![Number of species described for each marine realm (in alphabetical order, according to Spalding et al. [31]) and Udvardy 1975 for limnic realms.](https://www.researchgate.net/publication/350143987/figure/fig5/AS:1002702490308611@1616074311612/Number-of-species-described-for-each-marine-realm-in-alphabetical-order-according-to_Q320.jpg)
Available via license: CC BY
Content may be subject to copyright.
Diversity 2021, 13, 130. https://doi.org/10.3390/d13030130 www.mdpi.com/journal/diversity
Review
Fanworms: Yesterday, Today and Tomorrow
María Capa 1,*, Elena Kupriyanova 2, João Miguel de Matos Nogueira 3, Andreas Bick 4 and
María Ana Tovar-Hernández 5
1 Departament de Biologia, Universitat de les Illes Balears, 07122 Palma, Spain
2 Australian Museum Research Institute, Australian Museum, Sydney, NSW 2010, Australia;
elena.kupriyanova@australian.museum
3 Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo 05508-090,
Brazil; nogueira@ib.usp.br
4 Universität Rostock, Institut für Biowissenschaften, Allgemeine und Spezielle Zoologie, Universitätsplatz 2,
D-18055 Rostock, Germany; andreas.bick@uni-rostock.de
5 Universidad Autónoma de Nuevo León, Facultad de Ciencias Biológicas, Nuevo León 66455, Mexico;
maria_ana_tovar@yahoo.com
* Correspondence: maria.capa@uib.es
Abstract: Sabellida Levinsen, 1883 is a large morphologically uniform group of sedentary annelids
commonly known as fanworms. These annelids live in tubes made either of calcareous carbonate or
mucus with agglutinated sediment. They share the presence of an anterior crown consisting of ra-
dioles and the division of the body into thorax and abdomen marked by a chaetal and fecal groove
inversion. This study synthesises the current state of knowledge about the diversity of fanworms in
the broad sense (morphological, ecological, species richness), the species occurrences in the different
biogeographic regions, highlights latest surveys, provides guidelines for identification of members
of each group, and describe novel methodologies for species delimitation. As some members of this
group are well-known introduced pests, we address information about these species and their cur-
rent invasive status. In addition, an overview of the current evolutionary hypothesis and history of
the classification of members of Sabellida is presented. The main aim of this review is to highlight
the knowledge gaps to stimulate research in those directions.
Keywords: Sabellida; Sabellidae; Serpulidae; Fabriciidae; Annelida; polychaetes;
biodiversity assessment; systematics; methods; gaps of knowledge
1. Introduction
Sabellida Levinsen, 1883 is a morphologically uniform clade of sedentary annelids
historically given a rank of Order. Sabellida currently includes members of Fabriciidae
Rioja, 1923, Sabellidae Latreille, 1825, and Serpulidae Rafinesque, 1815 [1–3]. They are
commonly known as fanworms, feather-duster worms, or flowers of the sea, because their
radioles are arranged in a crown, protruding from the tube made of calcium carbonate or
mucus with agglutinated sediment (Figure 1). In addition to the presence of protective
tube and the prostomial crown made of radioles with secondary ramifications (generally
referred as pinnules, but see [4] for Fabriciidae), which are mainly used for feeding and
respiration, all members of Sabellida share the presence of chaetal inversion [thoracic
chaetigers with simple chaetae on notopodia and uncini (hooks) on neuropodia, and ab-
dominal chaetigers with opposite arrangement]. Sabellida includes about 1200 species
distributed world-wide, from tropical to polar waters and found in all habitats, from
freshwater to fully marine conditions, and intertidal to deepest ocean trenches.
The Sabellida concept and even the group name has changed over time. Since their
erection in the early 19th century, sabellids (including fabriciids), building soft sediment
tubes, and serpulids, building calcareous tubes, have always been considered related,
Citation: Capa, M.; Kupriyanova, E.;
Nogueira, J.M.d.M.; Bick, A.;
Tovar-Hernández, M.A. Fanworms:
Yesterday, Today and Tomorrow.
Diversity 2021, 13, 130.
https://doi.org/10.3390/d13030130
Academic Editor: Luc Legal
Received: 30 December 2020
Accepted: 10 March 2021
Published: 17 March 2021
Publisher’s Note: MDPI stays neu-
tral with regard to jurisdictional
claims in published maps and insti-
tutional affiliations.
Copyright: © 2021 by the authors. Li-
censee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and con-
ditions of the Creative Commons At-
tribution (CC BY) license (http://crea-
tivecommons.org/licenses/by/4.0/).
Diversity 2021, 13, 130 2 of 74
based on their general morphology and grouped into the section Amphitrites sabelliennes
[5], the family Serpulacei [6], family Serpulacea [7–9], Serpulidae [10], and finally Sabel-
lida [11,12].
Figure 1. Comparison of the radiolar crown structure among the three families of Sabellida. (a) Anterior end of Fabricia
stellaris, dorsal view; (b) Histological section of crown of F. stellaris at base; (c) Histological section of crown of F. stellaris
at mid-length; (d) Histological section of one radiole and presumed pinnules of F. stellaris; (e) Anterior end of Laonome
xeprovala, dorsal view; (f) Histological section of crown of Laonome xeprovala at base; (g) Histological section of crown of L.
xeprovala at mid-length; (h) Histological section of one radiole and pinnules of L. xeprovala; (i) Anterior end of Spirobranchus
lamarki, ventral view; (j) Histological section of crown of S. lamarcki at base; (k) Histological section of crown of S. lamarcki
at mid-length; (l) Histological section of one radiole and pinnules of S. lamarcki. Abbreviations: br: base of radioles; bv:
blood vessel; c: collar; coe: coelom; cu: cuticle; dl: dorsal lips; ep: epithelium; fg: faecal groove; hc: hyaline cartilage; mp:
mouth palp; op: opercular peduncle; p: pinnules; pl: parallel lamellae; r: radioles; sca: supporting cellular axis; vl: ventral
lips.
With the advent of cladistic analyses, close relationships of sabellids and serpulids
with Sabellariidae Johnston, 1865, Siboglinidae Caullery, 1914 and Oweniidae Rioja, 1917
have been suggested, and consequently the composition of Sabellida expanded to incor-
porate these three taxa (e.g., [13]) (Figure 2). However, subsequent molecular analyses
Diversity 2021, 13, 130 3 of 74
using increasing number of taxa and DNA markers revealed that the three late incorpo-
rated taxa were neither closely related to fanworms, nor to each other [14–16]. Morpho-
logical lines of evidence related to the ontogeny, internal anatomy, position of the ciliated
groove, as well as chaetal morphology and arrangement also supported this lack of close
relationship [17–26]. Consequently, Sabellida now again includes only fanworms (Figure
2), but the former sabellid subfamily Fabriciinae has been elevated to Fabriciidae based
on DNA evidence [1–3,24,27]. The sister group of Sabellida, according to the latest phylo-
genomic studies, is a clade including Spionidae Grube, 1850 and Sabellariidae [14,28,29].
Figure 2. History of the evolutionary hypotheses within Sabellida. The coloured taxa indicate the groups that had been
considered as members of Sabellida (or Serpulacea) according to the represented phylogenetic hypotheses. In light blue
are members of the currently accepted Fabriciidae, in dark blue are Sabellidae and Serpulidae are in orange. In green, pink
and yellow are other taxa previously considered as Sabellida.
Diversity 2021, 13, 130 4 of 74
Most of the taxonomic work in the Sabellida has aimed to document the regional
species diversity, rather than to provide comprehensive world-wide generic revisions.
These regional studies have been geographically unevenly distributed because of their
strong association to political, economic, historical and traditional context. Moreover,
available georeferenced databases (i.e., in Global Biodiversity Information Facility, GBIF,
https://www.gbif.org, accessed on 3 March 2021) are also biased, as not all biodiversity
information from museum collections and research institutions is shared with this service.
The information available in GBIF database not necessarily adequately reflects true spe-
cies richness and abundance in natural habitats, as more conspicuous, well-known or eas-
ier to identify species are predominant in such datasets.
The main aim of this study is to synthesise in a single, easily accessible publication
the current knowledge of evolutionary relationships, classification, species diversity and
distribution of Sabellida, paying special attention to the latest surveys and novel method-
ologies used for species delimitation. As some members of Sabellida are easily translo-
cated by anthropogenic means and establish outside of their native ranges, updated infor-
mation about their invasive status is provided. Another important goal was to highlight
the knowledge gaps in order to stimulate research in those directions.
2. Materials and Methods
The present study is a literature review of the information on the Sabellida species
diversity, distribution and ecology, highlighting the geographic areas that need further
scientific effort and the taxonomic groups that need revisions. The characters and methods
used for species delineation have been revised. We summarise the phylogenetic position
of Sabellida and the relationships within the group from a historic perspective.
The World Register of Marine Species (WoRMS) [30] database has been key for ac-
counting the number of current valid taxa and analyses of species richness. However, this
list has been further revised, including synonymies, new combinations, corrections of
names for gender agreement, years of publication, specification of habitats, type localities,
and assigning statuses such as inquirenda or indeterminable to taxa (Appendix A).
Scientific names for all taxa are followed by the authority the first time a taxon is
mentioned in the text and in the supplementary material tables (Tables S1–S3). However,
due to the high number of taxa dealt with in this review, the citations of authorships have
not been included in the reference list. Since many species are still reported as having
suspiciously wide distributions, generalised type localities (not details of precise collec-
tion locations) are included in Tables S1–S3). Original descriptions, details of type locali-
ties and synonymies can be found in WoRMS [30].
Biodiversity information (occurrence data) is referred to the geographic regions
(realms) proposed by Spalding et al. [31] for the marine and Udvardy [32] for limnic en-
vironments with terminological changes by Olson et al. [33]. Type localities instead of
currently reported distributions were used to assign each species to a biogeographic
realm. Available biodiversity records have been downloaded as global maps with georef-
erenced occurrences for Fabriciidae, Sabellidae and Serpulidae separately from the Global
Biodiversity Information Facility (GBIF platform, [34]). Distribution of the most common
taxa at global scale and species richness in each of the marine realms have been analysed
and discussed. In order to delimit these realms in the GBIF maps, polygons following the
boundaries of these realms have been drawn with the tools given at the GBIF platform.
DNA sequences available at the National Center for Biotechnology Information
(NCBI, [35]) and Barcode of Life Data System (BOLDSystems [36]) have been used to as-
sess the state of the genetic information available for each of the three groups of fanworms.
Moreover, currents trends, including phylogenomic data are discussed.
Diversity 2021, 13, 130 5 of 74
3. Results
3.1. Systematics
The history of the Sabellida as Fabriciidae + Sabellidae + Serpulidae) has been convo-
luted. Rafinesque [37] grouped the worms with calcareous tubes as Serpularia, now Ser-
pulidae. The subfamily Spirorbinae was established for small-bodied serpulids with spi-
rally coiled tubes [38] and the subfamily Filograninae for the taxa with pinnulated oper-
culum-bearing radioles or lacking opercula [39]. Thus, Serpulidae was subdivided into
Filograninae, Serpulinae, and Spirorbinae until Pillai [40] elevated the Spirorbinae to the
family status. However, even first morphology-based phylogenetic analyses suggested
that Spirorbinae are more closely related to Serpulinae than to Filograninae [19,41,42] and
that Filograninae is paraphyletic [41,43,44]. Moreover, further analyses integrating molec-
ular data [45–49] unequivocally found both traditional Serpulinae and Filograninae pa-
raphyletic, and Spirorbinae nested within Serpulidae. Thus, consensus that recognition of
Spirorbidae would make Serpulidae a paraphyletic group has prevailed and the rank of
the spirorbids was lowered back to Spirorbinae [50].
Initially, Sabellidae included the large-bodied species of fanworms. Rioja, in 1923
[39], divided Sabellidae in three subfamilies: Fabriciinae Rioja (1923), gathering species
with acicular uncini; Myxicolinae (only Myxicola Koch in Renier, 1847), having radioles
joined by a membrane for most of their length, abdominal uncinal tori forming almost
complete cinctures and tubes made of thick gelatinous mucus; and Sabellinae, character-
ised by avicular thoracic uncini, often with companion chaetae, distinct faecal groove and
ventral shields. Johansson [51] included Myxicola in Fabriciinae. Fauchald [12] followed
Rioja’s arrangement and recognized Sabellongidae Harman, 1969 (with Sabellonga Hart-
man, 1969) and Caobangiidae Chamberlin, 1919 (with Caobangia Giard, 1893) as valid taxa.
As a result of the first morphology-based phylogenetic analysis of Sabellidae (as per-
ceived at the time), using Serpulidae as the outgroup [42], only subfamilies Fabriciinae
and Sabellinae were recognised and their composition changed dramatically (Figure 2).
Caobangia, 1893 was included in Fabriciinae, while Myxicola, Sabellonga and some genera
previously considered as fabriciins (Chone Krøyer, 1856, Desdemona Banse, 1957, Euchone
Malmgren, 1866, Fabrisabella Hartman, 1969 and Jasmineira Langerhans, 1880) were recov-
ered in Sabellinae. The Sabellinae was defined by the presence of the “radiolar skeleton”
composed of at least two rows of vacuolated cells and dorsally fused radiolar lobes [42].
The subfamily Fabriciinae was characterised by the presence of rasp-shaped (having sev-
eral rows of teeth) abdominal uncini, absence of ventral lips, separated radiolar lobes (ex-
cept in Caobangia) and the absence of “radiolar skeleton” (except in Caobangia, with one
longitudinal row of vacuolated cells). Later Caobangia was transferred to Sabellinae, sim-
plifying the definition for Fabriciinae [52].
Analyses of molecular data have changed the understanding of the relationships
within Sabellida. Molecular data provided evidence of Serpulidae being sister to Fabrici-
inae, and Sabellinae the sister group of this clade [1]. Consequently, Fabriciinae was raised
to the family rank (Fabriciidae, Figure 2). Further studies supported the validity of the
three families, although relationships among them were not consistently supported
[2,24,27]. The latest study using transcriptomes for a broad range of sabellids recovered
Fabriciidae as sister to a clade of Sabellidae and Serpulidae [3] (Figure 2). Now it is gener-
ally accepted that Sabellidae does not include Fabriciidae [1,2,24,27] and is more closely
related to Serpulidae than to Fabriciidae [3].
3.1.1. Fabriciidae
Monophyly of Fabriciidae is supported by the branching patterns of the radiolar
crown, the absence of ventral lips, abdominal uncini with elongate handle referred to as
manubrium, and presence of radiolar hearts [4] (Table 1, Figure 3), as well as by repro-
ductive characters [27]. Relationships among fabriciids were first explored using morpho-
logical data [42,53–60]. Although the phylogenies were not fully resolved, these studies
Diversity 2021, 13, 130 6 of 74
recovered two main groups: one paraphyletic, branching off at the base of the tree and
including Fabriciola Friedrich, 1939, Manayunkia Leidy, 1859, Monroika Hartman, 1951, and
a clade with the remaining nine genera considered valid at the time. The position of
Pseudofabriciola Fitzhugh, 1990b varied with the different analyses [57].
Table 1. Morphological diagnostic features of the three taxa of Sabellida.
Feature Fabriciidae Sabellidae Serpulidae
Tube material mucus and sediment/none mucus and sediment * calcium carbonate
Radiolar lobes separated fused separated
Vacuolated cells supporting
radioles absent present absent
Operculum absent absent absent or present
Thoracic membrane absent absent present
Thoracic
uncini
acicular
a
vicular
**
avicular
Number of abdominal chae-
tigers
usually three (exceptionally
two or four) more than three more than three
Abdominal uncini with elongate and wide
handle (manubrium)
with short handle or
lacking handles lacking handles
Branchial hearts present absent absent
* Glomerula is an exception with a calcareous tube; ** Terebrasabella is an exception with three types
of thoracic uncini: acicular, avicular and palmate.
A recent comprehensive study assessing phylogenetic relationships within Fabrici-
idae incorporated DNA sequence and reproductive data into a morphological dataset [27].
The results corroborated the apomorphies proposed earlier: the absence of ventral lips,
modified abdominal uncini with elongate manubrium and presence of radiolar hearts,
together with six apomorphic reproductive traits: (1) spermatogenesis occurring only in
the thorax, (2) spermatids developed in large clusters with a central cytophore, (3) pres-
ence of a single dorsal sperm duct, (4) presence of a sperm nuclear projection, (5) sperm
nuclear membrane thickening, and (6) sperm extra-axonemal sheath. The study recovered
the two main groups already revealed by Fitzhugh [42,56,57,61,62]. One clade contained
Manayunkia and Echinofabricia Huang, Fitzhugh and Rouse, 2011 (Genus A in [57]), and
branched off basally, sister to all the other Fabriciidae. The second larger clade showed
Rubifabriciola Huang, Fitzhugh and Rouse, 2011 (the red-eyed ’Fabriciola‘), branching off
at the base, sister to six other genera. Some taxa need further study to assess their mon-
ophyly since Novafabricia labrus Fitzhugh, 1998 was not found nested within other species
in the genus (as in [57]), Monroika africana (Monro, 1939) formed a polytomy with the Ma-
nayunkia species, and there were not enough characters to support Augeneriella Banse, 1957
and Pseudoaugeneriella Fitzhugh, 1988 as distinct genera [27].
With one exception, genera of Fabriciidae have been revised and most of the revisions
were accompanied by phylogenies (Table 2). Brandtika Jones, 1974 was not included in
phylogenetic analyses [27,59] due to poorly preserved types and incomplete descriptions
[63].
Diversity 2021, 13, 130 7 of 74
Figure 3. Some fabriciid representatives showing a range of the diversity of forms found in the group. (a) cf. Fabriciola sp.,
deep-sea basin of the southwest Atlantic; (b,c,h) Fabricia stellaris, Baltic Sea; (d,f) Manayunkia athalassia, South Australia;
(e) Fabriciola sp., Brazil (g) Monroika sp., Argentina (c by A. Dietrich, d by G. Rouse, g by L. Armendariz).
Diversity 2021, 13, 130 8 of 74
Table 2. Fabriciid currently accepted genera that have undergone major or partial revisions and
phylogenetic analyses (based on morphological features, molecular data or both).
Genera Number of
Species * Taxonomic Revision Phylogenetic Studies
Augeneriella Banse, 1957 5 Banse 1957, Fitzhugh 1983,
1990a, 1993 Fitzhugh 1991a-b, 1992, 1993, 2010
Bansella
Fitzhugh, 2010 1 Fitzhugh 2010 Fitzhugh 2010
Brandtika
Jones, 1974 1 Fitzhugh 2001 NO
Brifacia Fitzhugh, 1998 2 Fitzhugh 1998; Giangrande
et al. 2014 Fitzhugh 2010
Echinofabricia
Huang, Fitz-
hugh and Rouse, 2011 4 Huang et al. 2011 Fitzhugh 1991a, 1992, 1993, 1998,
2010 (as genus A)
Fabricia de Blainville, 1828 1 Fitzhugh 1991b, 2010 Fitzhugh 1991a, 1992, 1993, 1998,
2010
Fabricinuda Fitzhugh,
1990b 7
Fitzhugh 1983, 1990b,
2002a; López and
Rodríguez 2008
Fitzhugh 1991a, 1992, 1993, 1998,
2002a, 2010; López and Rodríguez
2008
Fabriciola Friedrich, 1939 6 Fitzhugh 1991b, 1992, 1999;
Bick 2005
Fitzhugh 1991a, 1992, 1993, 1998,
1999, 2010
Manayunkia Leidy, 1859 10 Sitnikova et al. 2014, Atkin-
son et al. 2020
Fitzhugh 1991a, 1992, 1993, 1998,
2010; Sitnikova et al. 2014; Pudo-
vkina et al. 2016
Monroika
Hartman, 1951 1 Fitzhugh 1992 Fitzhugh 1992, 1998, 2010
Novafabricia
Fitzhugh,
1990c 11 Fitzhugh 1983, 1990c, 1998;
Bick 2005
Fitzhugh 1991a, 1992, 1993, 1998,
2010
Parafabricia
Fitzhugh,
1992
2
Fitzhugh
1992
Fitzhugh
1992,
1993,
1998,
2010
Pseudoaugeneriella
Fitz-
hugh, 1998 5 Fitzhugh 1998 Fitzhugh 1998, 2010
Pseudofabricia
Cantone,
1972 1 Fitzhugh 1995 Fitzhugh 1992, 1998, 2010
Pseudofabriciola Fitzhugh,
1990b 13
Fitzhugh 1990c, 1991b, 1993,
1996, 2002a; Fitzhugh et al.
1994, Fitzhugh and Sim-
boura 1995
Fitzhugh 1991a-b, 1993, 1994,
1996, 1998, 2002a, 2010; Fitzhugh
et al. 1994, Fitzhugh and Sim-
boura 1995
Raficiba
Fitzhugh, 2001 1 Fitzhugh 2001 Fitzhugh 2010
Rubifabriciola
Huang, Fitz-
hugh and Rouse, 2011 10 Huang et al. 2011 Huang et al. 2011
* Excluding subspecies.
3.1.2. Sabellidae
Monophyly of Sabellidae is supported by the presence of dorsal and ventral lips, the
presence of vacuolated cells supporting radioles and pinnules, and the dorsal fusion of
the radiolar lobes (Table 1, Figure 4) [2,3,24,42,52]. Currently, monophyletic clades Sabel-
linae and Myxicolinae are recognized within Sabellidae, the latter is composed of Amphi-
glenini and Myxicolini [3]. The current composition of the Sabellinae (now Sabellidae) has
not changed significantly since the early cladistic analyses [42,52], although nine genera
have been erected since (Table 3), and Megalomma Johansson, 1925 was replaced by Acro-
megalomma Gil and Nishi, 2017 because the name was preoccupied by a group of carabid
Diversity 2021, 13, 130 9 of 74
beetles. Fitzhugh [42] provided diagnoses of all genera accepted at the time, with their
potential apomorphies. The most recent review of morphology and diagnostic features of
genera and species identification is found in [24].
Phylogeny of Sabellidae has been largely assessed [2,64–70]. Monophyly of Acromeg-
alomma, Amphiglena Claparède, 1864, Branchiomma Kölliker, 1859, Chone, Dialychone Clapa-
rède, 1869, Paradialychone Tovar-Hernández, 2008 and Pseudobranchiomma Jones, 1962)
have been confirmed [68,71–74]. Members of the genera Chone, Dialychone and Paradialy-
chone are still problematic due to their small size and because genera and species are de-
lineated based on combination of features, such as details of uncini dentition (anterior and
posterior abdominal chaetigers) and radiolar crown structures (lips and pinnular append-
ages) that are often difficult to interpret. As a result, the position of some species within
either Dialychone, Paradialychone or Chone based on morphology is uncertain (e.g., P. am-
bigua Capa and Murray, 2015) and a molecular approach to this group is needed. The
genera Bispira Krøyer, 1856 [2,69,74], Euchone [67,75,76] and Perkinsiana Knight-Jones, 1983
[68] appear to be paraphyletic, whereas monophyly of Laonome Malmgren, 1866, Parasa-
bella Bush, 1905 and Sabellastarte Krøyer, 1856 should be assessed.
In the last two decades a number of sabellid genera have undergone major or partial
taxonomic revisions (Table 3) that included morphological comparisons of congeners, as
well as examination and re-description of types to detect potential synonyms or un-
described species. In a few of them, monophyly has been assessed through phylogenetic
analyses of mainly morphological data.
Table 3. Sabellid currently accepted genera that have gone through major or partial revisions and
phylogenetic analyses (either considering morphological features, molecular data or both).
Genera Number of
Species * Revision Phylogenetic Analyses
Acromegalomma Gil and Ni-
shi, 2017 38
Perkins 1984, Tovar-Hernández
and Salazar-Vallejo 2008; Capa
and Murray 2009; Tovar-Hernán-
dez and Carrera-Parra 2011, Gil
and Nishi 2017
Capa and Murray 2009,
Tovar-Hernández and
Carrera-Parra 2011
Amphicorina
Claparède,
1864 46 Rouse 1990 (as
Oriopsis
), Cochrane
2003 Cochrane 2003
Amphiglena Claparède, 1864 14 Capa and Rouse 2007; Tilic et al.
2019
Capa and Rouse 2007,
Tilic et al. 2019
Anamobaea
Krøyer, 1856 2 Tovar-Hernández et al. 2020 NO
Aracia
Nogueira, Fitzhugh
and Rossi, 2004 3 Nogueira et al. 2004; Tovar-Her-
nández 2014 Nogueira et al. 2010
Bispira Krøyer, 1856 24 Knight-Jones and Perkins 1998;
Capa 2008 Capa 2008
Branchiomma Kölliker, 1859 30 Tovar-Hernández and Knight-
Jones 2006
Capa et al. 2013; del
Pasqua et al. 2018
Caobangia
Giard, 1893 7 Jones 1974 NO
Chone Krøyer, 1856 20 Cochrane 2003, Tovar-Hernández
2005, 2006, 2007a, b, c, 2008 Tovar-Hernández 2008
Claviramus
Fitzhugh, 2002 5 Fitzhugh 2002; Nishi et al. 2019 NO
Dialychone
Claparède, 1869 19 Tovar-Hernández 2008 Tovar-Hernández 2008
Euchone Malmgren, 1866 35
Cochrane 2003, Giangrande and
Licciano 2006, Giangrande et al.
2017
Cochrane 2003
Diversity 2021, 13, 130 10 of 74
Euchoneira
Licciano, Gian-
grande and Gambi, 2009 1 Licciano et al. 2009 Licciano et al. 2009
Eudistylia
Bush, 1905 5 Hartman 1938, Banse 1979 NO
Hypsicomus
Grube, 1870 1 Perkins 1984 NO
Jasmineira Langerhans, 1880 19 Cochrane 2003, Capa and Murray
2015 Cochrane 2003
Laonome Malmgren, 1866 10 Fitzhugh 2002, Capa 2007, Bick et
al. 2018 Capa 2007
Notaulax
Tauber, 1879 26 Perkins 1984 NO
Paradialy
chone
Tovar-Her-
nández, 2008 16 Tovar-Hernández 2008 Tovar-Hernández 2008
Parasabella Bush, 1905 29
Perkins 1984, Giangrande 1994,
Tovar-Hernández and Harris 2010,
Capa and Murray 2015b, Keppel et
al. 2020
Capa and Murray
2015b
Perkinsiana Knight-Jones,
1983 16
Knight-Jones 1983, Giangrande
and Gambi 1997, Tovar-Hernán-
dez et al. 2012
NO
Potamethus
Chamberlin,
1919 11 Knight-Jones 1983 NO
Potamilla
Malmgren, 1866 10 Knight-Jones 1983 NO
Potaspina
Hartman, 1969 2 Capa 2007 Capa 2007
Pseudobranchiomma
Jones,
1962 19 Knight-Jones 1994, Knight-Jones
and Giangrande 2003 Capa and Murray 2016
Pseudopotamilla
Bush, 1904 23 Knight-Jones et al. 2017 Capa 2007
Sabella
Linnaeus, 1767 39 Knight-Jones and Perkins 1998 NO
Sabellastarte
Krøyer, 1856 8 Knight-Jones and Mackie 2003 Capa et al. 2010
Sabellomma
Nogueira, Fitz-
hugh and Rossi, 2010 4 Nogueira et al. 2010, Capa and
Murray 2015 Nogueira et al. 2010
Stylomma
Knight-Jones,
1997 2 Knight-Jones and Perkins 1998,
Capa 2007 Capa 2007
Terebrasabella
Fitzhugh and
Rouse, 1999 3 Murray and Rouse 2007 Murray and Rouse 2007
* Excluding subspecies.
