Procamallanus (Spirocamallanus) juana, Ailán-Choke, 2017

Ailán-Choke, Lorena Gisela, 2017, Observations on two Procamallanus (Spirocamallanus) species (Nematoda: Camallanidae) from freshwater fishes in Argentina, including description of Procamallanus (Spirocamallanus) juana sp. nov., Zootaxa 4323 (2), pp. 286-294 : 287-293

Procamallanus (Spirocamallanus) juana sp. nov.

( Figs 1–2 )

Type material. Holotype: female CH-N-FML #07729; allotype: male CH-N-FML #07730; paratypes (four females, five males) CH-N-FML #07731.

Type host. Pimelodus albicans Valenciennes ( Siluriformes , Pimelodidae ), Ichthyology Collection CI-FML #6467, collected 30 May 2013.

Additional host: Pimelodella gracilis (Valenciennes) ( Siluriformes , Heptateridae), Ichthyology Collection CI- FML #6519, collected 30 May 2013.

Type locality. Salado River , Añatuya, General Taboada Department, Province of Santiago del Estero (28° 48’42”S, 62°39’0.9”W), Northwest Argentina .

Etymology. The new species is named in honor of the memory of Juana Rosa Bennasar de Herrera (“Ms. Monona”), colleague, friend and for years Director of Zoology Area, FML.

Site of infection.Intestine.

Infection parameters. For P. albicans , prevalence: 75% (3/4); media intensity: 3.3 nematodes per fish and for P. gracilis , 75% (3/4); 4 nematodes per fish, respectively.

Measurements. Table 1.

General description. Medium-sized nematodes with finely, transversely striated cuticle. Mouth aperture rounded, provided and surrounded by six visible pores, fourteen submedian cephalic papillae arranged in three circles, two circlets (medium and external) with four papillae each; and the inner circlet with six larger papillae. Pair of medium amphids present ( Fig. 1D , 2A ). Buccal capsule orange-brown, thick-walled, barrel-shaped, slightly longer than wide, with simple well developed basal cephalic ring; wall of middle part of capsule strengthened by conspicuous thickenings appearing in lateral view as drop-shaped, extending anteriorly to anterior margin of capsule. In both sexes, inner surface of capsule provided with several spiral ridges, which may be complete and incomplete (not extending from one lateral margin of capsule to other) ( Figs. 1A, B, C ). Muscular esophagus somewhat shorter than glandular esophagus; both parts of esophagus slightly expanded near their posterior ends ( Figs. 1A, C ). Intestine narrow. Deirids, observed only in males; small, simple, with rounded end situated at about mid-way between posterior end of buccal capsule and nerve ring ( Figs. 2B, C ). Excretory pore located approximately in the middle of the muscular esophagus( Figs. 1A, C ). Tail of females pointed and of males conical ( Figs. 1F, G ).

Adult female (five gravid specimens): Buccal capsule with 5–7 inner spiral ridges ( Figs. 1C ). Deirids absent. Vulva pre-equatorial with conspicuous lips ( Fig. 1E , 2E ). Vagina muscular, directed posteriorly from vulva. Uterus containing larvae ( Figs. 1E ). Tail pointed with terminal spike ( Figs. 1F , 2F ).

Adult Male (six specimens): Buccal capsule with 5–7 inner spiral ridges ( Fig. 1B ). Deirids present ( Figs. 2B, C ). Spicules of similar shape, but very unequal in length, right spicule larger than left, both with pointed distal ends ( Fig 1G ). Six pairs of sessile caudal papillae: three pairs preanal and three pairs postanal ( Figs. 1G , 2D ). Gubernaculum absent. Posterior end of body ventrally bent, provided with narrow caudal alae. ( Figs. 1G , 2D ). Tail conical ( Fig 1G ).

