A new species of Stilestrongylus (Nematoda, Heligmonellidae) from the Atlantic Forest of Misiones, Argentina, parasitic in Euryoryzomys russatus (Cricetidae, Sigmodontinae)

A new species of Heligmonellidae (Trichostrongylina, Heligmosomoidea), Stilestrongylus kaaguyporai n. sp. is described from the small intestine of Euryoryzomys russatus (Rodentia, Cricetidae, Sigmodontinae) from the Argentine Atlantic Forest, in the Misiones province. The new species was found at Campo Anexo Manuel Belgrano, Reserva de Vida Silvestre Urugua-í and Parque Provincial Urugua-í, with a prevalence of 73% in 15 hosts examined. Stilestrongylus includes 24 Neotropical species, all parasitic in rodents, mostly Sigmodontinae. Stilestrongylus kaaguyporai n. sp. can be differentiated from its congeners by the following characters: caudal bursa dissymmetrical with right lobe larger and pattern of type1–4 in both lobes, rays 6 not forming a lateral trident with rays 4 and 5, rays 8 with dissymmetrical pathway, genital cone hypertrophied with a conspicuous hood-like projection and females with a marked dorso-ventral torsion of the posterior end. This report is the second record of a Stilestrongylus species in E. russatus, increasing to nine the number of parasitic species known from this host.

Parasites were fixed in 10% formaldehyde and preserved in 70% alcohol. The synlophe was studied following Durette-Desset (1985), and the nomenclature referring to the axis of orientation and other characters of the synlophe follows Durette-Desset and Digiani (2005) and Durette-Desset et al. (2017). The use of terms for the caudal bursa follows Durette-Desset and Digiani (2012). The nomenclature above the family group for the Strongylida (Nematoda) follows Durette- Desset and Chabaud (1993). Ridges are considered as dorsal or ventral with respect to the axis of orientation and not to the lateral hypodermal cords.
Measurements are given in micrometres, except where stated otherwise. Type specimens of parasites are deposited in the Helminthological Collection of the Museo de La Plata, La Plata, Argentina (MLP-He). The type host is deposited in the Mammal Collection of the Centro Nacional Patagónico (CNP), Puerto Madryn, Chubut and is mentioned in this manuscript under the field number (CG 553).
The research was conducted in compliance with Argentine laws (see Compliance with ethical standards).

Results
Parasitized rodents were found in all three localities sampled (CAMB, RVSU and PPU). The specimens studied were found in the small intestine of 11 of 15 (P = 73%) specimens of E. russatus harbouring 3-215 (mean = 67.3) worms.

