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To name but a few: descriptions of five new species of
Terebellides (Annelida, Trichobranchidae)
from the North East Atlantic
Julio Parapar1, María Capa2, Arne Nygren3, Juan Moreira4
1Departamento de Bioloxía, Universidade da Coruña, Spain 2Departament de Biologia, Universitat de les
Illes Balears, Spain 3Sjöfartmuseet Akvariet, Göteborg, Sweden and Institutionen för marina vetenskaper,
Göteborgs Universitet, Sweden 4 Departamento de Biología (Zoología) & Centro de Investigación en Biodi-
versidad y Cambio Global (CIBC-UAM), Facultad de Ciencias, Universidad Autónoma de Madrid, Spain
Corresponding author: Julio Parapar (julio.parapar@udc.es)
Academic editor: C. Glasby|Received 29 June 2020|Accepted 6 October 2020|Published 12 November 2020
http://zoobank.org/0F038B5B-120E-4583-8E85-4092C9798566
Citation: Parapar J, Capa M, Nygren A, Moreira J (2020) To name but a few: descriptions of ve new species of
Terebellides (Annelida, Trichobranchidae) from the North East Atlantic. ZooKeys 992: 1–58. https://doi.org/10.3897/
zookeys.992.55977
Abstract
e number of described species of the genus Terebellides Sars, 1835 (Annelida, Trichobranchidae) has greatly
increased in the last years, particularly in the North East Atlantic. In this context, this paper deals with several
putative species recently delineated by molecular means within a well delimited clade of Terebellides. Species
are characterised here by a combination of morphological characters, and a complementary nucleotide diag-
nostic approach. ree species were identied as the nominal species T. stroemii Sars, 1835, T. bigeniculatus
Parapar, Moreira & Helgason, 2011 and T. europaea Lavesque et al., 2019. Five species are described as new:
T. bakkeni sp. nov., T. kongsrudi sp. nov., T. norvegica sp. nov., T. ronningae sp. nov. and T. scotica sp. nov.
e distinctive morphological characters refer to the branchial shape, absence or presence of papillae on la-
mellae of anterior margin of branchial dorsal lobes, absence or presence of ciliated papillae dorsal to thoracic
notopodia, geniculate chaetae in one or two chaetigers, and the morphology of thoracic and abdominal
uncini teeth. Furthermore, the description of T. bigeniculatus is revised and complemented after examination
of type specimens. An updated identication key to all species of the genus in NE Atlantic and a proposal of
a classication of dierent types of abdominal uncini to be used in taxonomy are also included.
Keywords
DNA barcoding, DNA species delineation, identication key, integrative taxonomy, new species, North
East Atlantic, polychaetes, SEM, systematics
ZooKeys 992: 1–58 (2020)
doi: 10.3897/zookeys.992.55977
https://zookeys.pensoft.net
Copyright Julio Parapar et al. 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.
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Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
2
Introduction
e species richness in the genus Terebellides Sars, 1835 (Annelida, Trichobranchidae)
in the North East Atlantic (NEA hereafter) seemed to be well known after several taxo-
nomic studies (Holthe 1986; Jirkov 1989, 2001; Gagaev 2009; Parapar et al. 2011,
2016c; Jirkov and Leontovich 2013; Parapar and Hutchings 2014). Nevertheless, mo-
lecular taxonomy approaches performed recently in a comprehensive sample of NEA
Terebellides have substantially changed the understanding of the species diversity hid-
den within members of this genus in European waters. Studies by Nygren et al. (2018)
and Lavesque et al. (2019) showed a number of genetic lineages, compatible with the
species concept – independently evolving entities that are genetically (and phenotypi-
cally) distinct (Barraclough 2010). As a result, the total number of species in the NEA
has increased dramatically from seven to 32 (Nygren et al. 2018; Lavesque et al. 2019),
but some of these still remain unnamed or not formally described.
Terebellides is the most species-rich genus of trichobranchids, with 82 nominal spe-
cies (Parapar et al. 2020; Read and Fauchald 2020) but fairly homogeneous morpho-
logically. It is distinguished from other members in the family by their characteristic
branchiae with a single mid-dorsal stalk on segment 3. However, species identication
presents some diculties as there are no clear boundaries between the intraspecic
and interspecic variability of some of the morphological attributes considered of high
taxonomic relevance. Species diagnostic features mainly rely on details of the branchi-
ae, shape and size of anterior thoracic lateral lobes, and uncinal morphology (Parapar
and Hutchings 2014; Parapar et al. 2016a, 2016b). Surprisingly, analyses of DNA
sequences showed a large genetic diversity within the group, especially in mitochon-
drial markers, and while the genetic intraspecic divergence in the universal barcoding
marker cytochrome c oxidase subunit I (COI) ranged from 0 to 3.4%, the interspecic
distance between species varied from 8.8 to 22.9% (Nygren et al. 2018).
Phylogenetic analyses consistently showed that the NEA Terebellides are divided
into four major clades, named Groups A–D in Nygren et al. (2018). e aim of the
present paper is the systematic revision of members of Group A (according to Nygren
et al. 2018), and the morphological characterization of the species assessed after phylo-
genetic and species delimitation analyses of DNA sequence data (Nygren et al. 2018).
Given that there are some species complexes, with scarce morphological dierences
between the species, if any, a list of apomorphic nucleotides (present in all sequences
of a certain species and unique of that species) is also provided as a complementary
diagnostic feature (Rach et al. 2008; Wong et al. 2009).
Materials and methods
is paper is based on the study of 132 specimens identied as belonging to Group A
as dened in Nygren et al. (2018) and corresponding to several putative species. is
material is deposited in the Zoological Museum Bergen (ZMBN, Bergen, Norway),
New species of Terebellides from North East Atlantic 3
Göteborg Natural History Museum (GNM, Goteborg, Sweden), the Norwegian Uni-
versity of Science and Technology, University Museum (NTNU-VM, Trondheim,
Norway; Bakken et al. 2020) and the Senckenberg Museum Frankfurt (SMF, Frank-
furt, Germany).
e sampling area covered in this paper is mostly the Norwegian and Swedish
continental shelf but also includes some samples from the Irish and Celtic seas, North
Sea, Barents Sea, Greenland Sea, South Icelandic coast and the Arctic Ocean (Suppl.
material 1: Table S1; Nygren et al. 2018).
Light microscope images were obtained by means of an Olympus SZX12 stereomi-
croscope equipped with an Olympus C-5050 digital camera. Line drawings were made
with an Olympus BX40 stereomicroscope equipped with camera lucida. 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 micro-
scope at the Servizos de Apoio á Investigación (SAI, Universidade da Coruña, Spain).
Methyl green (MG) staining patterns and thoracic uncini morphology were char-
acterised based on the classication proposed by Schüller and Hutchings (2010) and
Parapar et al. (2020) respectively; specimens of similar/comparable size were used.
e species dealt within the present study are quite homogenous morphologically.
erefore, common traits shared by all members of Group A are described rst in order
to avoid repetition of the same characters in each species description.
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 1: Table S1. Unless specied, each registration number holds a sin-
gle specimen; associated GenBank DNA sequence accession numbers are provided in
Suppl. material 2: Table S2.
e present systematic account follows the phylogenetic hypothesis presented by
Nygren et al. (2018), after phylogenetic analyses of mitochondrial COI (ca. 658bp)
and 16S rDNA (ca. 440 bp), and the nuclear ITS2 (290–419 bp) and 28S rDNA
(ca. 760 bp) sequences from 513 specimens of Terebellides species from the NEA.
In their topology, four strongly supported major clades were recovered, and named
Groups A–D. We are herein dealing only with members of Group A. Other subgroups
(A1–A4) within Group A were established after analyses of combined datasets (Fig. 1;
Nygren et al. 2018). In the present study comparison of the morphological traits of
species within these subgroups were performed in order to nd potential characteristic
diagnostic features.
e COI universal barcoding gene proved to be very informative for species delim-
itation purposes alone, but insucient to resolve deeper relationships in the Terebellides
radiation (Nygren et al. 2018). However, in the present study further analyses based
on this mitochondrial marker alone have been performed in order to assess diagnos-
tic nucleotides for each of the species and establish genetic distances between them.
Phylogenetic analyses of COI Terebellides sequences in GenBank generated by Nygren
et al. (2018) and Lavesque et al. (2019) were performed, using Trichobranchus roseus
(Malm, 1874), Polycirrus sp., and Pista cristata (Müller, 1776) as outgroups (Nygren et
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
4
al. 2018). Four hundred and seventy-one sequences were aligned with MAFFT version
7.017 (Katoh et al. 2002), and with default parameters, trimming some starting nu-
cleotides of the sequence of Terebellides sp. (MN207188) to become 659 bp alignment.
Best-t model according to Bayesian information criterion – BIC (TVM+F+I+G4),
was calculated with IQTREE version 1.6.11 (Nguyen et al. 2015). Maximum likeli-
hood phylogenetic analyses were also run in IQTREE version 1.6.11 (Nguyen et al.
2015), with ultrafast bootstrap (Hoang et al. 2018). Tree topology and support val-
ues for the nodes are found in Fig. 2. Given the morphological homogeneity in the
Terebellides Group A species, GenBank accession numbers (COI sequences) are pro-
vided for each species, indicating those belonging to type series. Moreover, unequivo-
cal nucleotide diagnostic characters are provided as the positions in the alignment
(nucleotide), with the alignment available in Suppl. material 2: Table S2.
Abbreviations used in text, tables and gures:
abl anterior branchial lobe (lobe #5);
babv branchial aerent blood vessel;
bbv branchial blood vessel;
bdl branchial dorsal lobes;
bdl branchial dorsal lobes fusion line;
bdltp branchial dorsal lobe terminal
papilla;
blp branchial lamellar papillae;
bst branchial stem;
bt buccal tentacles;
bvl branchial ventral lobes;
bvltp branchial ventral lobe terminal
papilla;
cap capitium;
cbh contractile branchial heart;
cr ciliary row;
ct ciliary tuft;
ctrX capitium teeth row X;
dg digestive gland;
dpn dorsal projection of notopodium;
fore intestine;
fs fore stomach;
gc geniculate chaetae;
gr glandular region;
hs hind stomach;
loli lower lip;
MG Methyl Green;
nop notopodial protuberance;
np nephridial papilla;
oes oesophagus;
ooc oocytes;
ros rostrum;
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.
Systematics
e revision of the specimens of Terebellides Group A as found in Nygren et al.
(2018) resulted in the identication of three nominal species: Terebellides stroemii
Sars, 1835, Terebellides bigeniculatus Parapar, Moreira & Helgason, 2011 and T. eu-
ropaea Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa, 2019, and ve new
species described herein as T. bakkeni sp. nov., T. kongsrudi sp. nov., T. norvegica sp.
New species of Terebellides from North East Atlantic 5
nov., T. ronningae sp. nov. and T. scotica sp. nov. e remaining ve species will be
dealt with in future studies.
Species included in Group A have been grouped as follows: A) subgroup A1 (spe-
cies 10, 11, 12, 13, 18, 19; as in Nygren et al. 2018), B) subgroup A2 (species 6, 7, 8,
9; as in Nygren et al. 2018), C) subgroup A3 (clades 20 + 28, 21; as in Nygren et al.
2018) and D) subgroup A4 (species 23) (Figs 1, 2, Table 1); material will be described
here following this order. Material corresponding to species 12, 18, 19 (A1), 21 (A3)
and 23 (A4) is not described/named here. Species 18, 19 and 23 were represented by
1–3 specimens each (see Appendix S36 in Nygren et al. 2018) and are pending formal
description until more material is available. Clades 12 and 21 will be described else-
where by D. Gaeva and I. Jirkov (Shirshov Institute of Oceanology, Russia).