Diversity 2021, 13, 130 11 of 74
Figure 4. Some sabellid representatives showing a range of the diversity of forms found in the group. (a) Stylomma palma-
tum, Lizard Island, Australia; (b) Acromegalomma spp., Lizard Island, Australia; (c) Paradialychone ambigua, Lizard Island,
Australia; (d) Pseudobranchiomma paraemersoni, São Paulo, Brazil; (e) Laonome xeprovala, Sea of Azov; (F) Branchiomma sp.,
Mexico; (g) Bispira brunnea, Caribbean; (h) Notaulax sp., Lizard Island, Australia; (i) Anamobaea orstedii., Mexico; (j) Sabel-
lastarte magnifica, Mexico. (a,b,g, by M. Bok; e by V. Syomin, i,j by H. Bahena).
Diversity 2021, 13, 130 12 of 74
3.1.3. Serpulidae
Monophyly of Serpulidae is supported by the presence of calcareous tubes with com-
plex ultrastructures, distinct from the simple structure found in calcareous tubes of the
unique sabellid Glomerula piloseta (Perkins, 1991). The serpulid thorax is surrounded by
the thoracic membranes, which are absent in sabellids and fabriciids. Most serpulids have
an operculum (or several), a modification of the distal part of a radiole, acting as a plug
when animals hide in their tubes (Table 1, Figure 5).
The first formal phylogenetic analysis based on morphological data [43] recovered
monophyletic Spirorbinae (as sister group to Serpulinae, including Chitinopoma Levinsen,
1884, Crucigera Benedict, 1887, Serpula Linnaeus, 1758, Hydroides Gunnerus, 1768, Ficopo-
matus Southern, 1921, Galeolaria Lamarck, 1818, Spirobranchus Blainville, 1818) and pa-
raphyletic Filograninae (Filograna Berkeley, 1835, Microprotula Uchida, 1978, Protula Risso,
1826). Phylogenetic studies using DNA data inferred two major clades within Serpulidae,
e.g., [45–49]. The clade A comprised two clades: the Serpula-Crucigera-Hydroides (Clade AI
‘Serpula-group’) and the Spirobranchus-Ficopomatus-Ditrupa (Clade AII ‘Spirobranchus-
group’). The Clade B included a monophyletic Spirorbinae as sister group to the Protis-
Protula-Vermiliopsis-Chitinopoma (clade BI ‘Protula-group’). Position of serpulin genera,
such as Vermiliopsis and Chitinopoma within clade BI along with typical filogranins, made
both traditional Filograninae and Serpulidae paraphyletic.
Within Clade A, further assessment of AI ‘Serpula-group’ (Serpula, Crucigera, Hy-
droides) [77] supported monophyly of Hydroides, but Serpula was recovered as paraphyletic
basal grade and Crucigera was polyphyletic. Later studies assessed relationships within
the largest serpulid genus Hydroides [78–80]. Within AII ‘Spirobranchus-group’ several
studies examined relationships within the genus Spirobranchus [81–84] and demonstrated
sister group relationship between brackish-water genus Ficopomatus and freshwater mon-
otypic Marifugia Absolon and Hrabĕ, 1930 [46].
Within clade B, studies focused on Spirorbinae, classification of which is based [85]
on the six distinct types of brooding, two opercular (Pileolariinis and Januini) and four
tubular (Romanchellini, Paralaeospirini, Circeini, Spirorbini). It has been repeatedly ar-
gued that tube incubation precedes opercular brooding [85–88], but Thorp and Segrove
[89] advocated for an ancestral opercular incubation. Results of the first morphology-
based phylogenetic analysis of spirorbins [44] confirmed the ancestry of tube brooding,
but suggested that the opercular brooding arose once and the brooding cup of Januini is
a simplification of the brooding structure of Pileolariini. Another analysis of morphologi-
cal data [90] confirmed that opercular brooding is derived, but suggested that the two
types arose independently. No molecular spirorbin phylogeny is available to test this ar-
rangement. As neither traditional Serpulinae, nor Filograninae are monophyletic, re-clas-
sification based on a comprehensive integrative analysis and re-formulation of the sub-
family diagnoses are needed. Meanwhile Spirorbinae is accepted as nested within Serpu-
lidae, but other serpulid genera are not assigned into subfamilies. Most serpulid genera
have not been revised (Table 4).
Diversity 2021, 13, 130 13 of 74
Table 4. Serpulid currently accepted genera that have undergone major or partial revisions and
phylogenetic analyses (using morphological features, molecular data or both).
Genera Number of
Species * Revision Phylogenetic Analyses
Bathyditrupa Kupriyanova,
1993 1 Kupriyanova and Ippolitov 2015 NO
Bathyvermilia Zibrowius,
1973 7 Zibrowius 1973 NO
Crucigera Benedict, 1887 5 ten Hove and Jansen-Jacobs 1984
Kupriyanova et al. 2008
Ditrupa Berkeley, 1835 ten Hove and Smith 1990 NO
Ficopomatus Southern, 1921 6 ten Hove and Weerdenburg 1978 Kupriyanova et al. 2009;
Styan et al. 2017
Galeolaria Lamarck, 1818 3 NO Halt et al. 2009; Smith et
al. 2012
Hydroides Gunnerus, 1768 99
Bastida-Zavala and ten Hove
2002, 2003; Sun et al. 2015; Sun et
al. 2018
Sun et al. 2018
Laminatubus ten Hove and
Zibrowius, 1986 3 Rouse and Kupriyanova 2021 Rouse and Kupriyanova
2021
Marifugia Absolon and
Hrabe, 1930 1 Kupriyanova et al. 2009 Kupriyanova et al. 2009
Metavermilia Bush, 1905 15 Zibrowius 1971; Nishi et al. 2007 NO
Pseudochitinopoma
Zibrowius, 1969 5 Kupriyanova et al. 2012 NO
Pyrgopolon de Montfort, 1808 3 ten Hove 1973 NO
Serpula Linnaeus, 1758 30 NO Kupriyanova et al. 2008
Spirobranchus de Blainville,
1818 36 ten Hove 1970
Willette et al. 2015; Perry
et al. 2019; Pazoki et al.
2020
Spiraserpula Regenhardt,
1961 18 Pillai and ten Hove 1994 NO
Spirodiscus Fauvel, 1909 2 Kupriyanova and Nishi 2011,
Kupriyanova and Ippolitov 2015 NO
* Excluding subspecies.
Diversity 2021, 13, 130 14 of 74
Figure 5. Diversity within Serpulidae. (a) Vermiliopsis glandigera/pygidialis-complex sp., Lizard Island, Australia; (b) Serpula
sp., Lizard Island, Australia; (c) Hydroides lirs, Lizard Island, Australia (d) Spirobranchus corniculatus, Lizard Island, Aus-
tralia; (e) Pomatostegus actinoceras, Lizard Island, Australia.; (f) Protula sp., Lizard Island, Australia. (a–e by A. Semenov, f
by G. Rouse).
Diversity 2021, 13, 130 15 of 74
3.2. Diversity and Species Discovery
3.2.1. Number of Genera and Species
Within Fabriciidae, 17 genera, 82 species and four subspecies are currently consid-
ered valid (Table S1). This revised dataset differs from that of Pamungkas et al. [91], who
listed 21 genera and 91 species, but erroneously counted the genera Eriographis Grube,
1850, Leiobranchus Quatrefages, 1850, Leptochone Claparède, 1870 and Tuba Renier, 1804,
all of them already synonymised with the sabellid genus Myxicola (Fitzhugh 1989). Dis-
crepancy in the number of species is due to synonymisations and new combinations, as
recently updated in WoRMS.
The first fabriciid genus, Fabricia Blainville, 1828, was established to accommodate
Tubularia stellaria Müller, 1774, a species with only 12 chaetigers and smaller than the sa-
bellids described at that time [90]. In mid-19th century the genus Manayunkia was erected
and Fabriciola was established only in the 20th century. In the second half of the 20th cen-
tury, 11 genera were established and four genera were erected at the beginning of the 21st
century (Figure 6). It is remarkable that among the 17 currently valid Fabriciidae genera,
eight were established by Fitzhugh alone (Bansella Fitzhugh, 2010, Brifacia Fitzhugh, 1998,
Fabricinuda Fitzhugh, 1990a, Novafabricia Fitzhugh, 1990b, Parafabricia Fitzhugh, 1992,
Pseudoaugeneriella, Pseudofabriciola and Raficiba Fitzhugh, 2001) or with collaborators (Echi-
nofabricia and Rubifabriciola) [27].
According to Pamungkas et al. [91], whose data were collected in 2016, Sabellidae
comprises 42 genera and 493 valid species. Since 2016, 20 new species have been described
[74,92–103] and a new monotypic genus Euchonoides Magalhães, Bailey-Brock and Tovar-
Hernández, 2020 was established. After the WoRMS database has been updated (see Ma-
terials and Methods section), the current count is 42 genera and 512 valid species in Sabel-
lidae (Table S2). The first described genus was Sabella Linnaeus, 1767. From 1801 to 1850
only the genus Myxicola was established (Koch in [104]). The second half of the 19th cen-
tury was a productive period, with 15 genera established. In the 20th century, six genera
were erected in the first half, and nine in the second. Finally, from 2001, eight genera have
been erected (Figure 6).
According to Pamungkas et al. [91], Serpulidae comprises 576 species in 77 genera,
as they mistakenly included several fossil taxon names in the count of extant species. Ser-
pulidae now comprises 562 species in 69 genera, which includes 48 genera with 374 extant
species of Serpulinae sensu lato and 23 genera with 188 extant species of Spirorbinae (Table
S3). These numbers, however, do not include those of fossil taxa (180 species, in 53 genera),
not considered here. Out of 69 species of the genus Spirorbis Daudin, 1800, 46 were de-
scribed before Bailey [85] re-classified spirorbins according to the incubation methods and
never revised, so some of them upon a revision can be re-assigned to other genera.
The first serpulids described within the newly erected genus Serpula by Linnaeus
[105] were Spirobranchus triqueter (non Linnaeus, sensu Fabricius, 1780), as S. triquetra, Spi-
rorbis spirorbis (Linnaeus, 1758), as S. spirorbis, and Circeis spirillum (Linnaeus, 1758), as S.
spirillum. Serpula vermicularis Linnaeus, 1767, the type species of the type genus, was de-
scribed only nine years later. The monotypic genus Hydroides, with H. norvegica Gunnerus,
1768, was the second serpulid genus to be described in the 18th century. In the 19th cen-
tury, 28 genera, eight spirorbins and 20 serpulins, were described. In 1900–1959, 22 genera
(including three spirorbin) were described, while 48 genera were erected in the second
half of the 20th century (1960–2000). Finally, from 2001, four genera, including three ser-
pulin and one spirorbin, have been erected [49,106,107] (Figure 6).
Diversity 2021, 13, 130 16 of 74
Figure 6. Number of genera erected each decade in Fabriciidae, Sabellidae, and Serpulidae.
Diversity 2021, 13, 130 17 of 74
3.2.2. Taxonomists and Species Discovery
Kirk Fitzhugh is the most productive author in terms of the number of discovered
fabriciid species, with 27 species described alone and four in collaborations. Other author-
ities of fabriciid species include Karl Banse, Gesa Hartmann-Schröder and Greg Rouse,
with six species described by each, all as single authors (Table S1).
The most prolific author in terms of sabellid species discovery is Adolph Eduard
Grube, who described 40 species before 1881. Other productive taxonomists are María
Ana Tovar-Hernández (42 species: 36 as first or single author, 6 as co-author); María Capa
(29 species, all as first author or alone), Adriana Giangrande (29 species: 14 as first author
or alone, and 15 as co-author), Olga Hartman (18 species) and Gesa Hartmann-Schröder
(16 species) (Table S2).
The most productive serpulid taxonomist is Harry ten Hove who so far described 49
species, including seven alone. Gottfried Pillai described 46 species, including 31 species
described alone and 15 in collaboration with ten Hove. Phyllis and Wynn Knight-Jones
described 41 species, mostly spirorbins. Katherine Bush described 33 species, including 25
alone. Helmut Zibrowius described 31 species, including 29 alone and Elena Kupriyanova
authored 29 species, including eight alone. Other productive serpulid taxonomists (over
15 species described) are Minoru Imajima (21 species) and Alexander Rzhavsky (17 spe-
cies, mostly spirorbins) (Table S3).
3.2.3. Identification Keys, Diversity Assessments, and Recent Regional Taxonomic Stud-
ies
The key to all polychaete genera by Fauchald [12] includes all sabellids and serpulids
considered valid at the time, but it is outdated and not recommended for taxonomic work
anymore. A key to Fabriciidae genera recognized until 1998 was provided by Fitzhugh
[57]. In that study, the currently accepted Echinofabricia was named Genus A. The most
recently updated key to all fabriciid genera is that by Tovar-Hernández and Fitzhugh, in
press. The keys to Sabellidae genera were provided by Fitzhugh [42], Tovar-Hernández
[108] and most recently Tovar-Hernández and Fitzhugh [109]. The review by ten Hove
and Kupriyanova [110] includes diagnoses and a key to all serpulid genera (excluding
spirorbins) valid at the time.
Revision of literature reveals that intensive fieldwork and continuous taxonomic
studies by a single scientist in a specific area have had a great impact in biodiversity
knowledge of a region. However, large geographic regions have been scarcely studied,
not only in difficult to access deep-sea environments, but even in the intertidal and sub-
tidal zone either because not enough work has been put into taxonomic surveys, or mem-
bers of Sabellida were not among targeted groups. It is expected that our understanding
of species diversity will improve after efforts (financial, logistical, technological and taxo-
nomic expertise) are devoted to fill those gaps. Herein, information about the most recent
regional surveys and taxonomic revisions is provided, and the number of species de-
scribed in these areas given as a rough approximation of their biodiversity knowledge.
The regions with the overall highest number of type localities of described species
are the coastal areas of Europe, both coasts of North America, and Central and Western
Indo-Pacific, while the areas with lower number of original descriptions are the majority
of Africa, South America, as well as Tropical Eastern Pacific and Eastern Indo-Pacific (Fig-
ure 7).
Diversity 2021, 13, 130 18 of 74
Figure 7. Number of species described for each marine realm (in alphabetical order, according to Spalding et al. [31]) and
Udvardy 1975 for limnic realms.
The current state of biodiversity knowledge and a summary of the most recent (de-
fined here as last 20 years) comprehensive checklists, faunistic and taxonomic regional
studies (excluding single species descriptions) are organised below by marine realms. Ref-
erences to main comprehensive taxonomic studies are provided as recommendations for
getting started with faunas of each realm.
Diversity 2021, 13, 130 19 of 74
Arctic
This realm covers the Arctic Ocean down to Newfoundland in the western Atlantic,
including the northern half of Iceland, northern Russia, from the White Sea to the Bering
strait, and all northern Alaska and Canada. One fabriciid, 16 sabellid species, and 16 ser-
pulids have been described from the Arctic, most of them from the Western sector of the
Arctic Ocean (Figure 7, Tables S1–S3). Knight-Jones et al. [111] reviewed species of Pseu-
dopotamilla from Iceland, Greenland and the Canadian Arctic. Jirkov’s book [112] on Arc-
tic polychaetes, that includes diagnoses, illustrations, and keys to sabellids (including fab-
riciids) and serpulids (including spirorbins), as well as the recent comprehensive illus-
trated revisions with taxonomic keys to all Arctic Serpulidae (including Spirorbinae) by
Rzhavsky et al. [113,114] are recommended for studies in this region.
Temperate Northern Atlantic
This realm is delimited in the north with the Arctic realm, and in the south reaches
the coasts of Florida, including the northern half of the Gulf of Mexico, and is delimited
in the east by the Cape Verde archipelago and the coasts of Mauritania. It also includes
the Mediterranean and the Black Sea. Sixteen fabriciids, 124 sabellids, and 108 serpulids
have been described from this realm (Figure 7). Of these, one fabriciid, 18 sabellid, and 12
serpulid species were from the Western coasts of the Atlantic Ocean and three sabellids
were from northwest Africa. All the rest were described from European waters and the
Mediterranean (Tables S1–S3).
The book by Fauvel on sedentary polychaetes of France [115] provide descriptions
and illustrations of the common species of the north eastern Atlantic and western Medi-
terranean and is still been widely used despite being outdated. Relatively more updated
sources of serpulid diversity data in the Mediterranean are books by Zibrowius [116] and
Bianchi [117] that include keys, descriptions and illustrations. The illustrated key by
Knight-Jones [118] to the British Isles and North-West Europe is recommended as an ini-
tial source of data on Sabellidae, Fabriciidae and Serpulidae. The incoming book on Fauna
Ibérica includes chapters on Fabriciidae and Sabellidae and will be a new standard refer-
ence for the region [119,120].
Despite the overall high number of species described from this region, only a few
taxonomic and faunistic studies have been carried out on Sabellida in the last 20 years in
the Atlantic provinces of this realm. In particular, fabriciids were studied by Bick [121],
species of Euchone by Bick and Randel [122], Chone by Tovar-Hernández et al. [123,124]
and Pseudopotamilla by Knight-Jones et al. [111]. However, the notable exception has been
the Mediterranean, where much taxonomic activity, with particular emphasis on intro-
duced species, has taken place recently. Some representative contributions dealing with
Mediterranean fanworms include those by Çinar (on serpulids[125], on non-indigenous
species [126]), the general annelid checklist of polychaetes from Turkey [127], Selim et al.
(on Dialychone and Paradialychone [128]), Giangrande et al. (sabellids of the Ionian Sea
[129], on Acromegalomma [130]), the general papers on annelid diversity of the Adriatic Sea
[131,132] and the fabriciids and sabellids of the Adriatic [133], the checklist of Iberian spe-
cies [134] and the most recent one by Tilic et al. [103] dealing with Amphiglena. A checklist
of the polychaetes from the Black Sea includes three fabriciids, six sabellids, and 11 serpu-
lids [135].
Temperate Northern Pacific
The western side of this realm is demarcated by the Bering Strait in the north, and an
imaginary line from Taiwan to the south of Baja California Peninsula, in the south. The
number of fabriciids described in this realm is 11, eight of them from the Eastern side
(Table S1). The number of described sabellids is 83, 37 of which from the Western side,
and 46 from the Eastern side (Table S2). Out of 92 serpulid species described from this
region, 54 are from the western side (Table S3).
Diversity 2021, 13, 130 20 of 74
The catalogue of sedentary polychaetes from California [136], still widely used for
the region, is outdated and is not recommended. The monograph of polychaetes of the
Russian Far-East [136] and its English translation [137] that remains the main source of
keys and information on polychaetes of the region, including Sabellida, is also outdated
and thus should be used with caution.The revision of spirorbins from the east Pacific coast
[137] is still the most recent source of information on this group.
The most recent literature-based annotated checklist of polychaetes from Pacific
coasts of Russia lists 37 sabellids (including fabriciids) and 40 serpulids [138]. Sabellids
from Japan were recently reported by Nishi et al. [95,139] and Yoshihara et al. [140]. Tax-
onomic studies on serpulids of Japan are summarized in the book by Imajima [141] that
provides an illustrated key to 55 species of Serpulidae, but does not include sabellids. The
most recent account of Chinese polychaetes [142] provides diagnoses and keys to 64 spe-
cies of sabellids and 98 serpulid species, and is recommended as a source of biodiversity
data and taxonomic keys for China. The complementary revision [143] includes a checklist
of most annelid groups from the South China Sea, and lists three fabriciid, 33 sabellid and
72 serpulid species. Recent revisionary studies, including taxonomic keys, from the Pacific
coast of North America have reported seven species of sabellids and more than 40 serpu-
lids in the following contributions dealing with species of Hydroides from Northern Mex-
ico [144], serpulids from the Eastern Pacific [145,146], sabellids and serpulids from north-
ern Mexico [147,148], and sabellid Acromegalomma [149] and Notaulax species also from
Northern Mexico [101].
Tropical Atlantic
This realm is delimited in the north by the Temperate Northern Atlantic realm and
in the south by an imaginary line from Rio de Janeiro in the west to the southern border
of Angola in the east. It also includes the southern half of the Gulf of Mexico and the
Caribbean. Thirteen fabriciid species have been described from western side of the realm,
specifically from the Caribbean, and none from the eastern Atlantic (Table S1). Out of 56
sabellids described in the region, only one came from the African coasts (Table S2) and of
the 72 serpulids, only 10 were described from Africa (Table S3).
Zibrowius [150] made the first study on Brazilian serpulids. Other recommended tax-
onomic studies of serpulids (other than Hydroides) of Caribbean are those by ten Hove
[151–154].
Recent studies of the Caribbean fanworms included those describing fabriciids
[27,155]; revisions of species in Chone [156] and Branchiomma [157]; records and new spe-
cies of sabellids [155,158]; and selected serpulids, such as Hydroides [159], Serpula and
Spiraserpula [160]. The tropical coasts of South America have been scarcely studied. The
checklist of polychaetes of Brazilian Tropical Atlantic region reports 11 sabellid and 24
serpulid species for the area [161–164], with no fabriciids registered so far. However, sev-
eral of those are records of species described from Europe, North America and South Af-
rica, demanding further study. Additionally, Amaral et al. [163] checklist treated many
already synonymised species as valid.
The illustrated key of Sabellidae and Fabriciidae by Tovar-Hernández and Fitzhugh
[105] includes all species currently known for the Caribbean, whereas Caribbean Serpuli-
dae are available in [165].
Western Indo-Pacific
This large realm covers most of East coast of Africa, Madagascar, Arabian (Persian)
Gulf, the Red Sea, shelf of Bay of Bengal and Andaman Sea. The number of species de-
scribed in this realm is 93, including 11 fabriciids, 30 sabellids, and 52 serpulids (Figure 7,
Tables S1–S3). Out of 52 serpulids, only eight were described from African coasts.
An influential book on Indian polychaetes [166], unfortunately, lists European spe-
cies (and even illustrates specimens collected in France) and therefore, is not recom-
mended as an identification tool beyond the generic level. The most recent checklist by
Diversity 2021, 13, 130 21 of 74
Sivadas and Carvalho [167] includes two fabriciids, 11 sabellids and 34 serpulids from
India and critically evaluated annelid species richness in the region, stressing that native
species diversity of India is severely underestimated. The relatively large number of ser-
pulids described from Sri Lanka is due to the intense work of Pillai [40,168,169]. These
publications still remain as the only source of faunal information for that region.
An annotated literature-based checklist by Wehe and Fiege [170] is the best compila-
tion of annelid diversity in the area surrounding the Arabian Peninsula. The most recent
checklist of intertidal polychaetes of Kuwait by Al-Kadari et al. [171], based on newly col-
lected material, reported seven species of Sabellidae and 12 Serpulidae. A monograph on
Serpulidae from the Suez Canal by Ben-Eliahu and ten Hove [172] included 16 species. In
the Red Sea, Perry at al. [81] reviewed of serpulids of the genus Spirobranchus and sabellids
have not been studied since Knight-Jones [173].
Central Indo-Pacific
This realm comprising the largest number of ecoregions (40) includes part of the coast
of South-East Asia, from Taiwan to Malaysia, down to Tropical Australia from Coral Bay,
in the West, to Brisbane, in the East. The eastern boundary of this region is delimited by
an imaginary line from Fiji up to the south of Japan. The realm includes the Coral Triangle
recognized as the global centre of marine biodiversity [174], and fanworms are also di-
verse in this region. Ten fabriciids, 56 sabellids, and 74 serpulids have been described from
this realm (Figure 7), mainly from the Philippines and tropical Australia (Tables S1–S3).
Other than newly described species, 78 species of Sabellidae have been reported only from
the Gulf of Thailand, Indonesian Archipelago and the Philippine Seas [98,169], and at least
11 taxa are awaiting formal description [175,176]. Serpulidae from Hong Kong were most
recently revised by Sun et al. [177], who provided illustrations, diagnoses and taxonomic
keys. Tropical Australian sabellids belonging to 12 genera have been documented in a
series of recent studies [68,69,72–74,178]. Serpulids from Kimberley (Western Australia)
were revised by Pillai [106] and those from Lizard Island (Queensland) by Kupriyanova
et al. [179], whereas the revision of the genus Hydroides in Australia [180] includes both
tropical and temperate species. The most comprehensive treatment of Australian sabellids
and serpulids is still the interactive key by Wilson et al. [181], but it is outdated in the light
of the recent studies. The digital guide [182,183] allows distinguishing 38 native and non-
indigenous species of Serpulidae and 14 Sabellidae from Australia, and includes a glos-
sary with main diagnostic features for members of both groups.
Eastern Indo-Pacific
This small in terms of the coastline length Pacific realm includes Hawaii, Marshall,
Gilbert and Ellis Islands, Central and Southeast Polynesia, Marquesas, Eastern Island, and
the shelf around them. It hosts type localities of 18 fanworms, including two fabriciids,
eight sabellids, and eight serpulids (Figure 7, Tables S1–S3).
Fauna of this realm is poorly known beyond that of Hawaii. Out of eight serpulids
described from this realm, five were described from Hawaii. The latest studies include
those on serpulids of Hawaii (Hydroides [140], a key and records excluding spirorbins
[145], records of 16 species with a key [142], and serpulids from Cross Seamounts in the
Hawaiian chain [184]. Out of eight sabellids, five were described from Hawaii, and two
species of Branchiomma were reported most recently [185]. A recent study of serpulids
from atolls of Marshall Islands [186] reported 29 serpulids (including spirorbins). Small
number of publications dealing with members of Sabellida highlights the need for taxo-
nomic work in the area.
Diversity 2021, 13, 130 22 of 74
Tropical Eastern Pacific
This realm is delimited in the North by the Cape San Lucas, Baja California, by the
northern border of Peru in the South and includes the Galapagos Islands in the West. No
fabriciids have been described in this region (Table S1) and the number of described sa-
bellids is 12, five of them originally reported from coast of Panama and the rest from fur-
ther north (Figure 7, Table S2). The number of described serpulids is 30, most of them from
Galapagos, Panama and Mexico (Figure 7, Table S3).
Recent studies of Sabellida from the region include those dedicated to Panamanian
sabellids [187], some Acromegalomma [149] and Chone [124], and those focused on sabellids
and serpulids from Mexico [145,148,188]. Three sabellids and two serpulid species intro-
duced in the Galapagos Islands were reported by Keppel et al. [189].
Temperate South America
The realm covers both Pacific and Atlantic coasts of South America, from Peru to Rio
de Janeiro, respectively. Only one fabriciid was described from this region (Table S1).
Twenty-nine sabellids have been described (Figure 7), mainly from Chile and Argentina
(Table S2), and 21 serpulids were described at a variety of localities from Brazil to Peru
(Figure7, Table S3).
The publication by Zibrowius [150] remains the most comprehensive study on Bra-
zilian serpulids in both Tropical Atlantic and Temperate South America realms. More re-
cent publications reported three species of fabriciids, 29 of sabellids and 22 species of ser-
pulids for the Brazilian part of the Temperate South America realm [163] and 27 species
of serpulids and 17 sabellids for Argentina [190]. Tovar-Hernández et al. [99] studied sa-
bellids mainly from Argentina and Chile. A key to Sabellidae and Serpulidae from conti-
nental Chile is available in [191].
Temperate South Africa
This realm includes the coastline of Namibia and South Africa as well as Amsterdam
and St. Paul Islands. It hosts type localities of 38 species of Sabellida, including four fab-
riciids, 19 sabellids and 15 serpulids (Figure 7, Tables S1–S3). Of these, 30 have been de-
scribed in the littoral zone in South Africa, indicating that less taxonomic effort has been
devoted to other areas within this region. The recent papers re-described two serpulid
species based on type material (e.g., [192,193].
Although South African polychaetes, including fanworms, were summarized in the
influential book by Day [194], most of Sabellida included in the monograph are ‘cosmo-
politan species’ with European type localities (e.g., of 27 serpulids only six have type lo-
calities in South Africa), so native Sabellida species diversity is severely underestimated.
Spirorbins from South Africa have not been reviewed since studies of Knight-Jones [195]
and Knight-Jones and Knight-Jones [196].
