Research Article |
Corresponding author: María Barroso ( maria.p.barroso@udc.es ) Academic editor: Greg Rouse
© 2022 María Barroso, Juan Moreira, María Capa, Arne Nygren, Julio Parapar.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Barroso M, Moreira J, Capa M, Nygren A, Parapar J (2022) A further step towards the characterisation of Terebellides (Annelida, Trichobranchidae) diversity in the Northeast Atlantic, with the description of a new species. ZooKeys 1132: 85-126. https://doi.org/10.3897/zookeys.1132.91244
|
Several new species of genus Terebellides Sars, 1835 (Annelida, Trichobranchidae) have been recently described from the Northeast Atlantic Ocean after the detection of a large complex of species based on DNA sequence data from previous research. Some of those species (belonging to the so-called Group A) have already been described elsewhere. In this paper, we revise several Terebellides clades belonging to Groups B, C and D resulting in the identification of five nominal species: Terebellides gracilis Malm, 1874, Terebellides atlantis Williams, 1984, Terebellides williamsae Jirkov, 1989, Terebellides irinae Gagaev, 2009, and Terebellides shetlandica Parapar, Moreira & O’Reilly, 2016, plus one new species described here as Terebellides lavesquei sp. nov. All these species are characterised by a combination of morphological features complemented with a nucleotide diagnostic approach (specific COI nucleotides in the alignment position). Morphological characters used to discriminate between taxa refer to the branchial shape, presence/absence of ciliated papillae dorsal to thoracic notopodia and the morphology of thoracic and abdominal uncinal teeth. An updated identification key to all described species of this genus in NE Atlantic waters is also included.
DNA barcoding, DNA species delineation, identification key, integrative taxonomy, Northeast Atlantic, polychaetes, SEM, systematics
The genus Terebellides Sars, 1835 (Annelida) is distinguishable from other members of Trichobranchidae by the unique mid-dorsal stalk bearing the characteristic branchial lobes, provided with packed branchial lamellae. This taxon is morphologically homogenous and boundaries between species are difficult to assess because relevant characters rely on some microscopic details. These include features of branchiae, chaetae and uncini that need examination with Scanning Electron Microscopy (
A recent comprehensive molecular survey and a set of analytical methods (
The aim of the present study is the morphological and molecular characterisation of members of Groups B, C, and D after
This paper is based on the study of 215 Terebellides specimens belonging to Groups B, C, and D as defined in
Comparison of discriminating taxonomic characters of the species studied in this work. Cells in italics show discriminatory characters of each subgroup. (1) sensu
Groups | B | C | D | ||||
---|---|---|---|---|---|---|---|
Putative species sensu |
1 | 5 | 16 | 24 | 2 | 3 | |
Species (as reported/described herein) | T. shetlandica Parapar, Moreira & O’Reilly, 2016 | T. lavesquei sp. nov. | T. atlantis Williams, 1984 | T. irinae Gagaev, 2009 | T. williamsae Jirkov, 1989 | T. gracilis Malm, 1874 | |
Branchiae | type (1) | 3 | 2 | 3 | 4 | 2 | 2 |
papillae on lamellae edge | no | no | no | no | no | no | |
Thorax | ciliated papilla dorsal to notopodium | no (?) | no (?) | no (?) | no (?) | yes | yes |
chaetiger with geniculate chaetae | TC 6 | TC 6 | TC 6 | TC 6 | TC 6 | TC 6 | |
uncini type (2) | 4 | 3 | 3 | 3 | 1 | 1 | |
Abdomen | uncini type (3) | 2 | 2 | 2 | 2 | 1A | 1A |
Bathymetry – Above (A) / Below (B) 200 m depth (4) | A/B | A/B | B | B | B | B | |
Distribution – North (N) /South (S) of 60°N (4) | N/S(5) | N/S | N | N | N/S(5) | N/S(5) |
These specimens are part of a large collection of Terebellides specimens (table S1 in
Light microscope photographs were done using an Olympus SZX12 stereomicroscope equipped with an Olympus C-5050 digital camera. Line drawings were made with a Wacom CTL-4100K-S pen tablet based on photographs and observations made with an Olympus BX40 stereomicroscope. Specimens for Scanning Electron Microscopy (SEM) were prepared by critical point drying, covered with gold and examined and photographed under a JEOL JSM-6400 electron microscope at the Servizos de Apoio á Investigación (SAI, Universidade da Coruña, Spain).