0.1
2786_11
2854_14
842_5
Trichobranchus
2031_10
2793_5
2034_10
2313_18
1310_3
2476_8
2342_21
2277_22
2458_13
2867_24
861_9
2457_8
2448_7
2904_5
2271_2
1312_12
2235_4
1870_6
2875_28
2480_3
2268_16
2389_16
2337_13
2467_16
840_5
2805_26
1560_11
2325_16
2855_14
2030_15
2324_28
2010_15
2278_19
2859_7
2363_16
1943_6
858_1
2042_14
2045_4
2442_7
2800_27
2009_15
2453_1
2475_13
2807_26
2809_25
2043_15
1311_2
862_9
2323_11
2353_2
2801_25
2826_12
2233_4
2478_8
2314_18
2352_2
2445_1
2348_28
1207_3
2028_13
2866_24
849_6
2868_24
2463_3
2281_23
2222_12
2441_1
2887_3
2173_6
2469_16
2865_24
2449_7
2234_4
1948_1
Pista
2267_16
2806_12
1309_7
2302_20
2033_10
2044_14
2274_17
Polycirrus
2903_28
2349_20
2269_16
2194_12
2829_12
2921_13
97
100
100
100
73
81
85
94
100
100
100
100
85
98
100
100
100
100
100
100
100
100
98
100
98
98
100
100
99
100
100
100
100
94
100
97
100
100
100
100 100
100
100
100
100
100
100
A
B
C
D
Te rebellides
100
100
100
12
13
10
11
18
20+28
21
7
6
8
9
A1
A2
A3
A4
A
1
A4
A4
2467 16
2467 16
_23
19
23
Figure 1. Phylogenetic tree after Maximum Likelihood analyses on a concatenated dataset of cox1, 16S
rDNA, ITS2, and 28S rDNA (as in Nygren et al. 2018). Bootstrap support values above nodes. Coloured
squares indicate the major clades referred herein as Groups A–D. Within Group A, the focus of present
study, subgroups A1–A4 and species 6–13, 18–21, 23, 28 are labelled.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
6
15 2
3
26 27
16
5
4
14 17
1
24
25 22
21
12
18
13
T. kongsrudi sp. nov.
T. stroemii
T. bakkeni sp. nov.
T. europaea
T. ronningae sp. nov.
T. norvegica sp. nov.
T. scotica sp. nov.
T. bigeni
culatus
0.07
2475_13
2385_21
1205_13
2799_8
2818_12
1872_6
MN207182.1
2038_13
862_9
2775_8
1999_13
MN207181.1
2193_12
2024_10
1922_8
839_6
1313_6
2348_28
1995_8
2442_7
1869_6
MN207180.1
2452_7
MN207179.1
2875_28
2824_12
2036_8
846_6
2384_21
2377_21
MN207186.1
1923_13
2324_28
1944_6
2031_10
1309_7
2167_6
2202_12
1197_8
2214_8
2198_12
2173_6
2903_28
2317_13
2894_21
2171_12
2033_10
1942_6
1873_6
2199_12
1957_8
1959_13
1986_13
2347_11
1998_13
2000_8
2037_8
1315_6
2034_10
1956_13
859_9
1984_8
2831_21
2899_11
2829_12
2834_21
2817_21
2014_8
2224_12
2190_6
2827_12
1312_12
2314_18
2819_21
1870_6
2454_13
2816_21
TB25_10
1985_8
2323_11
2222_12
2196_12
845_6
1316_6
1996_8
2278_19
2833_21
829_7
1318_6
2457_8
2458_13
2832_12
2200_12
1199_8
2225_12
2776_13
2342_21
2194_12
1202_8
2184_13
1319_6
847_6
2774_6
2197_12
2823_21
TB26_10
2798_8
2172_6
2312_18
1943_6
2820_21
2195_12
2448_7
2826_12
2035_13
849_6
1314_6
2032_10
2896_8
2026_10
2806_12
2304_10
2921_13
2895_21
2456_8
2920_8
1991_8
1990_10
2001_8
T03_13
T01_13
860_6
2825_21
1960_13
2815_21
2925_8
2201_12
2028_13
2914_7
2329_28
1871_6
2321_10
850_6
2027_13
2015_8
MN207184.1
2836_21
1560_11
2337_13
2476_8
2449_7
1874_6
2215_13
2223_12
1946_8
1958_8
2859_7
1201_13
1321_6
2183_13
MN207188.1
2863_7
2002_8
1200_8
2281_23
1875_6
2813_13
1561_8
848_6
2349_20
2302_20
1988_8
2830_21
1198_8
1203_8
MN207183.1
2046_6
MN207185.1
2447_7
1994_8
2029_10
2313_18
2786_11
2013_8
2443_7
838_6
1317_6
2478_8
1992_8
1989_8
2450_7
2039_8
100
64
60
100
67
5
51
99
21
98
100
99
97
100
93
27
100
66
100
92
31
100
52
98
100
100
39
100
Terebellides
Group
A
100
100
58
100
97
100
100
65
81
6
100
93
100
20+28
10
11
8
T. lilasae
6
9
7
23
19
A2
A1
A1
A3
A1
A1
A4
Figure 2. Phylogenetic tree after Maximum Likelihood analyses on a dataset of cox1 (including all se-
quences in Nygren et al. 2018 and in Lavesque et al. 2019). Bootstrap support values above nodes. Species
other than members of Group A are collapsed. Species with names refer to those dealt with in present study.
New species of Terebellides from North East Atlantic 7
Family Trichobranchidae Malmgren, 1866
Genus Terebellides Sars, 1835 emended by Schüller & Hutchings, 2013
Type species. Terebellides stroemii Sars, 1835, redescribed by Parapar and Hutchings
(2014) and neotype deposited.
Terebellides Group A (sensu Nygren et al. 2018)
Description. e morphological features shared by all studied species in Group A are
itemized below. Some of these are also shared by Groups B, C and D as dened in
Nygren et al. (2018) (see Remarks below).
Body appearance. Complete individuals ranging from 10.0–50.0 mm in length.
Body tapering posteriorly with segments increasingly shorter and crowded towards
pygidium (Fig. 14A–C). Prostomium compact; large tentacular membrane surround-
ing mouth (Figs 5C, 14B), with typical buccal tentacles with expanded tips (Figs 15A,
20A). SGI as an expanded structure below tentacular membrane in a lower lip
(Figs 14C, 15A, 22A, 24A).
Branchiae. Branchiae arising as single structure from SGIII, with a single stalked
mid-dorsal stem (Figs 5A, 11C, 15A), one pair of dorsal (upper) partially fused lobes
(Figs 11B, 15B, 20A), and a pair of shorter ventral (lower) lobes (Fig. 5A, B) obscured or
Table 1. Comparison of discriminatin g taxonomic characters of the species studied in this work. Cells
with text in italic show discriminatory characters of each subgroup. Species 18, 19, and 23 were not stud-
ied and 12 and 21 only examined with SEM.
Subgroups A1 A2 A3 A4
Species sensu Nygren et al. (2018) 10 11 12 13 18 19 6 7 8 9 20 + 28 21 23
SPECIES
T. bakkeni
sp.nov.
T. stroemii
Sars,1835
Terebellides
sp.1
T. kongsrudi
sp.nov.
T. europaea
Lavesque
etal.,2019
T. ronningae
sp.nov.
T. norvegica
sp.nov.
T. scotica
sp.nov.
T. bigeniculatus
Parapar
etal.,2011
Terebellides
sp.2
(as reported/described here)
Branchiae type (1) 1111 – –1 1 1 1 1 (2) 1 (2) –
papillae on lamellae
edge
no no no no – – yes yes yes yes no no –
orax ciliated papilla dorsal to
notopodium
yes yes yes yes – – no no
(?)
no no yes yes –
chaetiger(s) with
geniculate chaetae
TC6 TC6 TC6 TC6 – – TC6 TC6 TC6 TC6 TC5 + TC6 TC5 + TC6 –
uncini type (3) 3 3 3 3 – – 3 1 3 3 3 3 –
Abdomen uncini type (4) 1A 2 2 1A – – 2 2 2 2 1B 1B –
Bathymetry – Above (A) / Below
(B) 200 m depth (5)
A / BA / BA A / BB B A A B A B A / BB
Distribution – North (N) /South
(S) of 60°N (5)
N N S N / S N N S (6) N / S N / S S (7) N N N
(1) sensu Parapar et al. (2016c); (2) sometimes irregular; (3) sensu Parapar et al. (2020); (4) this work; (5) dominant trend in bold; (6) Skager-
rak and Kattegat; (7) Irish Sea
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
8
not by dorsal ones (Figs 5A, C, 15A, B). Both dorsal and ventral branchial lobes ending
each posteriorly in short terminal papilla (Fig. 20B). Anterior projection of dorsal lobes
(fth lobe) present but short (Fig. 5A, B) and usually obscured by tentacular membrane
and buccal tentacles (Fig. 14A, C). Posterior dorsal lobes reaching TC4 (Figs 3, 4, 19).
Branchial lamellae provided with several parallel rows of cilia in inner face (Fig. 15C); cil-
iated papillae not present, ciliary tufts present, sometimes not clearly visible (Fig. 5B, D).
orax. Eighteen pairs of notopodia (SGIII-SGXX) (Fig. 14B, D), those of TC1
approximately as long as following ones (Figs 20A, 22A) or slightly shorter (Fig. 15A).
Lateral lappets and dorsal projections of notopodia in anterior thoracic chaetigers with
dierent degree of development depending on size and preservation conditions, but
both more conspicuous on TC2–4/5 (Figs 15A, 22A). All notochaetae as simple capil-
laries (Figs 11F, 15A). Neuropodia as sessile pinnules from TC5 or TC6 to body end,
with uncini in single or double rows, from TC7 throughout. Neuropodia on TC5 or
TC5 and TC6, provided with several sharply bent, acute-tipped, geniculate chaetae
(Figs 16B, 23A) with minute teeth forming an ill-dened capitium only visible with
SEM (Figs 12B, 25B). From TC7, neuropodia with one or several rows of uncini per
torus (Figs 16C, 23C), with long shafted denticulate hooks, with large main fang (ros-
trum) longer than upper crest of teeth (capitium), which is composed by several teeth
above main fang of decreasing length (Figs 23D, 25D, E).
Abdomen and pygidium. Approximately half as long as thorax and progressively
thinner (Fig. 14B). Neuropodia ranging from 18–38 chaetigers and forming erect pin-
nules (Figs 6F, 12F) with several uncini per torus, number depending of specimen
size. Uncini provided with several teeth above rostrum surmounted by a capitium
composed of several teeth of decreasing length (Figs 6G, 16E, 21F). Pygidium blunt,
as funnel-like depression.
Colour pattern. Colour in preserved specimens pale brown (Fig. 3). MG staining
pattern 1 sensu Schüller and Hutchings (2010: 10, g. 4) and characterised by com-
pact green colouration in CH1–3, then turning into striped pattern in CH4–12 and
fading in following segments.
Remarks. Among the aforementioned characters, branchial features might serve to
distinguish most of Group A species (except for A3 species) from those in Groups B–D.
ose include branchial size, lobes size (i.e., whether dorsal and ventral are of similar
size or dier), presence of terminal papilla/lament on posterior lobes, and presence of
ciliary structures (rows, tufts or buttons) on lamellae. Other taxa described or reported
worldwide bear similar branchiae including T. stroemii sensu Parapar et al. (2011) from
Iceland and sensu Parapar et al. (2013) from the Adriatic Sea, T. kerguelensis McIntosh,
1885 and T. longicaudatus Hessle, 1917 from Antarctic latitudes (Parapar and Moreira
2008a, 2008b), and T. kobei Hessle, 1917 from Japan (Imajima and Williams 1985).
e other species groups as found in Nygren et al. (2018) were not studied in
depth here and will be the aim of a subsequent study. However, Group B seems to
be characterised by having a shorter body and free branchial lobes; these features are
shared with T. atlantis Williams, 1984 and T. irinae Gagaev, 2009 as already suggested
by Nygren et al. (2018). Members of Group C are apparently not dened by any
New species of Terebellides from North East Atlantic 9
unique shared morphological character but show the same geographic distribution as
T. irinae. Finally, the three putative species in Group D were related to T. gracilis Malm,
1874 and T. williamsae Jirkov, 1989 by Nygren et al. (2018) even though the latter was
proposed to be synonymised with the former by Parapar et al. (2011). ese species
seem characterised by having ventral white colouration in a number of anterior chaeti-
gers and similar-sized branchial lobes; these characters are not shared with Group A.
Regarding Group A, six morphological characters have been considered to deline-
ate subgroups and species (Table 1). Two characters can be determined with the aid of
the STM: 1) general branchial shape, 2) number of thoracic chaetigers with geniculate
chaetae; four characters require SEM examination: 3) presence of papillae on lamellae
of dorsal branchial lobes, 4) presence of ciliated papillae dorsal to thoracic notopodia,
5) features of thoracic and 6) abdominal uncini shape dentition. Branchial typology
(1) is dened according to Parapar et al. (2016c) and thoracic uncini (5) follows Para-
par et al. (2020). Typology of abdominal uncini (6) is described here (see Discussion).
Furthermore, species will be also characterised according to geographic and bathy-
metric distribution according to available data.
Subgroup A1
Analyses of molecular data found low or no support for monophyly of this clade (Figs1,
2) and there is no apparent morphological synapomorphy supporting this clade either.
Cohesion of members of this group needs to be studied further, but meanwhile, it
is considered herein as a morphologically homogenous gathering of species 10–13
and 18–19 (Figs 1, 2). As it was indicated above, only species 10, 11, and 13 will be
described herein, of which 10 and 13 are new to science and 11 corresponds to T.stro-
emii; some comments on species 12 (Terebellides sp. 1 hereafter) are also provided.
Characters present only in subgroup A1
None (Table 1).
Character/s shared with subgroup A2
• Branchiae of type 1 (stroemii-type, comma-shaped), all four lobes fused for
approximately half of their length and ventral ones usually obscured by dorsal ones
(Fig. 11A–C).
• First thoracic neuropodia on TC6, with chaetiger provided with several sharp-
ly bent, acute-tipped geniculate chaetae (Figs 6A, 15A, 16B).
Character/s shared with subgroup A3
• Border of anterior region of dorsal branchial lamellae not provided with papil-
lary projections.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
10
• One ciliated papilla is present, dorsal to thoracic notopodia (Fig. 5F).
• oracic uncini type 3 (Figs 6E, 7E, F, 16D).
Character/s variable within subgroup A1
• Abdominal uncini type 1 (Fig. 6G) and 2 (Fig. 7G) (see Conclusions Section).
Lavesque et al. (2019) describe several species from French waters similar to those
of Group A in terms of body and branchial shape. Among them, Terebellides gralli
Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa, 2019 is described as lacking
papillary projections on branchial lamellae, but no mention is made to whether or
not ciliated papillae are present dorsal to thoracic notopodia. e sequences of this
species do not relate with those of any putative species as dened in Nygren et al.
(2018). Moreover, T. gralli diers morphologically from other congeners in having
longer branchiae that may reach TC4–6 (Lavesque et al. 2019: 169, g. 12A) instead
of only reaching TC3–4.
Terebellides bakkeni sp. nov.
http://zoobank.org/0D530A3C-65B2-4F9D-A78A-051AE5B62110
Figs 1, 2, 3A, 4A, 5, 6, 8A, 9, 17A; Table 1; Suppl. material 1: Table S1; Suppl. mate-
rial 2: Table S2
Species 10 Nygren et al. 2018: 18–22, gs 6, 10.
