Nereis oligohalina (Rioja, 1946)

Conde-Vela, Victor M. & Salazar-Vallejo, Sergio I., 2015, Redescriptions of Nereisoligohalina (Rioja, 1946) and N. garwoodi Gonzalez-Escalante & Salazar-Vallejo, 2003 and description of N. confusa sp. n. (Annelida, Nereididae), ZooKeys 518, pp. 15-49 : 18-23

Taxon classification Animalia Phyllodocida Nereididae

Nereis oligohalina (Rioja, 1946) Figures 1, 2, 6A, D, J–L, O, Q

Neanthes oligohalina Rioja 1946: 207-210, pl. 1, figs 3-6, pl. 2, figs 13-19; 1947: 529, 531; 1960: 295.

Nereis oligohalina Hartman 1951: 46; 1954: 414.

Type material.

Veracruz, Mexico. Neotype ECOSUR 0172 and paraneotypes ECOSUR 0173 (5), mouth of Actopan River (19°25'2.95"N, 96°19'32.28"W), Chachalacas Sandbar, Gulf of Mexico, 1 m depth, on Crassostrea virginica reef, fine sediment, April 10 2012, Coll. V.M. Conde-Vela, A.E. Te-Gómez.

Additional material.

Veracruz, Mexico. ECOSUR P2826 (15), and ECOSUR P2827 (37), Mouth of Actopan River (19°25'2.95"N, 96°19'32.28"W), Chachalacas Sandbar, Gulf of Mexico, 1 m depth, on Crassostrea virginica reef, fine sediment, April 10 2012, Coll. C. Licona-Rosado, V.M. Conde-Vela, A.E. Te-Gómez. ECOSUR P2828 (1) Laguna de Alvarado, St. 8 (18°45'20.34"N, 95°46'29.04"W), December 6 2012, in rocks, Coll. J.M. Aguilar-Camacho. ECOSUR-OH-P0760 (23), Las Barrillas, St. 4 (18°11'20.15"N, 94°35'56.97"W), December 5 2012, on Crassostrea virginica culture, Coll. J. Cruz-Terrón. ECOSUR-OH-P0761 (15), Laguna Grande, Mandinga, St. 28 (19°1'54.96"N, 96°4'8.10"W), December 10 2012, on oyster, 11.41‰, 27.24 °C, Coll. T.F. Villalobos-Guerrero, MA. Tovar-Hernández, J.M. Aguilar-Camacho. ECOSUR-OH-P0762 (3), Laguna Grande, Mandinga, St. 26 (19°2'20.64 ’’ N 96°4'24.24"W), December 10 2012, on mangrove and oyster, 10.74 ‰, 26.63 °C, Coll. J.M. Aguilar-Camacho, T.F.Villalobos-Guerrero. UANL-3918 (6), Estero Casitas, Nautla, March 25 1990, Coll. A. Contreras-Arquieta.

Neotype locality.

Mouth of Actopan River (19°25'2.95"N, 96°19'32.28"W), Gulf of Mexico, in Crassostrea virginica (Gmelin) reef, in muddy sediment, 1 m depth.

Description.

Neotype complete (ECOSUR 0172), atokous female. Body tapering, 38 mm long, 2.1 mm wide, 74 chaetigers, filled with oocytes. Body yellowish, reddish brown pigmentation present dorsally on first quarter of body, discoloring towards midbody chaetigers; lateral oblique pale lines along chaetigers 1-9 (Fig. 1A), replaced by fingerprint-like lines from chaetiger 10 (Fig. 6L), anterior margin of segments with thin transverse band (Fig. 1A). Prostomium with pigmentation reddish brown along inner half of palps and around eyes; two broad hourglass-shaped lines extending from antennae towards eyes, separated by a thin pale line and two oval patches, one on each side of darker areas (Fig. 1A). Peristomium pigmented, pale lines present (Fig. 1A).

Prostomium 1.5 times longer than wide; antennae cirriform, slightly passing palps; eyes subequal, black, in trapezoidal arrangement (Fig. 1A). Peristomium three times longer than first chaetiger; tentacular cirri with short ceratophores; dorsal cirri longer than ventral ones, longest posterodorsal cirri reaching chaetiger 6 (Fig. 1A).

