Terebellidae Johnston 1846

Family Terebellidae Johnston, 1846 (sensu stricto)

Figs 1C–D, 5–6

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 frequently present (Fig. 5B), in short rows at each lateral sides, or extending transversely across basal part of prostomium. Buccal tentacles all usually uniformly cylindrical. Peristomium usually forming lips only; lips expanded, relatively short upper lip, hood-like, about as long as wide; swollen, usually button-like and mid-ventral lower lip. Segment I terminating laterally to ventro-laterally, partially fused to expanded lower lip, or developed, forming lobes of variable extension and position. Lobes on anterior segments frequently present, of variable length, sometimes extending to SGV–VII (Figs 5B–D, 6A– D). Anterior segments highly glandular ventrally, with discrete, smooth to corrugated, rectangular to trapezoidal mid-ventral shields extending from anterior segments until termination of notopodia, or near it; mid-ventral groove extending from termination of mid-ventral shields. Two to three pairs of branchiae usually present (Figs 5A–D, 6A–D), but three genera have a single pair and several are abranchiate; branchial filaments originating all together from single point on body wall, on either side of branchiferous segments, unbranched, or, more frequently, originating from conspicuous main stalk on either side of pair, branching from one to several levels, in plumose (spiraled), dichotomous, pectinate or arborescent arrangement. Notopodia beginning on SGII–V, SGIV in most genera, usually extending to mid-body, around SGXX, but sometimes present on fewer segments or extending more posteriorly for variable extension, rarely until near posterior end; first pairs of notopodia inserted dorso-laterally, progressively more laterally, then vertically aligned; cylindrical to rectangular notopodia. Notochaetae originating from central core on top, distal lobes absent; notochaetae distally winged, wings of variable length and width, or serrate, sometimes with wings at midlength, basally to a serrated blade; some more specialised types of notochaetae may be present (Fig. 5E–G). Neuropodia beginning posteriorly to notopodia, on SGV–IX, usually on SGV; neuropodia in conjunction with notopodia as low, sessile ridges, sometimes continuing posteriorly until pygidium, but most taxa with rectangular to cylindrical or foliaceous neuropodial pinnules after notopodia terminate; neurochaetae as avicular uncini usually as long as high, with short triangular heel directed posteriorly, slightly curved and wide base, and dorsal button (Figs 1C–D, 6E–F); uncini arranged in double rows (Fig. 6E) from around SGXI usually until termination of notopodia, but several genera with double rows.

Remarks

In European waters, the Terebellidae s.s. are represented by 19 genera and 44 species (Table 1). Four genera are represented only by a single species: Artacama Malmgren, 1866; Baffinia Wesenberg-Lund, 1950; Laphania Malmgren, 1866; Leaena Malmgren, 1866 and Stschapovella Levenstein, 1957. Eleven of them are represented by two European species each: Amphitritides Augener, 1922; Axionice Malmgren, 1866; Lanassa Malmgren, 1866; Lanice Malmgren, 1866; Loimia Malmgren, 1866; Nicolea Malmgren, 1866; Paramphitrite Holthe, 1976; Phisidia Saint-Joseph, 1894; Pistella Hartmann-Schröder, 1996; Proclea Saint-Joseph, 1894 and Terebella Linnaeus, 1767 (Lavesque et al. 2021). The genus Eupolymnia Verrill, 1900 is represented by four species and the two most diverse European genera are Amphitrite Müller, 1771, with ten species, and Pista Malmgren, 1866 with eleven (Lavesque et al. 2021). In our recent paper focusing on French Terebellidae s.s. we have confirmed the synonymy of Neoamphitrite with Amphitrite, as suggested by several authors (Jirkov 2020; Hutchings et al. 2021a). In contrast, we consider that Amphitritides, Lanice Loimia and Paramphitrite are still valid genera (Read & Fauchald 2021), contrary to what was proposed by Jirkov (2020) (see details in Lavesque et al. 2021).

Main morphological characters of European species

BRANCHIAE. The number and shape of branchiae are very important to separate species of Terebellidae s.s. Typically, species 2–3 pairs of branchiae are present on SG II–III or II–IV, but members of some genera, as for Polycirridae, completely lack branchiae: Baffinia, Lanassa, Laphania, Leaena, Phisidia and Proclea. Terebella banksyi is characterised by having branchiae on discontinuous segments: SG II–III and V (Fig. 5D). Generally branchiae are branching (dichotomous or arborescent), originating dorsolaterally from a main stalk (Figs 5A–D, 6A–D) or a single point on body wall, but some species have multiple unbranching branchial filaments, like Amphitrite cirrata or A. rzhavskyi. The presence or absence and the size of the branchial stem is important, like in Eupolymnia (Figs 5A–B, 6D).