Material examined. Type material. Holotype: ZMBN116395. Paratypes (10 speci-
mens): Barents Sea (ZMBN116388, ZMBN116389), Norwegian coast and shelf
(ZMBN116390, ZMBN116391, ZMBN116392, ZMBN116393, ZMBN116394,
ZMBN116396, NTNU–VM61376, NTNU–VM61377).
Holotype. Complete specimen, 32.0 mm long and 2.0 mm width (Figs 3A, 4A).
GenBank accession numbers of material examined (COI). Holotype: MG025165;
Paratypes: MG025159, MG025160, MG025161, MG025162, MG025163,
MG025164, MG025165, MG025166, MG025168, MG025169, MG025170. Addi-
tional material: MG025167.
Diagnostic features of type material. Complete individuals ranging from
23.0–32.0 mm in length (Fig. 17A). Branchial dorsal lobes lamellae without papil-
lary projections. Ventral branchial lobes generally hidden behind dorsal ones (Figs 3A,
4A, 5A–C). Lateral lappets and dorsal projection of thoracic chaetigers present on
TC2(TC3)–TC5(TC4) (Fig. 5A). Geniculate chaetae in TC6 acutely bent, with low
marked capitium (Fig. 6A, B). Ciliated papilla dorsal to thoracic notopodia (Fig. 5F).
oracic uncini in one row with rostrum/capitium length ratio of approximately 2 : 1
and capitium with a rst row of three or four medium-sized teeth, followed by several
smaller teeth (Fig. 6C–E). Abdomen with 25–29 pairs of neuropodia (Fig. 6F) with
type 1 uncini (Fig. 6G).
New species of Terebellides from North East Atlantic 11
Figure 3. STM photographs of several Terebellides species. A Terebellides bakkeni sp. nov. (species 10; hol-
otype, ZMBN116395) B Terebellides stroemii Sars, 1835 (species 11; non-type specimen, ZMBN116397)
C Terebellides kongsrudi sp. nov. (species 13; holotype, GNM14632) D Terebellides bigeniculatus Parapar,
Moreira & Helgason, 2011 (species 20 + 28; non-type specimen, ZMBN116514) E Terebellides europaea
Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa, 2019 (species 6; non-type specimen, GNM14628)
F Terebellides ronningae sp. nov. (species 7; holotype, ZMBN116357) G Terebellides norvegica sp. nov.
(species 8; holotype, ZMBN416378) H Terebellides scotica sp. nov. (species 9; holotype, ZMBN116385).
Abbreviations: bdl – branchial dorsal lobe; bvl – branchial ventral lobe; TC – thoracic chaetiger.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
12
Nucleotide diagnostic features. Members of T. bakkeni sp. nov. share the follow-
ing unique nucleotides at these given positions of our alignement: 162 (G), 168 (C),
345 (G; shared only with one specimen from species 17).
Type locality. Nordland, Sortlaandssunder (Lofoten Islands); 119 m deep (Suppl.
material 1: Table S1).
Distribution and bathymetry. Barents Sea, Greenland Sea, northern Norwegian
coasts from the Lofoten Islands to Trondheim; at depths of102–378 m (Nygren et al.
Figure 4. Line drawings of several Terebellides species. A Terebellides bakkeni sp. nov. (species 10;
holotype, ZMBN116395), anterior end, right lateral view B Terebellides stroemii Sars, 1835 (species 11;
non-type specimen, ZMBN116397), anterior end, right lateral view C Terebellides kongsrudi sp. nov.
(species 13; holotype, GNM14632), anterior end, left lateral view D Terebellides bigeniculatus Parapar,
Moreira & Helgason, 2011 (species 20 + 28; non-type specimen, ZMBN116514), anterior end, left lateral
view. Abbreviations: bdl – branchial dorsal lobe; bvl – branchial ventral lobes; dpn – dorsal projection of
notopodium ; TC – thoracic chaetiger.
New species of Terebellides from North East Atlantic 13
2018) (Figs 8A, 9; Suppl. material 1: Table S1). One specimen found in North Iceland
at 1,250 m deep.
Etymology. is species is named after Dr. Torkild Bakken, from the NTNU–
University Museum, Trondheim (Norway), housing institution of some of the speci-
mens used in the present study, for his dedication to the study of Norwegian poly-
chaetes and his friendship.
Remarks. Terebellides bakkeni sp. nov. is a small-sized species, maximum-sized
specimens reaching 20.0 mm in length (n = 3). is species is characterised by the
presence of ciliated papilla dorsal to thoracic notopodia, lack of papillae on the mar-
gins of branchial lamellae and presenting abdominal uncini of type 1. Most of these
features are also shared by the closest relative, T. stroemii (species 11 herein), but they
dier in the morphology of the abdominal uncini, being of type 2 in T. stroemii and
type 1 in T. bakkeni sp. nov. (Table 1). One specimen studied with SEM showed
ciliary tufts in the inner side of the branchial lamellae (Fig. 5D). If this feature is not
an artefact and is conrmed in all members of the species – so far only two speci-
mens were examined under SEM – it would be an autapomorphy for the species. A
similar feature was found in the non-closely related T. gracilis, that is also present
in NEA. e ciliary tufts in T. bakkeni sp. nov. are, however, connected by rows of
cilia (Fig. 5D), while in T. gracilis they are conned to isolated tufts (Parapar et al.
2011: 12, g. 9c). On the other hand, there are no clear morphological dierences
between T. bakkeni sp. nov. and T. kongsrudi sp. nov. (species 13). ese sympatric
species dier in the southern limit of their geographic distribution: T. bakkeni sp.
nov., as T. kongsrudi sp. nov. are present above 65°N (Fig. 8A, C) while the latter and
T.stroemii reach more southern latitudes, such as the Skagerrak and Bergen respec-
tively (Fig.8B, C).
Of the 462 sequences, including all NEA species, and 659 positions in the COI
alignment, the 12 sequences assigned to T. bakkeni sp. nov. hold two unique nucleo-
tides positions, and an additional one only shared by a single specimen from another
clade (see Suppl. material 2: Table S2). e species also showed 0–1.9% of intraspecic
divergence in the COI marker, and a minimum of 11.5% uncorrected genetic distance
with congeners (in this case T. stroemii) (Nygren et al. 2018).
Terebellides stroemii Sars, 1835
Figs 1, 2, 3B, 4B, 7, 8B, 9, 10, 17A, 28D; Suppl. material 1: Table S1; Suppl. material
2: Table S2
Terebellides stroemii Sars, 1835: 48–50, pl. 13, g. 31a–e. Parapar and Hutchings 2014:
10, g. 5–10. Non Parapar et al. 2011: 14–17, gs 11, 12, 13G.
Species 11 – Nygren et al. 2018: 18–22, gs 6, 10. Non Clade 6 in Nygren et al. (2018)
(see Remarks).
Type locality. Helle, Manger, Bergenord (Norway) (Parapar and Hutchings 2014).
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
14
Material examined. 5 specimens (Suppl. material 1: Table S1), Norwegian coast
and shelf: ZMBN 116397, ZMBN 116398, ZMBN 116399, ZMBN 116400,
ZMBN 116401.
Figure 5. Terebellides bakkeni sp. nov. (species 10; paratypes, NTNU-VM-61376 and NTNU-
VM-61377), SEM micrographs. A anterior end, left lateral view B, C branchial lamellae D branchial
ciliary rows (framed in B) E nephridial papilla F thoracic notopodial papillae (framed: detail of one
papilla). Abbreviations: abl – anterior branchial lobe; bdl – branchial dorsal lobe; bvl – branchial ventral
lobe; cr – ciliary row; ct – ciliary tuft; dpn – dorsal projection of notopodium; np – nephridial papilla; TC
– thoracic chaetiger; tdp – thoracic dorsal papilla; tll – thoracic lateral lobes; tm – tentacular membrane.
New species of Terebellides from North East Atlantic 15
Additional material. Neotype (NHMOC5896) and seven “neoparatypes”
(NHMOC5899, NHMOC5902, NHMOC5904, NHMOC5905, NHMOC5907,
NHMOC5956, NHMOC5968) of T. stroemii (Suppl. material 1: Table S1).
GenBank accession numbers of material examined (COI). MG025171,
MG025172, MG025173, MG025174, MG025175.
Diagnostic features of studied material. Complete individuals ranging from
6.0–20.0 mm in length (Fig. 17A). Branchial dorsal lobes lamellae without papil-
lary projections. Ventral branchial lobes hidden behind dorsal lobes (Figs 3B, 4B).
Lateral lappets present on TC1–TC4; dorsal projection well marked from TC3–TC4
(Fig.7A). Geniculate chaetae in TC6, acutely bent (Fig. 7C) with low marked capit-
ium. Ciliated papilla dorsal to thoracic notopodia (Fig. 7B). oracic uncini in one
row with rostrum/capitium length ratio approximately 2 : 1 and capitium with a rst
row of three or four medium-sized teeth, followed by several smaller teeth (Fig. 7E, F).
Abdomen with 23–32 chaetigers (Fig. 17A) with type 2 uncini (Figs 7G, 28D).
Nucleotide diagnostic features. ere are no unique apomorphic nucleotides in
the fragments of COI analysed for T. stroemii, when considering all Terebellides species
present in the NEA (Suppl. material 2: Table S2). However, when comparing homolo-
gous nucleotide positions with members of only Group A (183 sequences in the COI
alignment), the following autapomorphies arise: 174 (C), 183 (C), 453 (A), 612 (C).
Distribution and bathymetry. Terebellides stroemii was traditionally considered
as a cosmopolitan species, but its known distribution seems in fact restricted to the
Norwegian coastline (Parapar et al. 2011; Parapar and Hutchings 2014; Lavesque et al.
2019). Specimens examined by Nygren et al. (2018) and in the present paper, obtained
after comprehensive sampling in the NEA, were found only in W Norway, between
115 and 388 m deep (Figs 8B, 10; Suppl. material 1: Table S1).
Remarks. In the ve sequences belonging to this species, there were four hap-
lotypes showing 0–1.1% of intraspecic divergence, and a minimum of 11.5% un-
corrected genetic distance with members of the closest relative, T. bakkeni sp. nov.
(Nygren et al. 2018).
Terebellides stroemii is a large species, reaching up to 52 mm in length (Parapar and
Hutchings 2014) and is characterised by the presence of ciliated papilla dorsal to tho-
racic notopodia, lack of papillae on margins of branchial lamellae, thoracic uncini of
type 3 and abdominal uncini of type 2. All these features are shared with T. kongsrudi
sp. nov.; T. bakkeni sp. nov. is also very close morphologically to T. stroemii but they
dier in the morphology of the abdominal uncini as explained above.
Nygren et al. (2018) misidentied species 6 as T. stroemii, but this was later cor-
rected by Lavesque et al. (2019) who pointed out that the molecular sequences of these
specimens t with those of T. europaea.
Specimens examined here bear thoracic uncini that are most similar to other mem-
bers of Group A; SEM examination showed, however, that some uncini have a rostrum
distal tip that is distinctly bent downwards (deformity?) (Fig. 7E, arrow) as already de-
scribed for the type specimens by Parapar and Hutchings (2014: 8, g. 7F, G), and attrib-
uted to preservation for too long in EtOH. However, we have found similar bent rostrum
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
16
among specimens of T. kongsrudi sp. nov. (Fig. 12D, arrow), T. ronningae sp. nov. (species
7) (Fig. 21C, arrows) and T. bigeniculatus (species 20 + 28) (Fig. 26E, frame) suggesting
this may not be related to preservation. e abdominal uncini are quite similar to those
described in Parapar and Hutchings (2014: 9, g. 8C–E) also showing a small gap among
the anteriormost teeth of rostrum (Parapar and Hutchings 2014: 8–9, g. 8F; Fig. 7G);
these features are not shared by other species of subgroup A1, i.e., T. bakkeni sp. nov. and
T. kongsrudi sp. nov. In all, species 11 agrees well with the redescription of T. stroemii.
Figure 6. Terebellides bakkeni sp. nov. (species 10; paratypes, NTNU-VM-61376 and NTNU-
VM-61377), SEM micrographs. A TC6 (TU1) geniculate chaetae B geniculate chaeta (arrow pointing to
capitium) C–E thoracic uncini F abdominal unciniger G detail of three abdominal uncini, frontal view.
New species of Terebellides from North East Atlantic 17
Geographic and bathymetric distribution of our specimens also agree with that of
T.stroemii (see Parapar and Hutchings 2014), with Manger (Norway) (i.e., type locality
of T. stroemii; Fig. 10) being its southernmost distribution limit. e other three taxa, i.e.,
species 5, T. europaea and T. bigeniculatus, were also found near Manger, but all can be
clearly distinguished morphologically from each other (see above and below for T.europaea
Figure 7. Terebellides stroemii Sars, 1835 (species 11; non-type specimen, ZMBN 116399), SEM mi-
crographs. A anterior end, right lateral view B TC6 to TC8, lateral view C geniculate chaetae D TC4
and TC5, nephridial papillae E, F thoracic uncini (arrow in E pointing to rostrum curved at distal end)
Gabdominal uncini. Abbreviations: bdl – branchial dorsal lobes; dpn – dorsal projection of notopodium;
np – nephridial papilla; TC – thoracic chaetiger; tdp – thoracic dorsal papilla; tm – tentacular membrane.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
18
and T. bigeniculatus) and species 5 belongs to Group B and seems closer morphologically
to T.atlantis. On the other hand, type specimens of T. stroemii come from depths of 55–
110m (Parapar and Hutchings 2014) as well as specimens belonging to T. europaea, T.ron-
ningae sp. nov., T. scotica sp. nov. (species 9) and species 12 (<200 m), and therefore they
seem to constitute a shallow-water assemblage of species from an ecological point of view.