Pharynx dissected; jaws light brown with 11 rounded teeth, extending to base (Fig. 1G). Maxillary ring: I = 12 cones in triangle, II = 32-31 cones in arc, III = 50 cones in an ellipse, IV = 34-32 cones in arc. Oral ring: V = 1 cone, VI = 4-4 pyramids in diamond, VII-VIII = 42 in two irregular rows, P-bars alternating with small pyramids in anterior-most row, similar-sized pyramids alternating in posterior-most row (in everted pharynx).

Parapodial cirri pattern: Dorsal cirri longer than upper dorsal ligules throughout body; basally inserted on anterior region, displaced medially on midbody and posterior chaetigers. Ventral cirri shorter than neuropodial ligules throughout body, longer in few anterior chaetigers, basally inserted on anterior region, progressively distant throughout body.

First two chaetigers uniramous, remaining ones biramous. Uniramous parapodia (Fig. 1C) with dorsal cirri basal, slightly longer than dorsal ligules. Dorsal ligules digitate; neuroacicular ligules subconical, subequal to dorsal ones; neuropodial ventral ligules digitate, slightly longer and basally twice as broad as dorsal ones. Ventral cirri slightly shorter than neuropodial ventral ligules; both dorsal and ventral cirri with similar width.

In anterior parapodia (Fig. 1D), dorsal cirri medial, slightly longer than notopodial dorsal ligules, extending beyond their tips. Notopodial dorsal ligules subconical; subequal to ventral ones; notopodial ventral ligules globose, notoacicular papillae conspicuous. Neuroacicular ligules globose, postchaetal lobes rounded, slightly shorter than neuroacicular ligules; neuropodial ventral ligules digitate, slightly shorter than neuroacicular ones. Ventral cirri shorter than neuropodial ligules; both dorsal and ventral cirri with similar width.

In middle and posterior parapodia (Fig. 1E, F), dorsal cirri medial, slightly shorter than notopodial dorsal ligules. Notopodial dorsal and ventral ligules subequal, subconical, longer than wide, notoacicular papillae conspicuous in middle parapodia only. Neuroacicular ligules subconical, wider than long, postchaetal lobes rounded, about half as long as neuroacicular ligules; neuropodial ventral ligules digitate, 3-4 times longer than wide, medially attached to neuroacicular ligules, 2-3 times longer than them. Ventral cirri half as long or one-third as long as neuropodial ventral ligules; dorsal and ventral cirri with similar width. Glandular masses slightly conspicuous on ligules in posterior parapodia (Figs 1F, 6Q).

In anterior and midbody parapodia notochaetae homogomph spinigers; neurochaetae homogomph spinigers and heterogomph falcigers in supra-acicular fascicles, heterogomph spinigers and falcigers in sub-acicular fascicles. In posterior parapodia, notochaetae homogomph spinigers and falcigers; neurochaetae as in anterior parapodia. Chaetae decreasing rapidly in number toward posterior end.

Notopodial homogomph spinigers pectinate (i.e. blade narrow with parallel teeth), teeth decreasing distally (Fig. 1N). Notopodial homogomph falcigers with sigmoidal blade, pectinate, distal tooth recurved, fused to blade (Fig. 1K). Neuropodial homogomph spinigers pectinate (Fig. 1H) or basally serrated (i.e. blade small with coarse teeth) (Fig. 1J), heterogomph spinigers pectinate (Fig. 1I); spinigers of similar size, teeth decreasing in size distally (Fig. 1N, O). Neuropodial heterogomph falcigers pectinate, distal tooth recurved, fused to blade, supra-acicular falcigers slightly broader than sub-acicular ones (Fig. 1L, M).

Pygidium not modified; anal cirri cirriform, as long as last 5-6 chaetigers (Fig. 1B).

Epitokes.

Male fully transformed (ECOSUR-OH-P0761) complete; body tapering, 9 mm long, 0.9 mm wide, 57 chaetigers. Partially transformed male (ECOSUR P2827) complete; body tapering, 38 mm long, 2.1 mm wide, 57 chaetigers. Partially transformed female (ECOSUR P2827) complete; body tapering, 20 mm long, 1.6 mm width, 55 chaetigers. All with body yellowish with brown pigmentation present dorsally on first quarter of body, discoloring towards midbody chaetigers; faint lateral lines (Fig. 2A, D, E). Prostomium with pigmentation as in atokes, but less intense (Fig. 2B).

Prostomium longer than wide; antennae cirriform, slightly wider than those present in atokous female, as long as palps; eyes subequal, two (Fig. 2D) or three times (Fig. 2B) larger than antennal basal width, black, in trapezoidal arrangement (Fig. 2B, D).