LOBES. Genera of Terebellidae s.s. are distinguished from each other by the presence (or absence) and morphology of anterior lobes, usually positioned laterally. These structures are flaps of tissues covering at least part of the preceding segment (Nogueira et al. 2010) (Figs 5B–C, 6A–D). They can be absent, as in Nicolea or Terebella, narrow, as in Paramphitrite birulai or large, as in Lanice and Eupolymnia (Fig. 5 A–C) and they also vary significantly in morphology and position, from ventral to dorso-lateral (Figs 5B–C, 6A–D).

NEPHRIDIAL AND GENITAL PAPILLAE. Terebellids are characterised by the presence of papillae situated close to the notopodia or between parapodial lobes. The nephridial papillae occur from SG III–V, while genital papillae are present from SG VI onwards and are prominent only when the animals are mature (Fig. 5C–D, 6C). When they are visible, the morphology and the number of these papillae and their number permit the discrimination of species, as for Amphitrite or Terebella for example.

NOTOPODIA AND NEUROPODIA. Terebellidae s.s. differ by the number of pairs of notopodia, the segment on which notopodia and neuropodia start and the morphology of both noto- and neurochaetae. Usually, notochaetae are present on 17 segments, beginning from SG IV, but several exceptions exist as for example for Lanassa (n<15) or Terebella (n>25, often present to the pygidium). Notochaetae of Terebellidae are divided in two types: distally smooth as in Pista, Eupolymnia or Lanice, or distally serrated as in Amphitritides or Paramphitrite (Fig. 5E), and each types are sub-divided in sub groups (Nogueira et al. 2010: table 4). Concerning the neurochaetae, each part of the uncinus (Fig. 1C–D) differ greatly among the genera of Terebellidae and their morphology should be examined in detail. For example, members of the genus Pista have long-handled uncini, with the handle originating from the heel (Fig. 1C), while uncini in most of the other genera have short-handles. Contrary to tendons which are soft and thin structures attached to uncini, handles are chitinous structures extended from the heel. Members of the genus Loimia are unique due to the presence of pectinate uncini, with teeth arranged vertically in a single row (Fig. 1D), while other species have multiple transverse rows of secondary teeth above the main fang (Fig. 6E–G). The dorsal button is generally well developed and situated about midway between the base of the main fang and the tip of the prow, but is inconspicuous in specimens of Lanice and can be closer to the tip of the prow, as in Eupolymnia gili or the base of the main fang, as for Artacama proboscidea. Finally, the prow and the heel vary in shape and can be distally rounded or pointed.

Key to European species of Terebellidae (sensu stricto) (after Lavesque et al. 2021).

1. Peristomium ventrally forming a large conical process...... Artacama proboscidea Malmgren, 1866

– Absence of peristomial ventral process............................................................................................. 2

2. Notochaetae on more than 25 segments, body uniform throughout................................................. 3

– Notochaetae on 25 or fewer segments, thorax and abdomen clearly defined................................... 5

3. Branchiae absent........................................................................ Baffinia hesslei (Annenkova, 1924)

– Branchiae present............................................................................................................4 (Terebella)

4. Branchiae on SG II–IV, five pairs of nephridial and genital papillae...................................................................................................................................................... Terebella lapidaria Linnaeus, 1767

– Branchiae on SG II–III and V, 12 pairs of nephridial and genital papillae.................................................................................... Terebella banksyi Lavesque, Daffe, Londoño-Mesa & Hutchings, 2021

5. Absence of branchiae........................................................................................................................ 6

– Presence of branchiae..................................................................................................................... 12

6. Uncini from CH 2.............................................................................................................................. 7

– Uncini from CH 3............................................................................................................ 11 (Proclea)

– Uncini from CH 7......................................................................... Laphania boecki Malmgren, 1866

7. Notopodia with two types of notochaetae........................................................................................ 8

– Notopodia with one type of notochaetae only................................................................................ 10

8. Notochaetae on 10 segments......................................................... Leaena ebranchiata (Sars, 1865)

– Notochaetae on more than 13 segments.......................................................................... 9 (Phisidia)

9. Uncini in double rows on about 24 segments, eyespots present........................................................................................................................................................... Phisidia oculata (Langerhans, 1880)

– Uncini in double rows on 9–10 segments, eyespots absent............ Phisidia aurea Southward, 1956

10. Notochaetae on 11 segments............................................................. Lanassa venusta (Malm, 1874)

– Notochaetae on 15 segments............................................. Lanassa nordenskioldi Malmgren, 1866

– Notochaetae on 16 segments............................................. Stschapovella tatjanae Levenstein, 1957

