On the diversity of the SE Indo-Pacific species of Terebellides (Annelida; Trichobranchidae), with the description of a new species

Systematic account

Terebellides hutchingsae spec. nov.

Material examined

THAILAND (Gulf of Thailand): Holotype: MNCN 16.01/17428 (St. 6). Paratypes: MNCN 16.01/17429 (St. 2, 4 specs); MNCN 16.01/17430 (St. 3, 3 specs); MNCN 16.01/17431 (St. 5, 3 specs); MNCN 16.01/17432 (St. 5, 1 spec. on SEM stub); MNCN 16.01/17433 (St. 6, 5 specs); MNCN 16.01/17434 (St. 7, 5 specs); MNCN 16.01/17435 (St. 8, 7 specs); MNCN 16.01/17436 (St. 8, 1 spec. on SEM stub); MNCN 16.01/17437 (St. 15, 2 specs); MNCN 16.01/17438 (St. 16, 6 specs); MNCN 16.01/17439 (St. 23, 1 spec. on SEM stub). MYANMAR (North Andaman Sea): Paratypes: MNCN 16.01/17440 (St. E7(2), 1 spec.); MNCN 16.01/17441 (St. E8(3), 1 spec.); MNCN 16.01/17442 (St. E11B(2), 4 specs); MNCN 16.01/17443 (St. E11B(3), 2 specs); MNCN 16.01/17444 (St. E14(2), 4 specs); MNCN 16.01/17445 (St. E15(2), 10 specs); MNCN 16.01/17446 (St. E16(1), 2 specs); MNCN 16.01/17447 (St. E16(3), 1 spec.); MNCN 16.01/17448 (St. 17(3), 1 spec.); MNCN 16.01/17449 (St. S2(2), 1 spec.); MNCN 16.01/17450 (St. S3(2), 4 specs); MNCN 16.01/17451 (St. S3(2), 1 spec. on SEM stub); MNCN 16.01/17452 (St. S3(3), 4 specs); MNCN 16.01/17453 (St. S4(2), 2 specs); GNM Polychaeta 14880 (St. S4(3), 1 spec.); GNM Polychaeta 14881 (St. WP2(2), 2 specs); AM 48834 (St. WP2(3), 2 specs); MNCN 16.01/17454 (St. WP2(3), 2 specs on SEM stub); AM 48835 (St. WP3(3), 1 spec.).

Description (based on holotype and paratypes) Complete individuals ranging from 9.0 to 14.0 mm in length (14 mm in holotype; Figs. 1A and 2A–2B) and 0.7 to 1.5 mm in maximum width at thoracic region (1.3 mm in holotype, excluding parapodia). Body tapering posteriorly with segments increasingly shorter and crowded towards pygidium. Prostomium compact; peristomium forming a tentacular membrane with large upper and lower lips surrounding mouth, sometimes almost devoid of buccal tentacles (Fig. 3A). Buccal tentacles of two types, short ventral tentacles uniformly cylindrical or slightly expanded at tips, and long dorsal tentacles more expanded at tips (Figs. 2B and 4A–4B). Lateral lappets on TC1–5 (SGIII–VII), being larger in TC1–3 (Figs. 2B, 3A, 4C and 6A ). No conspicuous dorsal rounded projection on anterior chaetigers or oval-shaped glandular region in TC3. Both notopodia and notochaetae in TC1 less developed than in following chaetigers (Figs. 3A, 4C and 4E).

Branchiae arising as single structure from SGII–III, with a single, mid-dorsal, stalk and two pairs of unfused lobes; lower (=ventral) (BL3–4) pair smaller and much shorter than upper (=dorsal) (BL1–2) pair of lobes (Figs. 3A–3B and 6B–6C). Upper and lower lobes with a short terminal pointed projection (although deciduous and sometimes damaged) (Fig 3C). Dorsal pair of branchial lobes with short anterior projection (fifth lobe; BL5) (Fig. 3D), sometimes hidden behind buccal tentacles (Figs. 2A and 2B). Loss of any of branchial lobes not observed. One side of branchial lamellae with parallel bent rows of cilia and well- developed ciliated papillae on edge of one side of each branchial lamella (Figs. 3D–3F).

Eighteen thoracic chaetigers (SGIII–XX), all with notopodia; neuropodia from SGVIII. Notopodia of TC1 smaller than following ones (Figs. 4C and 4E); all remaining notopodia similar in size. Thoracic neuropodia as sessile pinnules, from TC6 (SGVIII) to TC18 (SGXX), with uncini in single rows from TC7 (SGIX) throughout. Thoracic notochaetae similar in length, with textured surface (Fig. 4F). Ciliated papilla dorsal to each thoracic notopodia not observed. First thoracic neuropodia (TC6) with 4–7 geniculate acicular chaetae with minute teeth in their upper part forming a capitium easily overlooked without SEM (Figs. 6E–6F); sharply bend. Subsequent thoracic neuropodia with one row of about 8–10 uncini per torus (Fig. 5A); uncini as shafted denticulate hooks with long, pointed rostrum surmounted by 4–5 teeth and an upper crest of several smaller denticles of different sizes (Figs. 5A–5C). One finger-shaped nephridial papilla basal to branchial stem (Fig. 4E); genital openings, dorsal to notopodia in TC4 and TC5 ( Figs. 4D and 6D).