For staining procedures, 10 mg of Methyl Green (MG) colourant were dissolved in 5 ml of 20% ethanol and specimens were held in there for 30 s. MG staining patterns and thoracic uncini morphology were characterised based on the classifications proposed by
For each species, the list of the museum registration numbers and collection details (geographic area, locality, coordinates, depth, collecting date and habitat) is provided in Suppl. material
The correspondence between species numerals (
The present study deals with the main Terebellides groups B, C, and D, proposed by
The most distinctive taxonomic morphological characters for Terebellides include morphology of branchiae (sensu
abl anterior branchial lobe (lobe #5);
bdl branchial dorsal lobes;
bdltp branchial dorsal lobe terminal papilla;
bf branchial filament;
bvl branchial ventral lobes;
cap capitium;
cop copepod;
cr ciliary row;
ct ciliary tuft;
dpn dorsal projection of notopodium;
gc geniculate chaetae;
MG Methyl Green;
NEA Northeast Atlantic;
nc notochaetae;
ooc oocytes;
RvC rostrum vs. capitium length ratio;
SEM Scanning Electron Microscope;
SG segment;
STM stereomicroscope;
TC thoracic chaetiger;
tdp thoracic dorsal papilla;
tll thoracic lateral lappets;
tm tentacular membrane;
TU thoracic unciniger;
wTC white thoracic chaetiger.
Five lineages of the Terebellides Groups B, C, and D (sensu
Following
Terebellides stroemii Sars, 1835, redescribed by
The morphological features shared by all examined species in Group B in this paper (clades 1, 5, and 16) are itemised below. Some of these are also shared by Groups A, C, and D as defined in
Body appearance. Complete individuals ranging from 5.0–35.0 mm in length. Body tapering posteriorly with segments increasingly shorter and crowded towards pygidium. Prostomium compact; large tentacular membrane surrounding mouth (Figs
STM photographs of live specimens of several Terebellides species (non-type specimens) A, B Terebellides shetlandica Parapar, Moreira & O’Reilly, 2016 (species 1; A ZMBN116171 B ZMBN116181) C Terebellides lavesquei sp. nov. (species 5; GNM15112) D, E Terebellides williamsae Jirkov, 1989 (species 2; D GNM15108 E GNM15109) F Terebellides gracilis Malm, 1874 (species 3; GNM15111). Abbreviations: bdl – branchial dorsal lobe; bf – branchial filament; bvl – branchial ventral lobe; ooc – oocytes; wTC – white thoracic chaetiger.
STM photographs of several Terebellides species (A, C–F non-type specimens) A Terebellides shetlandica Parapar, Moreira & O’Reilly, 2016 (species 1; ZMBN116186) B Terebellides lavesquei sp. nov. (species 5; holotype, ZMBN116322) C Terebellides atlantis Williams, 1984 (species 16; ZMBN116472) D Terebellides irinae Gagaev, 2009 (species 24; ZMBN116498) E Terebellides williamsae Jirkov, 1989 (species 2; ZMBN116269) F Terebellides gracilis Malm, 1874 (species 3; ZMBN116283). Abbreviations: bdl – branchial dorsal lobe; bf – branchial filament; bvl – branchial ventral lobe; ooc – oocytes; wTC – white thoracic chaetiger.
Branchiae. Branchiae arising as single structure from SG 3, with a single stalked mid-dorsal stem (Figs
Thorax. Eighteen pairs of notopodia (SG 3–20), those of TC 1 ca. as long as subsequent ones or slightly shorter (Figs
Line drawings of several Terebellides species (A, C, D non-type specimens) A Terebellides shetlandica Parapar, Moreira & O’Reilly, 2016 (species 1; ZMBN116186), anterior end, right lateral view B Terebellides lavesquei sp. nov. (holotype; ZMBN116322), anterior end, left lateral view C Terebellides irinae Gagaev, 2009 (species 24; ZMBN116498), anterior end, ventral view D Terebellides gracilis Malm, 1874 (species 3; ZMBN116283), anterior end, right lateral view. Abbreviations: bdl – branchial dorsal lobe; bf – branchial filament; bvl – branchial ventral lobe; tm – tentacular membrane.
Terebellides shetlandica Parapar, Moreira & O’Reilly, 2016 (species 1; non-type specimens, ZMBN116181, ZMBN116204 and ZMBN116219), SEM micrographs A anterior end, dorsal view B anterior end, left lateral view C TC 6 (TU1), geniculate chaeta D thoracic uncinus E abdominal neuropodium F abdominal uncini. Abbreviations: bdl – branchial dorsal lobe; bf – branchial filament; bvl – branchial ventral lobe; cap – capitium; cop – copepod; dpn – dorsal projection of notopodium; TC – thoracic chaetiger; tll – thoracic lateral lobes; tm – tentacular membrane; TU – thoracic unciniger.
Terebellides lavesquei sp. nov. (non-type specimen, ZMBN116332), SEM micrographs A anterior end, left lateral view B branchial lamellae, detail C ciliary row, detail D copepod E copepod, anterior end. Abbreviations: bdl – branchial dorsal lobe; bf – branchial filament; cop – copepod; cr – ciliary row.