Temperate Australasia
The realm includes coasts of Southern Australia and New Zealand hosting type lo-
calities of 86 species of Sabellida. This number includes six fabriciids from Australia (Table
S1), 37 sabellids (28 described from the Australia and nine from New Zealand (Table S2)
and 41 serpulids (28 from Australia and 15 from New Zealand, Table S3) (Figure 7).
Spirorbins from southern Australia have not been studied since they were reviewed
by Knight-Jones et al. [197]. In New Zealand, spirorbins were studied by Vine [198], who
reported 24 species, nine of them new to science, while a list of sabellids and serpulids
was provided by Glasby and Read [199].
Sabellids from Australian temperate waters have been well documented in a series
of recent papers [68,69,72–74,200–202] along with records of temperate species. Most re-
cent papers on temperate Serpulidae are Sun et al. [203] and Styan et al. [204], whereas the
Australian Hydroides revision [180] also includes temperate species.
Diversity 2021, 13, 130 23 of 74
Southern Ocean
This large realm covers coasts of Antarctica and sub-Antarctic Islands. It hosts type
localities of a single fabriciid, 24 sabellid and 23 serpulid species (six serpulins and 17
spirorbins) (Figure 7, Tables S1–S3). Many of these species were discovered and described
as a result of Antarctic expeditions of the 19th and early 20th century (e.g., [205–210]).
The most recent contributions from the region are descriptions of two spirorbin spe-
cies from Kerguelen and Bouvet Islands [211]; species of Perkinsiana [212] and reports of
19 still undescribed sabellids from Falkland Islands [213],demonstrating the underesti-
mated diversity. There is no contribution summarizing Sabellida species diversity of this
region.
3.3. Diagnostic Characters and Techniques Used for Species Discrimination
Most species within Sabellida are characterised by a unique combination of morpho-
logical features. The most useful morphological characters used for Sabellidae species
identification are summarised in Capa et al. [24]; for Fabriciidae, see Bick [4]; for Serpuli-
dae, see ten Hove and Kupriyanova [110] and Kupriyanova et al. [214]. Since detailed
information is provided in these thorough revisions, only succinct identification guide-
lines are given below for each family.
3.3.1. Shortcuts to Identification of Fabriciidae
The small body size (most species are less than 5 mm long) and the absence of signif-
icant diagnostic characters make the identification of Fabriciidae difficult. All fabriciid
species possess a radiolar crown with three pairs of radioles (Figure 8a–c). The branches
are formed by successive longitudinal splitting of the radioles. The symmetrical branching
of the radioles leads to bi-pectinated radioles, as found in most genera (Figure 8c), whereas
pectinated radioles result in asymmetrical branching (Figure 8b), as in Manayunkia and
Monroika only [4]. Ventral filamentous appendages, present in some genera, are associated
with the radiolar crown (Figure 8b). These appendages have been described as non-vas-
cularized (e.g., in all species of Fabriciola, Pseudofabricia Cantone, 1972 and Rubifabriciola)
or vascularized (e.g., in all species of Augeneriella, Echinofabricia, Manayunkia, Monroika and
Pseudoaugeneriella, and also some species of Fabricinuda and Pseudofabriciola) [57]. These
appendages are branched only among species of Augeneriella.
Peristomial eyes (Figure 8f) are developed among most species of Fabriciidae, black
in most fabriciids, or red, as in Echinofabricia and Rubifabriciola [27].
The presence of thoracic pseudospatulate and transitional (=pilose, after Jones 1974)
chaetae is of taxonomic significance [4] (Figure 8g,k). However, the distribution of pseu-
dospatulate chaetae is not consistent within the genera. These chaetae occur on chaetigers
2–5 (some Manayunkia species), 2–8 (Raficiba barryi Fitzhugh, 2001), 3–5 (Monroika africana
and most Novafabricia species), 3–6 (Pseudoaugeneriella, some species of Augeneriella and
Novafabricia), 3–7 (Brifacia metastellaris Fitzhugh, 1998, Fabricia stellaris, Parafabricia ventric-
ingulata Fitzhugh, 1992, and some species of Augeneriella and Fabricinuda), or 3–8 (most
Fabricinuda species) [4]. Pseudospatulate chaetae are absent in Bansella, Echinofabricia, Fab-
riciola, Pseudofabriciola and Rubifabriciola [4]. Species of Rubifabriciola have pin-head chaetae
on the abdominal neuropodia [27] (Figure 8m). These chaetae have a blunt tip and a num-
ber of small teeth apically. Transitional chaetae (Figure 8k) replacing thoracic uncini occur
on the last thoracic chaetigers (chaetigers 6–8) of Brandtika spp., Manayunkia godlewskii
(Nusbaum, 1901), females of M. occidentalis Atkinson, Bartholomew and Rouse, 2020 and
M. zenkewitschii Sitnikova, Shcherbakov and Kharchenko, 1997 [4,215–217].
Diversity 2021, 13, 130 24 of 74
Figure 8. Main diagnostic characters for members of Fabriciidae. (a) Fabricia stellaris, dorsal view; (b) Pectinated radiolar
branching pattern, Manayunkia athalassia; (c) Bi-pectinated radiolar branching pattern, F. stellaris; (d) Thoracic uncini of
Manayunkia zenkewitschii; (e) Gamete bearing region in thorax; (f) Branchial heart (bh), spermathecal (s) and peristomial
eye (pe), in this order; (g) Thoracic chaetae, M. athalassia; (h) Abdominal uncini, Pseudoaugeneriella nigra; (i) Pygidial eye
(py); (j) Abdominal chaetae, M. athalassia; (k) Thoracic transitional chaetae (below), Manayunkia godlewskii; (l) Chaetal in-
version, M. athalassia; (m) Abdominal pin-ead chaeta, Rubifabriciola tonerella. (a,c by A. Dietrich; b by G. Christie).
Diversity 2021, 13, 130 25 of 74
The thoracic uncini are characterized by a long manubrium (homologous to handle
in sabellids) and a main fang surmounted by a series of smaller teeth (Figure 8d). A
slightly offset medium-sized tooth occurs between the large main fang and the smaller
apical teeth in Augeneriella, Fabricia, Fabricinuda, Monroika, Novafabricia, Parafabricia,
Pseudofabricia, Pseudoaugeneriella and some species of Pseudofabriciola [42]. The apical teeth
can also be approximately of the same size in Echinofabricia, or may gradually decrease in
size away from the main fang as in Fabriciola, Manayunkia and some species of Pseudofab-
riciola [57]. The abdominal uncini usually exhibit multiple rows of equal-sized teeth (Fig-
ure 8h). Only members of Novafabricia chilensis (Hartmann-Schröder, 1962) and N. gerdi
(Hartmann-Schröder, 1974) have uncini with a single row of teeth.
Fabriciids usually have three abdominal chaetigers (Figure 8j). However, Brandtika
spp., Fabriciola minuta Rouse, 1996, and Monroika africana have two abdominal chaetigers,
while Echinofabricia spp. has four [215,218,219].
The pygidium is triangular or bluntly rounded in most species, but has a ventral de-
pression in Pseudofabriciola analis Fitzhugh, Giangrande and Simboura, 1994. A pair of
black or dark brown pygidial eyes is present in most species of Fabriciidae (Figure 8j).
They are red in Echinofabricia (disappearing after fixation) and Rubifabriciola (persisting
after fixation), but are always absent in all species of Manayunkia and Monroika, Fabriciola
parvus Rouse, 1993 and two undescribed deep-sea species [220]. Unique among members
of Sabellida, emergent spicules are present in the epithelium of Echinofabricia species [27].
3.3.2. Shortcuts to Identification of Sabellidae
Sabellids are relatively easily to visually identify to the generic level because genera
are provided with unique and conspicuous diagnostic features (Figure 9). The diversity
of radiolar eyes within members of Sabellidae is remarkable (e.g., Figure 9a), and the eye
number, type and arrangement offer a very powerful taxonomic aid for genera and spe-
cies identification [24,69,221]. The large compound eyes located in the tips of dorsal radi-
oles are unequivocally characteristic of members of Acromegalomma, whereas the large sin-
gle and bulging compound eyes arranged, in a longitudinal row on the outer margin of
the radioles, are typical of members of Pseudopotamilla Bush, 1904 (Figure 9a). Anamobaea
Krøyer, 1856 and Notaulax Tauber, 1879 are easily recognized due to the presence of long
radiolar lobes with dorsal and ventral flanges. Other generic synapomorphies related to
the radiolar morphology are the dichotomously branching radioles, found only in Schizo-
branchia Bush, 1905 and Eudistylia Bush, 1905 (most likely due to a regeneration processes
[111,222]), and the external paired radiolar appendages, called stylodes, in members of
Branchiomma (Figure 9e). Euchone is recognisable by the presence of a typical pre-pygidial
depression with lateral wings, but this character is only visible in adults. Species of
Claviramus Fitzhugh, 2002 have radiolar tips with expanded flanges, rolled inwards or
bilobed, this feature is easily seen if radioles are complete. Potamethus Chamberlin, 1919 is
recognizable due the very long collar (2–4 times the length of next thoracic segment).
Other genera are recognised by unique traits, which are not evident to a naked eye and
require optic aids. These are the typical companion chaetae of members of Parasabella, the
absence of posterior peristomial ring collar in members of Amphiglena, or the presence of
a broad, oblique glandular (clitellum-like) ring on third abdominal segment in Eu-
chonoides. Internal structures, such as the rows of vacuolated cells supporting radioles,
dorsal lips and radiolar appendages, are of taxonomic significance and often used for spe-
cies discrimination [64,102,122,223–226].
Diversity 2021, 13, 130 26 of 74
Figure 9. Main diagnostic characters for members of Sabellidae. (a) Parasabella microphtalma, ventral view; (b) Compound
eyes on dorsal radioles, Pseudopotamilla sp.; (c) Radiolar internal structures, Chone infundibiliformis; (d) Pygidial morphol-
ogy, Bispira sp.; (e) Radiolar stylodes, Branchiomma sp.; (f) Collar, radiolar lobes and glandular girdle in second chaetiger,
Jasmineira sp.; (g) Abdominal chaetae, Parasabella sp.; (h) Thoracic chaetae, Parasabella sp.; (i) Thoracic uncini and compan-
ion chaetae, Notaulax sp.; (j) Parapodia morphology and arrangement of chaetae, Bispira sp.; (k) Abdominal uncini, No-
taulax sp.
Diversity 2021, 13, 130 27 of 74
3.3.3. Serpulidae Diagnostic Characters
Within Serpulidae, body symmetry separates serpulins from spirorbins, as serpulins
are bilaterally symmetrical, while spirorbins are curved in the direction of the tube coil.
Specific identification has been based on a combination of characters such as morphology
of the operculum and opercular peduncle, degree of development of the collar and tho-
racic membranes, and chaetal structures (Figure 10). Tube morphology and ultrastructure
are important for identification of both extant and fossil taxa [227] (Figure 10a–c). Serpulid
genera have been described on the basis of unique characters or on unique combinations
of characters (or absence of characters), rather than on presence of shared derived charac-
ters. Mentioned here morphological characters used for serpulid identification have been
described in details and illustrated in ten Hove and Kupriyanova [110], Wong et al. [228],
Kupriyanova et al. [214].
The operculum that is present in most serpulins and in all spirorbins is one of the
most important diagnostic characters (Figure 10d–h). The shape of the operculum varies
significantly, ranging from soft transparent vesicles to complex structures reinforced with
chitinous or calcareous endplates and spines. The distinct funnel-shaped opercula of Cru-
cigera and Serpula are composed of numerous radii (Figure 10d), while in Hydroides the
funnel is topped with a verticil of chitinous spines (Figure 10e). The operculum-bearing
radiole can be identical to others (e.g., Filograna, Apomatus Philippi, 1844), but usually is
modified into a smooth peduncle (Figure 10j). In cross-section, the peduncle is commonly
cylindrical, but it is flat ribbon-like in members of the genus Metavermilia Bush, 1905. Be-
low the operculum, the peduncle may bear diagnostic distal wings (e.g., Spirobranchus)
(Figure 10h).
The collar segment bears only notopodial (collar) chaetae that may be absent (e.g.,
Ditrupa Berkeley, 1835, Marifugia, Placostegus Philippi, 1844). The collar chaetae may bear
four types of diagnostic modified chaetae: bayonet-type (e.g., Serpula, Hydroides, Figure
10i), fin-and-blade (e.g., Chitinopoma, Protis Ehlers, 1887), Spirobranchus-type (e.g., Spiro-
branchus, Laminatubus ten Hove and Zibrowius, 1986) and Ficopomatus-type (see [214]).
Tonguelets, located between collar lobes, are diagnostic of the genera Spirobranchus and
Pyrgopolon de Montfort, 1808. The thoracic membranes (Figure 10l) may be ending at the
first (Ditrupa) or the second thoracic chaetiger (Chitinopoma), or may continue to the mid-
thorax (e.g., Pomatostegus, Vermiliopsis Saint-Joseph, 1894), to the last thoracic chaetiger
(some Spiraserpula Regenhardt, 1961 and Metavermilia spp.), or past the end of the thorax
forming the ventral apron (e.g., Ficopomatus, Serpula, Hydroides, Protula, Spirobranchus)
(Figure 10m). In most genera the thorax consists of seven chaetigerous segments (first with
collar chaetae only and six with both notopodia and neuropodia). The number of thoracic
segments varies from five (Tanturia Ben-Eliahu, 1976 and Bathyditrupa Kupriyanova, 1993)
or six (Laminatubus, Hyalopomatus Marenzeller, 1878, Spirodiscus Fauvel, 1909) to 10 (Kim-
berleya Pillai, 2009), while spirorbins have three to five thoracic segments.
In the posterior thoracic segments chaetae are supplemented by diagnostically im-
portant Apomatus or sickle-shaped chaetae (Figure 10n). The number of vertical teeth rows
in the thoracic and anterior abdominal uncini (saw-shaped, with one row of teeth, e.g.,
Hydroides, Serpula (Figure 10o); rasp-shaped, with several rows of teeth, e.g., Hyalopomatus,
Placostegus, Marifugia; or saw-to rasp-shaped, from with one tooth distally to a row of up
to five teeth near the peg, e.g., Filogranula Langerhans, 1884) is diagnostic. Posterior ab-
dominal uncini are always rasp-shaped (Figure 10p). Even more important is the shape of
the anterior tooth of uncini. The anterior teeth are either pointed fangs (e.g., Filograna,
Hydroides, and Serpula (Figure 10o, p), and pileolariin spirorbins), or a wide variety of
blunt ‘wedge’ shaped pegs (e.g., Pseudovermilia Bush, 1907, Spirobranchus, Galeolaria, Fi-
copomatus, Hyalopomatus, Chitinopoma, Pyrgolopon, Vermiliopsis, Protula).
The shape of abdominal chaetae is very important for generic diagnostics (Figure
10q–s). The simplest forms are capillary (Bathyditrupa) and acicular (Paumotella Chamber-
lin, 1919). The flat trumpet-shaped chaetae with a single row of teeth are found in Cruci-
Diversity 2021, 13, 130 28 of 74
gera, Hydroides, Serpula (Figure 10 q). Abdominal chaetae previously referred to as ‘genic-
ulate’ are two distinct types of chaetae, true trumpet-shaped, typical for, e.g., Ficopomatus,
Galeolaria, Placostegus, Spirobranchus (Figure 10s) that lack thoracic ‘Apomatus’ chaetae, and
flat geniculate are found in taxa with Apomatus chaetae, e.g., spirorbins, Apomatus, Chitin-
opoma, Vermiliopsis (Figure 10r).
Figure 10. Main diagnostic characters for members of Serpulidae. Centre: lateral view of a Serpula specimen removed from
the tube; (a–d) Tubes: Hyalopomatus biformis (a), Serpula vermicularis (b), Filograna implexa (c), Circeis armoricana (d); (e–h)
Opercula: Serpula (e), Hydroides (f), Spirobranchus (g) showing distal wings (h); (i) Special (bayonet) collar chaetae of Hy-
droides; (j) Peduncle; (k) Pseudoperculum; (l) Thoracic membranes; (m) Apron; (n) Thoracic Apomatus (sickle-shaped)
chaetae of Vermiliopsis; (o) Thoracic saw-shaped uncini of Hydroides; (p) Posterior abdominal rasp-shaped uncini of Hy-
droides; (q–s) Abdominal chaetae: flat trumpet-shaped of Serpula; (q), flat geniculate of Vermiliopsis; (r) true trumpet-shaped
of Spirobranchus (s). (a–c,f by E. Wong, d by A. Rzhavsky, e by G. Rouse, g,h by A. Semenov, j–m (central photo of Serpula)
by F. Verbiest, n–s (SEM images) by S. Lindsay).
Diversity 2021, 13, 130 29 of 74
3.3.4. Data and Techniques Used for Species Identification and Systematics
Initial Collection, Observation and Fixation in the Field
To identify individuals to the species level, specimens are first examined under a
stereomicroscope. If conditions in the field permit, they should be examined and photo-
graphed alive to document colouration. Removing individuals from their tubes, specially
serpulids, without any tube or specimen damage is rarely possible unless 0.05% phenol-
seawater solution is used for several hours [229–231]. This method does not work in spi-
rorbins (Bick pers. obs.) and it is unknown whether DNA is affected by phenol. It is im-
portant to examine and photograph intact tubes if they are broken to extract animals.
Fixation and preservation of specimens vary depending on further purposes of sam-
ples. Specimens aimed for a morphological study only are commonly fixed in a 4% solu-
tion of formaldehyde in sea water for 24–48 h, if possible after relaxation of individuals
(in magnesium chloride). Animals are then rinsed in distilled water and preserved in 70–
80% ethanol. For scanning electron microscopy (SEM) osmium tetraoxide is preferable as
a fixative.
Specimens aimed for genetic sequencing should avoid all contact with formaldehyde
as it degrades DNA, impeding amplification of the usual size fragments to be sequenced.
Best procedures for DNA sequencing include fixation of fresh specimens in high concen-
tration ethanol (the higher the better) and storing samples at 4–6 °C, or at least not in direct
sunlight at room temperature. The ethanol should be changed at least once, preferably
more often. RNA sequencing may need other protocols such as fixing with RNAlater. For
integrative (morphological and molecular) studies, a tissue sample taken from a specimen
should be fixed in ethanol and stored in a fridge or a freezer, while the rest of the specimen
should be fixed in formalin and preserved in ethanol. Further reading on fixation and
preservation of samples is found at Rouse and Pleijel [232].
Morphological Studies of Preserved Specimens
When examining freshly preserved or museum material lacking natural pigmenta-
tion, staining with methyl (or methylene) green (blue) helps to increase contrast and to
reveal glandular patterns, including thoracic ventral shields and glandular girdles [24].
Examination of chaetae requires higher magnification (>100x), therefore, chaetae and
noto- and neuropodia are dissected from the specimen, placed on a slide in a drop of eth-
anol, glycerin or permanent media, and covered with a cover glass. Applying gentle pres-
sure on the cover glass ensures that uncini and chaetae lay in a lateral position. Using SEM
is essential to reveal details of external features, such as ciliation, chaetal morphology and
body wall microstructure, as well as anatomical features not easily distinguished in small
specimens (appendages of the radiolar crown, for example). SEM is also an indispensable
tool to examine tube ultrastructure, important for taxonomy of serpulids (reviewed by
Ippolitov et al. [227]).
Structures of the radiolar crown, e.g., the rows of vacuolated cells supporting the
radioles, dorsal and ventral lips, dorsal radiolar and pinnular as well as ventral radiolar
appendages, and a parallel lamella in Sabellidae, dorsal lips and ventral filamentous ap-
pendages in Fabriciidae, are examined after fine sections with a sharp blade or, better,
histological semi-thin sections are made and mounted on temporary or permanent slides,
and stained with solutions, such as Mallory or Cason (e.g., [226]).
Morphometric characters such as counts (e.g., numbers of radioles or pinnules),
measurements and proportions of soft body parts (e.g., thorax to abdomen ratio, length of
dorsal lips) have traditionally been considered diagnostic for some taxa, but individuals
may show sexual dimorphism [216], size and age-related variability ([70,233] or their size
may be affected by anaesthetization and fixation techniques [234], which needs to be con-
sidered when comparing material.
For drawings to be made to scale, a camera Lucida attached to both the stereo- and
the compound scopes is used. Traditional ink drawing (pencil sketching followed by India
Diversity 2021, 13, 130 30 of 74
ink tracing) is currently supplemented or replaced by digital tracing of scanned pencil
sketches, using a drawing pad (e.g., [235]). Advances in digital photography and universal
availability of microscope-mounted digital cameras and Z-stacking software also resulted
in photographs of live or preserved specimens, rather than line drawings being used in
species descriptions. Use of SEM micrographs helps to illustrate both chaetal and soft
body diagnostic features characters with precision and objectivity. Micro-computed to-
mography techniques have been proved useful in studies of internal anatomy in sabellids
and serpulids ([49,236,237], and may offer taxonomically useful information.
Genetic Data
Genetic methods have been used in studies of Sabellida for nearly 20 years. The ear-
liest publication by Patty et al. [238] used the C1 regions of 28S (123 bp) of 16 species to
assess evolutionary relationships among Sabellidae. Kupriyanova et al. [45] published the
first phylogeny of Serpulidae based on analyses of 18S rDNA, 28S rDNA, and morpho-
logical characters of 29 taxa. Combination of molecular (18S rDNA, the D1 region of 28S
rDNA, and histone H3) and morphological datasets have been used to assess for the first
time the relationships within Fabriciidae [27]. Other studies of Sabellida have used a lim-
ited number of molecular markers commonly used in polychaete systematics [239]. Cur-
rently, the number of sequences in GenBank is 246 for Fabriciidae, 814 for Sabellidae, and
2880 for Serpulidae, figures that indicate the relative larger effort put into molecular stud-
ies in serpulids compared to the other two families (Figure 11). In addition, “BOLD Sys-
tems [36] includes 443 barcodes (fragments of COI gene) of Serpulidae, 349 of these rec-
ords are mined from GenBank and 19 diferent BOLD records are also shared with Gen-
Bank. Similarly, BOLD holds 692 COI sabellid barcodes, 399 of which are mined from
GenBank and 148 BOLD records that were also uploaded in GenBank. Among the uni-
dentified 105 sabellids there is an unknown number of sequences that belong to fabriciids
as this database still follows the old clasitication. Sumarising, there are 75 serpulid and
145 sabellid/fabriciid COI sequences available in BOLD, in addition to those found in Gen-
Bank.
The universal DNA barcoding fragment of COI gene is by far the most popular
marker for the Fabriciidae, accounting for 54% (133 sequences) of the sequences available
for this group (Figure 11), and Sabellidae, 38% (387 sequences) (Figure 11). For Serpulidae,
despite all efforts (reviewed in Sun et al. [78]), no COI sequences had been available until
Carr et al. [240] reported six. However, Sun et al. [76], who developed genus-specific pri-
mers to generate COI sequences for 11 species of Hydroides, showed that “serpulid” se-
quences in Carr et al. [240] are likely from bacteria. Progress in COI barcoding in serpulids
is mainly a result of new primer development [77]. Currently, the number of COI se-
quences for members of Serpulidae in Genbank is 564 (not including those mentioned
problematic sequences [240], Figure 11).
Other markers widely used in systematics studies of Sabellida are nuclear 18S (642
sequences for Serpulidae, 31 for Sabellidae, 22 for Fabriciidae), 28S RNA (387 for Serpuli-
dae, 60 for Sabellidae, 26 for Fabriciidae), mitochondrial cytochrome b (cytb) (637 for Ser-
pulidae and 54 for Sabellidae), nuclear internal transcribed spacer (ITS2), ATP synthase,
and Histone H3 (Figure 11). Mitochondrial 16S, widely used in sabellids (50 sequences in
Genbank), has not been successfully amplified for serpulids.
Manayunkia is the fabriciid genus with most sequences in GenBank (179). The Sabel-
lidae genera with most available sequences are Branchiomma (259), followed by Sabella (86)
and Sabellastarte (61). Among the serpulids, Hydroides is the genus with the highest num-
ber of sequences in GenBank (1366), followed by Spirobranchus (601); all the rest have at
least one order of magnitude less sequences available (Figure 12).
Diversity 2021, 13, 130 31 of 74
Figure 11. Number of sequences available in Genbank for Fabriciidae, Sabellidae; and Serpulidae.
Diversity 2021, 13, 130 32 of 74
Figure 12. Number of DNA sequences available in GenBank for genera in Fabriciidae, Sabellidae, and Serpulidae.
Although Sabellida are still behind other annelids in terms of genomic approach, sev-
eral studies recently reported mitochondrial genomes and used transcriptomes for resolv-
ing systematics and evolutionary questions within this group. The first Sabellida mito-
chondrial genome was published for the serpulid Spirobranchus giganteus (Pallas, 1776)
[241]. Mitochondrial genome sequences of ten Hydroides species have been reported in Sun
Diversity 2021, 13, 130 33 of 74
et al. [242]. The mitochondrial genomes of Sabella spallanzanii (Gmelin, 1791) and freshwa-
ter fabriciid Manayunkia occidentalis were recently published [243,244]. The phylogeny by
Tilic et al. [3] includes transcriptome sequences of 20 species of Sabellida (three fabriciids,
15 sabellids, and two serpulids), containing up to 3015 orthologous genes. Several other
studies have also dealt with expressed sequence tag (EST) libraries and transcriptomes to
address molecular mechanisms of larval settlement, or gene order and loss [245] in serpu-
lids, adding up to 4205 sequences of mRNAs of larval cDNA library. With current fast
adoption of the genomic approach, the number of sequences is expected to raise dramat-
ically in the near future.
Species Delimitation and Identification
Application of molecular methods in combination with traditional morphological
techniques or alone have expanded in the last two decades with regard to species delimi-
tation in annelids in general, and in Sabellida, in particular. These methods are sustained
by the definition of species as independently evolving entities (metapopulations), that are
genetically (and often phenotypically) distinct [246,247]. Thus, species are expected to be
reciprocally monophyletic clusters, morphologically distinct and/or genetically divergent,
as a result of evolutionary forces applied to closely related lineages. Molecular-based ap-
proaches have not only improved species delimitation by providing additional evidence
to morphological taxonomy, but also helped to reveal cryptic (only genetically distinct)
species [248].
In Fabriciidae, even though species appear morphologically similar due to the ani-
mal’s small size and the diagnostic features being difficult to recognize by non-specialists,
molecular approach to species identification and delimitation is still uncommon. Only one
species, Manayunkia occidentalis, has been described based mainly on genetic data [216].
In Sabellidae, boundaries between species within the genera Amphiglena, Bran-
chiomma, Parasabella, Pseudobranchiomma Jones, 1962, Sabellastarte and Sabellomma
Nogueira, Fitzhugh and Rossi, 2010 were assessed with molecular and morphological
data [70,72–74]. Results revealed cryptic diversity hidden in species complexes and helped
to assess the diagnostic features traditionally used for morphological species identifica-
tion [2,27,72–74,103,140].
In Serpulidae, the study of Halt et al. [249] was the first to name a new species in
Sabellida without morphological indicators, after analyses of DNA revealed two cryptic
species with non-overlapping distributions within Galeolaria caespitosa Lamarck, 1818. An-
other study revealed three genetic species with overlapping distributions within Ficopo-
matus enigmaticus (Fauvel, 1923), two cryptic and one morphologically distinct [204]. A
combination of molecular and morphological data helped to partially resolve species com-
plexes within the genera Hydroides [203,250,251] and Spirobranchus [84,193,252].
