Alitta succinea Leuckart 1847

Alitta succinea (Leuckart, 1847)

Figures 1 A −C, 2

Nereis succinea Leuckart, 1847: 154 −156, Pl. 2, Figs. 9, 11; Ehlers 1868: 570 −572, Pl. 22, Figs. 18−22; Heinen 1911: 60, Fig. 21; Gillandt 1979a: 43, 1979b: 23, 25, table 1.

Nereis (Neanthes) succinea Hartmann-Schröder 1996: 207 −209, Fig. 90 (partim).

Alitta succinea Bakken & Wilson 2005: 516 −517 (partim).

Neanthes succinea Sato 2013: 35 −42, Figs. 3 D–F, 4B, 15–17 (partim).

Type material. North Sea, Germany. Lectotype (ZMH P- 25975) and one paralectotype (ZMH P- 25976) designated by Sato (2013), both incomplete, damaged, Helgoland (no more data).

Topotype material. North Sea, Germany. ECOSUR-P2729, 30 specimens, off Dornumersiel, 53°42’N, 07°28’E, 2008−2013, oyster Crassostrea gigas reef. ECOSUR-OH-P734-P741, 8 specimens, off Dornumersiel, 53°42’N, 07°28’E, 2008−2013, oyster Crassostrea gigas reef. ECOSUR-P2730, 4 specimens, NWO Terminal, Jade, Wilhelmshaven, 53°33’27’’N, 08°09’45’’E, 2011.

Re-description based on atokous lectotype (variations for specimens indicated in parentheses). Lectotype incomplete, with 67 chaetigers (n= 12, µ= 99.0±7.2, ran: 80–119); TL= 50 mm (n= 12, µ= 67.6±14.5, ran: 32−115), L15= 17 mm (n= 43, µ= 14.7±1.2, ran: 6.5−24), W15= 2.5 mm (n= 43, µ= 2.9±0.3, ran: 1.0−5.0).

Prostomium anteriorly complete (Fig. 1 A), 1.4 times wider than long (µ= 1.2, ran: 0.8−1.4); mid-dorsal groove present. Palpophores suboval, as long as wide (usually slightly wider than long, µ= 1.2 times, ran: 0.9−1.5), 0.7 times width of prostomium (µ= 0.8, ran: 0.6−1.0). Antennae close together, short, conical, not exceeding palp tips (Fig. 1 A); extended posteriorly, reaching one-third of prostomium (µ= 0.3; ran: 0.2−0.4). Two pairs of eyes, similar sized, medium, dark, rounded (anterior pair occasionally reniform). Upper peristomial cirri reaching chaetiger 2 (n= 38, µ= 3.0±0.3, ran: 2−5); lower peristomial cirri reaching palp tips (occasionally shorter). Upper tentacular cirri reaching chaetiger 4 (n= 38, µ= 5.4±0.4, ran: 2−8); lower tentacular cirri one-half length of prostomium (rarely shorter). Cirrophores of upper tentacular cirri 1.5 (1.5−2.0) times longer than those of upper peristomial cirri. Apodous segment 1.5 (1.5−2.0) times larger than length of chaetiger 1.

Pharynx with yellow amber jaws, teeth broken, 5 complete (n= 39, µ= 9.3±0.3, ran: 8−11). Paragnaths all conical, except some pyramidal in VII −VIII. Paragnaths without plate-like basement. Maxillary ring: I= 3 (n= 42, µ= 3.3±0.4, ran: 1−9), in a longitudinal line (Fig. 1 A); IIa= 20 (n= 42, µ= 20.0±1.2, ran: 12−29), IIb= 21 (n= 42, µ= 20.7±1.2, ran: 11−29), two or three irregular curved rows with small-slender and large-coarse cones, the latter anteriorly placed (Fig. 1 A); III= 35 (n= 42, µ= 34.5±1.8, ran: 16−43), four irregular rows in a rectangular group (sometimes three irregular rows forming a trapezoid; Fig. 1 B); IVa= 28 (n= 42, µ= 23.4±1.2, ran: 16−34), IVb= 29 (n= 42, µ= 23.9±1.1, ran: 18−34), crescent-shaped, tapering anteriorly (Fig. 1 B, C). Oral ring: V= 0 (n= 42, µ= 2.0±0.3, ran: 0−4), when present, two longitudinal or transversal cones (Fig. 1 A), or three cones forming a triangle; VIa= 9 (n= 41, µ= 8.2±0.5, ran: 5−13), VIb= 9 (n= 41, µ= 8.5±0.7, ran: 6−18), arranged in circular group with concentric cone (Fig. 1 A); VII −VIII= 51 (n= 42, µ= 52.6±1.8, ran: 41−66), two rows with cones and pyramidal, anterior row continuous with alternating combination of cones and pyramidal, posterior row discontinuous, not interspersed, most posterior paragnaths very small (Fig. 1 B). Bare space between VI and VII −VIII as wide as palpophore (Fig. 1 A, C).