Remarks. The new species belongs to the genus Procamallanus Baylis, 1923 , which is characterized by the presence of a solid buccal capsule continuous with the inner surface smooth or with spiral ridges,spicules usually unequal, and caudal alae and gubernaculum present or absent in males. Three subgenera occur in Neotropical freshwater fishes. The new species herein described belongs to the subgenus Spirocamallanus Olsen, 1952 , because both males and females present spiral thickenings (ridges) in the buccal capsule and the base of the male capsule without teeth ( Moravec 1998).Between the species of Procamallanus (Spirocamallanus) recorded for the Neotropical Region, it is possibly distinguished as a morphological group that present caudal alae and unequal spicules, represented by P. (S.) rarus , P. (S.) solani Pinto, Fabio, Noronha & Rolas , P. (S.) paraguayensis (Petter) , P. (S.) freitasi (Moreira, Oliveira & Costas) , P. (S.) pimelodus Pinto, Fábio, Noronha & Rolas , P. (S.) dessetae (Petter, Golvan & Tcheprakoff) , P. (S.) rebecae (Andrade-Salas, Pineda-Lopez & Garcias-Magaña) and the new species herein described.

The general morphology of the new species is very similar to P. (S.) pimelodus ; both species are characterized by possessing three pairs of preanal papillae and caudal alae in males, the right spicule exceeds 0.70 mm and the vulva is pre-equatorial. However, both species differ in the number of cephalic papillae (14 vs. 8); the presence or absence of pores around the mouth aperture; the number of pairs of postanal papillae (3 vs. 8) and the shape of the female tail (pointed with a spike vs. conical without spike). By the presence of caudal alae in males, the new species also resembles P. (S.) rarus . Moreover both species were found in freshwater catfishes from Argentina. However, these species differ in that, P. (S.) juana sp. nov. has sessile caudal papillae, while those of P. (S.) rarus are pedunculated; the vulva in the new species is pre-equatorial while in P. (S.) rarus it is equatorial, and the spicules are simple in P. (S.) juana sp. nov. While P. (S.) rarus has unequal and dissimilar spicules, the large spicule with a small ventral outgrowth and the small spicule simple.

The presence of a digit-like projection provided with one or more small terminal cuticular spikes on the female tail, is a feature that the new species shares with some species of Procamallanus (Spirocamallanus) , parasites of freshwater and marine fishes ( Moravec et al. 2000). In the Neotropical Realm some species have this character. These include P. (S.) rebecae ; P. (S.) solani ; P. (S.) penneri (Fusco & Brooks); P. (S.) gobiomori Moravec , Salgado- Maldonado & Caspeta-Mandujano, 2000; and P. (S.) jaliscensis Moravec, Salgado-Maldonado & Caspeta- Mandujano, 2000; all of them are parasites of freshwater fishes ( Moravec 1998; Moravec et al. 2000). These species can be distinguished from P. (S.) juana sp.nov. by a series of morphological features (such as the number of spiral thickenings in the buccal capsule and the length of right spicule) and the geographical distribution.

Most of the species of Procamallanus (Spirocamallanus) have eight cephalic papillae arranged in two circlets. Nevertheless, the new species is the first in presenting fourteen cephalic papillae organized in three circlets, the external and median circlet formed by four papillae and the inner by six papillae, the papillae of the inner circlet distinctly large. Procamallanus (Spirocamallanus) halitrophus (Fusco & Overstreet) , P. (S.) rebecae , P.(S.) rigbyi Yooyen, Moravec & Wongsawad and P. (S.) similis Yooyen, Moravec & Wongsawad also have numerous cephalic papillae, all present 12 papillae organized in three circlets formed by four papillae each and the papillae of the external circlet are distinctly large ( Cardenas & Lanfredi, 2005; Yooyen et al. 2011). Nevertheless these species differ mainly in the host range and the geographical distribution. The first two species were recorded in the Neotropical Realm. Procamallanus (Spirocamallanus) halitrophus was record in marine fishes from the northern Gulf of Mexico and the coasts of Rio de Janeiro, Brasil; while P. (S.) rebecae was found in cichlid freshwater fishes from southern Mexico ( Moravec, 1998). In contrast to P. (S.) rigbyi and P. (S.) similis that were recorded in marine perciform fishes from the Gulf of Thailand ( Yooyen et al. 2011).

By the presence of pores surrounding the margin of the oral opening, P. (S.) juana sp. nov. resemble P. (S.) daleneae (Boomker) , P. (S.) spiralis Baylis and P. (S.) serranochromis Moravec & Van As. The first two present six pores, which coincides with the new species; while P. (S.) serranochromis has four pores in the cephalic end. Nevertheless, these species can be distinguished mainly from P. (S.) juana sp. nov. by the geographical distribution. Procamallanus (S.) daleneae and P. (S.) serranochromis were only recorded in African freshwater fishes. While, Procamallanus (S.) spiralis was also found in Africa and in different species of marine fishes in the Gulf of Suez, off the Atlantic and Pacific coasts of Mexico, in Philippine and Indonesian waters (off the Celebes), and in the Indian Ocean off the coast of Pakistan and India ( Moravec & Van As 2015).