Terebellides atlantis Williams, 1984 (species 16; non-type specimens, ZMBN116454 and ZMBN116459), SEM micrographs A anterior end, left lateral view B branchiae, detail C TC 6 (TU1), geniculate chaetae D thoracic uncini E abdominal neuropodium F abdominal uncini. Abbreviations: bf – branchial filament; bvl – branchial ventral lobe; cap – capitium; dpn – dorsal projection of notopodium; TC – thoracic chaetiger; TU – thoracic unciniger.
Abdomen and pygidium. Approximately half as long as thorax and progressively thinner (Fig.
Colour pattern. Colour in preserved specimens whitish or pale brown (Fig.
Among the aforementioned characters, branchial features might serve to distinguish most of Group B species from those of Groups A, C, and D. Those include size of branchial lobes, lobes not fused, presence of long filaments on ventral ones, and presence of ciliary rows on branchial lamellae. Other taxa described or reported worldwide bear the same type of branchiae (type 3), including Terebellides ehlersi McIntosh, 1885, T. intoshi Caullery, 1915, T. lobatus Hartman & Fauchald, 1971, T. mundora Hutchings & Peart, 2000 and T. sepultura Garraffoni & Lana, 2003 (
Terebellides shetlandica Parapar, Moreira & O’Reilly, 2016a: 211–225, figs 1–9, 11.
Species 1 –
30 specimens (Suppl. material
MG024894, MG024895, MG024896, MG024897, MG024898, MG024899, MG024900, MG024901, MG024902, MG024903, MG024904, MG024905, MG024906, MG024907, MG024908, MG024909, MG024910, MG024911, MG024912, MG024913, MG024914, MG024915, MG024916, MG024917, MG024918, MG024919, MG024920, MG024921, MG024922, MG024923, MG024924, MG024925, MG024926, MG024927, MG024928, MG024929, MG024930, MG024931, MG024932, MG024933, MG024934, MG024935, MG024936, MG024937, MG024938, MG024939, MG024940, MG024941, MG024942, MG024943, MG024944, MG024945, MG024946, MG024947, MG024948, MG024949, MG024950, MG024951, MG024952, MG024953, MG024954, MG024955, MG024956.
Complete individuals ranging from 5.0–16.0 mm in length (Fig.
MG staining pattern characterised by compact green colourant in SG 1–6, then turning into striped pattern in SG 7–14 and fading in following segments (Fig.
All sequences of Terebellides shetlandica share and are distinguished from other available Terebellides sequences in unique combinations of nucleotides (underlined) at the given position of our alignment: 78–98: CCAACCCGGAGCCTATTTAGGT, 186–192: CGGAAAC, 210–219: GCTAGGCGCC, 228–234: GGCATTC, 264–276: TCTCCCGCCTGCC, 288– 292: CGTT, 306: C, 333–342: CGTCTACCCT, 351–369: AGACAATATGGCACACGCC, 381–402: AGATCTGGCTATTTTCTCCCTA, 453–459: AGTAATA, 511–522: TCAGCTATAATC, 535–558: TTACTTCTTTCTCTGCCAGTTCTG.
NW Hutton Oilfield, between Shetland Islands and Norway, 61°10'N, 01°12'E (
Norwegian coast and shelf, North Sea, Skagerrak, Kattegat; 25–375 m deep; 92.7% of specimens present at depths below 200 m (Figs
Geographic distribution of species of Terebellides in Northeast Atlantic Ocean A Terebellides shetlandica Parapar, Moreira & O’Reilly, 2016 B Terebellides lavesquei sp. nov. C Terebellides atlantis Williams, 1984 D Terebellides irinae Gagaev, 2009 E Terebellides williamsae Jirkov, 1989 F Terebellides gracilis Malm, 1874. Pink star denotes the type locality of each taxon.
Body MG staining patterns in ventral view of Terebellides species. Terebellides shetlandica Parapar, Moreira & O’Reilly, 2016, Terebellides lavesquei sp. nov., Terebellides atlantis Williams, 1984, Terebellides irinae Gagaev, 2009, Terebellides williamsae Jirkov, 1989 and Terebellides gracilis Malm, 1874. Segments indicated in Arabic numbers.
Terebellides shetlandica is a small species, reaching up to 16 mm length and is characterised by having branchiae of type 3 and long filaments in ventral branchial lobes, thoracic uncini of type 4, abdominal uncini of type 2 and lacking papillae on margins of branchial lamellae (Table
Species 5 –
Type material. Holotype: ZMBN116322. Paratypes (16 specimens): Skagerrak (GNM15112); Norwegian coast (NTNU–VM61386, NTNU–VM61387, NTNU–VM68252, ZMBN116319, ZMBN116320, ZMBN116321, ZMBN116323, ZMBN116324, ZMBN116325, ZMBN116326, ZMBN116327, ZMBN116328, ZMBN116329, ZMBN116330, ZMBN116331, ZMBN116332).