Twenty seven to 30 abdominal chaetigers (30 in holotype). Abdominal neuropodia as erect pinnules, with about 30 uncini per torus (Fig. 5D). Uncini with 3–4 teeth above rostrum (Figs. 5E and 5F), surmounted by a row of an irregular number of shorter teeth and an upper crest of minute teeth. Pygidium blunt, funnel-like depression. No eggs were observed in body cavity of holotype, but mature females of smaller size were observed (9.0 mm length, 1.0 mm width). Colour in alcohol pale brown.

Methyl green staining ressembling pattern 1 of Schüller & Hutchings (2010), resulting in a solid green coloration from CH1 to CH9, then turning into striped pattern from CH10 to CH12 and fading in following segments. Additional pronounced staining also on short ventral branchial lobes (BL3–4) and postero-ventral part of branchial upper lobes (BL1–2).

Type locality

Gulf of Thailand, muddy bottom at 66 m depth.

Distribution and habitat

Specimens of T. hutchingsae spec. nov. were found in shallow water bottoms (45.5–51.0 m depth) about 80 km off the coast of Myanmar (North Andaman Sea) and in slight deeper bottoms (61.0–78.0 m depth) in the outer end of the Gulf of Thailand (Table 1 and Fig. 7). Sediments are typically muddy with high values of organic carbon (0.74–2.42%) and of silt and clay fraction (69.6%–95.4%).

Etymology

The species is named after Dr. Pat Hutchings, for her many contributions to the taxonomy of Terebelliform polychaetes in Australia and SW Pacific waters, and particularly to the genus Terebellides, and also for her key role in the study of Australian polychaetes.

Terebellides cf. woolawa Hutchings & Peart, 2000

MNCN 16.01/17455 (St. S4(3), 1 spec.); MNCN 16.01/17456 (St. WP3(3), 1 spec.).

Distribution and habitat

Both specimens of T. cf. woolawa were found in two shallow water stations (51.0 m depth) about 80 km off the mouth of the Irawadi river in the coast of Myanmar (North Andaman Sea) (Table 1).

Terebellides sp.

MNCN 16.01/17457(St. S4(3), 1 spec.).

Distribution and habitat

The specimen was found in a shallow water bottom (51 m depth) about 16 km off the coast of Myanmar (North Andaman Sea) (Table 1).

Key of SE Indo-Pacific species of Terebellides

The key here presented has been modified from a previous key of Australian Trichobranchidae by Hutchings & Peart (2000), which was based on a limited number of easy-to-detect characters: (1) number of chaetigers with geniculate chaetae, (2) degree of development of thoracic notopodia, and (3) shape of branchiae, giving special emphasis to the relative size of branchial lobes. Terebellides ypsilon Grube, 1878, from the Philippines, was not included because the description is very brief and following Hutchings & Peart (2000), who revised the type material, the taxon should be considered as undeterminable.

1. Those of first pair (segment 7) are shorter.

2. The position of GC in TC7 (SG9) is very unusual in the genus Terebellides; this feature is apparently only shared with T. pacifica Kinberg, 1866, a species which has been removed from synonymy with T. stroemii by Garraffoni, Lana & Hutchings (2005).

On Terebellides hutchingsae spec. nov.

Five species of Terebellides were previously described in the equatorial Indo-Pacific region (Fig. 7): T. intoshi Caullery, 1915, T. sieboldi Kinberg, 1866, T. ypsilon Grube, 1878, T. jorgeni Hutchings, 2007 and T. jitu Schüller & Hutchings, 2010. Terebellides intoshi is characterised by the large size of the notopodia and notochaetae from TC6 onwards (Fig. 8A ) and probably by the presence of two chaetigers with geniculate chaetae as well (see also the discussion on Terebellides sp.); T. sieboldi has geniculate chaetae in TC7 (SG9) instead of TC6 and T. ypsilon is considered undeterminable by Hutchings & Peart (2000) because type material no longer exists. The two most recently described species, Terebellides jorgeni and T. jitu, are the most similar to T. hutchingsae spec. nov. The overall shape of branchiae is quite similar in T. jorgeni and T. hutchingsae sp. nov., being lobes 1–4 unequally sized and entirely free (not fused), with upper (dorsal) ones larger than lower (ventral) ones, and with “surface of branchial lamellae weakly papillate” (cfr. p. 78 in Hutchings, 2007); the latter probably refers to the presence of ciliated papillae, which is a feature difficult to confirm in the original figures. On the other hand, T. jorgeni differs from the new species in: (1) the presence of glandular and whitish ventral part of anterior segments, SG5 to SG9 (CH3 to CH7) but specially on SG5 to SG7 (absent in T. hutchingsae sp. nov.), and bearing pronounced thickening and elevation of dorsal anterior margins forming dorsal crests; (2) genital openings are present in SG4 and SG5, instead of SG6 and SG7 (TC4 and TC5) as in T. hutchingsae spec. nov.; (3) the branchiae are formed by four lobes instead of five.