Finally, the Icelandic specimens reported as T. stroemii by Parapar et al. (2011) might
not correspond to this species. In fact, it is likely that they represent at least two dierent
species, namely T. bakkeni sp. nov. and T. kongsrudi sp. nov., both reported here to the North
and East of Iceland. erefore, the aforementioned specimens deserve further revision.
Terebellides kongsrudi sp. nov.
http://zoobank.org/541890B5-C55E-4716-BB42-0D87E7184885
Figs 1, 2, 3C, 4C, 8C, 9, 11, 12, 17B, 28A; Table 1; Suppl. material 1: Table S1; Suppl.
material 2: Table S2
Species 13 – Nygren et al. 2018: 18–22, gs 6, 10.
Material examined. Type material. Holotype: GNM14632. Paratypes (20 specs):
Barents Sea (ZMBN116409, ZMBN116411, ZMBN116414); Norwegian coast
and shelf (ZMBN116412, ZMBN116413, ZMBN116415, ZMBN116416,
ZMBN116417, ZMBN116418, NTNU-VM66568, NTNU-VM66570, NTNU-
VM66571, NTNU-VM66572, NTNU-VM68195, NTNU-VM72560, NTNU-
VM72561, NTNU-VM72562, NTNU-VM72563); Skagerrak (GNM15136,
GNM14632, GNM14638).
Holotype. Complete specimen, 50.0 mm long and 5.0 mm width (Figs 3C, 4C).
GenBank accession numbers of material examined (COI). Paratypes:
MG025201, MG025202, MG025203, MG025204, MG025210, MG025211,
MG025212, MG025214, MG025216, MG025217, MG025218, MG025219,
MG025223. Additional material: MG025199, MG025200, MG025205, MG025206,
MG025207, MG025208, MG025209, MG025213, MG025215, MG025220,
MG025221, MG025222, MG025224.
Diagnostic features of type material. Complete individuals 12.0–50.0 mm in length
(Fig. 17B). Branchial dorsal lobes lamellae without papillary projections. Ventral branchial
lobes hidden in between dorsal ones (Figs 3C, 4C, 11A–C). Lateral lappets and dorsal
projection of thoracic notopodia on TC2(3)–TC5(4) (Fig. 11A). Geniculate chaetae in
TC6, acutely bent, with low marked capitium (Fig. 12A, B). Two pairs of nephridial pores
in TC4 and TC5 and ciliated papilla dorsal to thoracic notopodia (Fig. 11D, E). oracic
uncini in one row with rostrum/capitium length ratio approximately 2 : 1 and capitium
with a rst row of 2–5 medium-sized teeth, followed by several smaller teeth (Fig. 12C–
E). Abdomen with 25–35 uncinigers (Fig. 12F) with type 1 uncini (Figs 12G, 28A).
Nucleotide diagnostic features. All sequences of T. kongsrudi sp. nov. share the
unique apomorphic nucleotides in positions 300 (G) and 624 (G) of our alignement.
Type locality. Skagerrak; 429–445 m deep (Fig. 8C; Suppl. material 1: Table S1).
New species of Terebellides from North East Atlantic 19
Distribution and bathymetry. Barents Sea, Greenland Sea, along the Norwegian
coast and shelf, reaching the Skagerrak to the South; 108–534 m deep (Nygren et al.
2018) (Figs 8C, 9; Suppl. material 1: Table S1).
Etymology. is species is named after Dr. Jon Anders Kongsrud, Department
of Natural History, Zoological Museum Bergen–ZMB (Norway), housing institution
of some of the specimens used in the present study, for his dedication to the study of
Norwegian polychaetes and his friendship.
Figure 8. Geographic distribution of A T. bakkeni sp. nov. B T. stroemii Sars, 1835 C T. kongsrudi sp.
nov. D T. bigeniculatus Parapar, Moreira & Helgason, 2011.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
20
Remarks. is is a large species reaching up to 50.0 mm long, and is characterised
by the presence of ciliated papilla dorsal to thoracic notopodia, lack of papillae on the
margins of branchial lamellae, thoracic uncini of type 3 and abdominal uncini of type
1. ese features are also shared by species 12 (sensu Nygren et al. 2018), which will
be described elsewhere (Gaeva and Jirkov, pers. comm.). Terebellides kongsrudi sp. nov.
is also morphologically similar to T. bakkeni sp. nov. (see above) but T. kongsrudi sp.
nov. and species 12 show a wider geographic distribution; on the contrary, species 12
is present at shallower depths (<200 m) while T. kongsrudi sp. nov. extends to deeper
depths (>500 m).
Finally, in the 26 sequences belonging to this species (see Suppl. material 2: Table
S2), there were fourteen haplotypes showing 0–1.9% of intraspecic divergence, and a
minimum of 8.2% uncorrected genetic distance with members of species 12 which is
the closest relative (sensu Nygren et al. 2018).
Terebellides sp. 1
Figs 1, 2, 9, 13; Table 1; Suppl. material 1: Table S1; Suppl. material 2: Table S2
Species 12 – Nygren et al. 2018: 18–22, gs 5, 6, 10.
Material examined. 4 specimens. Skagerrak. GNM 14630-4; GNM 14630-8.
Figure 9. Bathymetric distribution of Terebellides species studied in this work. Subgroups (A1–3) within
group A sensu Nygren et al. (2018) are indicated.
New species of Terebellides from North East Atlantic 21
Remarks. is species will be described elsewhere by D. Gaeva and I. Jirkov
(pers. comm.). In order to conrm characters here used to link species within each
subgroup, two specimens were examined under the SEM that share with subgroup
A1 the following features: branchiae type 1 sensu Parapar et al. (2016c) (Fig. 13A),
lack of papillae on border of branchial lamellae (Fig. 13B), geniculate chaetae on TC6,
ciliated papilla dorsal to thoracic notopodia (Fig. 13C, D), and thoracic uncini of type
3 (Fig. 13E). Nevertheless, abdominal uncini are of type 2 (Fig. 13F), as it occurs in
T. stroemii and dierently to T. bakkeni sp. nov. and T. kongsrudi sp. nov., that are the
most similar species within subgroup A1 (Table 1).
SubGroup A2
Molecular analyses of mitochondrial and nuclear markers recovered a strongly
supported subgroup A2 (Fig. 1). is subgroup is composed by species 6, 7, 8, and
9 (sensu Nygren et al. 2018). Analyses of the COI dataset alone also nd support for
this clade, and incorporate the recently described T. lilasae Lavesque, Hutchings,
Figure 10. Map of Hordaland area (SW Norway) showing collecting sites of Terebellides species as found
in Nygren et al. (2018) near type locality of T. stroemii Sars, 1835. Depth ranges shown in boxes.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
22
Dae, Nygren & Londoño-Mesa, 2019 (Fig. 2). ere are several morphological
features that are shared, and exclusive to, all members of subgroup A2, and includes
other NEA species (see below). ree (7, 8, 9) of these four species are described
herein as new to science and the fourth species (6) corresponds to T. europaea.
Figure 11. Terebellides kongsrudi sp. nov. (species 13; paratypes, ZMBN 116409 and ZMBN 116411),
SEM micrographs. A anterior end, left lateral view B branchiae, left side C anterior end, left lateral view
D TC1 and TC2, thoracic dorsal papillae E TC3, thoracic dorsal papilla (framed in C) F several thoracic
chaetigers, left lateral view. Abbreviations: abl – anterior branchial lobe; bdl – branchial dorsal lobe; bdltp
– branchial dorsal lobe terminal papilla; dpn – dorsal projection of notopodium; tdp – thoracic dorsal
papilla; tll – thoracic lateral lobes.
New species of Terebellides from North East Atlantic 23
Character/s present only in Group A2
• Border of anterior region of dorsal branchial lamellae provided with papillary
projections (Figs 15C, 20C, 22C).
• Ciliated papilla dorsal to thoracic notopodia not present.
Figure 12. Terebellides kongsrudi sp. nov. (species 13; paratype, ZMBN 116409), SEM micrographs.
ATC6 (TU1) geniculate chaeta B detail of geniculate chaeta (arrow pointing to capitium) C–E thoracic
uncini, lateral and frontal views (arrow in D pointing to rostrum curved at distal end) F abdominal un-
ciniger G abdominal uncini, frontal view (framed in F).
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
24
• Abdominal uncini type 2 (Figs 16E, 21F, 23E, 25F).
Character/s shared with subgroup A1
• Branchiae of type 1 (stroemii-type, comma-shaped), all four lobes fused for ap-
proximately half of their length and ventral ones usually obscured by dorsal ones (Fig.20A).
Figure 13. Terebellides sp. 1 (species 12; GNM 14630-4 and GNM 14640-8), SEM micrographs. A anterior
end, right lateral view B detail of anterior branchial lamellae C TC16 D notopodial papilla E thoracic uncini
F abdominal uncini. Abbreviations: abl – anterior branchial lobe; bdl – branchial dorsal lobe; bvltp – branchial
ventral lobe terminal papilla; TC – thoracic chaetiger; tdp – thoracic dorsal papilla; tll – thoracic lateral lobes.
New species of Terebellides from North East Atlantic 25
• First thoracic neuropodia on TC6, with chaetiger provided with several sharp-
ly bent, acute-tipped geniculate chaetae (Figs 15A, 16B).
Character/s shared with subgroup A3
None (Table 1).
Character/s variable within subgroup A2
• oracic uncini type 1 and 3 (Figs 21E, 16D).
Several species described by Lavesque et al. (2019) have a similar body and branchi-
ae appearance to those of subgroup A2 species; however, only four species bear papillae
on the anterior border of branchial lamellae: Terebellides boni Lavesque, Hutchings,
Dae, Nygren & Londoño-Mesa, 2019, T. europaea, T. gentili Lavesque, Hutchings,
Dae, Nygren & Londoño-Mesa, 2019 and T. lilasae. Molecular sequences were avail-
able for all except T. gentili, with T. europaea being the only species found among the
material sequenced and analysed by Nygren et al. (2018), as species 6, and initially
misidentied as T. stroemii.
Terebellides gentili does not t morphologically within any clade dened here be-
cause of having numerous marginal branchial lamellae that reach the posterior end of
dorsal lobes, the dorsal lobes are longer and reach TC5(TC6) instead of TC3(TC4),
and TC3 has a distinct whitish glandular region with a well-dened central white line.
On the contrary, T. lilasae was found within subgroup A2 according to molecular-
based analyses (Fig. 2); this species also ts well morphologically in A2 by having
similar branchiae (shape), papillae on branchial lamellae, thoracic uncini of type 3 and
abdominal uncini of type 2, only diering in having comparatively larger branchiae.
e original description does, however, not mention whether notopodial papillae are
present or not. is species was described from the French Mediterranean and Atlantic
waters and is not present in northern latitudes, as suggested by Lavesque et al. (2019)
and conrmed here. On the other hand, T. boni bears similar branchiae (shape, size,
papillae) and thoracic uncini of type 3 (Lavesque et al. 2019: 159, g. 4A–C) to those
of A2; however, it bears abdominal uncini of type 1 instead of type 2.
Terebellides europaea Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa, 2019
Figs 1, 2, 3E, 9–10, 14A, 15, 16, 17C, 18A, 19A; Table 1; Suppl. material 1: Table S1;
Suppl. material 2: Table S2
Terebellides europaea Lavesque et al. 2019: 163–165, gs 1, 7, 8.
Species 6 – T. stroemii (non Sars, 1835). Nygren et al. 2018: 18–22, gs 6, 10.
Material examined. 31 specimens: Norwegian coast and shelf (GNM14625,
GNM14628, GNM15107, GNM15114, GNM15115, GNM15116, GNM15120,
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
26
GNM15121, GNM15122, GNM15123, GNM15124, GNM15125, GNM15126,
GNM15127, GNM15128, ZMBN116334, ZMBN116335, ZMBN116343,
ZMBN116344, ZMBN116346, ZMBN116347); Irish Sea (ZMBN116336,
Figure 14. STM photographs of live specimens of several Terebellides species in lateral view. A Terebellides
europaea Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa, 2019 (ZMBN 116343) B Terebellides
ronningae sp. nov. (ZMBN 116349) C , D Terebellides norvegica sp. nov. (GNM 15131 and GNM 15130
respectively). Abbreviations: babv – branchial aerent blood vessel; bbv – branchial blood vessel; bdl –
branchial dorsal lobe; bst – branchial stem; bvl – branchial ventral lobes; cbh – contractile branchial heart;
dg – digestive gland; – fore intestine; fs – fore stomach; hs – hind stomach; loli – lower lip; oes – oe-
sophagus; ooc – oocytes; tm – tentacular membrane.
New species of Terebellides from North East Atlantic 27
ZMBN116337, ZMBN116338, ZMBN116339, ZMBN116340, ZMBN116341,
ZMBN116342).
GenBank accession numbers of material examined (COI). MG025072,
MG025073, MG025074, MG025075, MG025076, MG025077, MG025078,
MG025079, MG025080, MG025081, MG025082, MG025083, MG025084,
MG025085, MG025086, MG025087, MG025088, MG025089, MG025090,
MG025091, MG025092, MG025093, MG025094, MG025095, MG025096,
MG025097, MG025098, MG025099, MG025100, MG025101, MG025102,
MG025103, MG025104. Paratypes (not examined): MN207179, MN207181. Ad-
ditional sequences (material not examined): MN207180, MN207182.
