Polydora cornuta Bosc, 1802

Surugiu, Victor, 2012, Systematics and ecology of species of the Polydora - complex (Polychaeta: Spionidae) of the Black Sea, Zootaxa 3518, pp. 45-65 : 47-50

Polydora cornuta Bosc, 1802

Figure 2

Polydora cornuta Bosc, 1802: 150 –153, pl. 12, figs. 7–8; Claparède 1861: 542 –544, pl. 13, figs. 12–17 [in part]; Perejaslavzeva 1891: 262 –263; Blake & Maciolek 1987: 12 –14, fig. 1a–f (neotype and synonymy); Tena et al. 1991: 32 –35, fig. 3; Blake 1996: 171, fig. 4.28H; Radashevsky 2005: 3 –15, figs. 1–4 (synonymy); Surugiu 2005a: 66 –67; Çinar et al. 2005: 824 –826, fig. 3–4; Ergen et al. 2006: 200 –205 (ecology); Boltachova & Lisitskaya 2007: 33 –35, fig. 1; Daġli & Ergen 2008: 231 –233, fig. 3; Karhan et al. 2008: 5 –19 (ecology); Simboura et al. 2008: 123–124, fig. 2; Zhou et al. 2010: 5, fig. 1R–X; Selifonova 2011a: 48, fig. 1; Losovskaya 2011: 53; Bondarenko 2011: 12.

Polydora ligni Webster, 1880: 119 ; Mesnil 1896: 236; Hartman 1951: 82; Rasmussen 1973: 104 –111 [in part]; Blake & Kudenov 1978: 258, fig. 43h–j.

? Polydora ciliata . Codreanu & Mack-Firä 1961: 489 –490, figs. 9–11; Dumitrescu 1962: 66 [in part]; 1973: 43 [in part]; Bäcescu et al. 1963: 139, fig. 3 [in part]; Manoleli & Nalbant 1975: 524; Marinov 1977: 158 –159 [in part]; Ţigänuş 1982: 110; 1986: 20; Manoleli 1980: 113 –115; Surugiu & Manoleli 1998 –1999: 24 [in part]; Kisseleva 2004: 264 –266, fig. 107d [in part]. Non Johnston 1838.

? Polydora ciliata limicola . Losovskaya & Nesterova 1964: 1559 –1560; Kisseleva 1987: 42; Ţigänuş 1988: 23; 1990: 22; Vorobyova et al. 2008: 47. Non Annenkova, 1934.

? Polydora limicola . Losovskaya 1976: 102 –105; 1977: 66–67; 1978: 30; 2008: 357–360; Ţigänuş 1992: 54; Losovskaya & Zolotarev 2003: 248 –249; Vorobyova & Bondarenko 2009: 113 –119; Bondarenko 2009: 23–24. Non Annenkova, 1934.

Material examined. Black Sea: original label ʹ Polydora ciliata (Johnston, 1838) (M. Neagrä) Polychaeta 3ʹ MNINGA 30.294 (44); Bulgaria: Sta. 190–4/VA1, Varna (43°08.08ʹN, 28°02.89ʹE), 21.8 m, in muddy sand, 23 Mar 2008, coll. A. Teacä, MNINGA PLY032 (10); Romania: Sta. 66, Danube – Black Sea Canal (44°05ʹ61.6ʹ N, 28°38ʹ0 9.1ʹ E), 3 m, in mud covering artificial rocky substrate, 9 Aug 1999, MNINGA PLY033 (2); Sta. 78, Agigea (44°01ʹ45.6ʹ N, 28°39ʹ32.0ʹ E), 4 m, in columella of Nassarius reticulatus (Linnaeus, 1758) inhabited by Diogenes pugilator (Roux, 1829) , 3 Aug 2003 (1); Sta. 79, Agigea (44°04ʹ57.4ʹ N, 28°38ʹ36.3ʹ E), 4 m, in clayrock, 5 Aug 2003 (41); Sta. BS07/MA07 (43°46.47ʹN, 28°31.05ʹE), 33.5 m, in silty mud, 20 Apr 2007, coll. A. Teacä, MNINGA PLY034 (2); Sta. 177–8/DP5 (44°35.76ʹN, 29°11.43ʹE), 26.2 m, black mud with Melinna palmata Grube, 1870 and Mya arenaria Linnaeus, 1758 , 21 Mar 2008, coll. A. Teacä, MNINGA PLY035 (1); Sta. Ma08–1 Mangalia (43°49ʹ14.30ʹ N, 28°36ʹ56.53ʹ E), 14.2 m, Mytilus galloprovincialis Lamarck, 1819 bank, 11 Jun 2008, coll. A. Teacä, MNINGA PLY036 (13); Sta. Ma08–2 Mangalia (43°49ʹ14.30ʹ N, 28°36ʹ56.53ʹ E), 14.2 m, Mytilus galloprovincialis bank, 11 Jun 2008, coll. A. Teacä, MNINGA PLY037 (10); Ukraine: original label ʹ Polydora limicola , Odessa Bayʹ (176); original label ʹ Polydora limicola, Grigorievsky Limanʹ (103); Sta. 159–4/Phy7 (45°34.13ʹN, 30°17.38ʹE), 23.4 m, silty mud with Mytilus shells, 18 Mar 2008, coll. A. Teacä, MNINGA PLY038 (21).