Complete specimen, 34.0 mm long and 2.0 mm wide (Fig.
Complete individuals ranging from 5.0–35.0 mm in length (Fig.
MG staining pattern characterised by compact green colourant in SG 1–6, J-shaped glandular region in SG 3–5 and striped pattern in SG 7–14 (Fig.
All sequences of Terebellides lavesquei sp. nov. share and are distinguished from other available Terebellides sequences in unique combinations of nucleotides (underlined) at the given position of our alignment: 78–99: TCAACCCGGTGCTTACCTCGGT, 156–174: TTTAGTTATGCCAGTCTTC, 261–264: GTTA, 270–279: TCCAGCACTT, 315–336: AGTTGGGACCGGTTGAACCGTT, 351–369: AGACAATATAGCTCATGCG, 405–411: CTTGGCT, 426–447: CCTAGGATCAATTAACTTTATC, 459–483: CAACATACGCTGAAAAGGTTTACGA, 510–525: GTCCGCGGTTATCACA, 534–558: ACTTCTTTTATCCCTTCCAGTCTTG, 573–580: CATGCTTC, 606–627: CTTTTTCGACCCAGCTGGTGGG.
Hordaland, Lysefjord (Norway), 60°07'N, 05°04'E; 119 m deep.
Norwegian coast and shelf, Skagerrak; 115–534 m deep; ~ 50% of specimens collected at depths above 200 m (Figs
This species is dedicated to Nicolas Lavesque, Station Marine d’Arcachon, CNRS (France) for his remarkable recent contributions to the diversity of Terebellidae and Trichobranchidae in Atlantic waters.
Terebellides lavesquei sp. nov. is a medium-sized species, reaching up to 35 mm in length. It is characterised by the lack of papillae on margins of branchial lamellae and by having branchiae of type 2, filaments on ventral branchial lobes, thoracic uncini of type 3 and abdominal uncini of type 2 (Table
Branchial shape of T. lavesquei sp. nov. is similar to that of Terebellides narribri Hutchings & Peart, 2000, because both lobes are fused to each other for ca. half their length and have a high number of tightly packed lamellae. However, T. narribri have thoracic uncini of type 1 whereas T. lavesquei sp. nov. have thoracic uncini of type 3. Furthermore, T. lavesquei sp. nov. and T. shetlandica seem to have a more restricted bathymetric distribution in shallow waters (down to 534 and 375 m, respectively) whereas T. atlantis reaches depths of 2750 m (see below).
Terebellides atlantis Williams, 1984: 121–123, fig. 4, table 1.
Species 16 –
15 specimens (Suppl. material
MG025258, MG025259, MG025260, MG025261, MG025262, MG025263, MG025264, MG025265, MG025266, MG025267, MG025268, MG025269, MG025270, MG025271, MG025272, MG025273, MG025274, MG025275, MG025276, MG025277, MG025278, MG025279, MG025280, MG025281, MG025282, MG025283, MG025284, MG025285, MG025286, MG025287, MG025288, MG025289, MG025290, MG025291, MG025292, MG025293, MG025294, MG025295, MG025296, MG025297, MG025298, MG025299, MG025300, MG025301, MG025302, MG025303, MG025304, MG025305, MG025306, MG025307, MG025308, MG025309, MG025310, MG025311, MG025312.
Complete individuals ranging from 10.0–16.0 mm in length (Fig.
MG staining pattern characterised by compact green colourant in SG 1–6, J-shaped glandular region in SG 3–5 and striped pattern in SG 7–14 (Fig.
All sequences of Terebellides atlantis share and are distinguished from other available Terebellides sequences in unique combinations of nucleotides (underlined) at the given position of our alignment: 60–84: TATTCGTATTGAGCTAGGGCAACCT, 132–150: ACATGCATTTTTAATAATC, 171–189: TTTTATTGGTGGATTTGGT, 213–231: GGGAGCTCCTGATATAGCC, 264–294: ACTACCACCAGCCTTAATCTTATTAGTAAGC, 345–363: ATTATCTGATAATATGGCT, 384–399: CCTTGCTATTTTTTCA, 477–484: GCTACGAC, 549–573: TCCAGTCTTAGCTGGTGCAATCACT, 558–591: CCGT, 615–630: TCCAGCTGGTGGTGGT.