11. Ventral lobe of SG II smooth and moderately protruding.......... Proclea graffii (Langerhans, 1884)

– Ventral lobe of SG II papillose and clearly protruding......... Proclea malmgreni (Ssolowiew, 1899)

12. All notochaetae subdistally denticulate.......................................................................................... 13

– Notochaetae smooth........................................................................................................................ 26

13. Lateral lobes absent............................................................................................... 14 (Amphitritides)

– Lateral lobes present....................................................................................................................... 15

14. Notochaetae on 17–20 segments; 8 segments with nephridial and genital papillae............................................................................................................................. Amphitritides gracilis (Grube, 1860)

– Notochaetae on 24 segments; 11–13 segments with nephridial and genital papillae........................................................................................ Amphitritides kuehlmanni Arvanitidis & Koukouras, 1995

15. Two pairs of arborescent branchiae, on SG II–III................................................ 16 (Paramphitrite)

– Three pairs of unbranched branchiae, on SG II–IV....................................................17 (Amphitrite)

16. Branchiae separated by a wide dorsal gap, developed lateral lobes on SG II–IV, absence of nephridial papillae on SG IV........................................................................................................................................................... Paramphitrite dragovabeci Lavesque, Daffe, Londoño-Mesa & Hutchings, 2021

– Branchiae without dorsal gap, small lateral lobes on SG II–IV, presence of nephridial papillae on SG IV................................................................................ Paramphitrite birulai (Ssolowiew, 1899)

17. Notopodia present on 17 chaetigers................................................................................................ 18

– Notopodia present on more than 17 chaetigers............................................................................... 23

18. Branchiae with simple filaments..................................................................................................... 19

– Branchiae dichotomous.................................................................................................................. 21

19. Seven pairs of nephridial and genital papillae (SG III and SG VI–XI)........................................................................................................................................................ Amphitrite cirrata Müller, 1771

– Four pairs of nephridial and genital papillae (SG III and SG VI–VIII)......................................... 20

20. Branchiae arising from short stem or directly from body wall......................................................................................................................................... Amphitrite fauveli Jirkov, Ravara & Cunha, 2018

– Branchiae arising from large and stout stem............................... Amphitrite rzhavskyi Jirkov, 2020

21. Nine pairs of nephridial and genital papillae, on SG III–XI.......................................................................................................................................................... Amphitrite edwardsi (Quatrefages, 1866)

– Six pairs of nephridial and genital papillae, on SG III–VIII.......................................................... 22

22. Branchiae with few ramifications, neuropodia of first abdominal segment less than half size of neuropodia of last thoracic segment........................................... Amphitrite affinis Malmgren, 1866

– Branchiae with many ramifications, neuropodia of first abdominal segment about same size as neuropodia of last thoracic segment........................................... Amphitrite variabilis (Risso, 1826)

23. Notopodia present on 19 chaetigers................................ Amphitrite groenlandica Malmgren, 1866

– Notopodia present on more than 19 chaetigers............................................................................... 24

24. Notopodia present on 21 chaetigers, 9–10 pairs of nephridial and genital papillae.................................................................................................................................. Amphitrite grayi Malmgren, 1866

– Notopodia present on more than 21 chaetigers, more than 10 pairs of nephridial and genital papillae............................................................................................................................................ 25

25. Notopodia present on first 23–27 chaetigers, 16 pairs of nephridial and genital papillae, uncini in double rows on SGXI–XXV........................................................ Amphitrite figulus (Dalyell, 1853)

– Notopodia present on first 22–24 chaetigers, 13–15 pairs of nephridial and genital papillae, uncini in double rows almost to end of abdomen............................................ Amphitrite rubra (Risso, 1826)

26. Absence of lateral lobes.................................................................................................. 27 (Nicolea)

– Presence of lateral lobes................................................................................................................. 28

27. Notochaetae on 15 segments, branchiae with short stems........... Nicolea zostericola (Ørsted, 1844)

– Notochaetae on 17–18 segments, branchiae with long stems.... Nicolea venustula (Montagu, 1819)

28. Double rows of uncini in a back to back arrangement................................................................... 29

– Double rows of uncini in a face-to-face or intercalated arrangement............................................. 32

29. Uncini pectinate, with teeth in a single vertical row....................................................... 30 (Loimia)

– Uncini avicular, with several transverse rows of secondary teeth....................................31 (Lanice)

30. Eyespots present, pygidium without distinct papillae, thoracic uncini with 4–5 rows of secondary teeth.................................................................................................. Loimia medusa (Savigny, 1822)