Description. Specimens up to 20 mm long, 1.25 mm wide at chaetiger 5, with up to 80 chaetigers. Colour in life light tan with red branchiae, palps, and dorsal blood vessels. Preserved specimens pale yellowish. Body not pigmented, but larval pigmentation may persist in recently settled juveniles. Distal part of palps with a diffuse brown pigmentation dispersed along margins of ciliated groove. Pygidium white due to presence of numerous glandular epithelial cells.

Prostomium anteriorly bifurcated, flaring laterally, posteriorly prolonged by low narrow caruncle, reaching posterior margin of chaetiger 3 ( Fig. 2 A). Cirriform, anteriorly oriented occipital antenna present on caruncle between notopodia of chaetiger 1. Four black, rounded eyes in trapezoidal arrangement; anterior pair slightly larger and further apart. Lateral sides of caruncle with large ciliary bands. Palps long, extending posteriorly to chaetiger 20, prehensile, with a distinct longitudinal ciliated groove.

Chaetiger 1 with long, relatively slender cirriform notopodial lamellae; notochaetae absent; neuropodial postchaetal lamellae shorter, conical, with short capillaries ( Fig. 2 B). Chaetigers 2–4 and 6 with well-developed parapodial lobes and postchaetal lamellae, with ventral and dorsal bundles of limbate capillary chaetae ( Fig. 2 B).

Chaetiger 5 larger than adjacent segments ( Fig. 2 A), overlapping chaetiger 6 dorsally, with 5–10 major modified spines alternating with delicate companion chaetae, both arranged in a straight or slightly curved horizontal or oblique row ( Fig. 2 B). Major modified spines of chaetiger 5 falcate, with distinct lateral tooth and narrow slender subdistal longitudinal flange or keel situated laterally on main fang distal to lateral tooth ( Fig. 2 C). Companion chaetae slender, feather-like, often distally bifurcated, depending on wear, closely adhering to convex side of major spines ( Fig. 2 C). Postchaetal lamellae absent. Dorsal superior and ventral inferior capillaries on chaetiger 5 absent.

Ventral bidentate hooded hooks ( Fig. 2 E) from chaetiger 7, without any accompanying capillaries. Main fang of hook at right or slightly acute angle to shaft, with narrow angle (~25°) between apical tooth and main fang. Shaft of hooks slightly curved, with prominent constriction and distinct manubrium. Chaetiger 7 with 5–8 hooks, following chaetigers with up to 12 hooks arranged in vertical series; number of hooks decreases to about three on last few chaetigers. No special notochaetae on posterior segments.

Branchiae digitiform, long, thin, from chaetiger 7, continuing posteriorly to last few posterior segments, free from notopodial postchaetal lamellae ( Fig. 2 B). Pairs of branchiae meeting middorsally, with lengths gradually decreasing posteriorly.

Pygidium large, disc-like, with weakly glandular surface; anus located below narrow middorsal gap ( Fig. 2 F).

Habitat and ecology. Polydora cornuta occurs on various types of substrata (rocks, stems of reeds, watersoaked branches of bushes, seagrasses, clayrock, soft mud, sandy mud or sand) on which it builds fragile tubes of silt particles and fine sand grains. Tubes are brownish-yellowish, made from fine sand grains and detritus, up to 20 mm long and quite large enough to permit the animal to turn around 180° and reverse direction. The species prefers stagnant near-shore, eutrophicated water, rich in detritus and biogenic elements, 0–33.5 m. On hard substrates the species is frequently found on silted surfaces, in cracks of stones, between individual mussels or in empty tests of Amphibalanus improvisus (Darwin, 1854) filled with silt. Worms removed from tubes crawl actively. In clayrock the worm digs U- or Y-shaped burrows, lined by a membranous sheath, with densities up to 110,000 ind. m–2. This species was also found in the apical part of the columella of Nassarius reticulatus shells inhabited by the hermit crab Diogenes pugilator .