Atlantic Ocean, off New England, 39°56.5'N, 70°39.9'W (
Barents Sea, Greenland Sea, South Iceland, Norwegian coast and shelf; 219–2750 m deep (Figs
Terebellides atlantis is a small species, reaching up to 16 mm in length. It is characterised by the lack of papillae on margins of branchial lamellae, and by having branchiae of type 3 and filaments in ventral branchial lobes, thoracic uncini of type 3 and abdominal uncini of type 2 (Table
The morphological features of the examined species in Group C in this paper (clade 24) are itemised below. Some of these are also shared by Groups A, B, and D as defined in
Body appearance. Incomplete individuals ranging from 10.0–17.0 mm in length. Body tapering posteriorly with segments increasingly shorter and crowded towards pygidium. Prostomium compact; large tentacular membrane surrounding mouth (Fig.
Branchiae. Branchiae arising as single structure from SG 3, with a single stalked mid-dorsal stem, lobes not fused (Fig.
Thorax. Eighteen pairs of notopodia (SG 3–20) (Fig.
Terebellides irinae Gagaev, 2009 (species 24; non-type specimen, ZMBN116501), SEM micrographs. A anterior end, ventral view B TC 6 (TU1), geniculate chaetae C row of thoracic uncini D thoracic uncini E abdominal uncini F abdominal uncinus, detail. Abbreviations: tc – thoracic chaetiger; tm – tentacular membrane; tu – thoracic unciniger.
Abdomen and pygidium. Approximately half as long as thorax and progressively thinner (Fig.
Colour pattern. Colour in preserved specimens whitish (Fig.
Among the above-mentioned characters, branchial features might serve to distinguish most of Group C species from those of Groups A, B and D. Those include branchial lobes size, presence of filaments in ventral ones and lobes which are not fused. Other taxa such as Terebellides mira Schüller & Hutchings, 2013 and T. rigel Schüller & Hutchings, 2013 also bear branchiae with similar shape (
Terebellides irinae Gagaev, 2009: 474–478.
Species 24 –
6 specimens (Suppl. material
Incomplete individuals ranging from 10.0–17.0 mm in length (Fig.
MG staining pattern characterised by compact green colourant in SG 1–4, then turning into striped pattern in SG 5–14 and fading in following segments (Fig.
All sequences of Terebellides irinae share and are distinguished from other available Terebellides sequences in unique combinations of nucleotides (underlined) at the given position of our alignment: 177–204: CGGGGGGTTTGGAAACTGGTTAATCCCC, 213–225: TGGGGCCCCAGAC, 249–258: CATAAGGTTC, 273–303: GGCCCTCATCCTACTAGTCAGCTCAGCTGCT, 305–321: GGCTGGT, 327–336: ATGAACTGTA, 342–372: ACCACTTTCAGACAACATCGCTCATGCCGGA, 381–399: AGATCTAGCAATTTTCTCA, 426: CCTAGGTTCTATTAACTTCATCACAACAGTC, 483–499: TCTAGAACGAATCCCAC, 535–573: TTATTACTATCACTACCAGTGCTAGCCGGAGCTATTACC, 594–612: CATTAACACATCATTCTTC, 618–636: AGCCGGTGGTGGTGATCCT.
Arctic Ocean, 73°04'N, 157°12'W (
Arctic Ocean; 4038–4380 m deep (Figs
Terebellides irinae is a small species, reaching up to 17 mm in length and is characterised by the lack of papillae on margins of branchial lamellae, and by having branchiae of type 4, filaments in ventral branchial lobes, thoracic uncini of type 3 and abdominal uncini of type 2 (Table
The morphological features shared by all examined species in Group D in this paper (clades 2 and 3) are itemized below. Some of these are also shared by Groups A, B, and C as defined in
Body appearance. Complete individuals ranging from 5.0–34.0 mm in length. Body tapering posteriorly with segments increasingly shorter and crowded towards pygidium. Prostomium compact; large tentacular membrane surrounding mouth (Figs
Branchiae. Branchiae arising as single structure from SG 3, with a single stalked mid-dorsal stem (Figs
Terebellides williamsae Jirkov, 1989 (species 2; non-type specimens, ZMBN116249 and ZMBN116251), SEM micrographs A anterior end, left lateral view B branchial lamellae, detail C ciliary tufts, detail D TC and thoracic dorsal papilla E thoracic dorsal papilla, detail. Abbreviations: abl – anterior branchial lobe; bdl – branchial dorsal lobe; bvl – branchial ventral lobe; ct – ciliary tuft; dpn – dorsal projection of notopodium; TC – thoracic chaetiger; tdp – thoracic dorsal papilla; tm – tentacular membrane.
Thorax. Eighteen pairs of notopodia (SG 3–20) (Fig.
Terebellides williamsae Jirkov, 1989 (species 2; non-type specimen, ZMBN116249), SEM micrographs A TC 5–7, lateral view B TC 6 (TU1), geniculate chaetae C row of thoracic uncini D thoracic uncinus E abdominal neuropodium F abdominal uncini. Abbreviations: cap – capitium; gc – geniculate chaetae; nc – notochaetae; TC – thoracic chaetiger; TU – thoracic unciniger.