Biramous parapodia, except chaetigers 1 and 2, sub-biramous. Chaetigers 1 and 2 (Fig. 2 A) with dorsal cirrus nearly as long as dorsal ligule, basally attached. Dorsal ligule conical, slightly longer and wider, and 1.5 (1.5−1.8) times thicker than conical ventral ligule. Neuracicular ligule small, one-quarter length of ventral ligule. Neuropodial postchaetal lobe conical, large (even well developed in shortest specimens), nearly as long, wide, and slender as ventral ligule. Neuropodial inferior lobe tapered, small, thick, one-half length of neuropodial postchaetal lobe. Ventral cirrus three-quarter length of ventral ligule.

Anterior chaetigers (Fig. 2 B, C) with dorsal cirrus not gradually elongating or displacing distally on dorsal ligule, as long as dorsal ligule, attached to one-quarter of its length. Dorsal ligule conical to triangular shaped, thick, as long as and 2.2 (2.0−2.5) times wider than lanceolate median ligule. Notopodial prechaetal lobe progressively widening and slightly increasing in length; lanceolate, 0.5 to 0.7 times length and 0.4 to 0.7 times width of median ligule. Notopodial prechaetal lobe in chaetigers 3 to 66 (50−88), notoacicular papillae-like thereafter. Neuropodial postchaetal lobe becoming smaller, narrowing and thinning; lanceolate, 0.8 to 0.4 times length, 0.5 to 0.3 times width, and 0.8 to 0.5 times thickness of median ligule. Neuropodial inferior lobe becoming smaller, slightly thickening and widening; thick, from faintly elongated to rounded, one-third to three-quarters length of neuropodial postchaetal lobe; present in chaetigers 1 to 62 (48−88), neuracicular papillae-like thereafter. Neuracicular ligule as long as ventral ligule, 1.4 (1.3−1.6) times wider than it. Ventral ligule lanceolate, as long as median ligule, wider and thicker than it. Ventral cirrus becoming smaller; one-half to one-quarter length of ventral ligule.

Mid-body chaetigers (Fig. 2 D) with dorsal cirri subterminal on dorsal ligule, becoming slightly smaller and distally moving, 0.6 (0.5−0.7) times length of ligule, 2 times longer than triangular protruding tip of ligule. Dorsal ligule rectangular, 2 times longer than wide; 2.3 (2−2.5) times longer and 3.5 (3.5−4) times wider than lanceolate median ligule, reaching over one-half of width segment. Dorsal ligule expanding from about chaetiger 19 (15−24), markedly elongate and wider on following chaetigers, glandular edges not observed (faded due to long-term preservation in types; bearing a ventral glandular edge). Notopodial prechaetal lobe conical (sometimes lanceolate), 0.2 (0.2−0.3) times length and 0.4 (0.4−0.5) times width of median ligule. Neuropodial postchaetal lobe conical, 0.8 times length, 0.6 (0.5−0.7) times width and 0.3 times thickness of median ligule. Neuracicular ligule as long as ventral ligule. Ventral ligule lanceolate, 0.7 times length and 0.6 (0.5−0.7) times width of median ligule, slightly slenderer than it. Ventral cirrus reaching basis of ventral ligule.

Posterior chaetigers only available in topotype specimens (Fig. 2 E, F). Dorsal cirri subterminal on dorsal ligule, displacing distally and becoming smaller, 0.3 times length of dorsal ligule, clearly longer than conical, short protruding tip; terminal dorsal cirrus on last 7−14 chaetigers. Dorsal ligule pennant-like, 2 times longer than wide; 2.5−3 times length and 3 times width of median ligule, reaching three-quarters of chaetiger width. Notopodial prechaetal lobe notoacicular papillae. Neuropodial postchaetal lobe conical (sometimes tapered), becoming smaller, narrower and thinner, 0.7 to 0.5 times length and width of median ligule, 0.5 to 0.4 times slenderer than it; neuracicular papillae-like in last 6−12 chaetigers. Neuracicular ligule 0.3 times length of ventral ligule, 1.3−1.5 times wider than it. Ventral ligule tapered, 0.7 times length and width of median ligule, slightly slenderer than it. Ventral cirrus reaching basis of ventral ligule.