Diagnostic features of type material. Complete individuals ranging from 17.0–
46.0 mm in length and 2.0–5.0 mm in width (Fig. 17C). Branchial dorsal lobes la-
mellae provided with well-developed anterior papillary projections (Fig. 15C). Ventral
branchial lobes normally hidden by dorsal ones (Figs 3E, 15B, 19A) but sometimes
discernible below (Fig. 14A). Lateral lappets and dorsal projection on thorax present
on TC1–TC4 (Fig. 16A) or TC2–TC3 in (Fig. 15A). Geniculate chaetae acutely bent
(Fig. 16B). Ciliated papilla dorsal to thoracic notopodia not observed (Figs 15A, 16A).
oracic uncini in one or two rows (Fig. 16C) with rostrum/capitium length ratio for
approximately 2 : 1 (Fig. 16D), and capitium with a rst row of four medium-sized
teeth, followed by several smaller teeth. Abdomen with 29–38 uncinigers provided
with type 2 uncini (Fig. 16E). Epibiont ciliates observed in some specimens (Fig. 16F).
Nucleotide diagnostic features. All sequences belonging to T. europaea share the
unique apomorphic nucleotide in position 240 (C) of the alignement.
Type locality. Bay of Brest (Brittany, France) (Lavesque et al. 2019).
Distribution and bathymetry. Bay of Biscay (Lavesque et al. 2019); Kattegat,
Skagerrak, North Sea, Irish Sea, Celtic Sea and Norwegian coast and shelf, 8–173 m
deep (Nygren et al. 2018) (Figs 9, 10, 18A; Suppl. material 1: Table S1). Lavesque et
al. (2019) included the Ría de Ferrol (Galicia, NW Spain) as part of the Bay of Biscay,
but this locality belongs to the northern Galician Rias that are out of the western limit
of this bay.
Remarks. is species is characterised by the combination of the following fea-
tures: presence of papillary projections over the edge of the anterior border of dorsal
branchial lamellae, lack of ciliated papilla dorsal to thoracic notopodia, thoracic uncini
of type 3 and abdominal uncini of type 2. e original description states that body
length is less than 17 mm, but maximal length of specimens examined here was up to
46.0 mm. Examination of live and preserved specimens has revealed that the size ratio
between the ventral and dorsal branchial lobes is similar in all specimens; however,
their arrangement diers among specimens, i.e., the ventral lobes are visible in some
while in others are hidden behind the dorsal lobes.
Terebellides europaea was misidentied as T. stroemii by Nygren et al. (2018; spe-
cies 6) due to their morphological similarities and coexistence near the type locality
of the latter (Fig. 9). Nevertheless, Lavesque et al. (2019) found that members of spe-
cies 6 have papillae on the edge of the dorsal branchial lobes, unlike the neotypes of
T.stroemii described by Parapar and Hutchings (2014). Molecular analyses show that
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
28
the sequences of specimens found in the Bay of Biscay belong to species 6 (Lavesque et
al. 2019); examination of all specimens also conrmed the presence of the aforemen-
tioned papillae. Moreover, T. europaea is generally found in bottoms above 100 m deep
while T. stroemii is present in deeper environments (>100 m) (Fig. 9).
Figure 15. Terebellides europaea Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa, 2019 (species
6; non-type specimens, GNM15116 and GNM15118), SEM micrographs. A anterior end, right lateral
view B buccal tentacles and branchiae, left lateral view C branchial lamellae, detail. Abbreviations: bdl
– branchial dorsal lobe; bdltp – branchial dorsal lobe terminal papilla; blp – branchial lamellae papillae;
bst – branchial stem; bt – buccal tentacles; bvltp – branchial terminal lobe terminal papilla; cr – ciliary
row; dpn – dorsal projection of notopodium; gc – geniculate chaetae; gr – glandular region; loli – lower
lip; SG – segment; TC – thoracic chaetiger; tll – thoracic lateral lobes.
New species of Terebellides from North East Atlantic 29
In the 37 sequences analysed attributed to this species (see Suppl. material 2: Ta-
ble S2), there were ten haplotypes showing 0–0.8% of intraspecic divergence, and a
minimum of 8.8% uncorrected genetic distance with members of the closest relative,
T. ronningae sp. nov.
Terebellides ronningae sp. nov.
http://zoobank.org/7A447FDE-5934-483F-95F3-D178A0857A4A
Figs 1, 2, 3F, 9, 10, 14B, 17D, 18B, 19B, 20, 21, 28C; Table 1; Suppl. material 1:
Table S1; Suppl. material 2: Table S2
Species 7 – Nygren et al. 2018: 18–22, gs 5, 6, 10, Suppl. material 1: Table S1.
Material examined. Type material. Holotype: ZMBN116357. Paratypes (8 specs):
Norwegian coast (ZMBN 116350, ZMBN 116352, ZMBN 116353, ZMBN 116354,
ZMBN 116355, ZMBN 116356, ZMBN 116358, ZMBN 116359); Skagerrak
(ZMBN 116348, ZMBN 116349).
Holotype. Complete specimen, 19.0 mm long and 2.0 mm width (Figs 3F, 19B).
GenBank accession numbers of material examined (COI). Holotype:
MG025114; Paratypes: MG025105, MG025106, MG025107, MG025109,
MG025110, MG025111, MG025112, MG025113, MG025115, MG025116.
Additional material: MG025108,
Diagnostic features of type material. Complete individuals ranging from 12.0–
35.0 mm in length and 1.5–3.0 mm in width (Fig. 17D). Branchial dorsal lobes
lamellae with poorly-developed anterior papillary projections (Fig. 20C). Ventral
branchial lobes hidden (Fig. 20A) or not (Figs 3F, 19B) by dorsal ones. Lateral lap-
pets and dorsal projection ill-dened, only slightly developed on TC2 (Fig. 20A).
Geniculate chaetae acutely bent (Fig. 21A, B) and with very low capitium. Ciliated
papilla dorsal to thoracic notopodia not observed. oracic uncini in one row with
rostrum/capitium length ratio of approximately 2 : 1, and capitium with a rst row
of four or ve (sometimes six) large-sized teeth, followed by several progressively
smaller teeth (Fig. 21C–E). Abdomen with 24–35 uncinigers with type 2 uncini
(Figs 21F, 28C).
Nucleotide diagnostic features. All sequences of T. ronningae sp. nov. share the
unique apomorphic nucleotides in positions 129 (G), 399 (G) and 435 (G).
Type locality. Hordaland, Lyseord (Norway); 25–47 m deep (Figs 10, 18B).
Distribution and bathymetry. Norwegian coast and shelf, Skagerrak; 25–188 m
deep (Nygren et al. 2018) (Figs 9, 18B; Suppl. material 1: Table S1).
Etymology. is species is named after Dr. Ann-Helén Rønning, Head Engineer
of the Department of Technical and Scientic Conservation, Natural History Mu-
seum–NHMO (Oslo), for her help and friendship.
Remarks. Terebellides ronningae sp. nov. is characterised by the lack of ciliated
papilla dorsal to thoracic notopodia and the presence of papillary projections pointing
over the edge of the dorsal anterior border of branchial lamellae, thoracic uncini of
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
30
type 1 and abdominal of type 2 (Table 1). It is distinguished from the closest relatives
of subgroup A2 by the presence of thoracic uncini type 1 instead of type 3 (Table 1).
Specimens examined with SEM bear thoracic uncini with rostrum bendings (Fig.21C)
similar to those of other NEA species (see Discussion for T. stroemii). e branchial ventral
lobes show variability in their arrangement that is similar to that of T. europaea.
Figure 16. SEM images, Terebellides europaea Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa,
2019 (species 6; non-type specimen, GNM15116). A TC1 to TC4, lateral view B TC6 (TU1), geniculate
chaetae C thoracic double row of uncini D thoracic uncinus, capitium, upper view E abdominal uncini
F epibiont ciliate (position pointed by arrowhead) attached near TC5 nephridial papilla. Abbreviations:
cap – capitium; dpn – dorsal projection of notopodium; ros – rostrum; TC – thoracic chaetiger.
New species of Terebellides from North East Atlantic 31
Twelve sequences (see Suppl. material 2: Table S2), in ten haplotypes, have been
attributed to this species (Nygren et al. 2018). ey show 0–0.6% intraspecic diver-
gence, and a minimum of 8.8% uncorrected genetic distance, its closest relative being
T. europaea (Fig. 2).
Terebellides norvegica sp. nov.
http://zoobank.org/659C513E-01DD-43A0-AC29-D1A744EDA9B0
Figs 1, 2, 3G, 9, 10, 14C–D, 17E, 18C, 19C, 22, 23; Table 1; Suppl. material 1: Table
S1; Suppl. material 2: Table S2
Species 8 – Nygren et al. 2018: 18–22, gs 5, 6, 10, Suppl. material 1: Table S1.
Material examined. Type material. Holotype: ZMBN116378. Paratypes (36 specs):
Barents Sea (ZMBN11636, ZMBN116365, ZMBN116366, ZMBN116367);
Norwegian coast (GNM146323, NTNU-VM61388, NTNU-VM61389, NTNU-
Figure 17. Relationship between number of abdominal chaetigers and body length (complete speci-
mens) for Terebellides species described in this work.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
32
VM61390, NTNU-VM66569, NTNU-VM66573, NTNU-VM66574, NTNU-
VM68197, NTNU-VM68198, ZMBN116362, ZMBN116363, ZMBN116368,
ZMBN116369, ZMBN116370, ZMBN116371, ZMBN116372, ZMBN116373,
ZMBN116374, ZMBN116375, ZMBN116376, ZMBN116377, ZMBN116379,
ZMBN116380, ZMBN116381, ZMBN116382, ZMBN116383, ZMBN116384);
Skagerrak (GNM14637, GNM15131, GNM15232, GNM15134, ZMBN116361).
Holotype. Complete specimen, 19.0 mm long and 1.5 mm wide (Figs 3G, 19C);
female with oocytes in body cavity.
GenBank accession numbers of material examined (COI). Holotype:
MG025148. Paratypes: MG025119, MG025120, MG025122, MG025124,
MG025126, MG025127, MG025128, MG025129, MG025131, MG025132,
MG025134, MG025135, MG025136, MG025137, MG025138, MG025139,
MG025140, MG025141, MG025142, MG025143, MG025144, MG025145,
MG025146, MG025147, MG025149, MG025151, MG025152, MG025153,
MG025154, MG025155, MG025156. Additional material: MG025117, MG025118,
MG025121, MG025123, MG025125, MG025130, MG025133, MG025150.
Diagnostic features of type material. Complete individuals ranging from 20.0–
50.0 mm in length and 1.2–5.0 mm in width (Fig. 17E). Branchial dorsal lobes lamel-
lae with well-developed anterior papillary projections (Fig. 22C). Ventral branchial
lobes hidden (Figs 19C, 22A, B) or not (Fig. 3G) by dorsal ones. Lateral lappets and
dorsal projection low marked, only partially present on TC2 (Fig. 22A, D). Genicu-
late chaetae acutely bent, with poorly marked capitium (Fig. 23A, B). Ciliated papilla
dorsal to thoracic notopodia not observed. oracic uncini in one row (Fig. 23C) with
rostrum/capitium length ratio of approximately 2 : 1 and capitium with a rst row
of two or three medium-sized teeth, followed by several progressively smaller teeth
(Fig.23D). Abdomen with 29–38 chaetigers with type 2 uncini (Fig. 23E). Epibiont
ciliates observed in some specimens (Fig. 23F).
Nucleotide diagnostic features. All sequences of T. norvegica sp. nov. share the
unique apomorphic nucleotides in positions 48 (C) and 285 (G) of the alignement.
Type locality. Rogaland (Norway); at depths of between 226 and 242 m (Fig.18C).
Distribution and bathymetry. Barents Sea, Norwegian coast, Skagerrak; 190–
1,268 m deep (Nygren et al. 2018) (Figs 9, 18C; Suppl. material 1: Table S1).
Etymology. e name of the new species refers to the country where members of this
lineage were found, along the Norwegian coast from the Barents Sea to the Skagerrak Strait.
Remarks. Terebellides norvegica sp. nov. is characterised by the presence of mar-
ginal papillae in the anterior region of branchial dorsal lamellae, thoracic uncini
of type 3 and abdominal uncini of type 2, and by lacking ciliated papilla dorsal to
thoracic notopodia (Table 1). ese features are shared with species of subgroup
A2: T.europaea, T. ronningae sp. nov. and T. scotica sp. nov. (Table 1), apart from
the thoracic uncini type that is dierent in T. ronningae sp. nov. Furthermore, T.
norvegica sp. nov., T. europaea and T. scotica sp. nov. also show the same variability
in whether ventral branchial lobes are hidden or not by dorsal lobes. erefore, it
seems that members of these three species can only be distinguished according to
New species of Terebellides from North East Atlantic 33
the DNA sequences. However, they show little overlapping in their geographic dis-
tribution and bathymetric ranges (Figs 9, 18A, C, D). Terebellides norvegica sp. nov.
inhabits deep-water habitats (mostly below 200m) along the Norwegian coast; its
distribution only overlaps with that of T. europaea in southern waters (Skagerrak).
As stated before, T. europaea has a broader distribution reaching to the South NW
Iberian Peninsula and is generally found in shallower habitats (<100 m) similarly
Figure 18. Geographic distribution of A T. europaea Lavesque et al., 2019, B T. ronningae sp. nov.,
CT.norvegica sp. nov., D T. scotica sp. nov. Yellow frame showing Hordaland (Fig. 10).
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
34
to T. scotica sp. nov. Ciliate epibionts attached over dorsal body surface were also
observed (Fig. 23F).