Terebellides gracilis Malm, 1874 (species 3; non-type specimens, GNM15110 and ZMBN116313), SEM micrographs A branchiae, dorsal view B branchial lamellae, detail C ciliary tufts, detail D anterior end, right lateral view E branchiae, lateral view. Abbreviations: abl – anterior branchial lobe; bdl – branchial dorsal lobe; bdltp – branchial dorsal lobe terminal papilla; bf – filament; bvl – branchial ventral lobe; cr – ciliary row; ct – ciliary tuft; tll – thoracic lateral lobes; tm – tentacular membrane.
Terebellides gracilis Malm, 1874 (species 3; non-type specimen, ZMBN116282), SEM micrographs A anterior end, left lateral view B ciliary tufts and ciliary row, detail C dorsal projection of notopodium D pores of dorsal projection of notopodium, detail. Abbreviations: abl – anterior branchial lobe; bdl – branchial dorsal lobe; bvl – branchial ventral lobe; cr – ciliary row; ct – ciliary tuft; dpn – dorsal projection of notopodium; tdp – thoracic dorsal papilla.
Terebellides gracilis Malm, 1874 (species 3; non-type specimens, ZMBN116282 and ZMBN116313), SEM micrographs A TC 6 (TU1), geniculate chaetae B capitium of geniculate chaeta, detail C thoracic uncini D thoracic uncinus E abdominal neuropodium F abdominal uncini. Abbreviations: cap – capitium; TC – thoracic chaetiger; TU – thoracic unciniger.
Abdomen and pygidium. Approximately half as long as thorax and progressively thinner (Fig.
Colour pattern. Colour in preserved specimens whitish or pale brown (Fig.
Among the aforementioned characters, the white ventral colouration in anterior thoracic chaetigers may be a useful character to distinguish Group D species from those of Groups A–C. Other taxa described or reported worldwide showing this colouration pattern are Terebellides distincta Williams, 1984 and T. ceneresi Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019.
Terebellides williamsae Jirkov, 1989: 124.
Species 2 –
20 specimens (Suppl. material
MG024957, MG024958, MG024959, MG024960, MG024961, MG024962, MG024963, MG024964, MG024965, MG024966, MG024967, MG024968, MG024969, MG024970, MG024971, MG024972, MG024973, MG024974, MG024975, MG024976, MG024977, MG024978, MG024979, MG024980, MG024981, MG024982, MG024983, MG024984, MG024985, MG024986, MG024987, MG024988.
Complete individuals ranging from 9.0–34.0 mm in length (Fig.
MG staining pattern characterised by compact green colourant in SG 1–5 and SG 7–13, SG 6 white and SG 14 striped, J-shaped glandular regions in SG 3–5 (Fig.
All sequences of Terebellides williamsae share and are distinguished from other available Terebellides sequences in unique combinations of nucleotides (underlined) at the given position of our alignment: 59–62: TATC, 75–96: TGGACAACCTGGGGCATTCCTG, 132–144: TCATGCTTTTTTA, 153–157: TTTCC, 216–234: TGCTCCTGATATAGCTTTC, 264–277: CCTCCCTCCAGCTT, 315–318: GGTT, 327–342: CTGAACAGTATACCCC, 381–399: AGATTTGGCTATTTTTTCT, 414–432: TATCTCCTCTATTCTTGGC, 450–454: TACA, 515–529: AAAAATCACTACCA, 543–573: TTCACTTCCTGTATTAGCAGGAGCTATTACA, 600–609: CACTTCCTTT, 630–640: CGACCCAATTT.
Barents Sea, Norway, 74°30'N, 28°00'E (
Barents Sea, Greenland Sea, Norwegian coast and shelf, Skagerrak; at depths of 178–612 m but most of the specimens (97%) were collected above 200 m (Figs
Terebellides williamsae is a medium-sized species, reaching up to 34 mm in length; it is characterised by the lack of papillae on margins of branchial lamellae and by having branchiae of type 2 and posterior filaments in ventral branchial lobes, thoracic uncini of type 1 and abdominal uncini of type 1A (Table
Terebellides gracilis Malm, 1874: 67–105, p. 100.
Species 3 –
20 specimens (Suppl. material
MG024583, MG024584, MG024585, MG024586, MG024587, MG024588, MG024589, MG024590, MG024591, MG024592, MG024593, MG024594, MG024595, MG024596, MG024597, MG024598, MG024599, MG024600, MG024601, MG024602, MG024603, MG024604, MG024605, MG024606, MG024607, MG024608, MG024609, MG024610, MG024611, MG024612, MG024613, MG024614, MG024615, MG024616, MG024617, MG024618, MG024619, MG024620, MG024621, MG024622, MG024623, MG024624, MG024625, MG024626, MG024627, MG024628, MG024629, MG024630, MG024631, MG024632, MG024633, MG024634, MG024635, MG024636, MG024637.
