Trichobranchidae Malmgren 1866

Family Trichobranchidae Malmgren, 1866

Figs 1A, 7–8

Diagnosis (after Hutchings et al. 2021a, most important diagnostic characters highlighted in bold)

Transverse prostomium attached to dorsal surface of upper lip; basal part as thick crest, eyespots sometimes present; distal part at base of upper lip or extending along lip. Buccal tentacles of two types, uniformly cylindrical and expanded at tips, spatulate. Peristomium forming lips, sometimes also a ventral lobe, as an extension of the lower lip; lips expanded, circular upper lip, distal margin folded or convoluted; lower lip button-like, usually continuing by ventral lobe, or expanded, forming large scoop-shaped process (Figs 7A–C, 8A, C–D). Segment I usually short, frequently only visible ventrally; anterior margin of anterior segments with lobes as low, even-length collars covering posterior margins of preceding segments, at least ventrally; ventro-lateral or lateral lobes on anterior segments sometimes present. Anterior segments poorly glandular ventrally, smooth, discrete shields absent; midventral groove extending from posterior segments with notopodia. Two to four pairs of branchiae, beginning from SGII, each pair with single, thick and elongate, tapered or foliaceous filament, or two pairs fused in single four lobed structure originating mid-dorsally between SGII–III or II–IV (Figs 7C, 8C–D). Notopodia beginning from SGIII–VI, typically terminating at SGXX; short, conical notopodia, chaetae emerging from central core on top, distal lobes absent; narrowly-winged notochaetae in both rows throughout. Neuropodia beginning on same segment as notopodia or slightly posteriorly, rarely beginning before notopodia; sessile neuropodia until termination of notopodia, neurochaetae emerging directly from body wall, as rectangular to foliaceous pinnules after termination of notopodia; thoracic neurochaetae as acicular uncini (Figs 1A, 7D, 8F), sometimes with small hood or beard below main fang; avicular abdominal uncini, with secondary teeth in rows on top and laterally to main fang. Nephridial papillae on SGIII usually present, other papillae sometimes present on SGVI and SGVII, but reduced to inconspicuous in most taxa. Pygidium smooth to slightly crenulate, sometimes bilobed.

Remarks

In the past, the Trichobranchidae family was considered to be a subfamily of Terebellidae (Fauvel 1927; Day 1967; Garrafoni & Lana 2004), but recent phylogenetic analyses support the hypothesis of a valid family (Glasby et al. 2004; Nogueira et al. 2013). The family includes only three genera, i.e., Octobranchus Marion & Bobretzky, 1875, Terebellides Sars, 1835, and Trichobranchus Malmgren, 1866. For Trichobranchus and Octobranchus, only three species of each occur in Europe. The genus Terebellides is very speciose and is represented in Europe by 19 species, 13 of them described in the last two years (Lavesque et al. 2019b; Parapar et al. 2020a) (Table 1).

Main morphological characters for European species

The number of branchiae is the best character to discriminate the different genera, with Terebellides having a single large branchia, Trichobranchus with two or three pairs of branchiae and finally Octobranchus with four pairs.

Trichobranchus species are easy to differentiate based on the number of branchiae (two vs three) (Figs 7C, 8C) and the absence or presence of eyespots. In Octobranchus, the species differ by the shape of the branchiae (Fig. 8D) and the number of secondary teeth above the main fang of the uncini. Regarding Terebellides species, recent studies highlighted that several characters are very important for identification to the species level (Lavesque et al. 2019a; Parapar et al. 2020a, 2020b). However, as many cryptic species occur at a small geographical scale (Nygren et al. 2018), which currently are confirmed only by molecular analyses (Parapar et al. 2020a) much more work needs to be done to resolve all the species present.

