of type 1–4 in these specimens. Concerning the synlophe, only that of O. skrjabini is known: it shows 9 unequal ridges: three right-dorsal, five mid-ventral, plus one isolated, minute ridge, situated on the left, just above the left lateral field ( Durette-Desset & Pinto 1977). We consider these differences in the bursa and the synlophe enough for separating our specimens also from species of Oswaldonema .

The difficulty of assigning these specimens to any of the known genera of Viannaiidae requires the erection of a new genus. We propose for the new taxon the name of Ischilinema baldoi gen n. sp. n. A key to the genera of Viannaiidae parasitic in caviomorphs is proposed below.

Figures

FIGURES 1 – 10. Ischilinema baldoi gen. n. sp. n. 1, female, anterior extremity, right lateral view. 2, female, head, apical view. 3 – 11, synlophe in transverse sections of the body: 3, 4, at oesophago-intestinal junction, 3, male, 4, female; 5 – 6, at mid-body, 5, male, 6, female; 7 – 10, within distal third of body length, 7, male at 500 µ before caudal bursa, 8, female at 500 µ from posterior extremity, 9, male at beginning of spicules, 10, male, at 100 µ before caudal bursa. Abbreviations: R, right, V, ventral. All sections oriented as in Figure 3.

FIGURES 11 – 14. Ischilinema baldoi gen. n. sp. n. 11 – 12, male, caudal bursa, 11, bursa spread out, ventral view, 12, bursa folded, left lateral view, right branch of dorsal ray omitted. 13, male, spicules in situ, showing spicular alae. 14, female, posterior extremity, left lateral view. Abbreviations: 2 r- 8 r, right rays 2 to 8; 2 l- 8 l: left rays 2 to 8.