Notoaciculae on chaetigers 1 and 2 thin, 0.5 times width of neuroaciculae, directed 30−50° respect to neuroaciculae. Similar sized and shaped as neuroaciculae on following chaetigers. Notochaeta homogomph spinigers throughout. Spinigers of different size, long blades on upper spinigers, medium on lower ones; teeth short. Neurochaetae in upper fascicle with homogomph spinigers and heterogomph falcigers throughout. Falcigers long, somewhat wider than those from lower fascicle; teeth medium, terminal tendon 2 times longer than other teeth (Fig. 2 G). Spinigers of different size, long blades on upper spinigers, medium on lower ones; short teeth. Neurochaetae in lower fascicle with heterogomph spinigers and heterogomph falcigers throughout. Falcigers long with blades of different length, long on upper falcigers, shorter on lower ones; teeth medium, terminal tendon 1.5 times longer than other teeth (Fig. 2 H). Spinigers of different sizes with short teeth, long blades on upper spinigers (Fig. 2 I), medium (rarely short) on lower ones.

Pygidium with slender anal cirri, as long as last 8−15 chaetigers (n= 15, µ= 12.1±1.1); cirrophores well developed. Anus terminal, margin multidivided.

Live coloration. According to Leuckart (1847): “…red or reddish brown on the dorsal surface, which often extends from the head and parapodia of the anterior segments.”

Preserved coloration. Type material has lost the pigmentation due to long-term preservation; the specimens now appear cream colored. As stated by Ehlers (1868), Leuckart’s material and some other from Norderney: “…the dorsum is brownish purple in the most anterior segments, where the color is deeper, it is seen as a diffuse band forming a cross. The abdomen was colorless and whitish.”

Non-type epitokous male (ECOSUR-OH-P740). Complete specimen, with 87 chaetigers, TL= 41 mm, L15= 11.0 mm, W15= 2.8 mm. Body divided in three regions: pre-natatory, natatory and post-natatory. Eyes enlarged, rounded, black, not overlapping. Paragnaths as in atokous, without plate-like basement. Pre-natatory region with 14 chaetigers. Dorsal and ventral cirri modified in first 7 and 5 chaetigers, respectively. Chaetigers 8 to 14 with unmodified parapodia. Natatory region with 37 chaetigers. Heteronereis morphology in mid-natatory parapodia as follows (Fig. 2 J): dorsal cirri 2 times length of upper lamella, extending beyond lower lamella of dorsal ligule; 10 bulbous papillae on lower edge, largest distally, distal bare space equals four papillae breadth. Upper lamella of dorsal ligule reniform, 2 times wider than long, blunt tip, basal 60% attached to ligule. Lower lamella of dorsal ligule conical, reaching tip of median ligule, basal 40% attached to ligule. Notopodial prechaetal lobe large papilla. Median ligule lanceolate, extending beyond neuropodial postchaetal lobe, overlapping it. Neuropodial postchaetal lobe expanded, cordate, asymmetrical, conspicuous pointed lower apex; lower edge narrow, as wide as neuracicular ligule. Neuracicular ligule as wide as enlarged median ligule, flat upper edge. Ventral ligule fusiform, one-half width of neuracicular ligule, as long as neuropodial postchaetal lobe. Ventral cirri slightly longer than ventral ligule; 11 small bulbous papillae on lower edge, similar sized, terminal bare space equals width of one papillae. Upper lamella of ventral cirri nearly as long as lower lamella, 0.4 times width of it. Lower lamella reniform, 2 times wider than long, blunt tip, basis 60% attached to cirrus. Sesquigomph natatory chaetae not emerged yet. Post-natatory region with 36 chaetigers, one-half width of pre-natatory chaetigers. Pygidium unmetamorphosed, anus without papillae or pygidial rosette. Anal cirri as long as last 11 chaetigers.