Polydora cornuta is an opportunistic species. In areas subjected to severe disturbance and organic enrichment the species forms dense tube-mats that can reach densities up to 150,000 ind. m–2. This species is also a major component of the fouling of bottoms of ships and harbour installations. The species is also tolerant of reduced salinities; at the Romanian Black Sea coast it occurs at salinities ranging between 6.4–17.9 PSU.

Reproduction and development. Brooding females with large, slightly oval oocytes (80–100 μm), were observed in the coelomic cavity from April to August. Oocytes are deposited inside the maternal tube in special egg capsules and attached side-by-side in a loose beadlike string. The capsules are thin-walled, translucent, and attached to the inside wall of the tube by two thin extensions. Each capsule contains between 37 and 57 eggs, with up to 30 capsules per string. The larvae hatch at the 3-chaetiger stage and immediately start to swim in the water column. Late nectochaetes have two large ramified melanophores situated between median and lateral eyes. Dorsal pairs of transverse bands of pigment are present on chaetigers 3–7; from chaetiger 8 onwards they became ramified and stellate-shaped. Juveniles with 12–17 chaetigers, less than 2 mm long were observed in benthic samples from June to October. These early juveniles still possessed five pairs of band-shaped chromatophores, followed by pairs of large branching chromatophores on the dorsal surface.

Distribution. Polydora cornuta (often reported as P. l i g n i) has a worldwide distribution from temperate to tropical regions. The species has been reported from the Pacific ( Blake 1975; Kudenov 1982; Radashevsky 2005; Blake & Ruff 2007) and Atlantic coasts of North America ( Blake 1971; Kudenov 1982; Radashevsky 2005), Gulf of Mexico ( Rice & Simon 1980; Radashevsky 2005; Rice et al. 2008), Caribbean Sea ( Foster 1971), coasts of Brazil and Argentina ( Radashevsky 2005), southeastern Australia ( Blake & Kudenov 1978), Sea of Japan (Sato- Okoshi 2000; Radashevsky 2005), Yellow Sea ( Radashevsky 2005), Taiwan and China ( Radashevsky & Hsieh 2000; Zhou et al. 2010), Baltic Sea ( Ramberg & Schram 1983), Kattegat and Öresund ( Hartmann-Schröder 1996), North Sea ( Böggemann 1997), western Mediterranean Sea ( Tena et al. 1991), Aegean Sea ( Çinar et al. 2005; Ergen et al. 2006; Simboura et al. 2008), Sea of Marmara ( Daġli & Ergen 2008; Karhan et al. 2008; Çinar et al. 2011), Bosphorus Strait ( Karhan et al. 2008), and?Sea of Azov ( Kisseleva 1987). In the Black Sea the species was recorded from the coasts of Romania ( Surugiu 2005a), Bulgaria ( Todorova & Panayotova 2006), southern Crimea ( Boltachova & Lisitskaya 2007), northern Caucasus ( Selifonova 2011a), Odessa region ( Losovskaya 2011) and in front of the Danube Delta ( Bondarenko 2011) ( Fig. 1 ).

Remarks. Polydora cornuta specimens from the Black Sea agree with recent morphological descriptions provided by Blake and Maciolek (1987) and Radashevsky (2005). Radashevsky (2005) examined adult and larval morphology of P. cornuta from different parts of the world and concluded that variability is not sufficiently consistent to separate different geographic populations into additional species and that P. cornuta represents a single species. Rice et al. (2008), however, using molecular, reproductive morphology, and cross fertilization experiments were able to demonstrate the existence of genetically distinct and reproductively isolated North American populations from California, Florida and Maine, and clearly demonstrated that at least three cryptic species exist. Earlier studies by Rice and Simon (1980) and Rice (1991) provide additional evidence of incipient sibling speciation in this widely distributed spionid polychaete.

Polydora cornuta can be easily distinguished from the closely related Polydora ciliata , P. c a l c a re a (Templeton, 1836), P. w e b s t e r i, P. h a s w e l l i Blake & Kudenov, 1978 and P. l i m i c o l a by the presence of the occipital antenna (Table 1). However, there may be some instances where the antenna may be absent and as such there is some degree of intraspecific variation ( Rice & Simon 1980; Mustaquim 1986; Rice 1991). The most distinctive feature of P. c o r nu ta, however, is the feather-like companion chaetae that closely adhere to the major spines of chaetiger 5.