On the other hand, the internal anatomy of T. norvegica sp. nov. has been exam-
ined by transparency in one alive specimen (Fig. 14D). e digestive tract is divided
in an oesophagus clearly distinguishable between TC1 and TC3, that is followed by
the stomach and the associated digestive gland (TC4–TC7) and then by the intestine
(from TC11). Regarding the circulatory system, a double dorsal blood vessel is present
in anterior body end from which arise four aerent vessels at the level of branchial
stem and into the branchiae; the coelomic cavity bears oocytes from TC11. All these
internal features agree with those described by Jouin-Toulmond and Hourdez (2006)
and Parapar and Hutchings (2014) for other species of the genus.
Forty sequences (see Suppl. material 2: Table S2), in 33 haplotypes, have been
attributed to this species (Nygren et al. 2018). ey show 0–3.1% intraspecic diver-
gence, larger than in other Terebellides species, and a minimum of 10.5% uncorrected
genetic distance, with its closest relative being T. scotica sp. nov. (Fig. 1).
Terebellides scotica sp. nov.
http://zoobank.org/74511F62-C57D-4BF7-8B63-48997EB1C8E9
Figs 1, 2, 3H, 9, 17F, 18D, 19D, 24, 25; Table 1; Suppl. material 1: Table S1; Suppl.
material 2: Table S2
Species 9 – Nygren et al. 2018: 18–22, gs 5, 6, 10, Suppl. material 1: Table S1.
Material examined. Type material. Holotype: ZMBN116385. Paratypes (3 specs),
North Sea (ZMBN 116382, ZMBN 116386, ZMBN 116387).
Holotype. Complete specimen, 45.0 mm long and 4.5 mm width (Fig. 3H, 19D).
Additional material. SMA_BR_23 (GenBank number: MN207187) and SMA_
BR_33 (GenBank number: MN207188) of Terebellides sp. in Lavesque et al. (2019)
(Suppl. material 1: Table S1).
GenBank accession numbers of material examined (COI). Holotype:
MG025157. Paratype: MG025158.
Diagnostic features of type material. Complete individuals ranging from 6.0–
45.0 mm in length and 1.0–4.0 mm in width (Figs 9, 17F). Branchial dorsal lobes
lamellae provided with low anterior papillary projections (Fig. 24B). Ventral branchial
lobes hidden (Fig. 24A) or not (Figs 3H, 19D) by dorsal ones. Lateral lappets and
dorsal projection low marked being only discernible on TC1–3 (Fig. 24A). Geniculate
chaetae acutely bent and provided with hardly distinguishable capitium (Fig. 25A, B).
Ciliated papilla dorsal to thoracic notopodia not observed. oracic uncini in one or
two rows (Fig. 25C) with rostrum/capitium length ratio of approximately 2 : 1, and
capitium with a rst row of 2–4 medium-sized teeth, followed by several progressively
smaller teeth (Fig. 25D, E). Abdomen with 18–33 uncinigers provided with type 2
uncini (Fig. 25F).
New species of Terebellides from North East Atlantic 35
Nucleotide diagnostic features. ere are no unique apomorphic nucleotides in the
fragments of COI analysed for T. scotica sp. nov., when considering all Terebellides species
present in the NEA (Suppl. material 2: Table S2). However, when comparing homolo-
gous nucleotide positions with members of only Group A (192 sequences in the COI
alignment), the following autapomorphies arise: 279 (G), 444 (C), 517 (A), 630 (C).
Type locality. East Orkney Island; 85 m deep (Fig. 18D).
Distribution and bathymetry. North Sea; 48–111 m deep (Nygren et al. 2018)
(Fig. 18D; Suppl. material 1: Table S1). Two specimens (Terebellides sp. in Lavesque et
al. 2019) were identied as T. scotica sp. nov. according to molecular sequences; Bay of
Brest (France), in rhodolith beds, 5 m deep.
Figure 19. Line drawings of several Terebellides species. A Terebellides europaea Lavesque, Hutchings,
Dae, Nygren & Londoño-Mesa, 2019 (species 6; non-type specimen, GNM14628), anterior end, left
lateral view B Terebellides ronningae sp. nov. (species 7; holotype, ZMBN116357), anterior end, left lateral
view C Terebellides norvegica sp. nov. (species 8; holotype, ZMBN416378), anterior end, right lateral view
D Terebellides scotica sp. nov. (species 9; holotype, ZMBN116385), anterior end, left lateral view. Abbre-
viations: bdl – branchial dorsal lobe; bvl – branchial ventral lobe; TC – thoracic chaetiger.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
36
Etymology. is new species is named after Scotland, since its type locality is in
the Scottish Orkneys Islands.
Remarks. Among A2 species, T. scotica sp. nov., T. europaea and T. norvegica sp.
nov. have thoracic uncini of type 3 and show ventral branchial lobes that may be
Figure 20. Terebellides ronningae sp. nov. (species 7; paratypes, ZMBN 116349 and ZMBN 116353),
SEM micrographs. A anterior end, right lateral view B dorsal branchial lobes, terminal papilla C anterior
branchial lamellae papillae D TC4, nephridial papilla (framed: detail). Abbreviations: bdl – branchial dor-
sal lobe; blp – branchial lamellae papillae; bvltp – branchial ventral lobe terminal papilla; gr – glandular
region; np – nephridial papilla; TC – thoracic chaetiger.
New species of Terebellides from North East Atlantic 37
hidden in between dorsal lobes in some specimens. As stated previously, these species
can only be distinguished according to DNA sequences.
e specimen studied under SEM shows a small knob near the notopodial lobe
of TC1 (nop, Fig. 24C); its biological role is unknown and it may correspond to
an artefact.
Figure 21. Terebellides ronningae sp. nov. (species 7; paratypes, ZMBN 116349 and ZMBN 116353),
SEM micrographs. A TC6 (TU1), geniculate chaetae B geniculate chaeta, detail (framed in A) C–Etho-
racic uncini (arrows in C pointing to rostrum curved at distal end) F abdominal uncini. Abbreviations:
cap – capitium; ctr1/2 – rst and second rows of capitium teeth; ros – rostrum.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
38
Two dierent sequences (see Suppl. material 2: Table S2; 0.2% distance) have
been attributed to this species (Nygren et al. 2018). As stated above, the closest NEA
congener is T. norvegica sp. nov., at 10.5% genetic distance.
SubGroup A3
Analyses of molecular data recovered a strongly supported subgroup A3 (Figs 1, 2;
Nygren et al. 2018). is group is composed by species 20 + 28 (= T. bigeniculatus),
and species 21; the latter will be described elsewhere (Gaeva and Jirkov, pers. comm.)
but some comments are also provided here (Terebellides sp. 2 hereafter).
Character/s present only in subgroup A3
• Branchiae stroemii-type but irregular in many specimens, with all four lobes
slightly fused; ventral lobes shorter and slimmer than dorsal ones and not hidden
in between.
• First thoracic neuropodia on TC5; several sharply bent, acute-tipped genicu-
late chaetae present in two chaetigers (TC5 and TC6) (Fig. 26C).
Character/s shared with subgroup A1
• Border of anterior region of dorsal branchial lamellae not provided with papil-
lary projections.
• Ciliated papilla present, dorsal to thoracic notopodia (Fig. 27B).
• oracic uncini type 3 (Fig. 26E).
Character/s shared with subgroup A2
• None (Table 1).
Character/s variable within subgroup A3
• None (Table 1).
Terebellides bigeniculatus Parapar, Moreira & Helgason, 2011
Figs 1, 2, 3D, 4D, 8D, 9, 10, 26, 28E; Table 1; Suppl. material 1: Table S1; Suppl.
material 2: Table S2
Terebellides bigeniculatus Parapar, Moreira & Helgason, 2011: 6–10, gs 1b, 4–7.
Species 20 + 28 Nygren et al. 2018: 18–22, gs 6, 10.
Type locality. O North West Iceland; 333 m deep (Parapar et al. 2011).
New species of Terebellides from North East Atlantic 39
Material examined. 6 specimens: Barents Sea (ZMBN 116511); Norwegian
coast and shelf (ZMBN 116417, ZMBN 116510, ZMBN 116512, ZMBN 116513,
ZMBN 116514).
Figure 22. Terebellides norvegica sp. nov. (species 8; paratypes, GNM15130 and GNM15134), SEM
micrographs. A anterior end, left lateral view B branchial lobes, ventral view C anterior dorsal branchial
lamellae and papillae D TC4 to TC6, lateral view. Abbreviations: abl – anterior branchial lobe; bdl –
branchial dorsal lobe; bdl – branchial dorsal lobes fusion line; bdltp – branchial dorsal lobe terminal
papilla; blp – branchial lamellae papillae; bt – buccal tentacles; dpn – dorsal projection of notopodium;
gc – geniculate chaetae; gr – glandular region; loli – lower lip; np – nephridial papilla; TC – thoracic
chaetiger; tll – thoracic lateral lappets.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
40
Additional material. T. bigeniculatus: Holotype (IIH 24923) and 5 paratypes
(IINH 24925) (Suppl. material 1: Table S1).
GenBank accession numbers of material examined (COI). MG025318,
MG025319, MG025351, MG025352, MG025353, MG025354, MG025355.
Diagnostic features of studied material. Complete individuals ranging from
10.0–24.0 mm in length. Branchiae clearly tting with type 1 only in some specimens,
irregular in others; dorsal lobes lamellae not provided with papillary projections. Lat-
eral lappets from TC1-TC5 and well-marked dorsal projection of notopodia in TC3
(Figs 3D, 4D). Geniculate chaetae present in TC5 and TC6 (Fig. 26C), acutely bent
and provided with hardly distinguishable capitium (Fig. 26D). Ciliated papilla dorsal
to thoracic notopodia. oracic uncini of type 3, with rostrum/capitium length ratio
of approximately 2 : 1 (Fig. 26E), and capitium with a rst row of four medium-sized
teeth, followed by several progressively smaller teeth. Abdomen with 20–25 chaetigers
provided with type 1 uncini (Figs 26F, 28B).
Material examined herein corresponds to a few small and incomplete specimens.
erefore, the list of diagnostic characters given was developed with the aid of the type
specimens re-examined and the original description.
Nucleotide diagnostic features. All sequences of T. bigeniculatus share the unique
apomorphic nucleotides in positions 67 (G) and 138 (G) of the alignement.
Distribution and bathymetry. Around Iceland at both sides of the GIF Ridge;
179–968 m deep (Parapar et al. 2011). Material examined here also conrms its pres-
ence in shallow and deep bottoms of Norway and Barents Sea (Fig. 8D).
Remarks. In some of the species delimitation analyses performed, Nygren et al.
(2018) were able to distinguish between two closely related lineages, clades 20 and
28, but some analyses of nuclear and mitochondrial datasets lump them together in a
single entity. Given that all specimens examined share characteristic features that are
distinct from other Terebellides species studied herein, clades 20 and 28 have been con-
sidered in the present study as a single species and identied as T. bigeniculatus.
As stated above, the sequenced specimens are small and not well preserved, hin-
dering the examination of relevant morphological features with taxonomic value (i.e.,
branchial type). However, this species is characterised by having geniculate chaetae on
TC5 and TC6 instead of only on one chaetiger (Parapar et al. 2011: 7) as in congeners
listed in the Key of the present study. Furthermore, T. bigeniculatus is characterised by
the low fusion of the usually irregularly-shaped branchial lobes (Parapar et al. 2011:
7–8, gs 4, 5a, b), ventral lobes are not obscured by dorsal ones, the lack of marginal
papillae in the anterior region of the branchial dorsal lamellae, the presence of ciliated
papilla dorsal to thoracic notopodia, and by having thoracic uncini of type 3 and ab-
dominal uncini of type 1. However, it is likely that the irregular shape of the branchiae
may correspond to an artefact related to xation/preservation; other specimens show
instead well-dened branchiae that agree with those of A1 and A2 species but less de-
veloped (Fig. 26A, B; Parapar et al. 2011: 8, g. 5a). Regarding the four branchial types
as dened by Parapar et al. (2016c), branchiae of T. bigeniculatus might correspond
therefore to type 3 but with lobes showing a more variable shape.
New species of Terebellides from North East Atlantic 41
e original description states that nephridial papillae are located on TC3–TC4
or TC4–TC5 (Suppl. material 1: Table S1; Parapar et al. 2011: 7–9, gs 5c, 6d). Ex-
amination of the holotype and several paratypes conrmed that pores are on TC4 and
TC5, as in other Group A species. Nephridial pores, as found in most Terebellides spe-
cies, are usually at and can be easily overlooked when examined with STM and even
Figure 23. Terebellides norvegica sp. nov. (species 8; paratypes, GNM15130 and GNM15134), SEM
micrographs. A TC6 (TU1), geniculate chaetae B detail of geniculate chaeta, arrow pointing to capitium
(framed in A) C simple row of uncini D thoracic uncinus, capitium E abdominal uncini F ciliate epibi-
onts. Abbreviations: ctr1 – rst row of capitium teeth.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
42
SEM; those of T. bigeniculatus are larger and easier to distinguish comparatively with
STM (Parapar et al. 2011: 9, g. 6d).
Members of species 21 (see below, as Terebellides sp. 2) also bear geniculate chaetae
in two chaetigers; this feature had been considered as unique to T. bigeniculatus regard-
ing other NEA species. However, species 21 is present in Arctic waters (cf. Nygren et al.
Figure 24. Terebellides scotica sp. nov. (species 9; paratype, ZMBN 1163887), SEM micrographs.
Aanterior end, left lateral view B anterior dorsal branchial lamellae and papillae C TC1 and TC2, lateral
view (framed in A). Abbreviations: bdl – branchial dorsal lobe; blp – branchial lamellae papillae; dpn –
dorsal projection of notopodium; loli – lower lip; nop – notopodial protuberance; TC – thoracic chaetiger.