The idea of ‘DNA barcoding’ is that a species can be uniquely characterised by a short
DNA fragment and then identified by comparing such a fragment from an unknown spec-
imen to a reference DNA sequence [253]. Initially, a 650 base pair fragment of the mito-
chondrial COI was proposed as a standard barcoding gene for animals [253] because of
its variability among closely related taxa and supposed ease of amplification. Later, how-
ever, a number of other mitochondrial markers (cytb, e.g., [81–84,193,204,249,252] and nu-
clear (ITS, [82,249]) have been used, especially in serpulids where amplification of COI
proved to be challenging. The first attempts to use DNA data alone while ignoring any
morphological and biogeographic evidence to identify potentially invasive serpulids
[254], were rather a failure. The authors mistakenly claimed discovery of an Australian
species Spirobranchus taeniatus (Lamarck, 1818) (mostly likely Spirobranchus triqueter) and
North American Serpula columbiana Johnson, 1901 (almost certainly Serpula vermicularis)
attached to drifting marine litter in the Mediterranean, after comparing (minimum 97%
nucleotide identity was accepted) partial sequences of the conservative (thus unsuitable
for species-level barcoding) 18S gene with the limited set of sequences available in Gen-
Bank. Similarly, Langeneck et al. [255] criticised another paper by the same authors (Rech
Diversity 2021, 13, 130 34 of 74
et al. [256]) who identified specimens associated with floating debris in the Lagoon of
Venice as Hydroides sanctaecrucis, suggesting its presence in the Mediterranean might have
been overlooked due to misidentification as common H. dianthus. Rech et al. [256] again
did not examine the morphology of the specimens and used 18S sequences for identifica-
tion, accepting an identity ≥ 97% with sequences of H. sanctaecrucis in GenBank. However,
18S rDNA sequences are ill-suited for molecular identification because they have identity
close to 100% in closely related species. The low sequence identity shows that the speci-
mens in Rech et al. [256] study did not belong to H. sanctaecrucis, and the species name
should be removed from checklists of species non-indigenous for the Mediterranean [255].
3.4. Ecology, Distribution and Biogeography
3.4.1. Ecology
Fabriciidae
A review of the ecology and biology of Fabriciidae was published recently [4]. Most
fabriciids occur in intertidal and subtidal zones, mainly in sheltered areas on sandy,
muddy or rocky sediments, in mangroves, on red and green algal mats, and in seagrass
beds, with low benthic species richness.
Fabriciids are mainly distributed in marine and brackish ecosystems worldwide, but
species of the genus Manayunkia are also common in freshwater, and even hypersaline
lakes, where they survive salinities of 82 psu for several months [257]. The abundance of
some species tends to be very high in habitats with low biodiversity. The highest abun-
dances of Fabricia stellaris and Manayunkia aestuarina (over 106 ind. m−2) have been reported
in physiologically stressful conditions, such as sediments with a high organic matter con-
tent and waters of highly variable salinities [258–261]. A reduction in organic matter con-
tent from 1.8% to 1.0% in the Baltic Sea was followed by a reduction in fabriciid abundance
from 16 000 to 6000 ind. m−2 [262]. Giangrande et al. [263] found five fabriciid species in a
coastal Mediterranean system naturally acidified by carbon dioxide vent emissions.
Among these, Parafabricia mazzellae Giangrande, Gambi, Micheli and Kroeker, 2014 and
Brifacia aragonensis Giangrande, Gambi, Micheli and Kroeker, 2014 were most abundant
even in the extremely low pH zone (pH 6.6–7.2).
Fabriciidae species produce flexible tubes consisting of the finest sediment particles
stabilized by mucus. Detritus might also be deposited on the outside of the tubes. Fabrici-
ids are not obligatory tube dwellers and they can voluntarily leave their tubes and build
new ones. When outside, they crawl with the posterior end in front, while the radiolar
crown is folded up and dragged behind [264,265].
Fabriciids are suspension-feeders like other Sabellida, but Manayunkia spp. are de-
posit feeders. In addition to detritus, they ingest bacteria, heterotrophic protozoa, cyano-
phyceans and diatoms. The sizes of the ingested particles range from 1–2 µm to 2–7 µm
and occasionally reach up to 20 µm [265].
Some fabriciids are commensals of molluscs, e.g., the freshwater Brandtika asiatica
Jones, 1974 and Monroika africana [215,266], or the marine Rubifabriciola tonerella (Banse,
1959) and Novafabricia infratorquata (Fitzhugh, 1983) [231], but these species have been also
found in other substrates. Another example of commensalism is the occurrence of peritri-
chous ciliates on anterior chaetigers in Manayunkia aestuarina [4]. Manayunkia speciosa
Leidy, 1859 is an obligate invertebrate host of the myxozoan parasites Ceratonova shasta
(Noble, 1950) and Parvicapsula minibicornis Kent, Whitaker and Dawe, 1997, which cause
ceratomyxosis in salmon and trout in North America [267,268].
Diversity 2021, 13, 130 35 of 74
Sabellidae
A review of ecology and biology of sabellids was recently published [24]. Sabellids
are able to inhabit either hard or soft sediments. Species of Amphiglena, Bispira, Perkinsiana,
Pseudobranchiomma, Sabellomma, Sabellastarte and Stylomma Knight-Jones, 1997 mainly in-
habit littoral hard substrates, as epibionts of algae, or associated with biogenic structures,
including live coral or rubble [2,68,73,74,269,270]. Some species of Perkinsiana and Pseudo-
potamilla associated with dead coral and limestone sediments are capable of actively bor-
ing into the calcium carbonate [271,272].
Several species of Acromegalomma, Amphiglena, Branchiomma, Eudistylia, Notaulax, Par-
asabella, Pseudobranchiomma and Sabella are abundant in biofouling communities
[72,74,101,147,273–275,276]. Some of the soft bottom species need large and stable enough
surface (shell, rock, holdfast or root) to attach to build their tubes. This is characteristic of
species of Branchiomma, Parasabella, Bispira manicata (Grube, 1878), Acromegalomma, or the
Mediterranean Sabella spallanzanii, a species associated, in natural conditions, to Posidonia
K. Koenig seagrass roots [73,129,133,277,278]. However, other soft-bottom species can
build tubes within the sediment grains, like Euchonoides meone Magalhães, Bailey-Brock
and Tovar-Hernández, 2020. This species is found near a sewage outfall in Hawaii, reach-
ing 141,046 ind/m2, the highest densities ever reported for Sabellidae [279].
Sabellids have been only recently found in chemosynthesis-based environments,
such as hydrothermal vents, methane seeps and organic falls, and their diversity in such
habitats is poorly understood. Bispira wireni (Johansson, 1922) was reported from a hydro-
thermal vent from Okinawa, Japan [280]. Jasmineira sp. and an undetermined sabellid col-
onized bone and sunken wood in the southwestern Indian Ridge [281]. Unidentified sa-
bellids have been reported from methane seeps in the Gulf of Mexico [282] and Chile [283].
Recently, an undescribed species of Bispira was found at a deep-sea cold seep off the Pa-
cific coast of Costa Rica [284].
Although the group is typically marine, a few exceptional species have adapted to
brackish and even fresh water environments. The most remarkable example is the exclu-
sively freshwater genus Caobangia. Euryhaline sabellids are, for example, the Australian
Desdemona aniara Hutchings and Murray, 1984 and Laonome triangularis Hutchings and
Murray, 1984, Indian Potamilla leptochaeta Southern, 1921, American Aracia sinaloae Tovar-
Hernández, 2014, and the cryptogenic Desdemona ornata Banse, 1957, Euchone limnicola Re-
ish, 1959, and Laonome xeprovala Bick and Bastrop, 2018 [68,102,285–290]. Some species
typically found in fully marine conditions are tolerant to brackish water conditions, e.g.,
members of Euchone, Branchiomma and Parasabella [147,291], while Laonome calida Capa,
2007 and L. albicingillum Hsieh, 1995 have been reported in environments ranging from
fully marine to freshwater [68,292–294].
With the exception of Glomerula piloseta, that inhabits calcareous tubes, all sabellids
build tubes by secreting the mucous base and enforcing it with different size particles they
attach, including mud, sand, feces or biogenic fragments [24]. Smaller species are more
liable to leave the tubes if disturbed and can build new ones [295], but larger species, even
if capable to build new tubes, tend to inhabit the same one for longer periods or their
whole lives [270,296,297].
Until very recently, sabellids have been found mostly in areas of high productivity
and assumed to be obligatory suspension feeders [298]. However, a sabellid-bacterial
symbiosis, fueled by methane, between a still undescribed species of Bispira and methane-
oxidizing Methylococcales bacteria, has recently been reported from a methane seep [284].
This makes Bispira a new addition to the list of annelids (including Siboglinidae and two
new serpulids of the genus Laminatubus, see below) relaying on chemosynthetic symbi-
onts for nutrition.
Associations of sabellids with other organisms relate to their ability to bore into cal-
cium carbonate. The seven species of Caobangia are commensals or parasites of freshwater
gastropods and bivalves in rivers of southeastern Asia [289,299]. Terebrasabella heterounci-
Diversity 2021, 13, 130 36 of 74
nata Fitzhugh and Rouse, 1999 bores into the shells of marine gastropods, including aba-
lones and limpets, in South Africa and California [66,300,301]. Notaulax montiporicola To-
var-Hernández and ten Hove, 2020 associated with the living coral Montipora nodosa
(Dana, 1846) does not bore into coral, but uses crevices to settle and allows coral tissue to
grow around its tube [101].
Serpulidae
A review of ecology and biology of serpulids was recently published [214]. Serpulids
are typical on hard substrates in all marine environments. Inhabitants of areas with pre-
dominantly soft-sediments always attach to rocky outcrops, stones and shells, and can
deal with high sedimentation rate by building their tubes upwards to avoid being buried
in the sediment [302]. Many serpulids are notorious opportunistic foulers, capable of col-
onising any available hard substrates. The ability to settle and build large aggregations on
human-made surfaces makes serpulids important and troublesome members of fouling
communities. However, some show high habitat selectivity, resulting from non-random
larval settlement and juvenile survival (reviewed by Kupriyanova et al. [303]). A few un-
usual serpulids are pre-adapted to living unattached on soft substrates in subtidal-shelf
(Ditrupa) [110] or bathyal-abyssal (Bathyditrupa and Spirodiscus) environments [107]. How-
ever, larvae of free-living Ditrupa need to attach initially to small particles during settle-
ment and metamorphosis to start building the tube [304].
Serpulids are some of recognizable animals to inhabit the periphery of seeps and hy-
drothermal vents. Laminatubus alvini ten Hove and Zibrowius, 1986 and Protis hydrother-
mica ten Hove and Zibrowius, 1986 were the first serpulids to be formally described from
vent communities of East Pacific Rise and Laminatubus is known from other seeps (e.g.,
Pescadero Transform Fault, Gulf of California) and vents, e.g., Alarcon Rise, Gulf of Cali-
fornia [305]. Hyalopomatus mironovi Kupriyanova, 1993 and Protis sp. were reported from
hydrothermal vents of North Fiji [306]. Less is known about seep-associated serpulids, as
more species have been reported from fossil than modern hydrocarbon seeps [307]. Ser-
pulids (tentatively identified as members of Neovermilia Day, 1961) have been reported
from cold seep communities in Nankai Trough [308], the Peruvian active margin [309],
the Terevaka ridge [310], the Peru Trench, Middle American Trench off Mexico [311], and
the Barbados prism [312].
Although serpulids are predominately marine, some species of Hydroides tolerate
mixohaline conditions (e.g., [313], for H. elegans (Haswell, 1883)), while representatives of
Ficopomatus can cope with a wide range of salinities and are common in brackish-water
environments world-wide [110]. Marifugia cavatica Absolon and Hrabĕ, 1930, closely re-
lated to Ficopomatus, is the only known truly fresh-water serpulid, inhabitant of subterra-
nean caves of the Dinaric Alps [46].
Serpulids produce their calcareous tubes using a pair of calcium carbonate secreting
glands located on the collar. As obligate tube dwellers, they never leave their tubes and
cannot build new ones if removed. Adult serpulids lie in the tube with their dorsum facing
the substrate and locomotion is limited to partial emergence from and withdrawal into
the tube [314]. Hiding behaviour is a common antipredator tactic, and animals may adjust
the durations of such behaviour to current benefits and costs [315].
As suspension-feeders, serpulids show varying abilities in particle sorting and clear-
ance rates. High planktonic biomass removal (>50% of initial standing stock) and signifi-
cant differences in clearance for different components of the community by reef-building
Ficopomatus enigmaticus indicate that the serpulid can regulate planktonic biomass and
promote changes in plankton community structure [316]. Ditrupa arietina (Müller, 1776)
lives unattached in soft sediments and ingests diatoms, haptophytes, bacteria and cyano-
bacteria ranging from 1 to 50 µm in size, and the origin of the food is both planktonic and
benthic [317]. Recently metanotrophy (similar to that found for members of Bispira sp.)
has been reported, as a result of symbiosis between two species of the genus Laminatubus
Diversity 2021, 13, 130 37 of 74
(L. joicebrooskae Rouse and Kupriyanova, 2021 and L. paulbrooksi Rouse and Kupriyanova,
2021) and methane-oxidizing Methylococcales bacteria, from a seep off Costa Rica [284].
While a large number of serpulids is found in coral reefs on coral rubble (e.g., [318]:
Fiji, [319]: Okinawa, Japan, [179]: Queensland, Australia), only some taxa, such as Flori-
protis Uchida, 1978, Pseudovermilia, Spirobranchus and Vermiliopsis spp., are found in asso-
ciation with live corals. Some Spirobranchus species are reported as obligate associates of
corals to the extent that their successful settlement occurs only on live corals (e.g., [320–
322]), although recent observations indicate that while Spirobranchus larvae have a prefer-
ence for live corals, they will survive on other substrates [83]. Many serpulids form epi-
zootic associations with other invertebrates, mostly molluscs, crustaceans, bryozoans, and
sponges. For example, Hydroides spongicola Benedict, 1887 occurs symbiotically in the
chemically aggressive do-not-touch-me sponge Neofibularia nolitangere (Duchassin and
Michelotti, 1864), while Circeis paguri Knight-Jones and Knight-Jones, 1977 is associated
with hermit crabs (reviewed in [303]). Spirorbins are commonly found in specific epi-
phytic associations with macrophytes and their settlement can be stimulated by algal ex-
tracts [323,324].
3.4.2. Biogeography, Distribution and Bathymetry
Members of the Sabellida are found world-wide and, like most polychaetes, for much
of the 20th century were assumed to have naturally wide, even cosmopolitan, distribu-
tions (e.g., [166,194,325]). Darling and Carlton [326] use the term eucosmopolitan to refer
to the species with naturally broad distribution (found in two or more oceans). However,
recent studies overwhelmingly show that ‘cosmopolitan’ taxa represent complexes of ei-
ther morphospecies or cryptic species (reviewed in [327]). All evidence to date suggests
that polychaetes have restricted natural geographic and bathymetric distributions, thus
taxa reported with wide ranges should be treated as potential species complexes. Two
general exceptions to the rule of restricted distributions are deep-sea and invasive species.
Ranges of deep-sea polychaetes are expected to be wider than those found in shallow seas
as a result of stable environmental conditions over wide distances, a traditional view (e.g.,
[328]) also supported by recent studies (e.g., [329,330]). Annelids that are easily translo-
cated by anthropogenic means can establish and become invasive in remote localities, con-
sequently expanding their ranges [327]).
Biodiversity patterns may be influenced not only by intrinsic ecological and historical
factors, but also by ‘extrinsic factors’ sensu Giangrande and Licciano [331]. When a group
is studied by a few specialists working in a particular area, species distribution may cor-
relate with that of the specialists (‘author effect’). The concentration of taxonomic exper-
tise in some regions may increase the number of species in those areas compared to less
studied areas (‘concentration effect’).
Fabriciidae
Fabriciids have been described from all marine realms except for the Tropical Eastern
Pacific (Table S1). Temperate Northern Atlantic is the province with the highest number
of fabriciids (16 species), followed by Tropical Atlantic (13 species), Temperate Northern
Pacific and Western Indo-Pacific (11 species each), Central Indo-Pacific (10 species) and
Temperate Australasia (six species), Temperate Southern Africa (four species), Eastern
Indo-Pacific (two species), and Actic, Southern Ocean, and Temperate Southern America,
each with a single species (Table S1). Most of the 4739 georeferenced occurrences in GBIF
are also from the Temperate North Atlantic Realm and the Tropical Atlantic (Figure 13)
and refer to members of Fabricia, Fabricinuda and Manayunkia [34]. There are records from
neither Tropical Eastern Pacific nor from Western Indo-Pacific, the west coast of South
America, and the west coast of Africa. The historical records until 1999, compiled by Gian-
grande and Licciano [331], showed 55.8% of the total fabriciid species are found in the
tropics. Interestingly, the currently available information, based on species type localities
Diversity 2021, 13, 130 38 of 74
show sthat most species were described from the Atlantic Ocean, at all latitudes. Expla-
nation to latest results could be ‘concentration effect’, with taxonomic expertise accumu-
lated at both sides of the Atlantic, and poor state of knowledge elsewhere.
The species of most genera are distributed almost worldwide. The adaptability of
Fabriciidae to different environments and the wide distribution of some taxa can be
shown by the example of the genus Manayunkia. The ten extant Manayunkia species occur
worldwide in marine, brackish and freshwater habitats, as well as hypersaline lakes. Their
common ancestor was most likely already present in marine habitats [4]. There are ten
species adapted to freshwater conditions: M. speciosa and M. occidentalis (Nearctic); M.
zenkewitschii, M. baicalensis (Nusbaum, 1901) and M. godlewskii (Palearctic) [216,217]. One
species, M. athalassia Hutchings, Dekker and Geddes, 1981, was found in hypersaline lakes
in Australia [257], another species, M. mizu Rouse, 1996, in marine habitats [219,332] and
three species, M. aestuarina, M. caspica Annenkova, 1928), M. brasiliensis Banse, 1956, in
brackish environments[333,334] (Nogueira pers. obs.).
Figure 13. Georeferenced occurrences from GBIF. (a) Fabriciidae; (b) Sabellidae; (c) Serpulidae.
Most Fabriciidae occur in intertidal and subtidal waters. Only certain Pseudofabriciola
species (e.g., P. californica Fitzhugh, 1991, P. filamentosa (Day, 1963), P. filaris Fitzhugh,
a
b
c
Diversity 2021, 13, 130 39 of 74
2002, and P. longipyga Fitzhugh, Giangrande and Simboura, 1994), Fabricinuda longilabrum
Fitzhugh, 2002 and Raficiba barryi occur between depths of 50 m and 335 m [53,58,63,335].
The record of Fabricia sabella (Ehrenberg, 1937) reported by Hartman (1965) from 1000 m
off New England needs a revision because the nominal F. stellaris is a brackish-water spe-
cies from the Baltic Sea. In the southwest Atlantic, exceptionally, two yet undescribed spe-
cies provisionally assigned to the genera Fabriciola and Novafabricia have been found at
4500 m [220] and one other of Fabriciola from the Okhotsk Sea below 2000 m (Table 5).
Sabellidae
Sabellids have been described from all marine realms and all seven members of Cao-
bangia are known so far are from the Indo-Malay limnic realm. In the current analysis, the
Temperate Northern Atlantic is the realm with the highest number of sabellids described
(125 species), which represents 24% of the sabellids described worldwide, followed by the
Temperate Northern Pacific (79 species, 15%), Central Indo-Pacific (58 species, 11%), Trop-
ical Atlantic (56 species, 11%), Temperate Australasia (37), Western Indo-Pacific (20 spe-
cies), Temperate South America (28 species), Southern Ocean (24 species), Temperate
Southern Africa (18), Arctic (16 species), Tropical Eastern Pacific (15 species), Eastern
Indo-Pacific (8), 23 species non-marine and eight species with unknown type locality (Ta-
ble S2). Most of the 117 073 georeferenced occurrences in GBIF are from the Temperate
Northern Atlantic and the Tropical Atlantic realms, and records belong to members of
genera Euchone, Jasmineira, Chone and Sabella [34] (Figure 13). Other realms with large rep-
resentation of sabellids records are Tropical Atlantic, the Arctic and Temperate Australa-
sia. The number of described species and number of records is higher in the Atlantic than
in any other ocean, the result that contradicts the patterns showing an increase in sabellid
species richness towards the tropics, and mainly in the Indo-Pacific [331].
Some genera with few species, such as Anamobaea or Stylomma, and the freshwater
Caobangia, are exclusive of tropical environments [69,158,229], and others, such as Bran-
chiomma, Bispira, Acromegalomma, Notaulax, Sabellastarte, and Sabellonga, have either tropi-
cal or temperate distribution [149,157,336–338]. A few genera show a significant prefer-
ence for colder waters and are either well represented at greater depths or in higher lati-
tudes (e.g., members of Chone, Euchone, and Jasmineira). The Antarctic region is richer in
number of genera and species than the Arctic [24] (Figure 7), and genera, such as
Perkinsiana, are mainly distributed in the Southern Ocean [212].
Sabellids found below 6000 m have all been reported from the Western Pacific Ocean
(Table 5) and include species of the genera Jasmineira, Potamethus and Potamilla Malmgren,
1866 [339–344]. Species reported in the abyssal zone (2000–6000 m deep) include members
of the genera Chone, Euchone, Fabrisabella, Jasmineira, Potamilla, and Potamethus (Table 5).
The genus Potamethus is the most speciose deep-sea taxon (Table 5). Jasmineira filitovae Le-
venstein, 1961 is the deepest record (9735 m). Sabellids reported from between 1000 and
2000 m depths include species of Bispira, Chone, Euchone, Jasmineira, Perkinsiana, Potame-
thus, Potaspina and Pseudopotamilla [280,284,345–348]. Among all sabellids recorded below
1000 m, 13 have been identified to the genus level only, most probably constituting new
species.
Table 5. Deepest records for members of Sabellida below 1000 m.
Taxon
Depth (m)
References
FABRICIIDAE
Fabriciola
sp. (Okhotsk Sea) > 2000 Alalykina 2020
Fabriciola
sp. 4600 Baumhaker 2012
Novafabricia
sp. 4600 Baumhaker 2012
Diversity 2021, 13, 130 40 of 74
SABELLIDAE
Jasmineira
bermudensis
Hartman, 1965 1000 Original description
Potaspina
australiensis
Capa, 2007 1000 Original description
Euchone
magna
(Fauchald, 1972) 1071 Original description
Perkinsiana
assimi
lis
(McIntosh, 1885) 1100 Original description
Chone
gracilis
Moore, 1906 1244 Méndez 2006
Bispira
wireni
(Johansson, 1922) 1335 Capa et al. 2013
Potamethus
filiformis
Hartmann-Schröder, 1977 1430 Original description
Pseudopotamilla
intermedia
Moore, 1905 1682 Original description
Bispira
sp. (Costa Rica) 1887 Goffredi et al. 2020
Chone
sp. (Okhotsk Sea and N. Pacific abyss) > 2000 Alalykina 2020
Euchone
sp.
(Okhotsk Sea and N. Pacific abyss) > 2000 Alalykina 2020
Jasmineira
sp. (Okhotsk Sea and N. Pacific abyss) > 2000 Alalykina 2020
Potamethus
sp. 1 (Okhotsk Sea and N. Pacific abyss) > 2000 Alalykina 2020
Potamethus
sp. 2
(Okhotsk Sea) > 2000 Alalykina 2020
Potamethus
singularis
Hartman, 1965 2000 Original description
Potamilla
neglecta
(Sars, 1851) 2030 Hansen 1882
Potamethus
malmgreni
(Hansen,
1878)
2222
Original
description
Euchone
cf.
incolor
Hartman, 1965 2500 Alalykina 2020
Fabrisabella
similis
Fauchald, 1972 2520 Original description
Potamethus
scotiae
(Pixell, 1913) 2578 Original description
Euchone
papillosa
(Sars, 1851) 2900 Uschakov 1955; Levenstein 1969
Jasmineria
pacifica
Annenkova, 1937 2900 Original description
Jasmineira schaudinni Augener, 1912 3500 Augener 1912 (abyssal, no depth given);
Jirkov 1982, 2001
Chone
infundib
uliformis
Krøyer, 1856 3521 Wesenberg-Lund 1950
cf Sabellidae species 1 (Clarion-Clipperton Zone) 4029 Amon et al. 2017
Potamethus
mucronatus
(Moore, 1923) 4131 Original description, as
Notaulax
Potamilla abyssicola Uschakov, 1952 4200
Original
descript
ion;
Levenstein
1961
1969; Alalykina 2020
Potamethus
spathiferus
(Ehlers, 1887) 4360 Fauvel 1914
Euchone
incolor
Hartman, 1965 4862 Original description; Hartman 1971
?
Potamethus
sp. Mozambique Basin 5068 Hartman 1971
Potamehus
dubius
(Eliason, 1951) 5860 Original description
Jasmineira
sp.
Japan
6207
Levenstein
1961b
Potamethus
singularis
Hartman, 1965 6023 Original description; Hartman 1971
Sabellidae sp. Pacific Ocean 8042 Levenstein 1969; Lemche et al. 1976
Diversity 2021, 13, 130 41 of 74
Potamilla
sp. Kurile-Kamchatka Trench 8100 Uschakov 1952; Belyaev 1989
Jasmineira sp. Kermadec Trench Trench 8300 Kirkegaard 1956; Hartman and Fauchald
1971; Belayev 1972
Potamethus
sp. Izu-Bonin Trench 8735 Belayev 1989
Jasmineira
filitovae
Levenstein, 1961 (as
Potamethus
) 9735 Levenstein 1969, 1973; Belyaev 1989
SERPULIDAE
Laminatubus
joicebrooksae
Rouse and Kupriyanova
2021 1011 Original description
Hyalopomatus
madreporae
Sanfilippo, 2009 1146 Original description
Neovermilia
falcigera
(Roule, 1898) 1580 Zibrowius and ten Hove 1987
Metavermilia
ogasawaraensis
Nishi, Kupriyanova
and Tachikawa, 2007 1603 Original description
Zibrovermilia
zibrowii
Kupriyanova and Ippolitov,
2015 1710 Original description
Hyalopomatus
dieteri
Kupriyanova and Ippolitov,
2015 1980 Original description
Hyalopomatus
biformis
(Hartman, 1960) 1982 Kupriyanova and Nishi 2010
Metavermilia
zibrowii
Bailey-Brock and Magalhães,
2012 2013 Original description
Vermiliopsis
notialis
Monro, 1930 2016 Averintsev 1974
Bushiella
(Jugaria)
atlantica
(Knight-Jones, 1978) 2100 Original description
Bathyvermilia
islandica
Sanfilippo, 2001 2399 Original description
Filogranula
stellata
(Southward, 1963) 2464 Ben-Eliahu and Fiege 1996
Hyalopomatus
variorugosus
Ben-Eliahu and Fiege,
1996 2474 Original description
Lam
inatubus
paulbrooksi
Rouse and Kupriyanova,
2021 2478 Original description
Protis
browni
(Pixell, 1913) 2585 Original description
Protis
hydrothermica
ten Hove and Zibrowius 1986 2620 ten Hove and Zibrowius 1986
Hyalopomatus
marenzelleri
Langerhans, 1884 2800 Zibrowius 1968, 1969, 1977
Laminatubus
alvini
ten Hove and Zibrowius, 1986 2842 Original description
Neovermilia
cf.
sphaeropomata
(Benham, 1927) 3261 Rouse and Kupriyanova 2021
Apomatus
globifer
Théel, 1878 3384 Uschakov 1957
Hyalopomatus
cla
paredii
Marenzeller, 1878 3550 Kupriyanova and Jirkov 1997
Hyalopomatus
jirkovi
Kupriyanova, 1993 3949 Kupriyanova et al. 2011
Spirodiscus
grimaldii
Fauvel, 1909 4124 ten Hove and Kupriyanova 2009
Bathyvermilia
kupriyanovae
Bastida-Zavala, 2008 4190 Original description
Apomatus
similis
Marion and Bobretzky, 1875 4400 Fauvel (1909), Fauvel (1914)
Spirodiscus
groenlandicus
(McIntosh, 1877) 4440 Kupriyanova and Ippolitov 2015
Bathyvermilia
zibrowiusi
Kupriyanova, 1993 4550 Kupriyanova et al. 2011
Diversity 2021, 13, 130 42 of 74
Hyal
opomatus
sikorskii
Kupriyanova, 1993 4550 Kupriyanova et al. 2011
Protis
simplex
Ehlers, 1887 4810 Knight-Jones et al. (1997)
Protis
polyoperculata
Kupriyanova, 1993 5110 Original description
Hyalopomatus
mironovi
Kupriyanova, 1993 5216 Rouse and Kupriyanova 2021
Protis
arctica
(Hansen,
1879)
5300
Zibrowius
1969
Bathyvermilia
challengeri
Zibrowius, 1973 5719 Original description
Bathyvermilia
langerhansi
Fauvel, 1909 5987 Eliason 1951
Bathyvermilia
gregrousei
Kupriyanova and Ippoli-
tov, 2015 6050 Original description
Nidificaria
levensteinae
(Bailey-Brock and Knight-
Jones, 1977) 6096 Original description
Bathyditrupa
hovei
Kupriyanova, 1993 6330 Kupriyanova et al. 2011
Protis
sp. 2 8345 Kupriyanova et al. 2014
Protis
sp. 1 9735 Kupriyanova et al. 2014
Serpulidae
Serpulids have been described from all marine realms. The realm with highest num-
ber of species is the Temperate Northern Atlantic (108 species), followed by the Temperate
Northern Pacific (92), Central Indo-Pacific (74), Tropical Atlantic (71), Western Indo-Pa-
cific (52), Temperate Australasia (41), Tropical Eastern Pacific (28), Southern Ocean (23),
Temperate South America (21), Arctic (16), Temperate Southern Africa (15), Eastern Indo-
Pacific (8), and nine species with unknown type locality (Table S3). Of the 107 859 georef-
erenced records in GBIF (2020), more than half are within the Temperate Northern Atlan-
tic (mainly identified as Spirobranchus, Hydroides, Ditrupa and Spirorbis) and following
realms with highest occurrences are the Temperate Australasia (mainly Spirobranchus, Hy-
droides, Galeolaria and Serpula) and the Tropical Atlantic (Hydroides, Spirobranchus, Ver-
miliopsis and Pseudovermilia) (Figure13). There were no previous analyses of global serpu-
lid distribution patterns to compare with these data.