Figures 1-15
Description General: Small nematodes, strongly coiled sinistrally along ventral side in 3-5 spirals in males, more loosely and irregularly coiled in females. Excretory pore 68-90% of oesophageal length in males, 63-90% in females. Deirids are situated at level of excretory pore (Fig. 1). Head: Cephalic vesicle elongate. In apical view, rounded buccal opening surrounded by very thin ring. Two amphids, four externo-labial papillae and four submedian cephalic papillae observed (Fig. 2). Synlophe: (studied in one male and one female paratypes). In both sexes, cuticle bearing longitudinal, uninterrupted ridges appearing mainly on left side posterior to cephalic vesicle, up to oesophago-intestinal junction, disappearing just anterior to caudal bursa in male and anterior to vulva in female. Ridges with cuticular struts. Struts usually flanked by cuticular folds (Fig. 3). Number of ridges: at level of oesophago-intestinal junction, 21 in male and 24 in female (Figs. 4 and 5), at mid-body, 25 in male and 24 in female (Figs. 6 and 7). At about 530 anterior to bursa, 26 in male, and in female, at mid-uterus level, 24 ridges (Figs. 8 and 9). At oesophago-intestinal junction and at mid-body, ridges slightly unequal in size, with rightventral ridges smaller. Within distal third of body, ridges subequal in both sexes. Most ridges with marked orientation. In male, at oesophago-intestinal junction, and in female at level of uterus, right-ventral ridges oriented more perpendicularly to body surface. Double axis of orientation of ridges; right axis inclined at about 65°a nd left axis at 83°to sagittal axis in both sexes.
Holotype male: 3.72 mm long, 104 wide at mid-body, cephalic vesicle 70 long and 28 wide, nerve ring, excretory pore and deirids situated 200, 270 and 255 from apex, respectively. Oesophagus 335 long (Fig. 1). Caudal bursa dissymmetrical though not markedly, with right lobe larger and pattern of type 1-4 in both lobes (Fig. 10a). Prebursal papillae not observed. Rays on both lobes with similar development. Rays 3 straight, similar in length to rays 2, rays 4 and 5 divergent at extremities. In right lobe, ray 3 arising more distally than ray 6 from common trunk of rays 3 to 6, ray 6 similar in length to ray 3; in left lobe, rays 3 and 6 arising at about same level, ray 6 markedly shorter (Fig. 10a). Dorsal lobe medium sized. Rays 8 with different pathways, both arising from proximal third of dorsal ray: right ray 8 arising slightly proximally, close to lateral trunk of rays 2-6 and parallel to it; left ray 8 arising somewhat distally and separated at its origin from lateral trunk of rays 2-6 ( Fig. 10b). Both rays 8 contact ray 6 at the origin of the latter then directed posteriorly (Fig. 10a). Dorsal ray divided at distal third into two branches, these latter dividing apically into rays 9 (external) and 10 (internal). Genital cone 46 long by 30 wide at base, hypertrophied, with hood-like projection on dorsal lip, bearing sessile papillae 7 laterally (Fig. 11). Papilla 0 not observed. Gubernaculum 49 long and 26 wide at base in ventral view (Fig. 11). Spicules subequal, alate, 860 long, representing 23.4% of body length. Tips of spicules with marked distal bend and joined but not fused. Separated tips reveal left spicule fitting into right one (Fig. 12).
Stilestrongylus barusi is readily differentiated from these specimens by having a strongly dissymmetrical bursa with the left lobe very poorly developed, implying that the left lobe is smaller but also the left rays are markedly smaller than the right ones, in contrast with our specimens, in which rays on both lobes have a similar degree of development. Stilestrongylus dessetae and S. renaudae differ from these specimens by possessing subsymmetrical bursae and having, in both lateral lobes, rays 3, 4 and 5 parallel and apposed throughout most of their length, diverging distally at about the same level and forming a distinct lateral trident. This same pattern is observed in the left lobe of S. peromysci, in which the bursa has not been illustrated fully opened, and only the left lobe shows a more or less clear pattern of the rays 2 to 6. Concerning S. eta, there are four different illustrations of the bursa for this species provided by Travassos (1937) (three figures) and by Simões et al. (2011) (one figure), which account for some differences in the bursal symmetry and the disposition of the right lateral rays. However, all of them differ markedly from our specimens by having the left rays 4, 5 and 6 arising at the same level (vs. rays 6 markedly proximal in our specimens), and both rays 8 with a similar pathway, parallel to the lateral trunk of rays 2-6 (vs. left ray 8 bent posteriorly). In addition, the spicule length is half that of our specimens.
Furthermore, two characters mentioned in the Description seem to be peculiar to our specimens: the conspicuous dorsal hood-like projection on the male genital cone, and the marked bend and torsion of the posterior end of the female. We consider that the whole of these differences allows us to designate a new species, for which we propose the name Stilestrongylus kaaguyporai n. sp.
Since another species of Stilestrongylus, S. lanfrediae, can be found in the same host and area, it may be worthwhile to remark that S. lanfrediae is differentiated from the new species by a bursal pattern of type 2-2-1 in both lobes, a marked dissymmetry of the dorsal lobe involving both the rays 8 and the branches of the dorsal ray, and spicules thick and markedly striated.