New species of Terebellides from North East Atlantic 43
2018: g. 6) while the distribution of members of species 20 + 28 and identied here
as T. bigeniculatus agrees with that of the type specimens (see Fig. 8D).
Terebellides sp. 2
Figs 1, 2, 9, 27; Table 1; Suppl. material 1: Table S1; Suppl. material 2: Table S2
Species 21 Nygren et al. 2018: 18–22, gs 5, 6, 10.
Material examined. 4 specimens: Barents Sea. ZMBN 116481; ZMBN 116486.
Remarks. As explained for Terebellides sp. 1, two specimens were examined under
SEM; these share with T. bigeniculatus the irregular shape of branchial lobes (Fig. 27A),
the presence of geniculate chaetae on TC5 and TC6 (Fig. 27C–E) and abdominal unci-
ni of type 1B (Fig. 27G). ey share with subgroup A1 the presence of one ciliated pa-
pilla dorsal to thoracic notopodium (Fig. 27B) and thoracic uncini of type 3 (Fig.27F).
On the other hand, species 18 and 19 of A1 (not described here because of the few
specimens being available) and 23 (A4) have a geographic distribution similar to that
of T. bigeniculatus but their position in the cladogram by Nygren et al. (2018: g. 5)
suggests that they may not bear geniculate chaetae in two chaetigers.
ere are no unique diagnostic nucleotide positions that are shared by the two
haplotypes (in 18 sequences) in COI. Eighteen sequences, in one single haplotype,
have been attributed to this species (Nygren et al. 2018). Members of this species
show a minimum of 3.0% uncorrected genetic distance, with its closest relative being
T.bigeniculatus (Fig. 1).
Key to European species of Terebellides
e following key of European Terebellides species is based on Lavesque et al. (2019)
and updated by including all species of Group A (in bold) apart from those that will be
described elsewhere. e known geographic or bathymetric distribution has been used
when there is a lack of discriminatory morphological characters between some species
(e.g., subgroup A2).
1 Geniculate chaetae on TC5 and TC61 ...........................................................
....... (subgroup A3) T. bigeniculatus Parapar, Moreira & Helgason, 2011
– Geniculate chaetae on TC6 only ................................................................. 2
2 Branchial lamellae margins lacking papillae2 ............................................... 3
– Branchial lamellae margins with papillae ...................................................11
3 Lower branchial lobes with long posterior projections as laments ..............4
– Lower branchial lobes with short posterior projections ................................5
1 is character is also present in clade 21, which will be described elsewhere.
2 is character is also present in clade 12, which will be described elsewhere.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
44
4 Glandular region on TC3 present; branchial lamellae pointed; notochaetae from
TC1 longer than following ones; dorsal papillae absent .......................................
...T. parapari Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa, 2019
– Glandular region on TC3 absent; branchial lamellae rounded; all notochaetae
equal-sized; dorsal papillae present ................................................................
..................................... T. shetlandica Parapar, Moreira & O’Reilly, 2016
5 Ventral white band present on TC4 after MG staining ...............................6
– No distinct pattern on TC4 after MG staining ...........................................7
6 Large species (>30 mm in length); 5th branchial lobe present; notochaetae of
TC1 similar to following ones; main fang of thoracic uncini straight ............
................................................................................ T. gracilis Malm, 1874
– Small species (<20 mm in length); 5th branchial lobe absent; notochaetae of TC1
absent or shorter than following ones; main fang of thoracic uncini ‘eagle head’-
shaped ..................................................................................................................
.... T. ceneresi Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa, 2019
7 First notopodia and notochaetae longer than following ones .........................
......................................... T. mediterranea Parapar, Mikac & Fiege, 2013
– First notopodia and notochaetae similar or shorter than following ones ...... 8
8 Large-sized species (>50 mm); dorsal rounded projections on TC1–TC5 con-
spicuous ............................................................................ (subgroup A1) 9
– Small-sized species (<20 mm); dorsal rounded projections on TC1–TC5 ab-
sent; main fang of thoracic uncini straight ................................................10
9 Abdominal uncini type 13 ..... T. kongsrudi sp. nov. and T. bakkeni sp. nov.
– Abdominal uncini type 23 ..........................................T. stroemii Sars, 1835
10 5th branchial lobe absent .................................... T. atlantis Williams, 1984
– 5th lobe present .............................................................................................
....T. gralli Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa, 2019
11 Glandular region on TC3 round or oval ...................................................12
– Glandular region on TC3 otherwise ..........................................................13
12 Glandular region on TC3 stained white; branchial lamellae with rounded pa-
pillae; TC1–3 without conspicuous dorsal projection ....................................
...T. lilasae Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa, 2019
– Glandular region on TC3 stained blue; branchial lamellae with conical papil-
lae; TC1–3 with conspicuous dorsal projection .............................................
...T. boni Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa, 2019
13 Most branchial lamellae with marginal papillae; upper lip elongated ...................
...T. resomari Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa, 2019
– Only anterior branchial lamellae with marginal papillae; upper lip not elon-
gated ................................................................................ (subgroup A2) 14
14 oracic uncini type 14 ............................................... T. ronningae sp. nov.
– oracic uncini type 34 ............................................................................. 15
3 Types of abdominal uncini as described in this work.
4 Types of thoracic uncini sensu Parapar et al. (2020).
New species of Terebellides from North East Atlantic 45
15 Deep-water species; mostly below 200 m deep .............T. norvegica sp. nov.
– Shallow-water species; mostly above 100 m deep ......................................16
16 Present from Southern Norway to NW Iberian Peninsula ....................................
... T. europaea Lavesque, Hutchings, Dae, Nygren & Londoño-Mesa, 2019
– Present in the Shetland and Orkneys Islands and in Brittany ........................
.........................................................................................T. scotica sp. nov.
Discussion
Group A species: taxonomy and distribution
e comprehensive study by Nygren et al. (2018) revealed that the genus Terebellides
holds a large species diversity in NEA waters regardless its morphological homogene-
ity. Over 25 molecular entities that meet the requirements to be recognized as species
were recovered forming four main and robust clades (A–D); Group A is composed, in
turn, by thirteen species. Among the latter, members of only three species were identi-
ed herein as current nominal species: T. stroemii, T. bigeniculatus, and T. europaea; the
remaining ten represent undescribed taxa.
Within Group A, three subgroups (A1–A3) can be dened based on molecular
data, being only A2 and A3 well supported and congruent among all molecular analy-
ses and datasets (Figs 1, 2; Nygren et al. 2018) but also by morphological features. A1
and A2 gather species morphologically similar to T. stroemii, while species included
in subgroup A3 share morphological features with T. bigeniculatus. e original de-
scription of T. stroemii by Sars (1835) lacks detailed specic diagnostic features as
are recognised nowadays in many closely related species, most of them described in
the last years. On the contrary, T. bigeniculatus belongs to a small group of species
bearing geniculate chaetae in two thoracic chaetigers (TC5 and TC6) instead of one
(TC6), a distinct morphological trait for the group; T. bigeniculatus was described
from deep Icelandic waters by Parapar et al. (2011), and only later reported NEA
by Nygren et al. (2018). Terebellides europaea was recently described after molecular
analyses by Lavesque et al. (2019) and ts within species of A1+A2. Other species from
NEA, namely T. gracilis, T. atlantis, T. williamsae, T. irinae and T. shetlandica Parapar,
Moreira & O’Reilly, 2016, dier from members of Group A in shape and body length,
ventral colouration in a number of thoracic chaetigers, branchiae shape and degree of
fusion and relative size of dorsal/ventral lobes (see Holthe 1986; Jirkov 2001; Parapar
et al. 2011, 2016c). e aforementioned species t either within groups B, C, or D
sensu Nygren et al. (2018) and will be dealt with in a forthcoming paper.
e characters considered to delineate morphologically the aforementioned sub-
groups (A1–A3) should be taken with care because there are limitations due to number
of specimens available to be studied and their condition of preservation. However,
considering the variety and origin of the material examined we were able to elucidate
some general patterns on taxonomy and distribution of the studied species. us, all
studied species seem quite homogeneous in terms of general body features and share
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
46
many characters; however, presence/absence of some macroscopic/microscopic char-
acters has allowed their organization in the subgroups proposed above. Nevertheless,
some species could not be dierentiated according to morphological characters but
genetic data. On the other hand, geographic distributions of species do not show ap-
parent gaps; some species have a wider distribution and were more frequent in samples
such as T.norvegica sp. nov. and T. kongsrudi sp. nov.; this suggests that many previous
Figure 25. Terebellides scotica sp. nov. (species 9; paratype, ZMBN 1163887), SEM micrographs. A TC6
(TU1), geniculate chaetae B detail of geniculate chaeta (arrow pointing to capitium) C double row of
thoracic uncini D, E thoracic uncini, capitium F abdominal uncini. Abbreviations: cap – capitium; ctr1
– rst row of capitium teeth; ros – rostrum.
New species of Terebellides from North East Atlantic 47
reports of T. stroemii in NEA might correspond to the aforementioned species. Other
species apparently show a more restricted distribution, i.e., T. bakkeni sp. nov. in north-
ern Norway or have their limit of distribution in southern Norway, as T. europaea.
Similarly, there are no gaps in the bathymetric distribution of species, but some seem
to appear typically at shallow depths, reaching the continental shelf (0–200 m) such as
Figure 26. Terebellides bigeniculatus Parapar, Moreira & Helgason, 2011 (species 20 + 28; non-type
specimens, ZMBN 116512 and ZMBM 116513), SEM micrographs. A anterior end, left lateral view
B branchiae, ventral view C TC5 and TC6 (framed: geniculate chaetae location) D geniculate chaeta
(framed in C) E thoracic uncini (framed: uncinus rostrum with curved distal end) F abdominal uncini.
Abbreviations: bdl – branchial dorsal lobe; TC – thoracic chaetiger.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
48
T.europaea, T. ronningae sp. nov. and T. scotica sp. nov. On the contrary, T. bigenicu-
latus and T. norvegica sp. nov. are found at depths of below 200 m while T. stroemii,
T.bakkeni sp. nov. and T. kongsrudi sp. nov. show a wider bathymetric distribution.
Given the morphological homogeneity, DNA sequences have been shown to pro-
vide advantageous data and support when it comes to species delineation in Terebellides.
e most informative markers in previous studies are COI and ITS (Nygren et al.
2018; Lavesque et al. 2019). In the present study, analyses have been mainly based
on mitochondrial COI, the universal barcoding gene, because it oers no ambiguities
in the alignment process, and is the most commonly used in molecular taxonomy in
annelids (e.g., Borda et al. 2013; Tomioka et al. 2016; Álvarez-Campos et al. 2017;
Aguado et al. 2019; Grosse et al. 2020) and other taxa (e.g., Kekkonen and Hebert
2014). After species delimitation, identication to the correct nominal species level is
ideal, as species names allow the communication, study, quantication, classication,
use and management of life on the planet. is has been the motivation of recognis-
ing unequivocal diagnostic nucleotides in specic positions for the species described
in the present study. As with morphological traits, molecular diagnostic characters are
tested continuously when additional intraspecic and interspecic variation within the
groups has been found. Nevertheless, and as pointed out by previous studies, diagnos-
tic nucleotides may be an eective and relatively simple way for species identication
(Rach et al. 2008; Wong et al. 2009).
Comparisons with other NE Atlantic Terebellides
Lavesque et al. (2019) described eight new species of Terebellides from continental
France considering an integrative taxonomy approach. ose species could be infor-
mally grouped in two assemblages:
1. Species similar to Group A sensu Nygren et al. (2018) regarding body colour
and shape, and branchiae features: T. boni, T. europaea, T. gentili, T. gralli and T. lilasae.
2. Species closer to groups B, C or D sensu Nygren et al. (2018): T. ceneresi,
T.parapari and T. resomari.
e rst ve species were already discussed above. Regarding the remaining three
species, only T. ceneresi was sequenced by Lavesque et al. (2019) and according to their
phylogenetic analyses, it is not related to any species of Group A; in fact, it diers
from Group A species: a) in having a very distinct MG staining pattern corresponding
to a solid stain manifested in the rst ten thoracic chaetigers, being lighter in TC4;
b) the anterior branchial lobe (5th lobe) is not present; c) the outer edge of branchial
lamellae bears tufts of cilia. ese characters would relate T. ceneresi to Group D sensu
Nygren et al. (2018). is species was described with ‘eagle head’-shaped thoracic un-
cini, which are similar to those of T. stroemii, T. ronningae sp. nov. and T. kongsrudi sp.
nov. as described here and T. stroemii sensu Parapar and Hutchings (2014). However,
as explained above (see Remarks for T. stroemii), the taxonomic value of this character
New species of Terebellides from North East Atlantic 49
should be viewed cautiously and its consistent presence across the three aforemen-
tioned species needs to be assessed.
Terebellides parapari diers from Group A species in the shape and arrangement
of branchial lobes that are free from each other, and by the presence of terminal la-
ment in ventral lobes. ese features and its short body length relate T. parapari to
Figure 27. Terebellides sp. 2 (species 21; ZMBN 116481 and ZMBN 116486), SEM micrographs. Aanterior
end, left lateral view B TC10, thoracic dorsal papilla (framed in A) C , D geniculate chaetae of TC5 and TC6
respectively (framed in A) E TC6, geniculate chaeta (arrow pointing to capitium teeth) Fthoracic uncinus
G abdominal uncini. Abbreviations: TC – thoracic chaetiger; tdp – thoracic dorsal papilla.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
50
T. shetlandica and Group B sensu Nygren et al. (2018). Finally, T. resomari is unique
among NEA Terebellides because of having “not well packed (separated) disposition of
the branchial lamellae” (Lavesque et al. 2019: 177, g. 18B) and therefore branchiae
seem lacking a dened shape. In addition, this species also shows the “upper lip very
elongated with convoluted margins” (Lavesque et al. 2019: 177, g. 18C), that was
also reported by Parapar et al. (2020) for Terebellides sp. from the Atlantic African
coast. erefore, these unusual features do not allow for the allocation of T. resomari to
any group as dened by Nygren et al. (2018).