Non-type epitokous females. Three incomplete specimens, not completely metamorphosed, with L15= 15−16 mm (n= 3, µ= 15.7±0.7), W15= 2.5−3.0 mm (n= 3, µ= 2.7±0.3). Body divided in three regions: pre-natatory, natatory and post-natatory. Eyes similar sized, not enlarged. Paragnaths as in atokous, without plate-like basement. Pre-natatory region with 17 chaetigers. Dorsal and ventral cirri barely modified in first 5 and 4 chaetigers, respectively. Chaetigers 6 to 17 with parapodia unmodified. Natatory region with 30−33 chaetigers. Heteronereis morphology in mid-natatory parapodia as follows (Fig. 2 K): dorsal cirri smooth, 2 times longer than upper lamella, extending beyond lower lamella of dorsal ligule. Dorsal ligule not wholly transformed as in males; upper lamella reniform, 3 times wider than long, blunt tip, basis fully attached to ligule. Lower lamella of dorsal ligule conical, slightly longer than median ligule, basis fully attached. Notopodial prechaetal lobe small papilla. Median ligule lanceolate, lower edge curved, basal smooth; extending beyond neuropodial postchaetal lobe, not overlapping it. Neuropodial postchaetal lobe somewhat expanded, not greatly as in males, auriform, asymmetrical, lower apex with reduced pointed tip. Neuracicular ligule nearly as wide as ventral ligule, flat upper edge. Ventral ligule lanceolate, slightly longer than neuracicular ligule. Ventral cirri smooth, as long as ventral ligule. Upper lamella of ventral cirri nearly as long as lower lamella, 0.4 times width of it. Lower lamella suboval, nearly as wide as long, blunt tip, basal 50% attached to cirrus. Natatory chaetae not developed. Post-natatory region with more than 40 chaetigers, 0.6 times width of pre-natatory chaetigers. Pygidium not seen. Oocytes size: 86−120 µm (n= 100, µ= 101.8±1.2).

Habitat. Estuaries and harbors, 0−5 m depth, supralittoral (Gillandt 1979b). Epibiont on non-native oysters (Crassostrea gigas), other mollusks, and barnacles. Fouling on artificial substrates, such as buoys, ship hulls, and dock pilings.

Type locality. Helgoland, Germany.

Distribution. Western Germany.

Remarks. From the original description of Nereis succinea Leuckart, 1847 to the beginning of the 20th century, the identifications of the species were based on type or native material. Ehlers (1868) characterized the species using type and topotype materials; de Saint-Joseph (1898) described a similar species to N. succinea, N. (Neanthes) perrieri, which displayed longer tentacular cirri, jaws with fewer teeth and more chaetigers. Ehlers provided a specimen to Horst for comparative purposes with individuals from Zuiderzee (Netherlands). Then, Horst (1909, 1910) considered the length of the tentacular cirri as an uninformative taxonomic feature; meanwhile the other two features were highly variable. Therefore, he proposed N. (N.) perrieri as a junior synonym of N. succinea. Nevertheless, Heinen (1911) regarded the extension of the tentacular cirri as an important taxonomic feature to separate nereidids; this was the main feature used in the key to distinguish his new species Nereis reibischi from N. succinea (Heinen 1911: 42−43).

Most identifications, synonymies and characterizations of N. succinea between 1910 and 1980 were not based on type or topotypic material, but rather on published records based on specimens from different regions. McIntosh (1910) synonymized N. (N.) succinea with N. (Perinereis) marionii Audouin & Milne-Edwards, 1833 from the Gulf of Biscay based on the original descriptions. Later, Fauvel (1912) separated N. succinea from P. m ar i on i i; however, he synonymized Nereis lamellosa Ehlers, 1868 with N. succinea, suggesting the presence of this species in the Mediterranean Sea. Fauvel (1919) recorded N. (N.) succinea from America and implied similarities with Nereis glandulosa Ehlers, 1908 and N. limbata Ehlers, 1868. Subsequently, Fauvel (1923 a, b) reaffirmed that these two species, as well as N. lamellosa and N. perrieri, were junior synonyms of N. (N.) succinea, and he expanded the distribution to include the Western Atlantic and Indian Oceans.

In those years, N. succinea was treated as senior synonym of a number of morphologically similar species described worldwide. Thus, several new records of the species from widespread localities appeared: Black Sea (Annenkova 1929), Caribbean Sea (Augener 1933), South American Atlantic coast (Fauvel 1923a, b: synonym of N. limbata, Monro 1938: synonym of N. australis), Central American Pacific coast (Monro 1933: synonym of N. acutifolia; Hartmann-Schröder 1959), North American Pacific coast (Hartman 1938, 1954: synonym of N. saltoni; Rioja 1947, 1962), North American Atlantic coast (Hartman 1945; Rioja 1946; Berkeley & Berkeley 1953; Pettibone 1963), Baltic Sea (Banse 1954: synonym of N. reibischi; Smith 1963), African Atlantic coast (Tebble 1955; Fauvel & Rullier 1959), Western Pacific coast (Imajima 1972; Wilson 1984: synonym of Nectoneanthes oxypoda, 1988: synonym of N. alatopalpis), and other many localities (Hartman 1959). Since then, the name N. succinea has remained in different regions of the world (e.g., Wu et al. 1981; Khlebovich 1996; de León-González et al. 1999; de León-González & Solís-Weiss 2000; Dean 2001; Villalobos-Guerrero 2012; Sato 2013).