Peristomium twice as long as first chaetiger, slightly pigmented; tentacular cirri present; dorsal tentacular cirri longer than ventral ones, posterodorsal ones reaching to chaetiger 10 (Fig. 2B, D).

Fully transformed male with pharynx everted, jaws amber with 10 teeth, inner edge toothed throughout. Maxillary ring: I = 8 cones in triangle, II = 30-32 cones in arc, III: 40 cones in rectangle, IV: 28-28 pointed cones in arc. Oral ring: V = 1 cone, VI: 4-4 pyramids in diamond, VII-VIII: 46 in two irregular rows, pyramids alternating with small cones in most-anterior row, pyramids with similar size alternating in most-posterior row.

Male body divided into two regions (Fig. 2A). Pre-natatory region includes chaetigers 1-16, natatory region from chaetiger 17 to end of body. Partially transformed female divided into two inconspicuous regions, parapodial lamellae visible from chaetiger 24.

Parapodial cirri pattern: Anterior parapodia with dorsal cirri modified in chaetigers 1-7 in males, 1-5 in females; ventral cirri modified in chaetigers 1-5 in males, 1-4 in females; modification attenuated in females. Dorsal cirri subequal to upper dorsal ligules in anterior chaetigers, slightly longer throughout body; basally inserted in anterior-most region, displaced medially toward end of body. Ventral cirri shorter than neuropodial ventral ligules in unmodified chaetigers, subequal in modified region; basally inserted in anterior region, barely displacing ventrally throughout body.

Chaetigers 1-2 uniramous (Fig. 2F); modified dorsal cirri basal, subpyriform (i.e. basally broad, medially broader, distally narrow), slightly longer than dorsal ligules. Dorsal and neuropodial ventral ligule subequal, subconical. Neuroacicular ligule subconical, much shorter than ventral one; postchaetal lobes rounded. Modified ventral cirri subpyriform, subequal to neuropodial ventral ligule; both dorsal and ventral cirri with similar width.

Chaetigers 3-7 in males (Fig. 2G) and 3-5 in females, with slightly modified biramous parapodia. Modified dorsal cirri medial, cattail-like (i.e. basal section broad, long; cirrostyle markedly narrower), slightly longer than notopodial dorsal ligules, extending beyond them; basal section 2-3 longer than distal one. Notopodial dorsal ligules subconical, subequal to notopodial ventral one; notopodial ventral ligule subconical, notoacicular papilla conspicuous. Neuroacicular ligule subconical, postchaetal lobe rounded, shorter than neuroacicular ligule; neuropodial ventral ligule digitate, as long as neuroacicular one (Fig. 2G). Modified ventral cirri cattail-like, subulate in chaetigers 6-7 in males and 5 in females, shorter than neuropodial ventral ligules; modified dorsal and ventral cirrus with similar width.

Chaetigers 8-16 in males and 6-23 in females with parapodial proportions as in atokes, but with more acute ligules (Fig. 2H).

Remaining parapodia biramous, modified (Fig. 2I, J, L, M). Dorsal cirri medial, subulate, ventral margins sinuate in males only, longer than notopodial ligules; ba sal lamellae small, smallest in females, progressively smaller toward posterior region. Notopodial dorsal and ventral ligules subequal, subconical, notoacicular papillae conspicuous; ventral ligules with lamellae without projections along ventral margins. Neuroacicular ligules subconical, subequal to notopodial ventral ones; postchaetal lobes developing into flabellate lamellae, increasing in size posteriorly, decreasing in posterior-most chaetigers, some with slight projections in dorsal or ventral edge; neuropodial ventral ligules digitate, medially attached to neuroacicular ones. Ventral cirri subulate, subequal to neuroacicular ligules, with two basal lamellae of different sizes; dorsal cirri wider than ventral ones.

Prenatatory region with noto- and neurochaeta as in atokes, homogomph falcigers not observed, blades missing in most chaetae, number progressively reduced. In natatory region, noto- and neurochaetae sesquigomph chaetae with finely serrated, paddle-like blades (Fig. 2N).

In fully transformed males pygidium with anus surrounded by rosette of papillae (Fig. 2C); anal cirri sinuous, as long as last 5-6 chaetigers (Fig. 2C).