Complete individuals ranging from 5.0–29.0 mm in length (Fig.
MG staining characterised by compact green colourant in SG 1–5 and SG 7–13, SG 6 white and SG 14 striped (Fig.
All sequences of Terebellides gracilis share and are distinguished from other available Terebellides sequences in unique combinations of nucleotides (underlined) at the given position of our alignment: 39–63: TGGTACTTCAATAAGACTTCTTATC, 84–96: TGGGGCATTCCTG, 111–132: TTATAACACAATTGTTACTGCT, 138–157: TTTTTTAATAATTTTTTTCC, 216–234: TGCTCCTGATATAGCTTTC, 264–277: CCTCCCTCCAGCTT, 315–327: AGCTGGGACAGGT, 333–351: AGTCTACCCTCCTTTATCT, 381–399: AGATTTGGCTATTTTTTCT, 414–432: TATCTCCTCTATTCTTGGC¸ 450–545: TACA, 516–529: AAAAATCACTACCA, 543–552: TTCACTTCCT, 600–609: CACTTCCTTT, 630–640: CGACCCAATTT.
Atlantic Ocean, Norway (
South Iceland, Norwegian coast and shelf, Skagerrak; 237–1268 m deep (Figs
Terebellides gracilis is a medium-sized species, reaching up to 29 mm in length and is characterised by the lack of papillae on margins of branchial lamellae, having branchiae of type 2 and filaments in ventral branchial lobes, presence of thoracic uncini of type 1 and abdominal uncini of type 1A (Table
The following key of European species of Terebellides is based on those by
The characters considered were the ventral pigmentation of anterior thoracic chaetigers in live and fixed specimens, types of thoracic uncini (sensu
1 | White ventral colouration on anterior thoracic chaetigers | 2 |
– | No distinct ventral colouration on anterior thoracic chaetigers | 4 |
2 | Medium/large species (>20 mm in length); 5th branchial lobe present; notochaetae of TC 1 similar to subsequent ones; main fang of thoracic uncini straight; thoracic uncini with capitium composed of 2–3 large teeth and subsequent ones much smaller | 3 |
– | Small species (< 20 mm in length); 5th branchial lobe absent; notochaetae of TC 1 absent or shorter than subsequent ones; thoracic uncini with capitium composed of 4 or 5 mid-sized teeth and following of slightly smaller teeth | T. ceneresi Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019 |
3 | White ventral colouration on TC 1 to TC 4 | T. williamsae Jirkov, 1989 |
– | White ventral colouration only on TC 4 | T. gracilis Malm, 1874 |
4 | Branchial lobes all small and not fused; reduced dorsal lobes | T. irinae Gagaev, 2009 |
– | Branchiae otherwise | 5 |
5 | Lower branchial lobes with posterior projections as filaments; branchiae with lobes fused ~ 50% of their length or with lobes only fused at base; small/medium species (<40 mm in length) | 6 |
– | Lower branchial lobes with posterior projections; branchiae with large lobes almost completely fused; large species (> 40 mm in length) | 9 |
6 | Thoracic uncini with capitium composed of 5–7 small teeth, remaining ones similar in size at least in two rows | T. shetlandica Parapar, Moreira & O’Reilly, 2016 |
– | Thoracic uncini with capitium composed of 4–5 mid-sized teeth and followed by slightly smaller teeth | 7 |
7 | Branchiae with lobes fused ~ 50% of their length; medium-sized species (> 20 mm in length) | T. lavesquei sp. nov. |
– | Branchiae with lobes only fused at base; small species (< 20 mm in length) | 8 |
8 | Glandular region in TC 3 present; notochaetae from TC 1 longer than subsequent ones | T. parapari Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019 |
– | Glandular region in TC 3 not observed; all notochaetae of similar size | T. atlantis Williams, 1984 |
9 | Geniculate chaetae in TC 5 and TC 6; abdominal uncini with RvC = 1/0.7, capitium with 4–5 teeth and remaining ones smaller | T. bigeniculatus Parapar, Moreira & Helgason, 2011 |
– | Geniculate chaetae in TC 6 only | 10 |
10 | Branchial lamellae margins lacking papillae | 11 |
– | Branchial lamellae margins with papillae | 13 |
11 | Branchiae with lobes fused ~ 50% of their length | T. gralli Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019 |
– | Branchiae with large lobes almost completely fused | 12 |
12 | Abdominal uncini with RvC = 1/0.7, capitium with 4–5 teeth and remaining ones smaller | T. stroemii Sars, 1835 |
– | Abdominal uncini with RvC = 1/0.9, capitium composed of 3–5 large teeth in first row and 1–2 in a second row | T. kongsrudi Parapar, Capa, Nygren & Moreira, 2020 and T. bakkeni Parapar, Capa, Nygren & Moreira, 2020 |
13 | Glandular region in TC 3 round or oval | 14 |
– | Glandular region in TC 3 otherwise | 15 |
14 | Glandular region in TC 3 remained white with MG; branchial lamellae with rounded papillae; TC 1–3 without conspicuous dorsal projection | T. lilasae Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019 |