BRANCHIAE. Even if Terebellides branchiae seem to be very similar within the genus (Figs 7A–B, 8A–B), several morphological characters permit the discrimination of species, such as the presence of a fifth anterior branchial lobe (e.g., T. europaea), the degree of fusion of both upper and lower lobes (e.g.. not fused on T. ceneresi), the presence of long terminal filaments (e.g., in T. shetlandica) or short posterior processes (Fig. 7B), and finally the presence and the shape of papillae situated on the margins of the branchial lamellae (Fig. 8B) (e.g., T. lilasae).

NOTOCHAETAE FROM FIRST CHAETIGER. The size of notochaetae of the first chaetiger varies between species. For most of the species, these chaetae are of a similar size compared to those of the following chaetigers. However, they can be absent or much shorter (e.g., T. ceneresi) or much longer (e.g., T. mediterranea).

PRESENCE OF GENICULATE CHAETAE ON ONE OR TWO CHAETIGERS. The geniculate chaetae are exclusive to members of Terebellides and they are typically present on CH 6 (SG VIII) only (Fig. 8E), but in some species they are present on two chaetigers, as for example in T. bigeniculatus.

UNCINI DENTICULATION. The different types of uncini follow the classifications provided by Parapar et al. (2020b) for thoracic uncini (Fig. 8F) and Parapar et al. (2020a) for abdominal uncini. These

classifications are based on the ratio between the length of the main fang (rostrum) and the crest of secondary teeth (capitium), and the size and number of the secondary teeth.

THORACIC CILIATED PAPILLAE. Following the recent study of Parapar et al. (2020a), the absence or the presence of thoracic ciliated papillae allow for the discrimination of Terebellides species. These papillae are situated dorsally to the thoracic notopodia (see for example Parapar et al. 2020a; Fig. 7B).

METHYL GREEN PATTERN. The colouration of Terebellides specimens prior to identification is essential. Indeed, MG staining highlights the presence and the shape of the glandular region of the third thoracic chaetiger (e.g., undulating glandular region present and in members of T. gentili, oval for T. lilasae Fig. 7B) and the compact/striped pattern of the ventral part of anterior chaetigers (e.g., CH 4 (SG VI) white in T. ceneresi).

Key to European species of Trichobranchidae (after Lavesque et al. 2019a and Parapar et al. 2020a)

1. One large branchia consisting of a stem and four lobes with transverse lamellae.....5 (Terebellides)

– Two or three pairs of branchiae........................................................................... 2 (Trichobranchus)

– Four pairs of branchiae........................................................................................... 4 (Octobranchus)

2. Two pairs of branchiae...................................................................................................................... 3

– Three pairs of branchiae, eyespots present................................................................................................................................................................................. Trichobranchus glacialis Malmgren, 1866

3. Eyespots absent......................................................................... Trichobranchus roseus Malm, 1874

– Eyespots present.................................................................................................................................... Trichobranchus demontaudouini Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019

4. Pairs of branchiae of different shapes; abdominal uncini with three rows of secondary teeth above the main fang..................................................... Octobranchus floriceps Kingston & Mackie, 1980

– All pairs of branchiae similar; abdominal uncini with two rows of secondary teeth above the main fang..................................................................................... Octobranchus lingulatus (Grube, 1863)

– Bases of branchiae covered by dorso-lateral lobes, abdominal uncini with two rows of secondary teeth above the main fang.............................. Octobranchus sikorskii (Leontovich & Jirkov. 2001)

5. Geniculate acicular chaetae on CH 5 (SG VII) and CH 6 (SG VIII)............................................................................................................. Terebellides bigeniculatus Parapar, Moreira & Helgason, 2011

– Geniculate acicular chaetae on CH 6 (SG VI) only........................................................................... 6

6. Branchial lamellae without marginal papillae.................................................................................. 7

– Branchial lamellae with marginal papillae..................................................................................... 15

7. Lower branchial lobes with long filaments....................................................................................... 8

– Lower branchial lobes with or without short projections................................................................. 9

8. Glandular region on CH 3 (SG V) present; branchial lamellae pointed; notochaetae from CH 1 longer than following ones; dorsal papillae absent............................................................................................................... Terebellides parapari Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019