According to the original description, T. jitu is also similar to T. hutchingsae spec. nov. but all branchial lobes are of similar length and have half of their length fused, instead of the lower ones being much shorter and fused basally as in T. hutchingsae spec. nov.

Terebellides narribri Hutchings & Peart, 2000 and T. woolawa Hutchings & Peart, 2000 were described from the NE Australian coast. Both species share with T. hutchingsae spec. nov. branchiae with similar shape and composed by five lobes; T. narribri differs from the new species by having first thoracic notopodia (TN1) of same size as the following, and TC3 bearing large, white, oval pair of glandular patches. Terebellides woolawa is characterised by the great development of BL5 (but see discussion on T. cf. woolawa) and by having anterior thoracic segments with dorsal projections on lateral lappets, which are absent in T. hutchingsae spec. nov.

Out of the Indo-Pacific area, there are no reports yet of any species gathering the same set of characters as T. hutchingsae spec. nov. However, seven more species have been described with branchial lamellae having ciliated papillae (Solís-Weiss, Fauchald & Blankestein, 1991; Bremec & Elias, 1999; Parapar et al., 2016). These are T. klemani Kinberg, 1867, T. anguicomus Müller, 1858, T. carmenensis Solís-Weiss, Fauchald & Blankestein, 1991, T. parvus Solís-Weiss, Fauchald & Blankestein, 1991, T. lanai Solís-Weiss, Fauchald & Blankestein, 1991, T. totae Bremec & Elías, 1999 and T. persiae Parapar et al., 2016. Four of them differ from our new species in having “thoracic dorsal hump”: T. anguicomus (which also has 17 thoracic chaetigers instead of the 18 in T. hutchingsae spec. nov.), T. carmenensis, T. totae (which also has all four branchial lobes similar in length, while the ventral ones are much shorter in T. hutchingsae spec. nov.) and T. persiae. As for the three remaining species, T. klemani has all branchial lobes of similar length and free almost to base, and gently curved geniculate acicular chaetae instead of being sharply bent, T. lanai has only one type of buccal tentacles, instead of two, and branchial lobes are fused in most of their length; and T. parvus is characterized by having a very low number of abdominal segments (20–26 instead of 27–30 in our new species).

Finally, two species show tufts of cilia at the edge of the branchial lamellae: T. mediterranea Parapar, Mikac & Fiege, 2013, and T. gracilis (Malm, 1874) both from Iceland, sensu Parapar, Moreira & Helgason (2011), and from the Adriatic sea, sensu Parapar, Mikac & Fiege (2013), but in these two species the cilia arise directly from the lamella surface and not from the tip of a papilla as in T. hutchingsae spec. nov.

On Terebellides cf. woolawa and Terebellides sp.

Terebellides woolawa is characterised by the well-developed fifth branchial lobe (BL5) and the presence of dorsal rounded projections on lateral lappets of SG 3–6 (TC1–4). This large species was described from intertidal to shallow water habitats in eastern Australia (Fig. 7) and was found across most of Australian coasts (Hutchings & Peart, 2000). Specimens found in this study are large-sized, and agree fairly well with the original description; in particular, specimen MNCN 16.01/17455 shows the typical shape of the branchiae, which have five lobes, BL1–4 are fused up to half of their length, filamentous tips are short, and BL5 is well developed (Figs. 2C and 2D). Nevertheless, our specimens lack the characteristic dorsal lobes of anterior thoracic lateral lappets: this prevented to fully confirm the identity of our material.

In turn, the specimen identified as Terebellides sp. differs from T. hutchingsae spec. nov. and Terebellides cf. woolawa in two features: (1) BL5 is large-sized, about half the length of posterior lobes (BL1–4); and (2) TC5 and TC6 are both provided with acicular geniculate chaetae. Thus, BL5 is longer than in any other described species including T. woolawa. However, this might be due to the preservation state of the specimen, which is slightly deteriorated. Anyway, the combination of the two aforementioned characters may justify the erection of a new species, but we prefer to wait for eventually finding additional specimens to confirm its status.