Serpulids are common inhabitants of intertidal, subtidal and shelf locations, but they
can occur at all latitudes from intertidal to hadal depths. Spirorbin bathymetric distribu-
tion ranges from littoral to abyssal depths, but they are most commonly found in the sub-
littoral zone. The best known representatives of the genera Ficopomatus, Galeolaria, Hy-
droides, Salmacina Claparède, 1870, Serpula, Spirobranchus and Vermiliopsis are inhabitants
of shallower waters (below 500 m), and so are representatives of less known and more
cryptic genera, such as, for example, Chitinopoma, Floriprotis, Josephella Caullery and
Mesnil, 1896, Metavermilia, Pomatostegus, Pseudochitinopoma Zibrowius, 1969, Pseu-
dovermilia, Rhodopsis Bush, 1905, Semivermilia ten Hove, 1975 and Spiraserpula. Some gen-
era, e.g., Apomatus, Filogranula, Neovermilia and Protula may include both subtidal and
bathyal species.
Serpulids found below 2000 m were reviewed by Zibrowius [349], who corrected
Hartman’s [339] compendium of abyssal polychaetes by removing taxa typical of subtidal
and shelf depths (Hydroides, Ditrupa, Placostegus, Serpula, Spirobranchus). As a result, he
listed 25 species, including one unidentifiable specimen from Kermadec Trench (6620–
6730 m, [350]). Belyaev [344] added two unidentified hadal specimens from 6410–6757 m
(Aleutian Trench) to 9715–9735 m (Izu-Bonin Trench), the latter being the deepest record
for a serpulid. In their review, Paterson et al. [351] list only 26 serpulids from over 2000 m
world-wide, including five species from depths beyond 3500 m, all described by
Kupriyanova [352,353] from Kuril-Kamchatka Trench alone. Sanfilippo [354],
Diversity 2021, 13, 130 43 of 74
Kupriyanova et al. [355,356] Kupriyanova and Nishi [357], Bailey-Brock and Magalhães
[184], Kupriyanova and Ippolitov [107], and Rouse and Kupriyanova [358] recently pro-
vided additional records and descriptions of new deep-sea serpulid taxa. Kupriyanova et
al. [356] reviewed and revised hadal records below 5000 m, demonstrating that the deep-
est serpulid records (8345 and 9735 m) reported in Belyaev’s book [344]) belong to the
genus Protis.
Currently, 36 named species have published records below 1000 m, 28 of them are
reported from below 2000 m (Table 5), although Kupriyanova et al. [356] lists eight records
in open nomenclature (Bathyvermilia sp., Hyalopomatus sp., Protis sp., Serpulidae gen. sp.
A and B). In summary, serpulids from bathyal and abyssal depths (>1000 m) are found in
the genera Apomatus, Bathyditrupa, Bathyvermilia Zibrowius, 1973, Bushiella (Jugaria)
Knight-Jones, 1978, Filogranula, Hyalopomatus, Laminatubus, Metavermilia, Neovermilia, Nid-
ificaria Knight-Jones, 1984, Spirodiscus, Protis, and Zibrovermilia Kupriyanova and Ippoli-
tov, 2015, but only species of Bathyditrupa, Bathyvermilia, Hyalopomatus, and Protis are
found in the abyss, also penetrating into the hadal zone. Non-operculate Protula and oper-
culate Apomatus are often confused with non-operculate and operculate Protis sp., so that
abyssal records of supposed Protula and Apomatus might belong to Protis [356].
3.5. Non-Indigenous and Invasive Species
Shallow-water Sabellida, due to their sedentary tubicolous lifestyle, are common
members of biofouling communities and are easily translocated by anthropogenic means,
i. e., on ship hulls and floating marine debris [147]. Distribution as larvae in ballast water
has been suggested [359–362] and is the most plausible hypothesis for Sabella spallanzanii
[363,364], but larvae of sabellids and serpulids have never been reported from ballast wa-
ter samples. If become established in remote localities, such translocated taxa significantly
expand their ranges. However, some reported broad distributions are a reflection of un-
certain taxonomic status. Such species remain as widely distributed or even ‘cosmopoli-
tan’ only as long taxonomic uncertainty persists, and a molecular investigation usually
split hem into a number of geographically restricted species.
According to the literature survey of polychaetes reported outside their natural
ranges, Serpulidae and Sabellidae account for 22% of the total number of non-native pol-
ychaetes world-wide [365]. However, a critical assessment of non-indigenous species rec-
ords is needed. The number of such species is a function of the research effort put into
distinguishing non-native and native taxa, which in turn depends on the knowledge of
native diversity and the state of taxonomy of a group. Integrative taxonomic revisions of
species with reportedly global distributions are important because such taxa may include
cryptic invaders that are particularly difficult to track because they are often assumed to
be native species or wrongly assigned to other invasive species [366].
Several criteria for distinguishing non-indigenous from native species have been pro-
posed as lines of indirect evidence, such as a new record for an area, a new localised oc-
currence showing a population explosion, species with disjoint distribution, with insuffi-
cient natural dispersal capabilities to account for observed distribution range, or species
associated with means of human-made transport, e.g., found on ship hulls (e.g.,
[172,367,368]). In the last two decades, molecular genetics tools have proved indispensable
direct lines of evidence for assessing the status of a reportedly invasive taxon. The popu-
lation genetics studies allow testing if distant populations belong to same species, and also
if genetic variability of suspected new arrivals is lower than that observed in the native
range, which indicates a recent translocation (e.g., [72,74,204,294,368–370]). Molecular
data can also help to determine the origin of non-native populations. For example, haplo-
type variability analysis suggests that although serpulid Hydroides dianthus (Verrill, 1873)
was originally described from New England, its native range may be the Mediterranean
[250].
Diversity 2021, 13, 130 44 of 74
A good example of a sabellid with an uncertain invasive status is Laonome calida de-
scribed from the Calliope River, Australia, and later reported as introduced in the Neth-
erlands [294], Odra River and the Sea of Azov [371,372]. Simultaneously, the morpholog-
ically similar Laonome xeprovala was described from the Baltic Sea, and DNA sequences
from specimens from the Netherlands and Sea of Azov showed that they belong to the
same species [102]. Neither L. calida nor L. xeprovala had been reported from Europe before
2014, and increased occurrences suggest a recent invasion [373]. Molecular analyses, how-
ever, are needed to determine whether the European populations belong to the same spe-
cies found in Australia (implying that L. xeprovala could be a junior synonym of L. calida)
or a distinct non-indigenous species of unknown origin is found in Europe (in which case
L. xeprovala would be valid). Similarly, Branchiomma species are easily translocated outside
of their native ranges [72,129,147,374–379], but members of this genus are so morpholog-
ically homogenous that species identification using morphological characters only is
problematic. Therefore, assessing the identity of Branchiomma spp. with invasive potential
requires a comprehensive generic revision, including DNA-based species delimitation
analyses [72,379]. Other records still to be confirmed by molecular studies are the sabellids
Euchone variabilis Hutchings and Murray, 1984, Laonome triangularis, Desdemona aniara and
the three species of Pseudobranchiomma reported from Australia [74,126,380,381].
Diversity 2021, 13, 130 45 of 74
Table 6. List of translocated species, with presumned origin indicated by provinces or ecoregions (sensu Spalding et al. [31]). Those species that are included as unresolved,
require confirmation and two are not cosmopolitan (Branchiomma curtum and Parasabella pallida). NA: not applicable.
Species Type Locality Presumed
Origin Category
New occurrences (Out-
side of Expected Natu-
ral Range)
Molecular Markers Comments
Acromegalomma
claparedei
(Gravier,
1906)
Djibouti, Gulf of
Aden Red Sea ? Non-indige-
nous Western Mediterranean none Listed in the Mediterranean [382] but needs confirma-
tion [130].
Amphicorina pectinata (Banse, 1957) Masked Island,
New Zealand
Southern Island
New Zealand
? Non-indige-
nous
Western and Central
Mediterranean none
Redescribed from Italy and Spain without examina-
tion of types from New Zealand [383]. Included in the
Mediterranean checklists [365,381,384] but requires
confirmation.
Bispira polyomma Giangrande and
Faasse in Faasse and Giangrande,
2012
Yerseke Marina,
the Netherlands Unknown ? Non-indige-
nous NA none Found among cultured oysters, presumably as an in-
troduction [385].
Branchiomma bairdi (McIntosh,
1885) Bermuda Tropical North-
western Atlantic
Non-indige-
nous
Gulf of California, Aus-
tralia, Mediterranean,
Suez Canal, northeast-
ern Atlantic Ocean, Cal-
ifornia, Hawaii, Galapa-
gos, Madeira
COI, Cytb, 16S, 28S, ITS
Widest distribution reported for a sabellid
[72,126,129,147,185,189,376,377,379,386–388]. Some
records need confirmation [185].
Branchiomma boholense (Grube,
1878) Bohol, Philippines Western Coral
Triangle
Non-indige-
nous Mediterranean COI
Reported from the Mediterranean [375,389,390]. Çinar
[126] corrected his records as B. bairdi. Many records
of B. bairdi in the Mediterranean are B. boholense [379].
Branchiomma coheni Tovar-Hernán-
dez and Knight-Jones, 2006 Panama, Pacific Tropical Eastern
Pacific
Non-indige-
nous
Florida, Gulf of Califor-
nia none
Records from Tampa Bay and Gulf of California [391]
first since description. In Florida it was an early de-
tected non-indigenous species [391].
Branchiomma
conspersum
(Ehlers,
1887)
Key West, Florida,
USA Floridian Non-indige-
nous Hawaii ITS Reported from Hawaii [185]
Diversity 2021, 13, 130 46 of 74
Branchiomma curtum (Ehlers, 1901) Juan Fernández Is-
land, Chile Juan Fernández
Not translo-
cated ? Mexican Caribbean none
Caribbean
records
may
be
erroneous
[
391
]
.
Both
syn-
types of B. curtum and Caribbean specimens were ju-
veniles produced by fission [392]. See comments in
[391].
Branchiomma luctuosum (Grube,
1870) Red Sea Red Sea Non-indige-
nous Mediterranean, Brazil none Common in the Mediterranean as Lessepsian migrant
[129,389,390,393–401], and Brazil [234,402]
Desdemona ornata Banse, 1957 South Africa Agulhas ? Non-indige-
nous
Iberian Peninsula, UK,
Marmara Sea, Portugal none
Reported as introduced in Australia [403], Spain
[404], UK [405], Marmara Sea [406], Portugal [407]
and the Netherlands [408], but types of D. ornata were
not examined.
Euchone limnicola Reish, 1959 Los Angeles, Cali-
fornia, USA
Warm Temper-
ate Northeast
Pacific
? Non-indige-
nous Dunkerke, Australia none
Reported from Australia by McArthur [409] and in-
cluded in Hewitt et al. [380] based on McArthur dis-
sertation. Reported by Guyonnet and Borg [410] from
the French coast of North Sea.
Laonome calida Capa, 2007 Queensland, Aus-
tralia Unknown ? Non-indige-
nous
Australia (Queensland,
Northern Territory,
Western Australia),
? Europe (the Nether-
lands, Sea of Azov, Bal-
tic Sea, Mosel River)
none
Reported in Australian in fully marine but also estua-
rine conditions, in both pristine and port environ-
ments [68]. Bick et al. [102] suggest that European rec-
ords belong to Laonome xeprovala, not L. calida.
Laonome elegans Gravier, 1906 Red Sea Red Sea ? Non-indige-
nous East Mediterranean none
Listed in Zenetos et al. [383]. Presence in the Mediter-
ranean area as Lessepsian migrant needs to be con-
firmed.
Laonome triangularis Hutchings and
Murray, 1984
New South Wales,
Australia
East Central
Australian Shelf
? Non-indige-
nous Turkey none Reported as introduced in Turkey [126].
Laonome xeprovala Bick and Bastrop
in Bick et al. 2018 Estonia, Baltic Sea
Unknown Non-indige-
nous
the Netherlands, Sea of
Azov, Baltic Sea, Mosel
River
COI, 16S, 18S
Specimens from the Baltic Sea, the Netherlands and
the Sea of Azov possessed identical genotypes, but
unknown origin [102]. Confirmation that it is not the
same as L. calida is needed.
Diversity 2021, 13, 130 47 of 74
Myxicola infundibulum (Renier in
Meneghini, 1847) Devon, UK Northern Euro-
pean Seas
Non-indige-
nous
Australia, ?North
America COI, 16S
Analysed sequences of specimens from European and
Australian waters belong to same species; sequences
from Maine showed some differences [411].
Parasabella fullo Grube, 1878) Northern Japan
Temperate
Northwest Pa-
cific
Non-indige-
nous
Santa Barbara and San
Diego, California, USA none Collected on ship hulls in California, and a resident
population appears to exist in the region [412].
Parasabella pallida Moore, 1923 California, USA
Warm Temper-
ate Northeast
Pacific
Not translo-
cated NA none
Included in the list of translocated species by mistake
[294], as it was described from California [143] not the
Caribbean, as later fixed in [73].
Parasabella rugosa (Moore, 1904) San Diego, Califor-
nia, USA
Warm Temper-
ate Northeast
Pacific
Non-indige-
nous Australia none It was reported in Australia near an international port
as sp. cf. P. rugosa Capa and Murray [73].
Pseudobranchiomma emersoni Jones,
1962
Port Jackson, Ja-
maica
Tropical North-
western Atlantic
Non-indige-
nous Australia none As cf. P. emersoni in Capa and Murray [74].
Peudobranchiomma orientalis (McIn-
tosh, 1885) Hong Kong Unknown Non-indige-
nous Australia none As cf. P. orientalis in Capa and Murray [74]. Ethanol
fixed specimens are need for molecular analysis.
Pseudobranchiomma schizogenica To-
var-Hernández and Dean, 2014 La Paz, Mexico Tropical North-
western Atlantic
Non-indige-
nous Australia, Galapagos ITS, Cytb As cf. P. schizogenica in Capa and Murray [74] from
Australia, also reported in Galapagos [183].
Sabella spallanzanii (Gmelin, 1791) Malta Mediterranean Non-indige-
nous Australia, New Zealand COI, H3, 18S, 28S, 16S,
ITS
Considered an invasive pest in Australia and New
Zealand [202,364,370,413].
Sabellastarte spectabilis (Grube,
1878)
Bohol, Masalac,
Philippines and
Singapore
Western Coral
Triangle
? Non-indige-
nous
Sri Lanka, Solomon Is-
lands, Mauritius, Japan,
Taiwan, Hawaii, Malay-
sia, Saipan, Pakistan
COI, 16S
Reports of accidental introductions to Hawaii [414–
416] rely on invalid morphological features [70]. Evi-
dence for wide distribution exists [70].
Terebrasabella heterouncinata Fitz-
hugh and Rouse, 1999 South Africa Unknown Non-indige-
nous California, Chile none Parasite of red abalone. Reported from abalone farms
from California and Chile [66,300–419].
Diversity 2021, 13, 130 48 of 74
Ficopomatus enigmaticus (Fauvel,
1923)
France, native
range is unknown,
likely southerm
Australia
Unknown Non-indige-
nous
Europe, New Zealand,
Japan, USA (both
coasts), Argentina, Tu-
nisia, Egypt, Côte
d’Ivoire, South Africa
Cytb, COI
Reviewed by Dittmann [420]. Styan et al. [204] re-
vealed three species (not formally described) with
overlapping ranges in Australia, one of which is mor-
phologically distinct from the other two. Grosse et al.
[421] found two other species within the complex
Spain.
Ficopomatus uschakovi (Pillai, 1960) Sri Lanka Unknown ? Non-indige-
nous
Indo-Pacific, Western
Africa (Nigeria, Ivory
Coast), Brazil, Vene-
zuela, Colombian Car-
ibbean and southern
Mexican Pacific ?Aus-
tralia
none Several records given outside the native range [422–
425]. Likely a species complex [204].
Hydroides brachyacantha Rioja, 1941 Pacific coast of
Mexico
Warm Temper-
ate Northeast
Pacific
Native
Likely restricted to Pa-
cific coast of Mexico, no
evidence of transloca-
tions
18S, cytb, ITS
Belongs to a complex of species, records from warm-
temperate and tropical localities world-wide likely
belong to other species of H. brachacantha complex
[203].
Hydroides dianthus (Verrill, 1873) New England,
USA
Either East Coast
of the USA or
the Mediterra-
nean
Non-indige-
nous
Brazil, China, Japan,
West Africa, the Medi-
terranean (or US East
Coast), the Black Sea,
Texas
COI
Observed higher haplotypes diversity in the Mediter-
ranean contradicts the accepted native range of H. di-
anthus in the USA. The cryptic lineage found in Texas
was evidently introduced to the Black Sea recently
[250].
Hydroides dirampha Mörch, 1863 St. Thomas Island,
US Virgin Islands
Tropical North-
western Atlantic
Non-indige-
nous
Australia, Brazil, Japan,
Hawaii, New Zealand,
Panama, the Pacific
from Mexico and Cali-
fornia, and the Mediter-
ranean
18S, cytb, COI, 28S, ITS
Several records given outside the native range [426–
429]. Molecular data from Australia, Brazil, Panama
[78,79].
Diversity 2021, 13, 130 49 of 74
Hydroides elegans (Haswell, 1883) Sydney, Australia Unknown Non-indige-
nous
Sub-tropical world-
wide: Mediterranean-
Atlantic, Indo-West Pa-
cific, tropical Pacific
America, West Atlantic,
East Atlantic, South Af-
rica
Microsatellites, 18S,
cytb, COI, 28S
See [106]. Biofouling has been shown as a major mode
of dispersal for this species [430]. Molecular data from
Panama, California, Australia, Brazil, Italy and Spain
[79,421].
Hydroides ezonesis Okuda, 1934 Northern Japan
Warm Temper-
ate Northwest
Pacific
Non-indige-
nous France, UK, Australia 18S, 28S
Imported from Japan with oysters to the Atlantic
coast of France [431,432] then the UK and Australia
[359,432,433]. Molecular data from China, Japan [79].
Hydroides operculata (Treadwell,
1929) Gulf of Aden Western Indo-
Pacific
Native, some
species in the
complex maybe
non-indigenous
A complex of species,
no evidence of translo-
cations for any species
of the complex
18S, cytb, COI, 28S, ITS
Reports from South and East Africa, India, Pakistan,
Sri Lanka, Hong Kong, tropical Australia, and the
eastern Mediterranean likely belong to other species
of the H. operculata complex [251].
Hydroides sanctaecrusis Krøyer [in]
Mörch, 1863
Saint Croix, Virgin
Islands
Eastern Carib-
bean
Non-indige-
nous
Singapore, tropical
Australia, Hong Kong,
Taiwan, Florida, India.
Not found in the Medi-
terranean [240]
18S, COI, 28S, ITS
Records outside of the native range include
[78,180,362,434]. Molecular data from Florida [77],
Panama, Australia, India [79], Pacific Mexico [80].
Spirobranchus kraussii (Baird, 1865) Cape of Good
Hope, South Africa Agulhas
Native, some
species in the
complex non-
indigenous, but
not S. kraussi
Restricted to South Af-
rica, no evidence of
translocations
18S, cytb
Reports from warm-temperate and tropical localities
in the Indo-Pacific and Mediterranean Sea belong to
other species of S. kraussii complex [84,193].
Diversity 2021, 13, 130 50 of 74
Spirobranchus tetraceros (Schmarda,
1861) NSW, Australia East Central
Australian Shelf
Native, some
species in the
complex likely
non-indige-
nous, but not S.
tetraceros
Likely restricted to
south-eastern Australia,
no evidence of translo-
cations.
cytb
Reports from warm-temperate and tropical localities
world-wide belong to other species of the S. tetraceros
complex. At least one of these species was introduced
and established in the Mediterranean [252].
Diversity 2021, 13, 130 51 of 74
One of the best examples of a sabellid with the invasive status confirmed through a
combination of morphological and genetic data is Sabella spallanzanii. This large conspic-
uous Mediterranean native was introduced to Australia in 1965 and to New Zealand in
2008 [364,435,436]. Analyses of COI sequences from the native and non-indigenous pop-
ulations proved that the New Zealand incursion originated from Australia rather than
from the Mediterranean [370]. Other examples of sabellids with invasive status (but
ofunknown origin) confirmed with DNA analyses are Parasabella crassichaeta Capa and
Murray, 2015 and Pseudobranchiomma cf. schizogenica Tovar-Hernández and Dean, 2014,
reported from both Hawaii and Australia [73,74]. Out of seven nominal species of the ser-
pulid genus Hydroides reported as translocated outside of their natural range, five are con-
firmed invaders (Table 6). One of them, H. elegans, is the best-known cryptogenic poly-
chaete, reported from most sub-tropical locations world-wide [110], and biofouling as the
major mode of its dispersal was supported by DNA data [430]. Ficopomatus enigmaticus is
another cryptogenic serpulid, because, although it was described from France, its native
range is enigmatic (hence the name), likely to be southern Australia [420]. This typical
species has invaded warm-temperate estuaries world-wide, as confirmed by DNA studies
[204,437,438].
Ficopomatus uschakovi (Pillai, 1960), described from Sri Lanka, a tropical species with
supposedly wide distribution in Indo-Pacific, was recently reported as introduced to
South America [422–425]. The invasive status of the species has not been examined with
DNA, but preliminary molecular data (Kupriyanova unpubl.) suggest that this taxon is a
complex of species. Two nominal Hydroides species, H. brachyacantha Rioja, 1941 and H.
operculata (Treadwell, 1929), are examples of complexes of morphologically similar species
[180,251]. Similarly, the invasive status attributed to serpulids Spirobranchus kraussii
(Baird, 1865) and S. tetraceros (Schmarda, 1861) [365,439] is unjustified, as both are mem-
bers of species complexes [84,193,252].
The Mediterranean Sea leads the rank when it comes to reported introductions, with
13 serpulid and 10 sabellid non-indigenous species reported, mainly as a result of Les-
sepsian migration from the Red Sea [125,365,440,441]. In this region, 11 species of sabellids
and serpulids, mainly of the genera Branchiomma, Ficopomatus, and Hydroides, have been
listed among the top 100 worst invasive species, based on their economic and ecological
impacts [442]. However, taxonomic and invasive status of many of these taxa needs to be
revised.
3.6. Fanworms Are Important: Some Applications
3.6.1. Nuisance Fouling Species
Several serpulid species, predominantly of the genera Hydroides, Ficopomatus, and
Spirobranchus, are capable of colonizing a wide range of natural and artificial substrates
and settling gregariously, which makes them economically and ecologically important
fouling nuisance species.
Serpulid foulers constitute a significant financial burden to due to costs associated
with the removal of tubes from artificial structures. Millions of dollars are spent annually
to prevent the fouling of marine organisms, especially of Hydroides, on human-made struc-
tures [443]. Dense tube aggregates attach to underwater seawater intake pipes of power
plants reducing water flow and causing blockages. Fouled docks require cleaning mainte-
nance in harbours around the world. Fouling interferes with navigation and shipping in-
dustries by decreasing ship speed, while increasing the weight and drag of buoys
[444,445].
In marine aquaculture the key impact is the direct fouling of stock causing physical
damage, biological competition and environmental modification, while infrastructure,
such as aquaculture nets and cages, is also damaged. The conservative estimates of eco-
nomic loss to the aquaculture industry are 5–10% of production costs attributed to bio-
fouling [446].
Diversity 2021, 13, 130 52 of 74
Manayunkia speciosa and/or M. occidentalis (see [216]) are obligate hosts of the myxo-
zoan parasites Ceratonova shasta and Parvicapsula minibicornis, which cause ceratomyxosis
in salmon and trout in North America [267,268,447]. Management actions, such as flow
manipulations to increase the mortality of M. speciosa and disturbance of its habitat, have
been implemented [268].
3.6.2. Non-Indigenous and Invasive Species
Non-native to a region species translocated to another region can expand and have
significant impact on human health, economic interests or environmental values. Such
translocations of fouling species of Sabellida are well documented (e.g., [448–452]). Coun-
tries around the world have established biosecurity systems, aimed to prevent the intro-
duction and/or spread of non-indigenous organisms. Some Sabellida have been listed in
individual countries’ Laws and Regulations, indicating its status as unwanted non-indig-
enous species (invasive, pests, parasites, pathogens). For example, in New Zealand, Sabella
spallanzanii has been registered as a notifiable organism, subject to targeted surveillance
work, including study of population dynamics and reproduction, under the New Zealand
Biosecurity Act 1993 [364]. In Australia, non-indigenous marine species already found and
those not yet found but have demonstrated significant impacts elsewhere are ranked ac-
cording to their invasive impact and potential. For example, S. spallanzanii is regarded as
a high impact, notifiable invasive species, while Hydroides dirampha Mörch, 1863, H. dian-
thus, H. sanctaecrucis Krøyer in Mörch, 1863, H. ezoensis Okuda, 1934 are listed as medium
or low priority species [433]. In Mexico, sabellids Branchiomma bairdi (McIntosh, 1885) and
Terebrasabella heterouncinata and six serpulids (Ficopomatus enigmaticus, F. miamiensis
(Treadwell, 1934), F. uschakovi, Hydroides elegans, H. bispinosa Bush, 1910 and H. dirampha)
are regulated under the Diario Oficial de la Federación [453]. Ficopomatus enigmaticus is
the only annelid registered in the Spanish Catalogue of Exotic Invasive Species [421]. In
Brazil, the only species of Sabellida reported as invasive is Branchiomma luctuosum (Grube,
1870) [401].
3.6.3. Indicators of Pollution
Manayunkia speciosa is an indicator of moderate organic pollution, but is intolerant of
severe pollution or anoxic sediments [447,454,455]. Decrease of the organic content of the
sediment from 1.8% to 1.0% leads to reduction in abundance of its congener, M. aestuarina,
from 16 000 to 6000 ind.m2 in the Baltic Sea [262]. Euchonoides moeone was proposed as an
indicator of sediment organic enrichment in a sewage outfall in Hawaii [279].