– Glandular region on CH 3 (SG V) absent; branchial lamellae rounded; all notochaetae equal-sized; dorsal papillae present........................ Terebellides shetlandica Parapar, Moreira & O’Reilly, 2016

9. Ventral white band present on CH 4 (SG VI) after MG staining..................................................... 10

– No distinct pattern on CH 4 (SG VI) after MG staining...................................................................11

10. Large species (> 30 mm); 5 th branchial lobe present; notochaetae of CH 1 (SG III) similar to following ones; main fang of thoracic uncini straight.................................... Terebellides gracilis Malm, 1874

– Small species (<20 mm); 5 th branchial lobe absent; notochaetae of CH 1 (SG III) absent or shorter than following ones; main fang of thoracic uncini ‘eagle head’ (= curved) shaped................................................... Terebellides ceneresi Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019

11. First notopodia and notochaetae longer than following ones............................................................................................................................... Terebellides mediterranea Parapar, Mikac & Fiege, 2013

– First notopodia and notochaetae similar or shorter than following ones........................................ 12

12. Large-sized species (> 50 mm); dorsal rounded projections on CH 1– CH 5 conspicuous............... 13

– Small-sized species (<20 mm); dorsal rounded projections on CH 1– CH 5 absent; main fang of thoracic uncini straight................................................................................................................... 14

13. Abdominal uncini of type 1 (length of capitium about 0.7 length of the main fang, capitium simple consisting of a few, wide denticles).................................................................................................................................................... Terebellides kongsrudi Parapar, Capa, Nygren & Moreira, 2020 and Terebellides bakkeni Parapar, Capa, Nygren & Moreira, 2020 complex

– Abdominal uncini of type 2 (capitium of about same length as main fang, capitium complex composed of a first row of 4(5) denticles and a variable number of teeth in two more rows)..................................................................................................................... Terebellides stroemii Sars, 1835

14. Glandular region on CH 3 (SG V) and 5 th branchial lobe both absent................................................................................................................................................... Terebellides atlantis Williams, 1984

– Glandular region on CH 3 (SG V) and 5 th branchial lobe both present............................................................................ Terebellides gralli Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019

15. Glandular region on CH 3 (SG V) rounded or oval......................................................................... 16

– Glandular region on CH 3 (SG V) otherwise.................................................................................. 17

16. Glandular region on CH 3 (SG V) staining in white, branchial lamellae with rounded papillae, CH 1– 3 without conspicuous dorsal projection....................................................................................................................... Terebellides lilasae Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019

– Glandular region on CH 3 (SG V) staining in blue, branchial lamellae with conical papillae, CH 1–3 with conspicuous dorsal projection................................................................................................................................ Terebellides bonifi Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019

17. Most branchial lamellae with marginal papillae............................................................................. 18

– Only anterior branchial lamellae with marginal papillae................................................................ 19

18. Branchial lamellae with digitiform papillae, upper lip elongated; MG staining pattern as compact bands from CH 1–5.................................................................................................................................................... Terebellides resomari Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019

– Branchial lamellae with widely spaced, small and elongated digitiform papillae; MG staining pattern leaving white stripes from CH 1–5................................................................................................................................ Terebellides gentili Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019

19. Thoracic uncini type 1 (main fang vs capitium length ratio 2(3)/1; capitium with 2(3) large teeth, following ones much smaller).................................................................................................................................................................. Terebellides ronningae Parapar, Capa, Nygren & Moreira, 2020

– Thoracic uncini type 3 (main fang vs. capitium length ratio 1/1; capitium with 4(5) mid-sized teeth, following ones slightly smaller)..................................................................................................... 20

20. Deep-water species, mostly found below 200 m deep.............................................................................................................................. Terebellides norvegica Parapar, Capa, Nygren & Moreira, 2020

– Shallow-water species, mostly found above 100 m deep.................................................................................. Terebellides europaea Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019 and Terebellides scotica Parapar, Capa, Nygren & Moreira, 2020 complex