Procamallanus (S.) juana sp. nov. can be distinguished from all congeners, by possessing 14 cephalic papillae arranged in three circlets (one of six papillae and two remaining with four papillae); six pores distinctly surrounding the mouth aperture; a buccal capsule with 5–7 spiral ridges; three pairs of preanal and three pairs of postanal papillae in males and a terminal cuticular spike on the female tail. Thus in this paper, we propose the erection of the new species of Procamallanus (Spirocamallanus) , which is the 30th species of this genus for Neotropical Realm and the sixth for Argentina.

Procamallanus (Spirocamallanus) hilarii Vaz & Pereira, 1934

Specimens examined. Six males and one female CH-N-FML #7732 isolated from Hyphessobrycon anisitsi (Eigenmann, 1907) (CI-FML #6429) from Salado River , Añatuya, General Taboada Department, Province of Santiago del Estero (28° 48’42”S, 62°39’0.9”W) , Northwest Argentina .

Infection parameters. Prevalence: 57% (4/7), mean intensity 1.75 nematodes per fish.

Diagnosis. Medium nematodes with transversely striated cuticle. Buccal capsule with 13–18 spiral thickenings, basal ring well development. Muscular esophagus claviform, much shorter than glandular esophagus. Male with three pairs of preanal, 1–2 pairs adanal and three pairs of postanal papillae. Gubernaculum absent. Spicules short and subequal. Larger spicule 0.070–0.082, small spicule 0.050–0.062.Tail conical.In females, vulva in middle of body; uterus containing larvae. Tail rounded with terminal caudal appendix.

Remarks. The morphological and morphometric analyses of the specimens analyzed by light microscopy, allowed the identification of Procamallanus (Spirocamallanus) hilarii , agreeing with the original description. Procamallanus (S.) hilarii belongs to a morphological group of species without caudal alae and with short and similar spicules in males, represented by P. (S.) chimusensis (Freitas & Ibañez) , P. (S.) inopinatus Travassos, Artigas & Pereira , P. (S.) krameri (Petter) , P. (S.) neocaballeroi (Caballero-Deloya) , P. (S.) paraensis Pinto & Noronha , P. (S.) pintoi (Khon & Fernandes) and P. (S.) saofranciscencis (Moreira, Oliveira & Costas) ( Moravec et al. 2004).

By the general morphology, Procamallanus (S.) hilarii is most closely related with P. (S.) neocaballeroi . Both species present numerous spiral ridges (13–19) occupying the whole inner surface of the buccal capsule and a glandular esophagus at least three times longer than muscular esophagus. Procamallanus (S.) neocaballeroi can be readily distinguished from Procamallanus (S.) hilarii by possessing equal spicules and four pairs of preanal papillae and six pairs of postanal papillae. Moreover these species differ in the geographical distribution in the Neotropical Region. Procamallanus (S.) hilarii was recorded for Brazil, Perú and Argentina; while P. (S.) neocaballeroi has only been recorded in Mexico ( Moravec 1998).

Discussion. The genus Procamallanus Baylis, 1923 comprises numerous species described in a broad variety of host and geographical regions, in both marine and freshwater fishes. Although, many authors (Andrade–Salas et al. 1994) consider Spirocamallanus Olsen, 1952 as a distinct genus, Moravec & Sey (1988) consider Spirocamallanus a subgenus of Procamallanus to accommodate the species where both males and females have the buccal capsule with spiral ridges. Nevertheless, it is clear that this taxonomic system based on the morphology of the buccal capsule is more or less artificial and does not reflect the phylogenetic relationships ( Moravec & Thatcher 1997).

Andrade-Salas et al. (1994) proposed an alphabetic list with all nominal species grouped according to the geographical zones. However, this list is outdated, because later new species of Procamallanus were described. With respect to the Neotropical Realm, species of Procamallanus (Spirocamallanus) occur both in marine and continental water systems. To date, there are 29 species recorded from freshwater fishes, and they are widely distributed for the Neotropical Realm; mainly in Mexico, Lesser Antilles, Venezuela, Brasil, Paraguay, Perú and Argentina.