Transformation in females discrete; small lamellae on base of dorsal cirri, neuroacicular ligules and ventral cirri (Fig. 2K); size of lamellae increasing toward posterior end and becoming inconspicuous in far posterior chaetigers; other features as in atokous female.

Variation.

The results of the analysis of body variation and paragnath numbers are summarized in Tables 1 and 2. The effect of fixation techniques on the shape of specimens have been recently evaluated by Oliveira et al. (2010) for Laeonereis acuta (Treadwell, 1923). The authors concluded that techniques of fixation can influence the shape and body proportions, especially if specimens were not previously relaxed, leading to erroneous identifications.

In the case of Nereis oligohalina , fixation with 96% ethanol clearly affected the anterior portion of specimens with strong contraction of first segments, hence the tentacular cirri can reach more posterior chaetigers but without modifying their lengths, reaching up to chaetiger 14 (Table 1). Differences are not significant for L10, W3 and W10 (P =>0.05), but significant for L3 and rTC (P = <0.001, P = <0.0001). Maximum rTC for formalin specimens was preferred for the identification key because the data were less variable (Table 1). Nevertheless, these differences would not cause misidentification, because parapodial topology is not affected appreciably. Also pigmentation is very useful for recognizing the species.

In the maxillary ring, area I showed the least variation (Fig. 6J), and in oral ring areas V and VI rarely vary in one paragnath only (Fig. 6K), such that these areas can be regarded as the most stable ones. The fingerprint-like pattern starts in chaetigers 10-11 (Fig. 6L); it is size-independent, but in smaller specimens this pattern is faint; however, as shown below it is absent in the two other species. The divergence between parapodial rami reported by Rioja (1946) is evident in posterior chaetigers but only in some specimens, forming a furrow (Fig. 6O). Glandular masses appear more visible and also on neuropodial ligules (Fig. 6Q); perhaps these glands fade in specimens fixed with formalin, such as the type material. In mature specimens, the natatory region starts in chaetiger 15-17 in males, and 24-25 in females.

Remarks.

Nereis oligohalina (Rioja, 1946) is considered as a widespread species and even amphiamerican, but this stems from taxonomic confusion and the lack of type material. Designation of a neotype for Nereis oligohalina was considered necessary because there are no type specimens and being a problematic species, there must be an objective definition for it ( ICZN 1999, Art. 75.1). Consequently, a neotype has been selected, described and illustrated ( ICZN 1999, Art. 75.3.3); this neotype fits the original description by Rioja (1946) ( ICZN 1999 Art. 75.3.5). Because Rioja did not designate holotype, his material became syntypes and the species had two type localities ( ICZN 1999 Art. 73.2.3, 76.1): Estero de Larios, Tecolutla, and El Cocal, Estero Casitas, both in Veracruz, Mexico. Although topotypic specimens from Estero Casitas are available, they are in poor condition, and therefore better specimens collected from nearby Actopan River were preferred once they were shown to conform to the same species ( ICZN 1999, Recomm. 75A). The proposed neotype was collected in a similar environment and on oysters, as the original specimens ( ICZN 1999, Art. 75.3.6); but the neotype locality is modified accordingly ( ICZN 1999, Art. 76.3). The neotype was deposited in ECOSUR ( ICZN 1999, Art. 75.3.7), including ‘paraneotypes’ and part of the additional material.

Neanthes oligohalina Rioja, 1946 was correctly transferred to Nereis by Hartman (1951) because there are notopodial homogomph falcigers in posterior chaetigers. Hart man (1951, 1954) suggested that Nereis oligohalina was ‘inseparable’ from Nereis pelagica occidentalis Hartman, 1945, but not synonymized. Salazar-Vallejo (1989) noted that although Rioja clearly recognized the presence of notopodial homogomph falcigers, he maintained the species under Neanthes , even in later publications ( Rioja 1947, 1960, 1962).

The first synonymy involving these species was made by Pettibone (1956); she considered Nereis pelagica occidentalis different from Nereis pelagica and raised it to species level as Nereis (Nereis) occidentalis Hartman. Also, she regarded Neanthes oligohalina as a junior synonym of Nereis occidentalis being regarded as a variety. The detailed description provided by Pettibone allowed us to recognize differences in comparison to the Laguna Madre, Texas specimens. She recognized slight but important differences among these variants, mainly in paragnath number in areas V and VI; adding the relative size of neuropodial ligules in middle and posterior chaetigers. In the same work, she determined that Nereis largoensis Treadwell, 1931 was a junior synonym of Nereis pelagica , and that other material identified as Nereis largoensis based upon material examined by Treadwell corresponds to Nereis occidentalis ( Pettibone 1956). We follow, however, González-Escalante and Salazar-Vallejo (2003), who concluded that these three species are not synonyms.

