Terebellides gracilis (Malm, 1874)

Parapar, Julio, Mikac, Barbara & Fiege, Dieter, 2013, Diversity of the genus Terebellides (Polychaeta: Trichobranchidae) in the Adriatic Sea with the description of a new species, Zootaxa 3691 (3), pp. 333-350 : 335-338

Terebellides gracilis (Malm, 1874)

( Figures 2–4 , 12 b, 13)

Terebellides gracilis Malm 1874: 100 .

Terebellides gracilis —Hansson 1998: 77. Parapar et al. 2011: 11, Figs 8–10 , 13 c. Terebellides williamsae —Jirkov 1989: 124. Jirkov 2001: 529, Figs 1–4 .

Material examined. A total of 23 specimens were examined (27.4% of the total Terebellides specimens collected) all from station SJ 0 0 7: 27.02.2003 (PMR-14550, 2 specs.; PMR-14551, 1 spec.; PMR-14552, 1 spec. on SEM stub; PMR-14553, 1 spec. on SEM stub); 28.05.2003 (PMR-14554, 2 specs.; PMR-14555, 3 specs); 12.08.2003 (MNCN 16.01/14714, 1 spec.; MNCN 16.01/14715, 2 specs.); 23.01.0 4 (2 specs.) (coll. BM); 30.08.2004 (2 specs.) (coll. BM); 0 2.12.2004 (PMR-14556, 3 specs.; PMR-14557, 3 specs.).

Description of Adriatic Sea specimens. Complete specimens range from 12 to 18 mm in length and 1.2 to 0.7 mm in width; body tapering posteriorly with segments becoming increasingly shorter and crowded towards pygidium. Prostomium compact; tentacular membrane surrounding mouth, with many long buccal tentacles with expanded tips. SGI forming an expanded structure below tentacular membrane. Lateral lappets on SGIII–VIII ( CH 1–6) ( Fig. 2 a) being larger and continuing ventrally on SG III to VI, declining in size posteriorly. No conspicuous dorsal rounded projection in anterior chaetigers or oval-shaped glandular region in CH 3.

Branchiae arising as single structure from SGIII, consisting of single stalked structure located mid-dorsally ( Figs 2 a, 3a) made up of two posterior pairs of lobes fused along less than one third of their length; lower pair slightly shorter than upper pair. Pointed projection of posterior region of lobes present in lower lobes. Anterior branchial projection (fifth lobe) not conspicuous. Both sides of branchial lamellae provided with several parallel bent rows of cilia and outer tufts of cilia ( Figs 2 b, c; 3b). Branchial lamellae less tightly packed than in the other two Adriatic species.

Eighteen pairs of thoracic notopodia (SGIII–XX). Notopodia and notochaetae of first chaetiger not visible in some specimens ( Fig. 2 a, d); chaetae present only in larger specimens but much shorter than on subsequent notopodia ( Fig. 3 a). Neuropodia present as sessile pinnules from CH 6 (SGVIII) to pygidium and provided with uncini in single rows throughout ( Fig. 4 a). The absence of notochaetae in first chaetiger in most specimens may lead to the erroneous observation that first neuropodium is located on CH 5 instead of CH 6. First thoracic neuropodia provided with 5 – 7 sharply bent, acute tipped, geniculate acicular hooks ( Fig. 3 c). Minute teeth forming a capitium on geniculate chaetae not observed. Second and all subsequent thoracic neuropodia with up to 7–10 uncini per torus ( Fig. 4 a). Uncini provided with long shafted denticulate hooks with 2 – 4 teeth above main fang surmounted by 4 – 5 shorter teeth and an upper crest of several smaller denticles ( Fig. 4 b), dental formula MF:2– 4:4–5:∞.

Between 30−32 abdominal neuropodia as erect pinnules provided with about 22 uncini per torus ( Fig. 4 c); uncini with 5 teeth above main fang surmounted by a crest of 4–5 shorter teeth and a variable number of smaller teeth ( Fig. 4 d); dental formula MF:5:4–5:∞. Pygidium blunt, funnel-like depression.

One large, button-hole like nephridial opening on each notopodium of CH 4 and CH 5 ( Fig. 3 d).

MG staining pattern 2 ( Figs 12 b, 13a): compact green colouration in CH 1 – 10, quickly fading in following segments. CH 1 – 3 slightly and CH 4 much less stained than anterior and posterior ones. Colour in alcohol pale brown with four anterior thoracic chaetigers ventrally white ( Fig. 13 b).

Remarks. Hansson (1998) proposed to recover T. gracilis from the synonymy of T. stroemii due to the presence of four white ventrally colored thoracic segments (SGIII–VI; CH 1–4) in T. gracilis . Following this opinion, Parapar et al. (2011) redescribed the species from material collected in the BIOICE project in Iceland and proposed also T. williamsae Jirkov, 1989 as a junior synonym.