Discriminant vs. non-discriminant body characters in species delineation
is study has revealed that some of the traditionally morphological-based taxonomic
characters are not appropriate for Terebellides species identication. e number of
species in the genus is now large and their morphological homogeneity high. Regard-
ing Group A, two macroscopic characters have, however, been useful: 1) presence of
geniculate chaetae in one or two chaetigers (A1+A2 vs A3), 2) presence of papillary
projections in the border of branchial lamellae (A2 vs A1+A3). On the contrary, we
found that the development of lateral lappets and the presence of a dorsal projection
on the anterior thoracic notopodia seem dependent on size/age and preservation, and
therefore these characters should be taken with care for species identication. Simi-
larly, the species in Group A seem quite homogeneous when considering branchial
morphology, particularly within A1 and A2. Some of the morphological dierences
observed between Terebellides species rely in the exposure of the ventral lobes (hidden
or not behind the dorsal lobes). However, we have also observed some degree of vari-
ability between specimens belonging to the same species and could be due to size or
the contraction of specimens after xation.
Morphology of thoracic and abdominal uncini seems useful for species identi-
cation; such features need to be examined under SEM and are being considered in
descriptions of Terebellides in the last years. Recently, Parapar et al. (2020) describe
tentatively several types of thoracic uncini. e uncini of the NEA species treated here
are quite similar because of their phylogenetic proximity, being T. ronningae sp. nov.
the only species that dier in uncini type from other congeners of subgroup A2. ere
were, however, dierences in abdominal uncini that correspond to two morphologies
that agree well, in turn, with groups of species as dened by molecular-based phylo-
genetic analyses. Following Parapar et al. (2020), we propose here the use of similar
criteria for the characterization of abdominal uncini, that are based on the rostrum
vs. capitium length ratio (RvC), and the number of the capitium teeth and their rela-
tive size. erefore, considering our results after SEM examination and other previous
work, two main types of abdominal uncini can be dened:
Type 1
Capitium of ca. 0.7 of total length of rostrum (RvC = 1/0.7); capitium simple,
composed of a few wide denticles, being 3(5) in rst row and 1(2) in a second row
New species of Terebellides from North East Atlantic 51
(Fig.28A, B). In turn, Type 1A and 1B would dier in number of capitium teeth, be-
ing higher in B (Fig. 28A, B, Table 1). is typology is present in T. bakkeni sp. nov.
(1A), T. kongsrudi sp. nov. (1A) and T. bigeniculatus (1B; see also Parapar et al. 2011:
g. 7f). Type 1 uncini are apparently also present in T. gracilis (sensu Parapar et al.
2011, 2013), T. narribri Schüller & Hutchings, 2010, T. mediterranea Parapar, Mikac
& Fiege, 2013, T. toliman Schüller & Hutchings, 2013, T. ectopium Zhang & Hutch-
ings, 2018, T. kirkegaardi Parapar, Martin & Moreira, 2020 and T. longiseta Parapar,
Martin & Moreira, 2020 (Parapar et al. 2013, 2020; Schüller and Hutchings 2010,
2013; Zhang and Hutchings 2018).
Type 2
Capitium of almost same length as rostrum (RvC = 1/0.9); capitium much complex
than in Type 1, composed of a rst row of 4(5) denticles and a variable number of
teeth in two more rows with decreasing number and size posterior to them (Fig.28C,
D). Present in T. europaea, T. ronningae sp. nov., T. norvegica sp. nov., T. scotica sp.
Figure 28. SEM micrographs of abdominal uncini types of Terebellides species. A T. kongsrudi sp. nov.
(species 13; ZMBN-116409) B T. bigeniculatus Parapar, Moreira & Helgason, 2011 (species 20 + 28;
ZMBN-116513) C T. ronningae sp. nov. (species 7; ZMBN-116353) D Terebellides stroemii Sars, 1835
(species 11; ZMBN-116399). Abbreviations: ctr – capitium teeth row; ros – rostrum.
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
52
nov., and T. stroemii (Table 1). Type 2 is apparently also present in T. kergelensis
McIntosh, 1885 (sensu Parapar and Moreira 2008a), T. jitu Schüller & Hutchings,
2010, T. canopus Schüller & Hutchings, 2013, T. persiae Parapar, Moreira, Gil &
Martin, 2016, T. baliensis Hsueh & Li, 2017, T. guangdongensis Zhang & Hutch-
ings, 2018, T. augeneri Parapar, Martin & Moreira, 2020, T. fauveli Parapar, Martin
& Moreira, 2020, T. nkossa Parapar, Martin & Moreira, 2020, and T. ramili Parapar,
Martin & Moreira, 2020 (Parapar et al. 2016a, 2020; Hsueh and Li 2017; Zhang
and Hutchings 2018). is “more complex” type 2 condition of abdominal uncini
does not seem related to body size; for instance, small species such as T. atlantis sensu
Parapar et al. (2011: 5, g. 3f) and T. shetlandica (Parapar et al. 2016c: 218, g. 6f )
are provided with such uncini. e validity of this proposed uncini classication
should be assessed across species considering specimens of dierent sizes and across
abdominal chaetigers.
On the other hand, we observed dierences in whether the capitium is dened
or not in geniculate chaetae of TC5/TC6, as previously highlighted by Parapar et al.
(2011, 2013, 2016a, 2016b, 2016c). For instance, T. ginkgo Schüller & Hutchings,
2012 shows a well-dened capitium conformed by many large-sized teeth whereas
other species bear an almost inconspicuous capitium (e.g., T. bakkeni sp. nov., T. kong-
srudi sp. nov.) (Schüller and Hutchings 2012: 10, g. 5a–c; Figs 6G, 12G); Parapar et
al. (2011) also reported from Iceland several species with conspicuous capitium, i.e., T.
atlantis, T. gracilis and T. stroemii. In this sense, the specimens of T. stroemii examined
here bear a low capitium in comparison to those aforementioned from Iceland (Para-
par et al. 2011); this suggests that the latter might not correspond to T. stroemii but to
other taxa as explained above. Again, the taxonomic value of this character should be
tested in other species considering potential intraspecic variation.
Methyl Green staining pattern
e MG staining pattern was mostly similar across the studied species and according
to type 1 sensu Schüller and Hutchings (2010), being solid in three to ve anterior
chaetigers, TC1–TC3(5), striped in subsequent seven or eight chaetigers, i.e., TC4(6)–
TC10(11), and fading towards the end of the thorax at TC18; minor observed dif-
ferences can be attributed to body size, degree of contraction and preservation of
specimens. Parapar et al. (2011) reported a similar pattern for specimens identied as
T.stroemii from Iceland: solid in the rst six chaetigers after turning into a striped pat-
tern and fading in the posterior thoracic segments, while for T. bigeniculatus staining is
solid from TC1 to TC11, striped between TC12 and TC14, and then fading in the fol-
lowing segments. e rst pattern only partially agrees with that of T. stroemii (species
11) and the second one would match better with that of T. bigeniculatus (species 20 +
28) as examined here. Parapar and Hutchings (2014) reported a MG staining pattern
for neotypes of T. stroemii being solid from TC1 to TC3, striped from TC4 to TC12
and fading in the last thoracic segments; this is exactly the same pattern as observed in
T.stroemii from Norway (Suppl. material 1: Table S1).
New species of Terebellides from North East Atlantic 53
Nephridial papillae
Schüller and Hutchings (2010) and Parapar et al. (2011), among others, suggest that
position of thoracic papillae (nephridial/genital) should be considered as of taxonomic
value. We agree with this and have found that papillae are present always in TC4 and
TC5 in the species/clades studied here. is position has also been reported in T. graci-
lis sensu Parapar et al. (2011, 2013), T. mediterranea, T. kerguelensis, and T. hutchingsae
Parapar, Moreira & Martin, 2016. On the contrary, other species reported elsewhere
have such papillae in TC1 instead, including T. persiae Parapar, Moreira, Gil & Martin,
2016, T. mediterranea, and T. hutchingsae.
Conclusions
To sum up all results and according to the discussion of the aforementioned characters,
the general characteristics for each subgroup of Group A sensu Nygren et al. (2018)
are listed below. A1 and A2 are particularly close to each other and were informally de-
signed by Nygren et al. (2018) as “stroemii-group”; subgroup A3 is the most dissimilar,
with T. bigeniculatus as the typical species.
Subgroup A1
Species are similar morphologically and dier from A2 in lacking papillae on branchial
lamellae and in having ciliated papillae on thoracic notopodia. Regarding morphology
and distribution, T. bakkeni sp. nov. and T. kongsrudi sp. nov. are closest to each other
than to T. stroemii. Terebellides stroemii (as species 11 here) shows also a similar geo-
graphic and bathymetric distribution (Table 1), but seems less frequent across Norway
and diers in abdominal uncini type (cf. Fig. 7G vs. Figs 6G, 12G).
Subgroup A2
e subgroup is morphologically homogeneous. It diers from A1 in having lamellae
papillae and by the lack of thoracic ciliated papillae (at least not observed with SEM).
e most recognisable species is T. ronningae sp. nov. because of having thoracic uncini
of type 1, a long rostrum and a capitium provided with long rst row teeth; the other
three species bear thoracic uncini of type 3 and dier of each other in the geographic
(T. europaea, T. scotica sp. nov.) and bathymetric distribution (T. norvegica sp. nov.).
Subgroup A3
is subgroup is composed by T. bigeniculatus (species 20 + 28) and species 21 (not
formally described here). Branchial shape is irregular and geniculate chaetae are present
in two thoracic chaetigers (TC5 and TC6). Other features are shared with A1 such as
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
54
lack of lamellae papillae; thoracic uncini type 3 or presence of thoracic ciliated papillae.
e bathymetric distribution of species is similar to A1.
Acknowledgements
We would like to thank all people involved in Nygren et al. (2018) paper, specially
Torkild Bakken (NTNU–University Museum, Trondheim, Norway) and Jon Anders
Kongsrud (Zoological Museum, Bergen, Norway), for providing part of the speci-
mens of the dierent species studied here. Many thanks also to Ann Helén Rønning
and Åse Ingvild Wilhelmsen (Natural History Museum–University of Oslo, Norway)
and Gudmundur Gudmundsson (Icelandic Institute of Natural History, Reykjavik)
for providing the type specimens of T. stroemii and T. bigeniculatus respectively. anks
also to Ada Castro and Catalina Sueiro (Servizos de Apoio á Investigación, Universi-
dade da Coruña) for SEM assistance, to María Candás (Estación de Bioloxía Mariña
da Graña–Ferrol, Universidade de Santiago de Compostela, Spain) for assistance with
the stereomicroscope photographs, and to Antonio Fernández y García de Vinuesa
(Ministerio de Transición Ecológica y Reto Demográco, Spain) and Juana Agudo
González (DHL España) for their unvaluable help with Customs paperwork related to
the shipment of type specimens of T. stroemii and T. bigeniculatus.
is study was partly supported by the FAUNA IBÉRICA research project Polychaeta
VII, Palpata, Canalipalpata II (PGC2018–095851–B–C64) funded by the Agencia Estatal
de Investigación, Ministerio de Ciencia e Innovación, and coordinated by JP. Funding was
also provided from the Ramón y Cajal program (RYC-2016- 20799) funded by Spanish
MINECO, Agencia Estatal de Investigación, Comunidad Autónoma de las Islas Baleares
and the European Social Fund to MC. Financial support was also provided by the Nor-
wegian Taxonomy Initiative (Cryptic polychaete species in Norwegian waters, knr 49-13,
project no. 70184228 to AN; Polychaetes in the Norwegian Sea, project no. 70184227;
Polychaetes in Skagerrak, project no.70184216; and the MAREANO program.
Authors deeply thank Pat Hutchings and one anonymous reviewer as well as Chris
Glasby, Zookeys Subject Editor, for their constructive comments on the manuscript.
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Supplementary material 1
Table S1. Locality and collecting data, museum registration numbers and refer-
ences to gures of Terebellides specimens
Authors: Julio Parapar, María Capa, Arne Nygren, Juan Moreira
Data type: occurences
Explanation note: Locality and collecting data, museum registration numbers and ref-
erences to gures of Terebellides specimens described in this work. Country names
are transcribed from original museum vials.
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/zookeys.992.55977.suppl1
Julio Parapar et al. / ZooKeys 992: 1–58 (2020)
58
Supplementary material 2
Table S2. List of COI sequences considered in present study (Group A), museum
vouchers and GenBank accession numbers
Authors: Julio Parapar, María Capa, Arne Nygren, Juan Moreira
Data type: COI sequences, museum vouchers and GenBank accession numbers
Explanation note: List of COI sequences considered in present study (Group A), mu-
seum vouchers and GenBank accession numbers. Abbreviations of housing institu-
tions: ZMBN = Department of Natural History, University Museum of Bergen;
GNM = e Gothenburg Museum of Natural History; NTNU-VM = Norwegian
University of Science and Technology, University Museum, Trondheim; SMF =
Senckenberg Museum Frankfurt.
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/zookeys.992.55977.suppl2
Available via license: CC BY
Content may be subject to copyright.