Nereis oligohalina differs from Nereis occidentalis in some diagnostic features. In Nereis oligohalina there are 8-15 paragnaths on area I and 1-2 on area V, whereas in Nereis occidentalis there are 2-3 paragnaths on area I and no paragnaths on area V. Further, in Nereis oligohalina neuropodial ventral ligules are 2-3 times longer than neuroacicular ligules, but in Nereis occidentalis neuropodial ventral ligules from posterior chaetigers are shorter than neuroacicular ones. Regarding chaetae, and as an additional difference, in Nereis oligohalina the notopodial homogomph falciger has the distal tooth less developed than in Nereis occidentalis .

Another synonymy was made by Day (1973), who regarded Nereis pelagica occidentalis Hartman and Nereis occidentalis fide McCloskey as junior synonyms of Nereis falsa de Quatrefages, 1865; however, in the list of synonyms of these two species he did not include Pettibone (1956), therefore Nereis oligohalina was not considered by him. Nereis falsa , has a rather complex or confusing delineation; according to Fauvel (1923) it differs from similar species by having different numbers of paragnaths in areas I and V, and different proportions in parapodial ligules. In fact, Nereis falsa is another species regarded as widely distributed and requires a critical revision and we could anticipate a restriction of its distribution to the Mediterranean region because its type locality is the Black Sea.

On the other hand, Nereis oligohalina has been recorded along American Atlantic coasts from northeastern Brazil, chiefly in ecological (community assemblages on Spartina alterniflora and mangroves), or population studies (secondary production and population dynamics), as well as part of taxonomic or genetic studies ( Amaral et al. 2012). A detailed record was made by Santos and Lana (2003); unfortunately, a commentary and one plate was based upon specimens collected in Todos Los Santos Bay, and indicated that their material agrees with the original description regarding neuropodial ventral ligules in posterior parapodia, and the feature was less developed in specimens from other localities but were regarded as the same because the prostomial pigmentation and paragnath number remained constant ( Santos and Lana 2003). Lana et al. (2006) however, considered their previous record as a probable misidentification requiring a revision. Liñero-Arana and Díaz (2007) recorded Nereis oligohalina from Venezuela in La Restinga Lagoon, Margarita Island, associated with Crassostrea rhizophorae (Guilding), and recognized that their specimens resembled Brazilian ones and differed from those described by Rioja, mainly in parapodial morphology. These two publications pointed out the need for a revisionary work, recognizing Nereis oligohalina as valid species, but that their specimens were probably not the same as those described from Mexico because of parapodial features; at least the specimens from South America were regarded as a different species that should be clarified elsewhere.

Records of Nereis oligohalina from the Eastern Tropical Pacific ( Berkeley and Berkeley 1958, 1960) belong to a new species described below.

Habitat.

The species is associated with red mangrove Rhizophora mangle and with oysters. It has been found in Gulf of Mexico estuaries, including Tecolutla, Casitas-Nautla and Actopan (these estuaries have sand bars in their respective mouth rivers), and from coastal lagoons such as Mandinga and La Mancha. These systems have direct connection with the sea, some with seasonal closure of their mouths, with polyhaline to mesohaline waters ( Lara-Domínguez et al. 2011).

The neotype and associated specimens were found in Crassostrea virginica (Gmelin) reef, in the Actopan river mouth. The specimens studied by Rioja (1946) from the Tecolutla estuary were found on mangrove roots covered by cirripedians, whereas specimens from the Casitas-Nautla estuary were collected between oysters (possibly Crassostrea virginica ) and mytilids as Ischadium recurvum (Rafinesque) (reported as Mytilus recurvatus (sic) by Rioja); as Rioja indicated, Nereis oligohalina specimens cohabit with an Alitta species in the Actopan river mouth. This species has been reported as Nereis occidentalis Hartman, together with Polydora websteri Hartman, as epifauna of Crassostrea virginica ( Ruiz-Guerrero and López-Portillo Guzmán 2006), and on Rhizophora mangle roots ( Ruiz and López-Portillo 2014), from La Mancha.

Distribution.

Restricted to the southwestern Gulf of Mexico.