– Eyespots absent, pygidium with 14 distinct papillae, thoracic uncini with 6 rows of secondary teeth............................. Loimia ramzega Lavesque, Bonifácio, Londoño-Mesa, Le Garrec & Grall, 2017

31. Ventral shields fused on SGII–IV, notopodia short, neuropodia as low ridges, upper lip dorsally pigmented...................................................................................... Lanice conchilega (Pallas, 1766)

– Ventral shields well defined on SGIII–IV, notopodia well developed, neuropodia prominent, upper lip without pigmentation............................................................................................................................................................... Lanice kellyslateri Lavesque, Daffe, Londoño-Mesa & Hutchings, 2021

32. Notopodia on 15–16 segments, a single pair of short dichotomously branchiae..........33 (Axionice)

– Notopodia on 17 segments.............................................................................................................. 34

33. Notopodia on 15 segments............................................................. Axionice flexuosa (Grube, 1860)

– Notopodia on 16 segments.......................................................... Axionice maculata (Dalyell, 1853)

34. Short-handled avicular uncini throughout...................................................................................... 35

– Long-handled avicular uncini, at least on anterior neuropodia (i.e., SGV–VII).................40 (Pista)

35. A single pair of plumose branchiae.................................................................................36 (Pistella)

– Three pairs of branching branchiae......................................................................... 37 (Eupolymnia)

36. Branchial filaments arranged in distinct tiers, ventral shields on SG II–XV, dorsal crest on SG III..................................................................................... Pistella rovignensis Mikac & Hutchings, 2017

– Branchial filaments arranged in spiral, ventral shields on SG VI–XX, dorsal crests on SG II–IV........................................................................................................... Pistella lornensis (Pearson, 1969)

37. Branchiae with long stems.............................................................................................................. 38

– Branchial stems short or absent...................................................................................................... 39

38. Abdominal neuropodia dorsally pointed, lateral lobes translucent.................................................................................................. Eupolymnia gili Lavesque, Daffe, Londoño-Mesa & Hutchings, 2021

– Abdominal neuropodia rounded, lateral lobes not translucent................................................................................................... Eupolymnia lacazei Lavesque, Daffe, Londoño-Mesa & Hutchings, 2021

39. First pair of branchiae without stem, lateral lobes on SG III bilobed, lateral lobes of SG II small................................................................................................ Eupolymnia nebulosa (Montagu, 1819)

– First pair of branchiae with short stem, lateral lobes on SG III spherical, lateral lobes of SG II welldeveloped............... Eupolymnia meissnerae Lavesque, Daffe, Londoño-Mesa & Hutchings, 2021

40. A single branchia inserted mid-dorsally on SG II............................................................................................................................ Pista labruneae Lavesque, Daffe, Londoño-Mesa & Hutchings, 2021

– All branchiae paired........................................................................................................................ 41

41. One or two pairs of branchiae......................................................................................................... 42

– Three pairs of branchiae....................................................................... Pista cretacea (Grube, 1860)

42. One pair of branchiae...................................................................................................................... 43

– Two pairs of branchiae.................................................................................................................... 46

43. Absence of lateral lobes on SG II................................................... Pista mirabilis McIntosh, 1885 *

– Presence of lateral lobes on SG II................................................................................................... 44

44. Lateral lobes present on SG I–III, small on SG I and III............................................................................................................................................................................. Pista bansei Saphronova, 1988 *

– Lateral lobes present on SG II–III, well developed on SG III........................................................ 45

45. Lateral lobes well developed on SG II, asymmetrical on SG III.................................................................................................................. Pista colini Labrune, Lavesque, Bonifácio & Hutchings, 2019

– Lateral lobes narrow on SG II, rectangular on SG III................................................................................................................................................................... Pista adriatica Mikac & Hutchings, 2017

46. Uncini of SG V very high, with a vertical prow........................ Pista mediterranea Gaillande, 1970

– Uncini of SG V with regular size.................................................................................................... 47

47. Absence of long-handled uncini on SG X (CH 5)........................................................................... 48

– Presence of long-handled uncini on SG X...................................................................................... 49

48. Lateral lobes on SGI short, on SGIV long............................................. Pista cristata (Müller, 1776)

– Lateral lobes on SGI large, on SGIV very small................................................................................................................................. Pista sauriaui Lavesque, Daffe, Londoño-Mesa & Hutchings, 2021

49. Lateral lobes on SG I small, on SG IV well developed, eyespots absent......................................................................................................................................................... Pista wui Saphronova, 1988 *

– Lateral lobes on SG I absent, on SG IV small, almost inconspicuous, eyespots present.................................................................... Pista miosseci Lavesque, Daffe, Londoño-Mesa & Hutchings, 2021

* doubtful record, probably a misidentification.