In Argentina, there are five species of Procamallanus (Spirocamallanus) ( P. (S.) inopinatus , P. (S.) rarus , P. (S.) huacraensis , P.(S.) hilarii and P. (S.) pintoi ) recorded from characiform and siluriform freshwater fishes, mainly distributed in the regions northwest and northeast of the country. In the province of Corrientes, northeast region, it was registered P. (S.) inopinatus in Totora y Perez Lagoon, Riachuelo basin, and Riachuelo River Lagoon; and P. (S.) rarus in Parana River. Procamallanus (S.) inopinatus presents a wide host range. It was recorded from specimens of Characiformes ( Brycon orbignyanus Valenciennes , Poptella paraguayensis Eigemann , Leporinus maculatus Müller & Troschel , Serrasalmus marginatus Valenciennnes , S. spilopleura Kner , Pygocentrus nattereri Kner ) and Siluriformes ( Luciopimelodus pati Valenciennes and Pseudoplatysoma corruscans Spix & Agassiz). By contrast, P. (S.) rarus was only found in P. albicans ( Chemes & Takemoto 2011) . Moreover, there are many records of both species in Brasil. Procamallanus (S.) inopinatus is also recorded from Paraguay and Venezuela and P. (S.) rarus from Perú ( Moravec 1998). The new species herein described is most closely related with P. (S.) rarus by the presence of caudal alae and both species were found in the same host, P. albicans .

With respect to the northwest region, there are three species recorded: P. (S.) huacraensis , P. (S.) pintoi and P. (S.) hilarii . The first two were found only in catfishes: Trichomycterus corduvensis and T. spegazzini respectively (All Trichomycteridae ). Procamallanus . (S.) huacraensis was registered from Huacra and Vis-Vis Rivers, and Dike Agua Fresca (Catamarca Province). While, there is a unique record of P. (S.) pintoi in irrigation ditch tributary of River Yacones (Vaqueros municipality, Salta Province). Procamallanus (S.) hilarii was recorded in a wide host spectrum: Salminus brasiliensis Cuvier (= S. maxillosus Valenciennes ), Megaleporinus obstusidens Valenciennes (= Leporinus obstusidens Valenciennes ), Oligosarcus jenynsii Günther , Hoplias malabaricus Bloch, A. abramis Jenyns, A. lacustris Lutken, A. rutilus Jenyns, Piabina thomasi Fowler (all characids); Pimelodus albicans Valenciennes ( Pimelodidae , Siluriformes ) and Jenynsia alternimaculata Fowler ( Anablepidae , Cyprinodontiformes ). Its geographical distribution includes dam, rivers, streams and tributaries from several localities of the provinces of Tucumán, Santiago del Estero and Salta (Northwest Argentina) ( Ailan et al. 2014; Antelo et al. 2016; Ramallo 2008). Procamallanus (S.) juana sp. nov. was also found in P. albicans . Thus both species ( P. (S.) juana sp. nov. and P. (S.) hilarii ) share the same host species and present records in the province of Santiago del Estero. However, these species differ in their general morphology, mainly in the presence of caudal alae, the number of spiral ridges in the buccal capsule and the number of caudal papillae in males ( Moravec 1998).

With the new finding, the number of species of Procamallanus (Spirocamallanus) was extended for the Neotropical Realm. Moreover, P. (S.) hilarii extends its host range and geographical distribution.

Figures

FIGURE 1. Procamallanus (Spirocamallanus) juana sp. nov. (A) Male, anterior end, lateral view. (B) Male, head, lateral view. (C) Female, anterior end, lateral view. (D) Female, apical view. (E) Female, vulva, lateral view. (F) Female, tail, lateral view. (G) Male, posterior end with spicules and papillae, ventral view.

FIGURE 2. Procamallanus (Spirocamallanus) juana sp. nov. (SEM micrographs) (A) Male, cephalic end. Six pores (white arrows), amphids (black arrows). Scale = 10 µm. (B) Anterior end of male, sublateral view. Deirid (white arrow). Scale = 10 µm. (C) Detail deirid. Scale = 1 µm. (D) Posterior end of male, ventral view. Preanal papillae (white arrows). Scale = 10 µm. (E) Female, vulva, subventral view. Scale = 10 µm. (F). Female, posterior end, lateral view. Scale = 10 µm.