Two other closely related species of Polydora having occipital antennae are P. c i r ro s a Rioja, 1943 from Western Mexico, but ranging from southern California to Ecuador and P. n u c h a l i s Woodwick, 1953 from southern California. Blake (1996) considered P. c o r n u t a, P. c i r ro s a, and P. nuchalis to represent a distinct species-group within the genus Polydora .

Polydora cornuta does exhibit variability in the presence of dorsal superior and ventral inferior fascicles of capillary chaetae on chaetiger 5, typically both these fascicles are absent ( Blake 1971; Kudenov 1982; Rice & Simon 1980; Mustaquim 1986; Sato-Okoshi 2000; Radashevsky 2005). Thus P. cornuta can be separated from P. ciliata , P. calcarea , P. w e b s t e r i, P. haswelli , P. limicola and P. nuchalis , all of which have both these chaetal fascicles. P. c i r ro s a, however, lacks these fascicles. The absence of noto- and neuropodial capillaries on chaetiger 5 in P. c o r n u t a is apomorphic because they are present in most other species of Polydora ( Blake 1996) . However, Blake and Maciolek (1987), based on material from the type locality of P. cornuta , indicated that P. c o r nu ta can possess 3–4 notopodial capillaries on one or both sides. Additionally, neuropodial capillaries may be present on chaetiger 5 in juveniles of P. c o r n u t a having fewer than 22–24 chaetigers ( Michaelis 1978; Radashevsky 2005). Rice (1991) and Rice et al. (2008: Fig. 2 B) indicated that in Florida populations most (~75%) of the specimens possess both dorsal superior and ventral inferior fascicles, lending further support to the concept that sibling species are present.

In adult Polydora cornuta the body lacks dorsal black pigmentation ( Ramberg & Schram 1983; Mustaquim 1986; Hartmann-Schröder 1996). However, Sato-Okoshi (2000) reported that some specimens had black pigmentation on the lateral side of anterior (1–10) chaetigers; this pigment is absent on individuals from the Black Sea.

Figures

FIGURE 1. Map showing records of Polydora, Dipolydora, and Pseudopolydora in the Black Sea and the Mediterranean: Polydora cornuta (blue circles): (1) Tena et al. (1991); (2) Radashevsky (2005), Surugiu (2005 a); (3) Çinar et al. (2005), Ergen et al. (2006); (4) Todorova & Panayotova (2006); (5) Boltachova & Lisitskaya (2007); (6) Daġli & Ergen (2008), Çinar et al. (2011); (7) Karhan et al. (2008); (8) Simboura et al. (2008); (9) Bondarenko (2011); (10) Losovskaya (2011); (11) Selifonova (2011). Polydora websteri (red triangles): (12) Surugiu (2005 a); (13) Lisitskaya et al. (2010). Dipolydora quadrilobata (yellow squares): (14) Požar-Domac (1978), Castelli et al. (1995); (15) Todorova & Panayotova (2006); (16) present study. Dipolydora caulleryi (black diamonds): (17) Dumitrescu (1960); (18) Castelli et al. (1995); (19) Simboura & Nicolaidou (2001). Pseudopolydora antennata (white stars): (20) Carrazzi (1895); (21) Dumitrescu (1960); (22) Simboura & Nicolaidou (2001); (23) Çinar et al. (2011).

FIGURE 2. Scanning electron micrographs of adult Polydora cornuta Bosc, 1802, Agigea (44 ° 04 ˏ 57.4 ˏˏN, 28 ° 38 ˏ 36.3 ˏˏE), 5 Aug 2003: (A) Anterior end, dorsal view, showing basal part of palps, occipital antenna, ciliary bands of nuchal organs and nototrochs on chaetigers 3, 4 and 7; (B) Anterior end, left lateral view, showing occipital antenna on caruncle, enlarged chaetiger 5 with notochaetae arranged in a slightly curved horizontal row, branchiae from chaetiger 7, parapodial lobes and postchaetal lamellae; (C) Chaetiger 5, right side ventral view, showing heavy falcate spines with lateral tooth and subterminal flange (indicated by the arrow) and companion chaetae with disheveled, feather-like distal tip (right) and with compact, broomlike distal tip (left); (D) Chaetiger 5, left side dorsal view, showing different degrees of wear of major spines; (E) Neuropodial hooded hooks of chaetiger 8, left lateroventral view (dorsal side is to the left and the anterior end is down), showing external openings of secretory cells of glandular pouches; (F) Posterior end, right laterodorsal view, showing terminal anus and numerous glandular epithelial cells on disk-like pygidium. Scale bars: A and F, 200 μm; B, 300 μm; C – E, 20 μm.