Sabella spallanzanii can trap anthropogenic micro-particles and glue these to their
tubes, and it has been proposed as an indicator of microlitter pollution in sheltered and
polluted environments such as ports [456]. Larvae of Hydroides elegans have been used as
indicators for biomonitoring and ecotoxicology tests (e.g., [457–459]).
Some sabellids and serpulids have been suggested as bioindicators of heavy metal
pollution. For example, the tube of Sabella spallanzanii is an important compartment in
metal retention and suitable for evaluation of the pollution by traced elements [460], while
Branchiomma bairdi and B. luctuosum, invasive sabellids in the Mediterranean, can accu-
mulate high concentrations of arsenic (As), cadmium (Cd), chromium (Cr) and lead (Pb),
considered to be priority toxic or ubiquitous persistent, bioaccumulative and toxic (PBT)
substances under the EU Water Framework Directive [461]. Some studies have focused
on the effects of heavy metals on larval development and metamorphosis using serpulid
larvae (Hydroides elegans: [462,463]); Galeolaria caespitosa: [464]).
3.6.4. Bioremeditators
As suspension feeders, Sabella spallanzanii, Branchiomma luctuosum and B. bairdi have
been tested as bioremediators for aquaculture waste-water treatment in polluted coastal
areas [273,274,465–470]. However, these three taxa are invasive in some areas, and may
Diversity 2021, 13, 130 53 of 74
pose a threat to native ecosystems. Nevertheless, the use of non-indigenous species as
bioremediator may allow to transform a potential risk into a benefit, with high potential
commercial gain and economic feasibility [470]. Due to their important role in organic
sediment bioremediation, the Food and Agriculture Organization of the United Nations
(FAO, Roma, Italy) recommended Sabella as one of organisms with most potential for the
development of integrated multi-trophic aquaculture systems [471].
Ficopomatus enigmaticus is a dominant species in estuaries and lagoons, where it can
affect the community structure and contribute to the invertebrate biomass [472,473]. Due
to its ability to build extensive reefs, F. enigmaticus is considered an ecosystem engineer
that can modify estuarine ecosystem, changing water flow, sedimentation rates, and cre-
ating a structured hard substrate habitat in a soft-sediment environment. Large aggrega-
tions of F. enigmaticus remove suspended particulate matter, reduce excess nutrient loads
and improve oxygen levels in enclosed waters, thereby improving the water quality and
environmental conditions for other benthic species (reviewed in [420]). Davies et al. [474]
stressed that because of the fundamental role F. enigmaticus played in the maintenance of
water quality of an enclosed system near Cape Town, South Africa, eradication of this
non-indigenous species should not be a management option.
3.6.5. Models Organisms in Research
Sabellids are used as models in regeneration biology, most notably in studies exam-
ining the developmental basis and functional ecology of regeneration [222,475–477].
Members of the genus Myxicola are known for the giant axon [478] that directly innervates
the worm’s muscles, presumably aiding in super-fast retraction into the tubes [479]. The
outsized nerves make this species a model organism for studies of neuroanatomy, neuro-
activity and electrophysiology [480–482]. Myxicola’s giant axons were also used for testing
the effects of the anticonvulsant Carbamazepine on the ionic conductance [483]. Moreo-
ver, the mucus of Myxicola infundibulum (Renier in Meneghini, 1847), with natural antibac-
terial and antioxidant compounds, showed potential for drug prospection [470].
Hydroides elegans is easily adapted for laboratory research because of its rapid gener-
ation time (three weeks) and ease of propagation. The adults spawn and eggs easily ferti-
lise, their larvae become metamorphically competent in several days and readily settle in
the laboratory. Thus, H. elegans has been declared an important model organism [484] and
has been used routinely during last two decades in hundreds of experimental embryo-
logical, larval ecology and biofouling studies, including tests of newly formulated marine
coatings (e.g., [485–490]). Other Hydroides species, such as H. ezoensis and H. dianthus, have
also acted as model organisms for larval ecology research (e.g., studies of mechanisms of
gregarious settlement by [491–493]. Spirobranchus lamarcki (Quatrefages, 1866) has pro-
vided an important model system for molecular and embryological work, including stud-
ies on the organization and expression of its developmental genes (e.g., [494–497]). Re-
cently H. elegans and S. triqueter have served as models in ocean acidification and bio-
mineralization research (e.g., [498–500]).
3.6.6. Objects of Ornamental Trade
Sabellida includes some of the most beautiful marine invertebrates due to their col-
ourful radiolar crowns. They are listed among the ten most imported ornamental inverte-
brates [501]) and are amongst the most photographed polychaetes found in marine guides
and featured on postcards, stamps, calendars, T-shirts and even tattoos. Largest sabellids
(Anamobaea, Bispira, Notaulax, Sabella and Sabellastarte) and serpulids such as Christmas
tree worms (Spirobranchus) and coco worms (Protula) are popular in the aquarium trade.
The vast majority of ornamental sabellids and serpulids are tropical species, although a
market for cold-water species has been growing [502,503]. Efforts to culture sabellids (e.g.,
Sabellastarte spectabilis (Grube, 1878) [504–506], Sabella pavonina Savigny, 1822 [270,507] and
Bispira brunnea (Treadwell, 1917) [508] are well under way. Aquaculture can provide en-
vironmental benefits by reducing collecting pressure on highly traded species.
Diversity 2021, 13, 130 54 of 74
3.7. Future Perspectives in Fanworm Research
As it is clear from this review, knowledge of Sabellida biodiversity is incomplete and
the reported species numbers appear to be an underestimation of the true diversity. This
review highlights that some of the lesser known coastal and continental shelf areas includ-
ing Hudson complex, the Atlantic coast of South America (especially the tropical Atlantic
region, excluding the Caribbean Sea), the coastlines along the Arabic Sea and Gulf of Ben-
gal, and the Far East of Russia. However, Africa, with the exception of South Africa and
Morocco, is by far the most neglected continent when it comes to taxonomic studies.
More surveys into deep-sea (abyssal and hadal), chemosynthesis-based (hydrother-
mal vents, methane seeps and organic falls) and freshwater habitats are needed for a better
understanding of the Sabellida diversity and adaptations to these habitats. The fact that
undescribed species have been collected in recent deep-sea cruises along several world-
wide regions (e.g., [284,509,510]) provides evidences for deep sea fanworms still awaiting
to be discovered. Studies of symbiotic/commensal relationships with other organisms,
e.g., molluscs, corals, sponges, or examinations of bacterial microbiomes may reveal not
only new taxa, but also new ecological relationships and trophic networks (e.g., [284,490]).
Importantly, the diversity of some remote areas, including deep sea environments, is
poorly known not only because of the obvious logistical difficulties with collecting, but
also due the insufficient number of experts and their unbalanced distribution across the
globe known as ‘taxonomic impediment’ (e.g., [94,511]). We need to train and sustain
more systematists able to discover, describe, identify and classify species and also to in-
crease efforts directed to manage and curate existing research collections [355].
As many more species are yet to be discovered, either in the field or in museum col-
lections, particular attention should be paid to setting a high standard for the new species
descriptions, which would include use of modern microscopic techniques (e.g., SEM,
Phase Contrast), assessment of intra- and interspecific variability, and preparation of qual-
ity informative illustrations (digital drawings and high-quality digital photographs of
stained fixed or live specimens, when possible). Exploration of both new characters, e.g.,
ultrastructure of calcareous serpulid tubes that proved useful for species delimitation
[107,227,512], and new techniques to examine existing morphological characters, e.g., to-
mography and 3D reconstructions (e.g., [237]) should significantly improve species de-
scriptions in the future and aid species delimitations.
Although multivariate morphometrics have been used to analyse differences among
annelid species and populations (e.g., [513,514]), this technique is not very common for
species delimitation because body shapes of these soft-bodied organisms vary depending
on the fixation or anaesthetization methods [234]. We suggest that application of morpho-
metrics to chaetal or opercular traits should be explored. However, regardless of availa-
bility DNA data, morphological studies must include statistical assessment of intraspecific
variability and its sources (such as size-dependent, ontogenetic, environmental) (e.g.,
[72,278,515]).
Understanding of true species diversity of Sabellida requires world-wide revisionary
studies of existing species and their distribution ranges. As early species descriptions are
often very short and sometimes poorly illustrated, further re-descriptions of older species
(especially described before mid-20th century) are needed, ideally based on topotypical
material (as, e.g., done for serpulid Spirobranchus kraussii by Simon et al. [193]). For the
species with lost or lacking types, neotypes should designated (e.g., as for Pseudopotamilla
reniformis (Bruguière, 1789) by Knight-Jones et al. [111]), preferably accompanied by DNA
sequence data (e.g., as done for Hydroides brachyacantha by Sun et al. [197]. It is imperative
that the type material (holotype, type series, additional specimens showing intraspecific
variability, and DNA extractions) is always deposited in properly curated permanent mu-
seum collection(s) where it is maintained in optimal conditions [516].
Contrary to previous conceptions that the ocean has no boundaries and that poly-
chaetes more often than other organisms have cosmopolitan distributions [327], it now
Diversity 2021, 13, 130 55 of 74
became clear that the genetic and species diversity of marine invertebrates is highly struc-
tured geographically and significant species diversity is hidden in former ‘cosmopolitan
polychaete species’. Therefore, resolution of ‘cosmopolitan species’ should be one of the
main goals of revisionary studies of Sabellida. This goal is only achieved with application
of fast-developing molecular tools such as DNA sequencing and genomics/transcriptom-
ics. Molecular tools and analytical methods are indispensable to further improve our un-
derstanding of the species diversity, but also to trace the pathways and origins of invasive
species, to determine biogeographic boundaries between species, and to provide reliable
phylogenic hypotheses. Robust well-resolved phylogenies with significant taxon coverage
using transcriptome and mitochondrial genome data are important to address important
character evolution questions (e.g., photoreceptor evolution and evolution of the repro-
ductive and larval strategies in Sabellidae and Serpulidae). Finally, in the future molecular
identification of species by non-specialists might replace morphology-based identifica-
tions only if reliable databases of reference sequences supported by voucher specimen
depositories are built.
Supplementary Materials: The following are available online at www.mdpi.com/1424-
2818/13/3/130/s1, Table S1: Fabriciidae, species and type localities; Table S2: Sabellidae, species and
type localities; Table S3: Serpulidae, species and type localities.
Author Contributions: Conceptualization, M.C. and M.A.T.-H.; validation, M.C., E.K., A.B.,
J.M.d.M.N. and M.A.T.-H.; writing—original draft preparation M.C., E.K., A.B., J.M.d.M.N. and
M.A.T.-H.; writing—review and editing, M.C., E.K., A.B., J.M.d.M.N. and M.A.T.-H.; visualization,
M.C., E.K., A.B., J.M.d.M.N. and M.A.T.-H.; coordination, M.C., E.K., A.B., J.M.d.M.N. and M.A.T.-
H.; funding acquisition, M.C. and E.K. All authors have read and agreed to the published version
of the manuscript.
Funding: MC was funded by 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. EK was funded by the Australian Biological Research Study (ABRS) grant
RG18-21. JMMN was funded by a productivity grant from “CNPq—Conselho Nacional de Desen-
volvimento Científico e Tecnológico, Brazil, level 2”.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: Not applicable.
Acknowledgments: We would like to thank Mike Bok (Lund University, Sweden), Alexander Se-
menov (Moscow University, Russia), Greg Rouse (Scripps Institution of Oceanography, UCSD,
USA), Graeme Christie (Australia), Anna Dietrich (Institute for Applied Ecosystem Research, Ger-
many), Vitaly Syomin (P.P. Shirshov Institute of Oceanology), Humberto Bahena (Ecosur, Mexico),
Eunice Wong (University of Texas at Austin, USA), Alexander Rzhavsky (Russian Academy of Sci-
ences, Russia), Orlemir Carrete (Universidade de São Paolo, Brazil)and Floor Verbiest (Rijksmu-
seum van Natuurlijke Historie, Leiden) for letting us use some their fantastic pictures of live ani-
mals. Laura C. Armendáriz (Instituto de Limnología “Dr Raúl A. Ringuelet”, CONICET UNLP, Ar-
gentina) and Sue Lindsay (Macquarie University) provided with SEM micrographs. Alisson Ricardo
da Silva (Museu da Casa Brasileira, Brazil), helped with the elaboration of the figures. We appreciate
Geoff Read (NIWA New Zealand) for updating WoRMS and also Vollrath Wiese (Haus der Natur,
Cismar) for helping us to clarify identity of Sabella species described by Gmelin. Further thanks are
due to the publisher De Gruyter for permission to use the following images from chapter 7.4.8 Fab-
riciidae Rioja, 1823, from Handbook for Zoology, vol. 3 (Eds. G. Purschke, M. Böggemann and W.
Westheide), De Gruyter GmbH, Berlin/Boston, 2021: 7.4.8.1A; 7.4.8.2 A, C; 7.4.8.6 D. We appreciate
helpful comments from three anonymous reviewers.
Conflicts of Interest: The authors declare no conflict of interest.
Diversity 2021, 13, 130 56 of 74
Appendix A
Fabriciidae and Sabellidae species with doubtful identity requiring further investiga-
tion (inquirenda), indeterminable or incorrect assignation.
Fabriciidae
1. Manayunkia siaukhu Annenkova, 1938 inquirenda. Based on the description, M. siaukhu
has pygidial eyes [517] and thus does not fulfill diagnostic features for the genus.
Sabellidae
2. Clymeneis Rathke, 1843 inquirenda
Clymeneis and its type species Clymeneis stigmosa Rathke, 1843 are of doubtful identity
requiring further investigation. Description was based in specimens inquirenda (?) appar-
ently without crown and types have not been found. It has not been reported over more
than a century, but recently mentioned in the paper about original specimens and type
localities of early described polychaete species from Norway [518].
3. Sabella aculeata Gmelin in Linnaeus, 1788. Insecta: Trichoptera.
4. Sabella ammonita Gmelin in Linnaeus, 1788. Insecta: Trichoptera.
5. Sabella arenaria Montagu, 1803 indeterminable
Described based on the tube only, the worm is unknown [42] (pp. 552).
6. Sabella arundinacea Gmelin in Linnaeus, 1788. Insecta: Trichoptera.
7. Sabella clavata Gmelin in Linnaeus, 1788. Insecta: Trichoptera.
8. Sabella compressa Montagu, 1803 indeterminable
Original description was based only in the tube. Hartman [325] (pp.559) suggested
that the tube is perhaps from a pectinariid.
9. Sabella conica Gmelin in Linnaeus, 1788. Insecta: Trichoptera.
10. Sabella corticalis Gmelin in Linnaeus, 1788. Insecta: Trichoptera.
11. Sabella dimidiata Gmelin in Linnaeus, 1788. Insecta: Trichoptera.
12. Sabella flabellata Savigny, 1820 inquirenda
Declared as inquirenda by Knight-Jones and Perkins [337] (pp. 398).
13. Sabella fixa Gmelin in Linnaeus, 1788. Insecta: Trichoptera.
14. Sabella grossa Baird, 1865 inquirenda
Declared as inquirenda by Knight-Jones and Mackie [338] (pp. 2296).
15. Sabella helicina Gmelin in Linnaeus, 1788. Insecta: Trichoptera.
16. Sabella nigra Gmelin in Linnaeus, 1788. Insecta: Trichoptera.
17. Sabella sabulosa Gmelin in Linnaeus, 1788. Insecta: Trichoptera.
18. Sabella setiformis Montagu, 1803 indeterminable
The tube was the only structure described, the worm is unknown [519] (pp.553).
19. Sabella stagnalis Gmelin in Linnaeus, 1788. Insecta: Trichoptera.
20. Sabella subcylindrica Montagu, 1803 indeterminable
Only the tube was described, animal unknown [519] (pp. 552-553).
21. Sabella teredula Chiereghini in Siebold, 1850 indeterminable
Only the tube was described [520] (pp. 369).
22. Sabella trigona Chiereghini in Siebold, 1850 indeterminable
Only the tube was described [520] (pp. 369).
23. Sabella uncinata Gmelin in Linnaeus, 1788. Insecta: Trichoptera.
24. Sabella vegetabilis Gmelin in Linnaeus, 1888. Insecta: Trichoptera.
25. Sabella zonalis Stimpson, 1854 inquirenda
Declared inquirenda by Knight-Jones and Perkins [337] (pp. 405).
Diversity 2021, 13, 130 57 of 74
References
1. Kupriyanova, E.K.; Rouse, G.W. Yet another example of paraphyly in Annelida: Molecular evidence that Sabellidae contains
Serpulidae. Mol. Phylogenet. Evol. 2008, 46, 1174–1181, doi:10.1016/j.ympev.2007.10.025.
2. Capa, M.; Hutchings, P.; Aguado, M.T.; Bott, N.J. Phylogeny of Sabellidae (Annelida) and relationships with other taxa inferred
from morphology and multiple genes. Cladistics 2011, 27, 449–469, doi:10.1111/j.1096-0031.2010.00341.x.
3. Tilic, E.; Sayyari, E.; Stiller, J.; Mirarab, S.; Rouse, G.W. More is needed—thousands of loci are required to elucidate the relation-
ships of the ‘Flowers of the Sea’ (Sabellida, Annelida). Mol. Phylogenet. Evol. 2020, 151, 106892, doi:10.1016/j.ympev.2020.106892.
4. Bick, A. Fabriciidae Rioja, 1923. In Handbook of Zoology Annelida, Volume 3: Pleistoannelida, Sedentaria III and Errantia I; Purschke,
G., Westheide, W., Böggemann, M., Eds.; De Gruyter: Berlin, Germany; Boston, MA, USA, 2021; pp. 1–33.
5. Savigny, J.-C. Systèmes des Annélides, Principalement de Celles des Côtes de l’Égypte et de la Syrie, Offrant les Caractères tant Distinctifs
que Naturels des Ordres, Familles et Genres, Avec la Description des Espèces Système des Annelides (I); Commission des sciences et arts
d’Egypte: Paris, France, 1822; Vol. 1, pp. 1–128.
6. Burmeister, H. Handbuch Der Naturgeschichte. Zum Gebrauch bei Voresungen; Zweite Abt. Zoologie.: Berlin, Germany, 1837; pp.
1–858.
7. Grube, A.E. Die Familien der Anneliden. Archiv Für Naturgeschichte 1850, 16, 249–364.
8. Grube, A.E. Beschreibungen Einiger von Georg Ritter von Frauenfeld Gesammelter Anneliden und Gephyreen des Rothen
Meeres. Verhandlungen der Kaiserlich Königlichen Zoologisch-Botanischen Gesellschaft in Wien 1868, 18, 629–650.
9. Malmgren, A.J. Nordiska Hafs-Annulater. Öfversigt af Königlich Vetenskapsakademiens Förhandlingar 1866, 22, 355–410.
10. Hatschek, B. System Der Anneliden, ein vorläufiger Bericht. Sitzungsberichte des Deutschen Naturwissenschaftlich-Medi-
cinischen Vereines für Böhmen”Lotos“ in Prag. Neue Folge 1893, 13, 123–126.
11. Dales, R.P. The nature of the pigments in the crown of sabellid and serpulid polychaetes. J. Mar. Biol. Assoc. UK 1962, 42, 259–
274.
12. Fauchald, K. The polychaete worms. Definitions and keys to the orders, families and genera. Nat. Hist. Mus. LA County Sci. Ser.
1977, 28, 1–188.
13. Fauchald, K.; Rouse, G.W. Polychaete systematics: Past and present. Zool. Scr. 1997, 26, 71–138.
14. Andrade, S.C.S.; Novo, M.; Kawauchi, G.Y.; Worsaae, K.; Pleijel, F.; Giribet, G.; Rouse, G.W. Articulating “Archiannelids”: Phy-
logenomics and annelid relationships, with emphasis on meiofaunal taxa. Mol. Biol. Evol. 2015, 32, 2860–2875, doi:10.1093/mol-
bev/msv157.
15. Weigert, A.; Bleidorn, C. Current status of annelid phylogeny. Org. Divers. Evol. 2016, 16, 345–362, doi:10.1007/s13127-016-0265-
7.
16. Helm, C.; Bok, M.J.; Hutchings, P.; Kupriyanova, E.; Capa, M. Developmental studies provide new insights into the evolution
of sense organs in Sabellariidae (Annelida). BMC Evol. Biol. 2018, 18, 149–162, doi:10.1186/s12862-018-1263-5.
17. Wilson, D.P. The development of the sabellid Branchiomma vesiculosum. J. Cell Sci. 1936, 78, 534–603.
18. Berrill, N. Functional morphology and development of segmental inversion in sabellid polychaetes. Biol. Bull. 1977, 153, 453–
467.
19. Smith, R.S. Relationships within the Order Sabellida (Polychaeta). Ophelia Suppl. 1991, 5, 249–260.
20. Bartolomaeus, T. Structure and formation of thoracic and abdominal uncini in Fabricia stellaris (Müller, 1774)–implication for
the evolution of Sabellida (Annelida). Zool. Anz. J. Comp. Zool. 2002, 241, 1–17.
21. Kieselbach, D.; Hausen, H. Chaetal arrangement provides no support for a close relationship of Sabellidae and Sabellariidae
(Annelida). J. Morphol. 2008, 269, 104–117, doi:10.1002/jmor.10537.
22. Capa, M.; Hutchings, P.; Peart, R. Systematic revision of Sabellariidae (Polychaeta) and their relationships with other poly-
chaetes using morphological and DNA sequence data: Systematics of Sabellariidae. Zool. J. Linn. Soc. 2012, 164, 245–284,
doi:10.1111/j.1096-3642.2011.00767.x.
23. Capa, M.; Parapar, J.; Hutchings, P. Phylogeny of Oweniidae (Polychaeta) based on morphological data and taxonomic revision
of Australian fauna: Oweniid phylogeny and Australian fauna. Zool. J. Linn. Soc. 2012, 166, 236–278, doi:10.1111/j.1096-
3642.2012.00850.x.
24. Capa, M.; Giangrande, A.; Nogueira, J.M.M.; Tovar-Hernández, M.A. Sabellidae Latreille, 1825. In Handbook of Zoology, Annelida,
Volume 2: Pleistoannelida, Sedentaria II; Purschke, G., Böggemann, M., Westheide, W., Eds.; De Gruyter: Berlin, Germany, 2019;
pp. 164–212.
25. Capa, M.; Hutchings, P. Sabellariidae Johnston, 1865. In Handbook of Zoology, Annelida, Volume 2: Pleistoannelida, Sedentaria II;
Purschke, G., Böggemann, M., Westheide, W., Eds.; De Gruyter: Berlin, Germany, 2019; pp. 144–163.
26. Capa, M.; Parapar, J.; Hutchings, P.; Mortimer, K. In 4. Palaeoannelida. Annelida; Purschke, G., Böggemann, M., Westheide, W.,
Eds.; De Gruyter: Berlin, Germany, 2019; pp. 91–132. ISBN 978-3-11-029158-2.
27. Huang, D.; Fitzhugh, K.; Rouse, G.W. Inference of phylogenetic relationships within Fabriciidae (Sabellida, Annelida) using
molecular and morphological data. Cladistics 2011, 27, 356–379, doi:10.1111/j.1096-0031.2010.00343.x.
28. Weigert, A.; Helm, C.; Meyer, M.; Nickel, B.; Arendt, D.; Hausdorf, B.; Santos, S.R.; Halanych, K.M.; Purschke, G.; Bleidorn, C.;
et al. Illuminating the base of the annelid tree using transcriptomics. Mol. Biol. Evol. 2014, 31, 1391–1401, doi:10.1093/mol-
bev/msu080.
29. Struck, T.H.; Golombek, A.; Weigert, A.; Franke, F.A.; Westheide, W.; Purschke, G.; Bleidorn, C.; Halanych, K.M. The evolution
of annelids reveals two adaptive routes to the interstitial realm. Curr. Biol. 2015, 25, 1993–1999, doi:10.1016/j.cub.2015.06.007.
Diversity 2021, 13, 130 58 of 74
30. WoRMS 2020, Sabellida. Available online: http://www.marinespecies.org/aphia.php?p=taxdetails&id=882 (accessed on 2 March
2021).
31. Spalding, M.D.; Fox, H.E.; Allen, G.R.; Davidson, N.; Ferdaña, Z.A.; Finlayson, M.; Halpern, B.S.; Jorge, M.A.; Lombana, A.;
Lourie, S.A.; et al. Marine ecoregions of the World: A bioregionalization of coastal and shelf areas. BioScience 2007, 57, 573–583,
doi:10.1641/B570707.
32. Udvardy, M.D. A Classification of the Biogeographical Provinces of the World; IUCN Occasional Paper 18: Morges, Switzerland,
1975; pp. 1–49.
33. Olson, D.M.; Dinerstein, E.; Wikramanayake, E.D.; Burgess, N.D.; Powell, G.V.; Underwood, E.C.; D’amico, J.A.; Itoua, I.; Strand,
H.E.; Morrison, J.C. Terrestrial ecoregions of the world: A new map of life on Earth a new global map of terrestrial ecoregions
provides an innovative tool for conserving biodiversity. BioScience 2001, 51, 933–938.
34. GBIF 2020. Available online: https://www.gbif.org/es/ (accessed on 3 March 2021).
35. NCBI 2020. Available online: https://www.ncbi.nlm.nih.gov (accessed on 3 March 2021).
36. Ratnasingham, S.; Hebert, P.D.N. BOLD: The Barcode of Life Data System (http://www.barcodinglife.org). Mol. Ecol. Notes 2007,
7, 355–364.
37. Rafinesque, C.S. Analyse de la Nature ou Tableau de l’Universe et Des Corps Organize; De l'imprimerie de Jean Barravecchia: Pa-
lermo, Italy, 1815.
38. Chamberlin, R.V. The Annelida Polychaeta. Mem. Mus. Comp. Zool. 1919, 48, 1–518.
39. Rioja, E. Estudio sistemático de las especies Ibéricas del Suborden Sabelliformia. Trab. Mus. Nac. Cien. Nat. (Ser. Zool.) 1923, 48,
1–144.
40. Pillai, G. Studies on a collection of spirorbids from Ceylon, together with a critical review and revision of spirorbid systematics
and an account of their phylogeny and zoogeography. Ceylon J. Sci. (Biol. Sci.) 1970, 8, 100–172.
41. ten Hove, H.A. Towards a phylogeny in serpulids (Annelida; Polychaeta). In Proceedings of the First International Polychaete Con-
ference; Hutchings, P.A., Ed.; Linnean Society of New South West: Sydney, Australia, 1984; pp. 181–196.
42. Fitzhugh, K. A systematic revision of the Sabellidae-Caobangiidae-Sabellongidae complex (Annelida: Polychaeta). Bull. Am.
Mus. Nat. Hist. 1989, 192, 1–104.
43. Kupriyanova, E.K. Life history evolution in serpulimorph polychaetes: A phylogenetic analysis. Hydrobiologia 2003, 496, 105–
114.
44. Macdonald, T.A. Phylogenetic relations among spirorbid subgenera and the evolution of opercular brooding. Hydrobiologia
2003, 496, 125–143.
45. Kupriyanova, E.K.; Macdonald, T.A.; Rouse, G.W. Phylogenetic relationships within Serpulidae (Sabellida, Annelida) inferred
from molecular and morphological data. Zool. Scr. 2006, 35, 421–439, doi:10.1111/j.1463-6409.2006.00244.x.
46. Kupriyanova, E.K.; ten Hove, H.A.; Sket, B.; Zakšek, V.; Trontelj, P.; Rouse, G.W. Evolution of the unique freshwater cave-
dwelling tube worm Marifugia cavatica (Annelida: Serpulidae). Syst. Biodivers 2009, 7, 389–401, doi:10.1017/S1477200009990168.