– | Glandular region in TC 3 stained blue with MG; branchial lamellae with conical papillae; TC 1–3 with conspicuous dorsal projection | T. bonifi Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019 |
15 | Branchial ciliary tufts present | T. gentili Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019 |
– | Branchial ciliary tufts absent | 16 |
16 | Most branchial lamellae with marginal papillae; mouth with upper lip elongated | T. resomari Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019 |
– | Only anterior branchial lamellae with marginal papillae; upper lip not elongated | 17 |
17 | Thoracic uncini with capitium composed of 2–3 large teeth and subsequent ones much smaller | T. ronningae Parapar, Capa, Nygren & Moreira, 2020 |
– | Thoracic uncini with capitium composed of 4 or 5 mid-sized teeth and following slightly smaller ones | 18 |
18 | Deep-water species; usually at depths below 200 m | T. norvegica Parapar, Capa, Nygren & Moreira, 2020 |
– | Shallow-water species; mostly at depths above 100 m | T. europaea Lavesque, Hutchings, Daffe, Nygren & Londoño-Mesa, 2019 and T. scotica Parapar, Capa, Nygren & Moreira, 2020 |
According to
The apparently morphological homogeneity of members of Terebellides has hidden an unexpected species richness in the Northeast Atlantic. Species delimitation analyses of DNA sequence data have allowed to reveal some of the Terebellides species that otherwise would have gone unnoticed (
An integrative approach, that aims at considering different sources of evidence, has become a common and grounded method for general species delineation (
In the present study, following the aims and methods of the similar previous study by
Group B comprises eight species; one of them was identified herein as T. atlantis, matching the diagnostic characters and distribution of T. atlantis, originally described by
The range of distribution of all nominal species identified here is expanded.
On the other hand, T. ceneresi shares many morphological similarities with T. williamsae and T. gracilis and therefore was related to Group D by
Among the remaining clades that will be described elsewhere, clades 4, 14 and 26 do not correspond either to T. atlantis or T. shetlandica because of differences in the branchiae type (i.e., type 2: incompletely fused lobes) and the absence of posterior filaments in branchial ventral lobes; they also differ in geographic distribution, being the aforementioned clades restricted to some areas in NEA. Likewise, clade 25 does not fit within T. irinae due to being medium sized and by having branchiae of type 1 (=large lobes almost totally fused). Finally, clade 15 does not match either to T. williamsae or T. gracilis because of having a ventral colouration extending across more segments (TC 1–10 vs TC 1–4 or TC 4 in T. gracilis and T. williamsae respectively).
In this work, the following characters have been studied in all specimens: morphology of branchiae (sensu
Among the species studied here, branchiae of T. lavesquei sp. nov., T. williamsae, and T. gracilis correspond to type 2, T. shetlandica and T. atlantis to type 3, and T. irinae to type 4. Regarding thoracic uncini, T. williamsae and T. gracilis have type 1, T. lavesquei sp. nov., T. atlantis, and T. irinae have type 3 and T. shetlandica bears type 4. Finally, considering abdominal uncini, T. williamsae and T. gracilis have type 1A and T. shetlandica, T. lavesquei sp. nov., T. atlantis, and T. irinae have type 2.
The species key is an update to those by
A total of five nominal species has been identified as belonging to Terebellides Groups B, C, and D (according to
The five species identified herein have been characterised based on morphological and molecular characters. The most relevant morphological features discriminating between species are branchial shape, ventral pigmentation of anterior thoracic chaetigers in live and fixed specimens, and the morphology of thoracic and abdominal uncini. For the molecular recognition of the species described, short sequences of nucleotides among the COI alignment have been provided as diagnostic to ease the identification.
We would like to thank all people involved in the paper by
Abiotic data and more information of the material used
Data type: Abiotic data
Explanation note: The table shows the abiotic data and more information of the material used: Specimen voucher, Site, Geographic area, Locality, Latitude, Longitude, Depth, Collecting date, Habitat, Remarks and figures.
List of COI sequences considered in present study
Data type: Molecular data
Explanation note: List of COI sequences considered in present study (Group B, C and D), museum vouchers and GenBank accession numbers.