On the other hand, four species of Terebellides were previously described as having geniculate chaetae in two thoracic chaetigers. Two species are known from the French Polynesia and Iceland: T. biaciculata Hartmann-Schröder, 1992 and T. bigeniculatus Parapar, Moreira & Helgason, 2011, respectively. The other two belong to the Indo-Pacific region: T. akares Hutchings, Nogueira & Carrerette, 2015 and T. intoshi Caullery, 1945 sensu Imajima & Williams (1985), from North-East Australia and Japan, respectively. We follow Parapar, Moreira & Helgason (2011) in considering that type material of T. intoshi from South China Sea probably does not have two chaetigers with geniculate chaetae. Thus, the Japanese material would belong to a different species. Anyway, they differ from Terebellides sp. in the branchial shape and the greater development of thoracic notopodia from TC6 (Fig. 8A). In turn, T. akares, have branchiae bearing a much shorter BL5 and the posterior ventral lobes (BL3–4) are completely free from each other, contrary to Terebellides sp., in which these lobes are fused in most of their length (Fig. 2F). The observed differences between these Indo-Pacific species and Terebellides sp. reinforce is status as new species, so that further efforts should be addressed to find new materials allowing to formally describe it.

On Terebellides stroemii in Indo-Pacific waters

The North Atlantic species and type species of the genus Terebellides, T. stroemii Sars, 1835, was also widely reported in the Indo-Pacific area. For instance, in Indonesia by Caullery (1944), in South Korea by Gallardo (1967), in Hong Kong by Shin (1982), in Singapore by Tan & Chou (1993) and in the Australian coasts by Stephenson, Williams & Lance (1970), Stephenson, Williams & Cook (1974), Knox & Cameron (1971), Hutchings (1977), Amoureux (1984), Hutchings & Murray (1984) and Hutchings et al. (1993) (Fig. 7). In the Southern Pacific Ocean, the presence of T. stroemii was denied by Hutchings & Peart (2000) after examining Norwegian material. Indeed, these authors already reassigned part of these Indo-Pacific reports to other species, while others specimens were not. Among them, the material reported by Caullery (1944) and collected during the Siboga expedition might well correspond to more than one species according to the description and illustrations. The shape of the branchiae in specimen from station 271 (Fig. 147 in Caullery, 1944; redrawn here in Fig. 8B) and station 311 (Fig. 148 in Caullery, 1944; redrawn here in Figs. 8C and 8D) sharply differs in BL5 size; the specimen of station 311 is more similar in branchial shape to T. hutchingsae spec. nov. but differs in the high degree of fusion of dorsal and ventral lobes in Caullery’s material (see Fig. 8D). The specimen reported by Gallardo (1967) cannot be properly identified because the description is quite brief (e.g., “The branchia has the typical shape…”) and only a lateral view of a thoracic uncinus is illustrated and this is not relevant in species discrimination. More recently, Parapar & Hutchings (2015) redescribed T. stroemii based on Norwegian specimens collected by Michael Sars near the type locality. Therefore, the type species is now well-illustrated based on the most recent, taxonomically robust characters. This redescription, together with the previous observations and our present results, certainly allows us to strongly support the absence of T. stroemii from Indo-Pacific waters.

Taxonomic relevance of the ciliated papillae of branchial lamellae

One of the most relevant diagnostic characters of T. hutchingsae spec. nov. is the presence of ciliated papillae in branchial lamellae. This character was long ignored in Terebellides descriptions and was discussed by Parapar, Moreira & O’Reilly (2016) and Parapar et al. (2016). In fact, several recently described species from across the world oceans show this feature (Table 2), namely T. gracilis Malm, 1874 sensu Parapar, Moreira & Helgason (2011), off Iceland; T. jorgeni Hutchings, 2007, from Indonesia; T. gracilis Malm, 1874 sensu Parapar, Mikac & Fiege (2013) and T. mediterranea Parapar, Mikac & Fiege, 2013, from the Adriatic Sea; T. akares Hutchings, Nogueira & Carrerette, 2015, from the Great Barrier Reef (NE Australia); T. persiae Parapar et al., 2016, from the Persian Gulf and T. cf. woolawa Hutchings & Peart, 2000 sensu Parapar et al. (this work) from South Myanmar. This character is probably much more widespread and shows at least two different morphotypes: (1) low papillae as it was found in T. gracilis from Iceland and the Mediterranean, and (2) well developed papillae in the rest of species. The presence of these low ciliated papillae reported in Icelandic and Adriatic specimens of T. gracilis by Parapar, Moreira & Helgason (2011) and Parapar, Mikac & Fiege (2013) was confirmed in the holotype. Therefore, these ciliated papillae appear as a robust taxonomic character and we strongly recommend taking it into account in future descriptions of new species within the genus.