47. Lehrke, J.; Harry, A.; Macdonald, T.A.; Bartolomaeus, T.; Bleidorn, C. Phylogenetic relationships of Serpulidae (Annelida: Pol-
ychaeta) based on 18S rDNA sequence data, and implications for opercular evolution. Org. Divers Evol. 2007, 7, 195–206.
48. Kupriyanova, E.K.; Nishi, E. Serpulidae (Annelida, Polychaeta) from Patton-Murray Seamounts, Gulf of Alaska, North Pacific
Ocean. Zootaxa 2010, 2665, 51–68, doi:10.11646/zootaxa.2665.1.3.
49. Prentiss, N.K.; Vasileiadou, K.; Faulwetter, S.; Arvanitidis, C.; ten Hove, H.A. A new genus and species of Serpulidae (Annelida,
Polychaeta, Sabellida) from the Caribbean Sea. Zootaxa 2014, 3900, 204–222.
50. Rzhavsky, A.V.; Kupriyanova, E.K.; Sikorski, A.V. Two new species of serpulid polychaetes (Annelida) from the Barents Sea.
Fauna Norv. 2013, 32, 27–38.
51. Johansson, K.E. Beiträge Zur Kenntnis der Polychaeten-Familien Hermellidae Sabellidae und Serpulidae. Zool. Bidr. Uppsala
1927, 11, 1–184.
52. Fitzhugh, K. Further revisions of the Sabellidae subfamilies and cladistic relationships among the Fabriciinae (Annelida: Poly-
chaeta). Zool. J. Linn. Soc. 1991, 102, 305–332.
53. Fitzhugh, K. Systematics of several fabriciin fan worms (Polychaeta: Sabellidae: Fabriciinae) previously referred to Fabricia or
Fabriciola. J. Nat. Hist. 1991, 25, 1101–1120.
54. Fitzhugh, K. On the systematic position of Monroika africana (Monro) (Polychaeta: Sabellidae: Fabriciinae) and a description of
a new fabriciin genus and species from Australia. Proc. Biol. Soc. Wash. 1992, 105, 116–131.
55. Fitzhugh, K. Additions to the description of the fanworm genus Pseudofabricia Cantone, 1972 (Polychaeta: Sabellidae: Fabrici-
inae). Contrib. Sci. 1995, 456, 1–6.
56. Fitzhugh, K. New fanworm species (Polychaeta: Sabellidae: Fabriciinae) in the genus Pseudofabriciola Fitzhugh. J. Nat. Hist. 1996,
30, 1267–1286.
57. Fitzhugh, K. New fan worm genera and species (Polychaeta, Sabellidae, Fabriciinae) from the Western Pacific, and cladistic
relationships among genera. Zool. Scr. 1998, 27, 209–245, doi:10.1111/j.1463-6409.1998.tb00438.x.
58. Fitzhugh, K. New species of Fabricinuda Fitzhugh and Pseudofabriciola Fitzhugh (Polychaeta: Sabellidae: Fabriciinae), with an
emendation of Pseudofabriciola australiensis (Hartmann-Schröder). J. Nat. Hist. 2002, 36, 893–925, doi:10.1080/00222930110034580.
59. Nogueira, J.M.D.M.; Fitzhugh, K.; Rossi, M.C.S. A new genus and new species of fan worms (Polychaeta: Sabellidae) from
Atlantic and Pacific Oceans—the formal treatment of taxon names as explanatory hypotheses. Zootaxa 2010, 2603, 1–52.
Diversity 2021, 13, 130 59 of 74
60. Fitzhugh, K.; Giangrande, A.; Simboura, N. New species of Pseudofabriciola Fitzhugh, 1990 (Polychaeta: Sabellidae: Fabriciinae),
from the Mediterranean Sea. Zool. J. Linn. Soc. 1994, 110, 219–241.
61. Fitzhugh, K. Fabricinuda, a new genus of Fabriciinae (Polychaeta: Sabellidae). Proc. Biol. Soc. Wash. 1990, 103, 161–178.
62. Fitzhugh, K. Two new genera of the Subfamily Fabriciinae (Polychaeta: Sabellidae). Am. Mus. Novit. 1990, 2967, 1–19.
63. Fitzhugh, K. A new deep-water genus and species of Fabriciinae fanworm (Polychaeta: Sabellidae) from Antarctica. Contrib. Sci.
2001, 491, 1–8.
64. Fitzhugh, K. A new species of Megalomma Johansson, 1927 (Polychaeta: Sabellidae: Sabellinae) from Taiwan, with comments on
sabellid dorsal lip classification. Zool. Stud. 2003, 42, 106–134.
65. Rouse, G.; Fitzhugh, K. Broadcasting fables: Is external fertilization really primitive? sex, size, and larvae in sabellid polychaetes.
Zool Scr. 1994, 23, 271–312, doi:10.1111/j.1463-6409.1994.tb00390.x.
66. Fitzhugh, K.; Rouse, G.W. A remarkable new genus and species of fan worm (Polychaeta: Sabellidae: Sabellinae) associated
with marine gastropods. Invertebr. Biol. 1999, 118, 357–390.
67. Cochrane, S. Snowflakes and feather-dusters–some challenges for soft-bottom fanworm systematics. Hydrobiologia 2003, 496,
49–62.
68. Capa, M. Taxonomic revision and phylogenetic relationships of apomorphic sabellids (Polychaeta) from Australia. Invertebr.
Syst. 2007, 21, 537, doi:10.1071/IS07002.
69. Capa, M. The genera Bispira Krøyer, 1856 and Stylomma Knight-Jones, 1997 (Polychaeta, Sabellidae): Systematic revision, rela-
tionships with close related taxa and new species from Australia. Hydrobiologia 2008, 596, 301–327, doi:10.1007/s10750-007-9105-
2.
70. Capa, M.; Bybee, D.R.; Bybee, S.M. Establishing species and species boundaries in Sabellastarte Krøyer, 1856 (Annelida: Sabelli-
dae): An integrative approach. Org. Divers. Evol. 2010, 10, 351–371, doi:10.1007/s13127-010-0033-z.
71. Tovar-Hernández, M.A. Phylogeny of Chone Krøyer, 1856 (Polychaeta: Sabellidae) and related genera. J. Nat. Hist. 2008, 42,
2193–2226.
72. Capa, M.; Pons, J.; Hutchings, P. Cryptic diversity, intraspecific phenetic plasticity and recent geographical translocations in
Branchiomma (Sabellidae, Annelida). Zool. Scr. 2013, 42, 637–655, doi:10.1111/zsc.12028.
73. Capa, M.; Murray, A. Integrative taxonomy of Parasabella and Sabellomma (Sabellidae: Annelida) from Australia: Description of
new species, indication of cryptic diversity, and translocation of some species out of their natural distribution range: Australian
Parasabella and Sabellomma. Zool. J. Linn. Soc. 2015, 175, 764–811, doi:10.1111/zoj.12308.
74. Capa, M.; Murray, A. Combined morphological and molecular data unveils relationships of Pseudobranchiomma (Sabellidae,
Annelida) and reveals higher diversity of this intriguing group of fan worms in Australia, including potentially introduced
species. ZooKeys 2016, 622, 1–36, doi:10.3897/zookeys.622.9420.
75. Giangrande, A.; Licciano, M. The genus Euchone (Polychaeta, Sabellidae) in the Mediterranean Sea, addition of two new species
and discussion on some closely related taxa. J. Nat. Hist. 2006, 40, 1301–1330.
76. Licciano, M.; Giangrande, A.; Gambi, M.C. A new genus of Sabellidae (Annelida, Polychaeta) from Antarctica, with discussion
of relationships among plesiomorphic genera within Sabellinae. Zootaxa 2009, 2226, 28–42, doi:10.11646/zootaxa.2226.1.3.
77. Kupriyanova, E.K.; Bastida-Zavala, R.; Halt, M.N.; Lee, M.S.Y.; Rouse, G.W. Phylogeny of the Serpula-Crucigera-Hydroides clade
(Serpulidae: Annelida) using molecular and morphological data: Implications for operculum evolution. Invertebr. Syst. 2008, 22,
425–437, doi:10.1071/IS08011.
78. Sun, Y.; Kupriyanova, E.K.; Qiu, J.W. COI Barcoding of Hydroides: A road from impossible to difficult. Invertebr. Syst. 2012, 26,
539–547, doi:10.1071/IS12024.
79. Sun, Y.; Wong, E.; Ahyong, S.T.; Williamson, J.E.; Hutchings, P.A.; Kupriyanova, E.K. Barcoding and multi-locus phylogeogra-
phy of the globally distributed calcareous tubeworm genus Hydroides Gunnerus, 1768 (Annelida, Polychaeta, Serpulidae). Mol.
Phylogenet. Evol 2018, 127, 732–745, doi:10.1016/j.ympev.2018.06.021.
80. Tovar-Hernández, M.A.; Villalobos-Guerrero, T.F.; Kupriyanova, E.K.; Sun, Y. A new fouling Hydroides (Annelida, Sabellida,
Serpulidae) from Southern Gulf of California. J. Mar. Biol. Assoc. UK 2016, 96, 693, doi:10.1017/S0025315415000764.
81. Smith, A.M.; Henderson, Z.E.; Kennedy, M.; King, T.M.; Spencer, H.G. Reef formation versus solitariness in two New Zealand
serpulids does not involve cryptic species. Aquat. Biol 2012, 16, 97–103.
82. Willette, D.A.; Iniguez, A.R.; Kupriyanova, E.K.; Starger, C.J.; Varman, T.; Toha, A.H.; Maralit, B.A.; Barber, P.H. Christmas tree
worms of Indo-Pacific coral reefs: Untangling the Spirobranchus corniculatus (Grube, 1862) complex. Coral Reefs 2015, 34, 899–
904.
83. Perry, O.; Bronstein, O.; Simon-Blecher, N.; Atkins, A.; Kupriyanova, E.; ten Hove, H.; Levy, O.; Fine, M. On the genus Spiro-
branchus (Annelida, Serpulidae) from the Northern Red Sea, and a description of a new species. Inverterb. Syst. 2018, 32, 605,
doi:10.1071/IS17061.
84. Pazoki, S.; Rahimian, H.; Struck, T.H.; Katouzian, A.R.; Kupriyanova, E.K. A new species of the Spirobranchus kraussii-complex
(Annelida, Serpulidae) from the Persian Gulf and Gulf of Oman. Zootaxa 2020, 4748, 401–430.
85. Bailey, J.H. Methods of brood protection as a basis for reclassification of the Spirorbinae (Serpulidae). Zool. J. Linn. Soc. 1969, 48,
387–407.
86. Thorp, C.H. The structure of the operculum in Pileolaria granulata (L.) (Polychaeta: Serpulidae) and related species. J. Exp. Mar.
Biol. Ecol. 1975, 20, 215–235.
87. Knight-Jones, P.; Thorp, C.H. The opercular brood chambers of Spirorbidae. J. Linn. Soc. (Zool.) 1984, 80, 121–133.
Diversity 2021, 13, 130 60 of 74
88. Nishi, E. On the origin of brooding characteristics in spirorbids with the phylogeny of sabellids and serpulids (Annelida, Poly-
chaeta, Sedentaria). Proc. Jap. Soc. Syst. Zool. 1993, 49, 6–12.
89. Thorp, C.; Segrove, F. The opercular moult in Spirorbis spirorbis (L.) and S. pusilloides Bush (Polychaeta: Serpulidae). J. Exp. Mar.
Biol. Ecol. 1975, 19, 117–143.
90. Rzhavsky, A.V.; Kupriyanova, E.K. Evolution of spirorbin brooding: A phylogenetic analysis and a test of an oxygen limitation
hypothesis. Invertebr. Zool. 2019, 16, 409–430, doi:10.15298/invertzool.16.4.09.
91. Pamungkas, J.; Glasby, C.J.; Read, G.B.; Wilson, S.P.; Costello, M.J. Progress and perspectives in the discovery of polychaete
worms (Annelida) of the world. Helgol. Mar. Res. 2019, 73, 4.
92. Fitzhugh, K. A Revision of the genus Fabricia Blainville, 1828 (Polychaeta: Sabellidae: Fabriciinae). Sarsia 1990, 75, 1–16.
93. Cepeda, D.; Lattig, P. New reports and description of a new species of Sabellidae (Annelida) for the Iberian Peninsula and
Balearic Archipelago. Mar. Biol. Res. 2017, 13, 832–853.
94. Giangrande, A.; Wasson, B.; Lezzi, M.; Licciano, M. Description of Euchone anceps sp. nov. (Annelida: Sabellidae) from the Med-
iterranean Sea and Northeast Atlantic, with remarks on the difficulty of generic definition. Eur. Zool. J. 2017, 84, 193–207.
95. Çinar, M.E.; Giangrande, A. A new species of Pseudobranchiomma (Sabellidae, Polychaeta) from the Sea of Marmara (Turkey).
Mar. Biodivers 2018, 48, 1563–1569.
96. López, E.; Olivier, F.; Grant, C.; Archambault, P.A. new species and four new records of sedentary polychaetes from the Cana-
dian High Arctic. J. Mar. Biol. Assoc. UK 2017, 97, 1685–1694, doi:10.1017/S0025315416000953.
97. Nishi, E.; Gil, J.; Tanaka, K.; Kupriyanova, E.K. Notaulax yamasui sp. n. (Annelida, Sabellidae) from Okinawa and Ogasawara,
Japan, with notes on its ecology. ZooKeys 2017, 660, 1–16.
98. Nishi, E.; Tanaka, K.; Tovar-Hernández, M.A. A new species of Claviramus (Annelida, Sabellida, Sabellidae) from the Ariake
Inland Sea, Kyushu, Japan. ZooKeys 2019, 880, 25–32. doi:10.3897/zookeys.880.36281.
99. Tovar-Hernández, M.A.; de León-González, J.A.; Bybee, D.R. Sabellid worms from the Patagonian Shelf and Humboldt Current
System (Annelida, Sabellidae): Phyllis Knight-Jones’ and José María Orensanz’s collections. Zootaxa 2017, 4283, 1–64,
doi:10.11646/zootaxa.4283.1.1.
100. Tovar-Hernández, M.A.; Harry, A.; Vinn, O.; Zatoń, M.; de León-González, J.A.; García-Garza, M.E. Fan worms (Annelida:
Sabellidae) from Indonesia collected by the Snellius II Expedition (1984) with descriptions of three new species and tube micro-
structure. PeerJ 2020, 8, e9692, doi:10.7717/peerj.9692.
101. Tovar-Hernández, M.A.; García-Garza, M.E.; de León-González, J.A. Sclerozoan and fouling sabellid worms (Annelida: Sabel-
lidae) from Mexico with the establishment of two new species. Biodivers. Data J. 2020, 8, e57471, doi:10.3897/BDJ.8.e57471.
102. Bick, A.; Bastrop, R.; Kotta, J.; Meißner, K.; Meyer, M.; Syomin, V. Description of a new species of Sabellidae (Polychaeta, An-
nelida) from fresh and brackish waters in Europe, with some remarks on the branchial crown of Laonome. Zootaxa 2018, 4483,
349–364, doi:10.11646/zootaxa.4483.2.7.
103. Tilic, E.; Feerst, K.G.; Rouse, G.W. Two new species of Amphiglena (Sabellidae, Annelida), with an assessment of hidden diversity
in the Mediterranean. Zootaxa 2019, 4648, 337–353, doi:10.11646/zootaxa.4648.2.8.
104. Renier, S.A. Osservazioni postume di Zoologia Adriatica, del Professore Stefano Andrea Renier, Membro Effettivo dell’Instituto
Italiano, Pubblicate per Cura dell’IR Istituto Veneto Di Scienze, Lettere er Arti a Studio Del Membro Effettivo Prof. G. Me-
neghini. Giovanni Cecchini: Venezia, Italia, 1847, pp. 1–122.
105. Linnaeus, C. Systema Naturae, 10th ed.; L. Salvius: Holmiae, Sweden, 1758; Vol. 1. pp. 1–823.
106. Pillai, T.G. A revision of the genera Galeolaria and Pyrgopolon (Polychaeta: Serpulidae), with discussions on opercular insertion
as a character in their taxonomy and relationships, and their zoogeography. Zootaxa 2009, 2060, 47–58.
107. Kupriyanova, E.K.; Ippolitov, A.P. Deep-sea serpulids (Annelida: Polychaeta) in tetragonal tubes: On a tube convergence path
from the Mesozoic to Recent. Zootaxa 2015, 4044, 151–200.
108. Tovar-Hernández, M.A. Taxonomic update of the sabellids (Polychaeta: Sabellidae) from Chile and taxa established by prof.
Ernst Ehlers, with a key to genera of Sabellinae. An. Inst. Patagon. 2010, 38, 7–29, doi:10.4067/S0718-686X2010000200002.
109. Tovar-Hernández, M.A.; Fitzhugh, K. Sabellidae Latreille, 1825. In Poliquetos (Annelida: Polychaeta) de México y América Tropical,
2nd ed.; De León-González, J.A., Bastida-Zavala, J.R., Carrera-Parra, L.F., García-Garza, M.E., Salazar-Vallejo, S.I., Solís-Weiss,
V., Tovar-Hernández, M.A., Eds.; Universidad Autónoma de Nuevo León: Monterrey, Mexico, 2021; Volume 3, in press.
110. ten Hove, H.A.; Kupriyanova, E.K. Taxonomy of Serpulidae (Annelida, Polychaeta): The state of affairs. Zootaxa 2009, 2036, 1–
126, doi:10.11646/zootaxa.2036.1.1.
111. Knight-Jones, P.; Darbyshire, T.; Petersen, M.E.; Tovar-Hernández, M. What is Pseudopotamilla reniformis (Sabellidae)? Compar-
isons of populations from Britain, Iceland and Canada with comments on Eudistylia and Schizobranchia. Zootaxa 2017, 4254, 201–
220.
112. Jirkov, I. Polikhety Severnogo Ledovitogo Okeana [Polychaeta of the Arctic Ocean.]; Janus-K Press: Moscow, Russia, 2001; pp. 1–632.
(In Russian)
113. Rzhavsky, A.V.; Kupriyanova, E.K.; Sikorski, A.V.; Dahle, S. Calcareous Tubeworms (Polychaeta, Serpulidae) of the Arctic Ocean;
KMK Scientific Press: Moscow, Russia, 2014; pp. 1–187.
114. Rzhavsky, A.; Kupriyanova, E.; Sikorski, A. Field guide to Calcareous Tubeworms (Polychaeta, Serpulidae) of the Arctic Ocean; KMK
Scientific Press: Moscow, Russia, 2018; pp. 1–184.
115. Fauvel, P. Polychètes sédentaires. Addenda aux errantes, Arachiannélides, Myzostomaires. In Faune de France; Paul Lechevalier:
Paris, France, 1927; Volume 16, pp. 1–494.
Diversity 2021, 13, 130 61 of 74
116. Zibrowius, H. Étude morphologique, systématique et écologique des Serpulidae (Annelida Polychaeta) de La région de Mar-
seille. Recl. Trav. Stn. Mar. Endoume Bull. 1968, 43, 81–252.
117. Bianchi, C.N. Les espèces de Serpuloidea (Annélides, Polychaètes) des lagunes côtières Italiennes. Rapp. Commis. Int. Mer. Médit.
Monaco 1981, 27, 195–196.
118. Knight-Jones, P. Sabellidae and Serpulidae. In The Marine Fauna of the British Isles and North West Europe; Hayward, P.J., Ryland,
J.S., Eds.; Clarendon Press: Oxford, UK, 1990; Volume 1, pp. 271–287.
119. López, E.; Cepeda, D. Familia Fabriciidae Rioja, 1923. In Fauna Ibérica; Museo Nacional de Ciencias Naturales, Consejo Superior
de Investigaciones Científicas: Madrid, Spain, 2020; in press.
120. Cepeda, D.; López, E. Familia Sabellidae Latreille, 1825. In Fauna Ibérica; Museo Nacional de Ciencias Naturales, Consejo Supe-
rior de Investigaciones Científicas: Madrid, Spain, 2020; in press.
121. Bick, A. Redescription of Fabriciola tonerella Banse, 1959, and a new record of Novafabricia infratorquata (Fitzhugh, 1983) from the
Mediterranean Sea, with a key for the Fabriciinae (Annelida: Polychaeta) of the Mediterranean Sea and the North-East Atlantic.
Zool. Anz. J. Comp. Zool. 2005, 244, 137–152.
122. Bick, A.; Randel, N. Ontogenetic variations in characters of Euchone analis (Krøyer, 1856) (Polychaeta, Sabellidae, Sabellinae)
from Spitsbergen, and new assignments of Oriopsis ingelorae Plate, 1995 and O. liefdefjordensis Plate, 1995. Acta Zool. 2005, 86,
145–157.
123. Tovar-Hernández, M.A.; Licciano, M.; Giangrande, A. Revision of Chone Krøyer, 1856 (Polychaeta: Sabellidae) from the Eastern
Central Atlantic and Mediterranean Sea with descriptions of two new species. Sci. Mar. 2007, 71, 315–338, doi:10.3989/sci-
mar.2007.71n2315.
124. Tovar-Hernández, M.A. Revision of Chone Krøyer, 1856 (Polychaeta: Sabellidae) from North America and descriptions of four
new species. J. Nat. Hist. 2007, 41, 511–566, doi:10.1080/00222930701250912.
125. Çinar, M. Serpulid species (Polychaeta: Serpulidae) from the Levantine coast of Turkey (Eastern Mediterranean), with special
emphasis on alien species. Aquat. Invasions 2006, 1, 223–240, doi:10.3391/ai.2006.1.4.6.
126. Çinar, M.E. Alien polychaete species (Annelida: Polychaeta) on the Southern coast of Turkey (Levantine Sea, Eastern Mediter-
ranean), with 13 new records for the Mediterranean Sea. J. Nat. Hist. 2009, 43, 2283–2328.
127. Çinar, M.E.; Dağli, E.; Şahin, G.K. Checklist of Annelida from the coasts of Turkey. Turk. Zool. Derg. 2014, 38, 734–764.
128. Selim, S.A.; Rzhavsky, A.V.; Britayev, Т.А. Dialychone and Paradialychone (Polychaeta: Sabellidae) from the Mediterranean Coast
of Egypt with description of Dialychone egyptica sp. n. Invertebr. Zool. 2012, 9, 105–114, doi:10.15298/invertzool.09.2.03.
129. Giangrande, A.; Cosentino, A.; Presti, C.L.; Licciano, M. Sabellidae (Annelida) from the Faro coastal lake (Messina, Ionian Sea),
with the first record of the invasive species Branchiomma bairdi along the Italian Coast. Mediterr. Mar. Sci. 2012, 13, 283–293.
130. Giangrande, A.; Caruso, L.; Mikac, B.; Licciano, M. The genus Megalomma (Annelida: Sabellidae) in the Mediterranean Sea, with
description of two new species from Italian and Croatian Coasts. Ital. J. Zool. 2015, 82, 521–534.
131. Mikac, B.A. Sea of worms: Polychaete checklist of the Adriatic Sea. Zootaxa 2015, 3943, 1–172.
132. Mikac, B.; Licciano, M.; Jaklin, A.; Iveša, L.; Giangrande, A.; Musco, L. Diversity and distribution patterns of hard bottom pol-
ychaete assemblages in the North Adriatic Sea (Mediterranean). Diversity 2020, 12, 408.
133. Mikac, B.; Giangrande, A.; Licciano, M. Sabellidae and Fabriciidae (Polychaeta) of the Adriatic Sea with particular retrospect to
the Northern Adriatic and the description of two new species. J. Mar. Biol. Assoc. UK 2013, 93, 1511–1524.
134. López, E.; Cepeda, D. Catálogo de las especies de Sabellidae Latreille, 1825 y Fabriciidae Rioja, 1923 (Annelida; Sabellida) citadas
en la Península Ibérica e Islas Baleares y Chafarinas. Graellsia 2017, 73, e064, doi:10.3989/graellsia.2017.v73.184.
135. Kurt Şahin, G.; Çınar, M.E. A check-list of polychaete species (Annelida: Polychaeta) from the Black Sea. J. Black Sea/Medit.
Environ. 2012, 18, 10–48.
136. Hartman, O. Atlas of the Sedentariate Polychaetous Annelids from California; Allan Hancock Foundation, University of Southern
California: Los Angeles, CA, USA, 1969; pp. 1–812.
137. Knight-Jones, P.; Knight-Jones, E.W.; Dales, R.P. Spirorbidae (Polychaeta Sedentaria) from Alaska to Panama. J. Zool. 1979, 189,
419–458.
138. Buzhinskaja, G. Polychaetes of the Far East. Seas of Russia and Adjacent Waters of the Pacific Ocean.: Annotated Checklist and Bibliog-
raphy; KMK Scientific Press: Moscow, Russia, 2013; pp. 1–131.
139. Nishi, E.; Tanaka, K.; Tovar-Hernández, M.A.; Giangrande, A. Dialychone, Jasmineira and Paradialychone (Annelida: Polychaeta:
Sabellidae) from Japan and adjacent waters, including four new species descriptions. Zootaxa 2009, 2167, 1–24.
140. Yoshihara, T.; Hiruta, S.; Katoh, T.; Kajihara, H. Three species of Amphicorina (Annelida, Sabellida, Sabellidae) from Japan, with
descriptions of two new species. Zookeys 2012, 187, 45–62, doi:10.3897/zookeys.187.2662.
141. Imajima, M. Kankeidoubutsu Tamourui (Annelida Polychaeta); Biological Research Co.: Tokyo, Japan, 1996; pp. 1–530. (In Japanese)
142. Sun, R.; Yang, D. Polychaeta III. Sabellida. In Fauna Sinica: Invertebrata; Science Press: Beijing, China, 2014; 54, pp. 1–495.
143. Glasby, C.J.; Lee, Y.-L.; Hsueh, P.-W. Marine Annelida (excluding clitellates and siboglinids) from the South China Sea. Raffles
Bull. Zool. 2016, 34, 178–234.
144. Bastida-Zavala, J.R.; ten Hove, H.A. Revision of Hydroides Gunnerus, 1768 (Polychaeta: Serpulidae) from the Eastern Pacific
Region and Hawaii. Beaufortia 2003, 53, 67–110.
145. Bastida-Zavala, J.R. Serpulids (Annelida: Polychaeta) from the Eastern Pacific, including a brief mention of Hawaiian serpulids.
Zootaxa 2008, 1722, 1–61.
Diversity 2021, 13, 130 62 of 74
146. Bastida-Zavala, J.R.; McCann, L.D.; Keppel, E.; Ruiz, G.M. The fouling serpulids (Polychaeta: Serpulidae) from United States
coastal waters: An overview. Eur. J. Taxon. 2017, 344, 1–76, doi:10.5852/ejt.2017.344.
147. Tovar-Hernández, M.A.; Méndez, N.; Villalobos-Guerrero, T.F. Fouling polychaete worms from the Southern Gulf of California:
Sabellidae and Serpulidae. Syst. Biodivers 2009, 7, 319–336.
148. Bastida-Zavala, J.R.; Buelna, A.S.R.; De León-González, J.A.; Camacho-Cruz, K.A.; Carmona, I. New records of sabellids and
serpulids (Polychaeta: Sabellidae, Serpulidae) from the Tropical Eastern Pacific. Zootaxa 2016, 4184, 401–457.
149. Tovar-Hernández, M.A.; Carrera-Parra, L.F. Megalomma Johansson, 1925 (Polychaeta: Sabellidae) from America and other
world-wide localities, and phylogenetic relationships within the genus. Zootaxa 2011, 2861, 1–71, doi:10.11646/zootaxa.2861.1.1.
150. Zibrowius, H. Contribution a l’etude des Serpulidae (Polychaeta Sedentaria) du Bresil. Bol. Inst. Oceanogr. 1970, 19, 1–32.
151. ten Hove, H.A. Serpulinae (Polychaeta) from the Caribbean: I-the genus Spirobranchus. Stud. Fauna Curaçao 1970, 32, 1–57.