Descriptions of specimens from diverse regions were combined and the morphology of the species has not been defined accurately. Wilson (1984, 1988) studied some specimens from Germany and other countries. He did not find convincing differences between them and even he considered Nectoneanthes a junior synonym of Neanthes. Hartmann-Schröder (1996) briefly characterized N. succinea based on material from both the Western and Eastern shores of Germany and Denmark. She did not include paragnath numbers of some areas and the ranges of meristic features were very wide in epitokous forms. Bakken & Wilson (2005) characterized N. succinea but non-topotype material was used; they transferred the species to Alitta Kinberg, 1865, which included three species: Alitta brandti Malmgren, 1865, A. grandis (Stimpson, 1853) and A. virens. Sato (2013) rejected the synonymy of Nectoneanthes with Neanthes and the transference of N. succinea to Alitta, keeping the species in Neanthes. Furthermore, he characterized the species by a combination of features based both on type material and on material from Japan and other regions.

In the present study, we sought to characterize N. succinea based exclusively on type and topotypic materials, incorporating recent taxonomic revisions in Nereididae. Also, we consider that N. succinea must be retained in Alitta (see comments above).

As with A. succinea, A. virens has a complex taxonomic history. Sars (1835) described the species from Bergen (Norway), but it has been widely recorded in temperate and boreal waters from the Northern Hemisphere (Imajima 1972; Khlebovich 1996; Khlebovich & Jirkov 2001; Bakken & Wilson 2005). This species is morphologically similar to A. brandti (Sea of Okhotsk, Russia) and A. grandis (Grand Manan Island, Canada), both were synonymized under A. virens on different occasions (Ehlers 1868; McIntosh 1910; Fauvel 1923b). Khlebovich et al. (1980) and Khlebovich (1996) validated the species based on the variability of paragnaths number, reproductive strategies, and behavior of larvae; however, these authors also based descriptions on specimens combined from different regions. We retain all three species within the complex “ A. virens ” pending a complete morphological study based on type and/or topotypic materials to evaluate the taxonomic status of these species.

According to the most recent characterizations of A. virens from boreal waters (Khlebovich 1996; Khlebovich & Jirkov 2001), the differences between A. succinea and A. virens are the proportions of dorsal ligules, the position and extension of dorsal cirri, the presence of heterogomph falcigers, and paragnaths numbers in all areas. Alitta succinea bears a pennant-like dorsal ligule on posterior chaetigers, dorsal cirrus (sub-) terminally attached on posterior chaetigers, extending beyond ligule, and heterogomph falcigers throughout. Meanwhile, A. virens bears a cordate dorsal ligule on posterior chaetigers, dorsal cirrus mid-dorsally attached to dorsal ligule on posterior chaetigers, not reaching the tip of ligule, heterogomph falcigers only in anterior chaetigers (except in juveniles). The paragnaths of A. virens are as follow: Area I= 1 (seldom 2), II= 5−8, III= 7−11, IV= 13−18, V= 0 (seldom 1), VI= 1 (seldom 2), and VII −VIII= 15−25; while A. succinea has Area I= 3−4, II= 19−22, III= 32−37, IV= 22−25, V= 1−3 (seldom 4), VI= 7−9, and VII −VIII= 50−55. Alitta succinea was described having 1 or 2 paragnaths in area V (Leuckart 1847; Ehlers 1868); however, the type materials lack paragnaths in this area; they probably become dislodged due to long-term preservation.

Differences between atokous and epitokous specimens of A. acutifolia n. comb. and A. succinea are described in the taxonomic remarks of the former species (see below).

Alitta succinea differs from Nectoneanthes oxypoda in many features, aside from the generic ones (see remarks of Alitta): 1) body size, 2) shape of dorsal ligule on posterior chaetigers, 3) presence of notopodial prechaetal lobe, 4) presence of heterogomph spinigers in upper neurochaetae, 5) size and shape of inferior neuropodial lobe, 6) number of paragnaths in area III, 7) appearance of first natatory chaetigers in epitokous specimens, and 8) shape of neuropodial postchaetal lobe in male epitokes (Sato 2013).