Terebellides gracilis was until now found in the Norwegian and Barents Seas (Malm 1874; Jirkov 1989) and Iceland (Parapar et al. 2011). Our Mediterranean records extend the range of the species into quite different ecological conditions compared to those where it was recorded so far. However, the finding of this species in the Northern Adriatic Sea is not so surprising and it supports the strong boreal affinity of this region, as well as its ecological and biogeographical similarities with the North Atlantic, which have previously been documented (Bianchi et al. 2004; Boero & Bonsdorff 2007). The Adriatic Sea is the northernmost Mediterranean region and together with the Gulf of Lions and the Northern Aegean Sea the coldest sector of the Mediterranean. It is geomorphologically, hydrographically and biogeographically a peculiar Mediterranean region with lower average temperatures that allow the presence of a specific flora and fauna with cold water affinities (Mikac & Musco 2010). Our research showed that Adriatic specimens of T. gracilis are slightly shorter than boreo-arctic specimens. This feature could be a morphological variability due to the different ecological conditions in which specimens are living. Further molecular analyses could possibly assist to clarify this phenomenon.

Adriatic specimens are slightly shorter (12–18 vs 10–25 mm) and have less abdominal chaetigers (30–32 vs. about 43) and less uncini (22 vs. 45) than boreo-arctic specimens. Also, the chaetae from first thoracic chaetiger are less conspicuous than in Icelandic specimens and the dental formula of thoracic uncini differs, with two teeth surmounting the main fang in North Atlantic specimens (MF:2:5:∞) but 2−4 in Adriatic ones (MF:2−4:4−5:∞).

The staining pattern coincides with one of the Icelandic specimens although Parapar et al. (2011) erroneously reported pattern 4 for those specimens instead of 2 (Parapar et al. 2011, page 19, Table 1).

Habitat. Found at shelf depths (385–390 m) in Scandinavian and Russian waters (Jirkov, 1989; 2001; Hansson, 1998). North and South coast of Iceland; 68 to 2076 meters depth (Parapar et al., 2011). In the Adriatic Sea the species was found on the offshore station in silty sand at 31 m.

Distribution. Norwegian Sea and Barents Sea (Malm 1874; Jirkov 1989); Iceland (Parapar et al. 2011) and Adriatic Sea. Our finding in the Adriatic Sea represents the first record of this species in the Mediterranean Sea, and considerably expands the southern boundary of this species.

Figures

FIGURE 1. Map of the study area showing collecting stations.

FIGURE 2. SEM micrographs of Terebellides gracilis (Malm, 1874) from the Adriatic Sea (station SJ 007) (a) anterior end, latero-ventral view; (b) edge of branchial lamellae; (c) detail of branchial ciliation; (d) detail of first three thoracic chaetigers. Scales: (a) 450 µm, (b) 45 µm, (c) 10 µm, (d) 200 µm. CH 1 = chaetiger 1, CT = cilia tufts.

FIGURE 3. SEM micrographs of Terebellides gracilis (Malm, 1874) from the Adriatic Sea (station SJ 007) (a) anterior end, latero-dorsal view; (b) edge and inner side of branchial lamellae; (c) geniculate chaetae of chaetiger 6 (broken at distal end); (d) detail of nephridial opening of thoracic chaetiger 5. Scales: (a) 300 µm, (b) 50 µm, (c) 15 µm, (d) 25 µm. CT = cilia tufts; CR = cilia rows.

FIGURE 4. SEM micrographs of Terebellides gracilis (Malm, 1874) from the Adriatic Sea (station SJ 007) (a) thoracic unciniger; (b) thoracic uncini; (c) abdominal unciniger; (d) abdominal uncini. Scales: (a) 25 µm, (b) 10 µm, (c) 30 µm, (d) 5 µm.

FIGURE 8. SEM micrographs of Terebellides mediterranea spec. nov., from the Adriatic Sea (station SJ 007) (a) tip of buccal tentacle; (b) detail of nephridial opening of first thoracic chaetiger; (c) nephridial opening of thoracic chaetigers 4 and 5; (d) detail of nephridial opening of thoracic chaetiger 5. Scales: (a) 50 µm, (b) 25 µm, (c) 100 µm, (d) 45 µm.

FIGURE 9. SEM micrographs of Terebellides stroemii Sars, 1835 from the Adriatic Sea (station LIM K 5) (a, b) anterior end, latero-ventral view, of two specimens; (c) papillar projections on edge of branchial lamellae; (d) ciliation of branchial lamellae. Scales: (a, b) 1 mm, (c) 100 µm, (d) 50 µm. CR = cilia rows; PP = papillar projection; star marking position of glandular region of fifth chaetiger.

FIGURE 10. SEM micrographs of Terebellides stroemii Sars, 1835 from the Adriatic Sea (station LIM K 5) (a) geniculate chaetae of chaetiger 6; (b) detail of geniculate chaeta capitium; (c) thoracic uncini; (d) detail of rostral teeth of thoracic uncini. Scales: (a) 50 µm, (b) 5 µm, (c) 10 µm, (d) 3 µm.

FIGURE 12. Methyl green staining of three Terebellides species found in the Adriatic Sea. LM pictures of anterior region in ventral (a – c) and lateral view (d – e). (a, d – e) T. mediterranea spec. nov., (b) T. gracilis, (c) T. stroemii.

FIGURE 13. Diagrammatic representation of several diagnostic body characters in three Adriatic Terebellides species. (a) Body staining patterns—following Schüller & Hutchings (2010) — in ventral view; chaetigers indicated in Arabic numbers, (b) Branchial and chaetiger characters in lateral view; segments indicated in Roman numbers. LBL = lower branchial lobes; UBL = upper branchial lobes; TM = tentacular membrane; LL = lower lobe; UL = upper lobe. Ventral (a) and lateral (b) lappets marked by bold lines.