152. ten Hove, H.A. Serpulinae (Polychaeta) from the Caribbean: II-the genus Sclerostyla. Stud. Fauna Curaçao 1973, 43, 1–21.
153. ten Hove, H.A. Serpulinae (Polychaeta) from the Caribbean: III-the genus Pseudovermilia. Stud. Fauna Curaçao 1975, 47, 46–101.
154. ten Hove, H.A. Serpulinae (Polychaeta) from the Caribbean: IV Pseudovermilia madracicola sp. n., a symbiont of corals. In Natu-
urwetenschappelijke Studiekring voor Suriname en de Nederlandse Antillen; Van Der Steen, L.J., Ed.; 1989; Volume 123, pp. 135–144.
155. Giangrande, A.; Licciano, M.; Gambi, M.C. A collection of Sabellidae (Polychaeta) from Carrie Bow Cay (Belize, Western Car-
ibbean Sea) with the description of two new species. Zootaxa 2007, 1650, 41–53, doi:10.11646/zootaxa.1650.1.3.
156. Tovar-Hernández, M.A. Redescription of Chone americana Day, 1973 (Polychaeta: Sabellidae) and description of five new species
from the Grand Caribbean Region. Zootaxa 2005, 1070, 1–30, doi:10.11646/zootaxa.1070.1.1.
157. Tovar-Hernández, M.A.; Knight-Jones, P. Species of Branchiomma (Polychaeta: Sabellidae) from the Caribbean Sea and Pacific
Coast of Panama. Zootaxa 2006, 1189, 1–37, doi:10.11646/zootaxa.1189.1.1.
158. Tovar-Hernández, M.A.; Salazar-Vallejo, S.I. Sabellids (Polychaeta: Sabellidae) from the Grand Caribbean. Zool. Stud. 2006, 45,
24–66.
159. Bastida-Zavala, J.R.; ten Hove, H.A. Revision of Hydroides Gunnerus, 1768 (Polychaeta: Serpulidae) from the Western Atlantic
Region. Beaufortia 2002, 52, 103–173.
160. Bastida-Zavala, R. Serpula and Spiraserpula (Polychaeta, Serpulidae) from the Tropical Western Atlantic and Gulf of Guinea.
ZooKeys 2012, 198, 1–23.
161. Nogueira, J.; Knight-Jones, P.A. New species of Pseudobranchiomma Jones (Polychaeta: Sabellidae) found amongst Brazilian
coral, with a redescription of P. punctata (Treadwell, 1906) from Hawaii. J. Nat. Hist. 2002, 36, 1661–1670.
162. Nogueira, J.M.D.M.; Abbud, A. Three new serpulids (Polychaeta: Serpulidae) from the Brazilian Exclusive Economic Zone.
Zoosymposia 2009, 2, 201–227.
163. Amaral, A.C.Z.; Nallin, S.A.H.; Steiner, T.M.; Forroni, T. de O.; Gomes-Filho, D. Catálogo das Espécies de Annelida Polychaeta do
Brasil; Unicamp: Campinas, Brazil, 2013; pp. 1–159.
164. Costa, D. de A.; Fernandes, H.F.; da Silva, F. de A.; Christoffersen, M.L. Checklist de espécies de Polychaeta (Annelida) da Praia
do Seixas, João Pessoa, Estado Da Paraíba, Nordeste do Brasil. Rev. Bras. Gestão Amb. Sust. 2017, 4, 313–320.
165. Bastida-Zavala, J.R.; Sánchez Ovando, J.P. Serpulidae Rafinesque 1815. In Poliquetos (Annelida: Polychaeta) de México y América
Tropical, 2nd ed.; De León-González, J.A., Bastida-Zavala, J.R., Carrera-Parra, L.F., García-Garza, M.E., Salazar-Vallejo, S.I., So-
lís-Weiss, V., Tovar-Hernández, M.A., Eds.; Universidad Autónoma de Nuevo León: Monterrey, Mexico, 2021; Volume 3, in
press.
166. Fauvel, P. Annelida Polychaeta. In Fauna of India, Pakistan, Ceylon, Burma and Malaya; The Indian Press Ltd: Allahabad, India,
1953; pp. 1–507.
167. Sivadas, S.K.; Carvalho, R. Marine Annelida of India: Taxonomy and status evaluation and an updated checklist. J. Threat. Taxa
2020, 12, 16647–16714.
168. Pillai, G. Some marine and brackish-water serpulid polychaetes from Ceylon, including new genera and species. Ceylon J. Sci.
(Biol. Sci.) 1960, 3, 1–40.
169. Pillai, T.G. Annelida Polychaeta of Tambalagam Lake, Ceylon. Ceylon J. Sci. (Biol. Sci.) 1961, 4, 1–40.
170. Wehe, T.; Fiege, D. Annotated checklist of the polychaete species of the seas surrounding the Arabian Peninsula: Red Sea, Gulf
of Aden, Arabian Sea, Gulf of Oman, Arabian Gulf. Fauna Arabia 2002, 19, 7–238.
171. Al-Kandari, M.; Sattari, Z.; Hussain, S.; Radashevsky, V.I.; Zhadan, A. Checklist of intertidal Polychaetes (Annelida) of Kuwait,
Northern Part of the Arabian Gulf. Reg. Stud. Mar. Sci. 2019, 32, 100872.
172. Ben-Eliahu, M.N.; ten Hove, H.A. Serpulidae (Annelida: Polychaeta) from the Suez Canal—from a Lessepsian migration per-
spective (a monograph). Zootaxa 2011, 2848, 1–147, doi:10.11646/zootaxa.2848.1.1.
173. Knight-Jones, E.W.; Knight-Jones, P.; Oliver, P.G.; Mackie, A.S.Y. A new species of Hyalopomatus (Serpulidae: Polychaeta) which
lacks an operculum: Is this an adaptation to low oxygen? In Interactions and Adaptation Strategies of Marine Organisms; Naumov,
A.D., Hummel, H., Sukhotin, A.A., Ryland, J.S., Eds.; Springer: Dordrecht, The Netherlands, 1997; pp. 145–151.
174. Veron, J.E.; Devantier, L.M.; Turak, E.; Green, A.L.; Kininmonth, S.; Stafford-Smith, M.; Peterson, N. Delineating the Coral Tri-
angle. Galaxea 2009, 11, 91–100.
175. Fitzhugh, K. Fan worm polychaetes (Sabellidae: Sabellinae) collected during the Thai-Danish BIOSHELF Project. Phuket Mar.
Biol. Center Spec. Publ. 2002, 24, 353–424.
176. Al-Hakim, I.; Glasby, C.J. Polychaeta (Annelida) of the Natuna Islands, South China Sea. Raffles Bull. Zool. 2004, 21, 25–45.
177. Sun, Y.; ten Hove, H.A.; Qiu, J.W. Serpulidae (Annelida: Polychaeta) from Hong Kong. Zootaxa 2012, 3424, 1–42.
Diversity 2021, 13, 130 63 of 74
178. Murray, A.; Rouse, G.W. Two new species of Terebrasabella (Annelida: Sabellidae: Sabellinae) from Australia. Zootaxa 2007, 1434,
51–68.
179. Kupriyanova, E.K.; Sun, Y.; ten Hove, H.A.; Wong, E.; Rouse, G.W. Serpulidae (Annelida) of Lizard Island, Great Barrier Reef,
Australia. Zootaxa 2015, 4019, 275–353.
180. Sun, Y.; Wong, E.; ten Hove, H.A.; Hutchings, P.A.; Williamson, J.E.; Kupriyanova, E.K. Revision of the genus Hydroides (An-
nelida: Serpulidae) from Australia. Zootaxa 2015, 4009, 1–99.
181. Wilson, R.S.; Hutchings, P.A.; Glasby, C.J. Polychaetes: An. Interactive Identification Guide; CSIRO Publishing: Collingwood, VIC,
Australia, 2003; pp. 1–24.
182. Kupriyanova, E.K.; Wong, E.; Hutchings, P.A. Invasive Polychaete Identifier–an Australian Perspective. Version 1.1 2013. Avail-
able online http://polychaetes.australianmuseum.net.au/ (accessed on 3 March 2021).
183. Kupriyanova, E.; Hutchings, P.; Wong, E. A fully illustrated web-based guide to distinguish native and introduced polychaetes
of Australia. Manag. Biol. Invasions 2016, 7, 305–312, doi:10.3391/mbi.2016.7.3.10.
184. Bailey-Brock, J.H.; Magalhães, W.F. A new species and record of Serpulidae (Annelida: Polychaeta) from Cross Seamount in
the Hawaiian Chain. Zootaxa 2012, 3192, 49–58.
185. Keppel, E.; Tovar-Hernández, M.A.; Ruiz, G. New records of the non-indigenous species Branchiomma bairdi and B. conspersum
(Polychaeta: Sabellidae) on the Pacific Coast of North America. Bioinvasions Rec. 2018, 7, 229–236, doi:10.3391/bir.2018.7.3.03.
186. Bailey-Brock, J.H.; Magalhães, W.F.; Brock, R.E. Coral reef inhabiting tubeworms (Polychaeta: Serpulidae) from Enewetak, Kwa-
jalein, Rongelap and Utirik Atolls, Marshall Islands. J. Mar. Biol. Assoc. UK 2012, 92, 967–988.
187. Capa, M.; López, E. Sabellidae (Annelida: Polychaeta) living in blocks of dead coral in the Coiba National Park, Panama. J. Mar.
Biol. Assoc. UK 2004, 84, 63–72.
188. Yáñez-Rivera, B.; Tovar-Hernández, M.A.; Galván-Villa, C.M.; Ríos-Jara, E. Tubicolous polychaete worms (Annelida) from Ba-
hía de Chamela Islands Sanctuary, Mexico, with the description of a new bamboo worm. Biodivers. Data J. 2020, 8, e57572,
doi:10.3897/BDJ.8.e57572.
189. Keppel, E.; Keith, I.; Ruiz, G.M.; Carlton, J.T. New records of native and non-indigenous Polychaetes (Annelida: Polychaeta) in
the Galapagos Islands. Aquat. Invasions 2019, 14, 59–84.
190. Elías, R.; Jaubet, M.L.; Ferrando, A.; Saracho, M. Historia y perspectivas de los estudios sobre poliquetos en Argentina. In Poli-
quetos de Sudamérica; Díaz-Díaz, O., Bone, D., Rodríguez, C.T., Delgado-Blas, V.H., Eds.; Poliquetos de Sudamérica. Volumen
especial del Boletín del Instituto Oceanográfico de Venezuela: Cumaná, Venezuela, 2017; pp. 3–23.
191. Rozbaczylo, O.: Moreno, R.A.; Díaz-Díaz, Ó. Poliquetos Bentónicos en Chile. In Poliquetos de Sudamérica; Díaz-Díaz, O., Bone,
D., Rodríguez, C.T., Delgado-Blas, V.H., Eds.; Poliquetos de Sudamérica. Volumen especial del Boletín del Instituto Oceanográ-
fico de Venezuela: Cumaná, Venezuela, 2017; pp. 51–70.
192. Kupriyanova, E.K.; ten Hove, H.A.; Nishi, E.A. Taxonomic revision of Pseudochitinopoma Zibrowius, 1969 (Annelida, Serpulidae)
with description of two new species. Zootaxa 2012, 3507, 57–78, doi:10.11646/zootaxa.3507.1.3.
193. Simon, C.A.; van Niekerk, H.H.; Burghardt, I.; ten Hove, H.A.; Kupriyanova, E.K. Not out of Africa: Spirobranchus kraussii (Baird,
1865) is not a global fouling and invasive serpulid of Indo-Pacific Origin. Aquat. Invasions 2019, 14, 221–249.
194. Day, J.H. A Monograph on the Polychaeta of Southern Africa. Part II. Brit. Mus. Nat. Hist. Publ. 1967, 656, 459–878.
195. Knight-Jones, P. New species and a new subgenus of Spirorbinae (Serpulidae: Polychaeta) from Kenya. J. Zool. 1972, 166, 1–18.
196. Knight-Jones, P.; Knight-Jones, E.W. Spirorbinae (Polychaeta: Serpulidae) from South Africa, including three new species. Mar.
Biol. 1974, 25, 253–261.
197. Knight-Jones, E.W.; Knight-Jones, P.; Llewellyn, L.C. Spirorbinae (Polychaeta: Serpulidae) from Southeastern Australia. Notes
on their taxonomy, ecology and distribution. Rec. Aust. Mus. 1974, 29, 107–151.
198. Vine, P.J. The marine fauna of New Zealand. Spirorbinae (Polychaeta: Serpulidae). NZOI Mem. 1977, 68, 1–66.
199. Glasby, C.J.; Read, G.B. A chronological review of polychaete taxonomy in New Zealand. J. R. Soc. N. Z. 1998, 28, 347–374.
200. Capa, M.; Rouse, G.W. Phylogenetic relationships within Amphiglena Claparède, 1864 (Polychaeta: Sabellidae), description of
five new species from Australia, a new species from Japan, and comments on previously described species. J. Nat. Hist. 2007,
41, 327–356, doi:10.1080/00222930701194938.
201. Capa, M.; Murray, A. Review of the genus Megalomma (Polychaeta: Sabellidae) in Australia with description of three new spe-
cies, new records and notes on certain features with phylogenetic implications. Rec. Aust. Mus. 2009, 61, 201–224.
202. Murray, A.; Keable, S.J. First report of Sabella spallanzanii (Gmelin, 1791) (Annelida: Polychaeta) from Botany Bay, New South
Wales, a northern range extension for the invasive species within Australia. Zootaxa 2013, 3670, 391–395.
203. Sun, Y.; Wong, E.; Tovar-Hernández, M.A.; Williamson, J.E.; Kupriyanova, E.K. Is Hydroides brachyacantha (Serpulidae: An-
nelida) a widespread species? Invertebr. Syst. 2016, 30, 41–59, doi:10.1071/IS15015.
204. Styan, C.; McCluskey, C.; Sun, Y.; Kupriyanova, E. Cryptic sympatric species across the Australian range of the global estuarine
invader Ficopomatus enigmaticus (Fauvel, 1923) (Serpulidae, Annelida). Aquat. Invasions 2017, 12, 53–65,
doi:10.3391/ai.2017.12.1.06.
205. Baird, W. Description of a new species of annelids belonging to the Family Amphinomidae. Trans. Linn. Soc. London 1864, 24,
449–450.
206. Baird, W. Description of several new species and varieties of tubicolous annelids (= Tribe Limivora of Grube), in the collection
of the British Museum. J. Linn. Soc. Zool. 1865, 8, 10–22.
Diversity 2021, 13, 130 64 of 74
207. Ehlers, E. Polychaeten der Hamburger Magalhaenischen Sammelreise. Ergeb. Hambg. Magalhaenischen Sammelreise Liefersung
1897, 2, 1–147.
208. Gravier, C. Sur les Annélides Polychètes Recueillies par l’Expédition Antarctique Française (Terebelliens, Serpuliens). Bull. Mus.
d’Hist. Nat. Paris 1907, 13, 46–52.
209. Pixell, H.L.M. Polychaeta of the Families Serpulidae and Sabellidae, collected by the Scottish National Antarctic Expedition.
Trans. R. Soc. Edinburgh 1913, 49, 347–358.
210. Benham, W.B. Polychaeta. British Antarctic “Terra Nova” Expedition, 1910. Nat. Hist. Rep. Zool. 1927, 7, 47–182.
211. Rzhavsky, A.V. Two new species of Pileolaria (Polychaeta: Spirorbidae) from the Southern hemisphere with a brief review of
related species. Inverterb. Zool. 2010, 7, 81–91.
212. Tovar-Hernández, M.A.; Yáñez-Rivera, B.; Giangrande, A.; Gambi, M.C. Notes on the species of Perkinsiana (Polychaeta: Sabel-
lidae) from Antarctica with the description of P. brigittae sp. nov. Zootaxa 2012, 3485, 56–68.
213. Neal, L.; Paterson, G.L.; Blockley, D.; Scott, B.; Sherlock, E.; Huque, C.; Glover, A.G. Biodiversity data and new species descrip-
tions of polychaetes from offshore waters of the Falkland Islands, an area undergoing hydrocarbon exploration. ZooKeys 2020,
938, 1–86.
214. Kupriyanova, E.K.; Rzhavsky, A.; ten Hove, H.A. Serpulidae Rafinesque, 1815. In Handbook of Zoology, Annelida, Volume 2: Pleis-
toannelida, Sedentaria II; Purschke, G., Böggemann, M., Westheide, W., Eds.; De Gruyter: Berlin, Germany, 2019; pp. 213–275.
215. Jones, M.L. Brandtika asiatica new genus, new species, from Southeastern Asia and a redescription of Monroika africana (Monro)
(Polychaeta: Sabellidae). Proc. Biol. Soc. Wash. 1974, 87, 217–230.
216. Atkinson, S.D.; Bartholomew, J.L.; Rouse, G.W. The invertebrate host of salmonid fish parasites Ceratonova shasta and Parvicap-
sula minibicornis (Cnidaria: Myxozoa), is a novel fabriciid annelid, Manayunkia occidentalis sp. nov. (Sabellida: Fabriciidae).
Zootaxa 2020, 4751, 310–320.
217. Sitnikova, T.Y.; Shcherbakov, D.Y.; Kharchenko, V.V. On taxonomic status of polychaetes of the genus Manayunkia (Sabellidae,
Fabriciinae) from the open Lake Baikal. Zool. Zhurnal 1997, 76, 16–27.
218. Monro, C.C.A. On a collection of Polychaeta from near the Mouth of the River Congo. Rev. Zool. Bot. Afr. 1939, 32, 213–225.
219. Rouse, G. New Fabriciola and Manayunkia species (Fabriciinae: Sabellidae: Polychaeta) from Papua New Guinea. J. Nat. Hist.
1996, 30, 1761–1778.
220. Baumhaker, H Taxonomische Untersuchungen an Sabellidae und Fabriciidae (Annelida: Polychaeta) der Tiefsee des Südwest-
Atlantiks. Master’s Thesis, University of Rostock, Rostock, Germany, 2012.
221. Bok, M.J.; Capa, M.; Nilsson, D.-E. Here, there and everywhere: The radiolar eyes of fan worms (Annelida, Sabellidae). Integr.
Comp. Biol. 2016, 56, 784–795, doi:10.1093/icb/icw089.
222. Brown, S.D.; Emlet, R.B. Natural radiole damage and regeneration in the feather duster worm Schizobranchia insignis. Invertebr.
Biol. 2020, e12307, doi:10.1111/ivb.12307.
223. Orrhage, L. On the structure and homologues of the anterior end of the polychaete families Sabellidae and Serpulidae. Zoomor-
phology 1980, 96, 113–167.
224. Giangrande, A. The genus Chone (Polychaeta, Sabellidae) in the Mediterranean Sea with description of C. longiseta n. sp. Boll.
Zool. 1992, 59, 517–529.
225. Tovar-Hernández, M.A.; Sosa-Rodríguez, T. Redescription of Chone infundibuliformis Krøyer, 1856 (Polychaeta: Sabellidae) and
histology of the branchial crown appendages, collar and glandular ridge. Zootaxa 2006, 1115, 31–59,
doi:10.11646/zootaxa.1115.1.2.
226. Capa, M.; Nogueira, J.M. de M.; Rossi, M.C.S. Comparative internal structure of dorsal lips and radiolar appendages in Sabel-
lidae (Polychaeta) and phylogenetic implications. J. Morphol. 2011, 272, 302–319, doi:10.1002/jmor.10914.
227. Ippolitov, A.P.; Vinn, O.; Kupriyanova, E.K.; Jäger, M. Written in stone: History of serpulid polychaetes through time. Mem.
Mus. Vic. 2014, 71, 123–160.
228. Wong, E.; Kupriyanova, E.K.; Hutchings, P.; Capa, M.; Radashevsky, V.I.; ten Hove, H.A. A graphically illustrated glossary of
polychaete terminology: Invasive species of Sabellidae, Serpulidae and Spionidae. Mem. Mus. Vic. 2014, 71, 327–342,
doi:10.24199/j.mmv.2014.71.25.
229. Handley, S.J. Spionid polychaetes in Pacific oysters, Crassostrea gigas (Thunberg) from Admiralty Bay, Marlborough Sounds,
New Zealand. N. Z. J. Mar. Freshw. Res. 1995, 29, 305–309, doi:10.1080/00288330.1995.9516665.
230. Bick, A. Morphology and ecology of Dipolydora armata (Polychaeta, Spionidae) from the Western Mediterranean Sea. Acta Zool.
2001, 11, 177–187.
231. Bick, A. Polychaete communities associated with gastropod shells inhabited by the hermit crabs Clibanarius erythropus and Cal-
cinus tubularis from Ibiza, Mediterranean Sea. J. Mar. Biol. Assoc. UK 2006, 86, 83–92, doi:10.1017/S0025315406012884.
232. Rouse, G.W.; Pleijel, F. Polychaetes; Oxford University Press: London, UK, 2001; pp. 1–354.
233. Bick, A. Bedeutung Postlarvaler Ontogenetischer Merkmalsvariationen für die Taxonomie der Spionidae und Sabellidae; Habilita-
tionsschrift an der Mathematisch-Naturwissenschaftliche Fakultät Fakultät der Universität Rostock: Rostock, Germany, 2007.
234. Costa-Paiva, E.M.; Paiva, P.C. Anaesthetization and fixation effects on the morphology of sabellid polychaetes (Annelida: Pol-
ychaeta: Sabellidae). J. Mar. Biol. Assoc. UK 2007, 87, 1127– 1132.
235. Coleman, C.O. “Digital inking”: How to make perfect line drawings on computers. Org. Div. Evol. Electr. Suppl. 2003. 14, 1–14.
Diversity 2021, 13, 130 65 of 74
236. Paterson, G.L.; Sykes, D.; Faulwetter, S.; Merk, R.; Ahmed, F.; Hawkins, L.E.; Dinley, J.; Ball, A.D.; Arvanitidis, C. The pros and
cons of using micro-computed tomography in gross and micro-anatomical assessments of polychaetous annelids. Mem. Mus.
Vic. 2014, 71, 237–246.
237. Parapar, J.; Candás, M.; Cunha-Veira, X.; Moreira, J. Exploring annelid anatomy using micro-computed tomography: A taxo-
nomic approach. Zool. Anz. 2017, 270, 19–42.
238. Patti, F.P.; Gambi, M.C.; Giangrande, A. Preliminary study on the systematic relationships of Sabellinae (Polychaeta, Sabelli-
dae), based on the C1 domain of the 28S rDNA, with discussion of reproductive features. Ital. J. Zool. 2003, 70, 269–278.
239. Halanych, K.M. A review of molecular markers used for annelid phylogenetics. Integr. Comp. Biol. 2006, 46, 533–543,
doi:10.1093/icb/icj052.
240. Carr, C.M.; Hardy, S.M.; Brown, T.M.; Macdonald, T.A.; Hebert, P.D.N. A Tri-Oceanic perspective: DNA barcoding reveals
geographic structure and cryptic diversity in Canadian polychaetes. PLoS ONE 2011, 6, e22232, doi:10.1371/jour-
nal.pone.0022232.
241. Seixas, V.C.; de Moraes Russo, C.A.; Paiva, P.C. Mitochondrial genome of the Christmas Tree Worm Spirobranchus giganteus
(Annelida: Serpulidae) reveals a high substitution rate among annelids. Gene 2017, 605, 43–53.
242. Sun, Y.; Daffe, G.; Zhang, Y.; Qiu, J.-W.; Kupriyanova, E.K. Another blow to the conserved gene order in Annelida: Mitoge-
nomics reveals extensive gene rearrangement in the tubeworm genus Hydroides (Serpulidae). Mol. Phylogenet. Evol. 2021, 107124.
243. Tilic, E.; Atkinson, S.D.; Rouse, G.W. Mitochondrial genome of the freshwater annelid Manayunkia occidentalis (Sabellida: Fab-
riciidae). Mitochondrial DNA B 2020, 5, 3313–3315.
244. Daffe, G.; Sun, Y.; Ahyong, S.T.; Kupriyanova, E.K. Mitochondrial genome of Sabella spallanzanii (Sabellida: Sabellidae). Mito-
chondrial DNA B 2020, 6, 499–501.
245. Takahashi, T.; McDougall, C.; Troscianko, J.; Chen, W.-C.; Jayaraman-Nagarajan, A.; Shimeld, S.M.; Ferrier, D.E. An EST screen
from the annelid Pomatoceros lamarckii reveals patterns of gene loss and gain in animals. BMC Evol. Biol. 2009, 9, 1–17.
246. De Queiroz, K. Species concepts and species delimitation. Syst. Biol. 2007, 56, 879–886, doi:10.1080/10635150701701083.
247. Barraclough, T.G. Evolving entities: Towards a unified framework for understanding diversity at the species and higher levels.
Phil. Trans. R. Soc. B Biol. Sci. 2010, 365, 1801–1813.
248. Nygren, A. Cryptic polychaete diversity: A review. Zool. Scr. 2014, 43, 172–183.
249. Halt, M.N.; Kupriyanova, E.K.; Cooper, S.J.B.; Rouse, G.W. Naming species with no morphological indicators: Species status of
Galeolaria caespitosa (Annelida: Serpulidae) inferred from nuclear and mitochondrial gene sequences and morphology. Invertebr.
Syst. 2009, 23, 205–222, doi:10.1071/IS09003.
250. Sun, Y.; Wong, E.; Keppel, E.; Williamson, J.E.; Kupriyanova, E.K. A global invader or a complex of regionally distributed
species? clarifying the status of an invasive calcareous tubeworm Hydroides dianthus (Verrill, 1873) (Polychaeta: Serpulidae)
Using DNA Barcoding. Mar. Biol. 2017, 164, 28–1–28-12, doi:10.1007/s00227-016-3058-9.
251. Sun, Y.; Al-Kandari, M.; Kubal, P.; Walmiki, N.; Kupriyanova, E.K. Cutting a Gordian knot of tubeworms with DNA data: The
story of the Hydroides operculata-complex (Annelida, Serpulidae). Zootaxa 2017, 4323, 39–48, doi:10.11646/zootaxa.4323.1.3.
252. Palero, F.; Torrado, H.; Perry, O.; Kupriyanova, E.K.; Ulman, A.; Genis-Armero, R.; ten Hove, H.A..; Capaccioni-Azzati, R. Fol-
lowing the Phoenician example: Western Mediterranean colonization by Spirobranchus cf. tetraceros (Annelida: Serpulidae). Sci.
Mar. 2020, 84, 83–92.
253. Hebert, P.D.; Ratnasingham, S.; De Waard, J.R. Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among
closely related species. Proc. R. Soc. London Biol. Sci. 2003, 270, S96–S99.
254. Rech, S.; Borrell Pichs, Y.J.; García-Vazquez, E. Anthropogenic marine litter composition in coastal areas may be a predictor of
potentially invasive rafting fauna. PLoS ONE 2018, 13, e0191859.
255. Langeneck, J.; Lezzi, M.; Del Pasqua, M.; Musco, L.; Gambi, M.C.; Castelli, A.; Giangrande, A. Non-indigenous polychaetes
along the coasts of Italy: A critical review. Mediterr. Mar. Sci. 2020, 21, 238–275.
256. Rech, S.; Salmina, S.; Pichs, Y.J.B.; García-Vazquez, E. Dispersal of alien invasive species on anthropogenic litter from European
mariculture areas. Mar. Poll. Bull. 2018, 131, 10–16.
257. Hutchings, P.; De Decker, P.; Geddes, M.C. A new species of Manayunkia (Polychaeta) from ephemeral lakes near the Coorong,
South Australia. Trans. R. Soc. S. Aust. 1981, 105, 25–28.
258. Schütz, L. Über Verbreitung, Ökologie und Biologie des Brackwasserpolychaeten Manayunkia aestuarina (Bourne) Insbesondere
an den Küsten Schleswig-Holsteins. Faun. Mitt. Norddeut. 1965, 9, 226–234.
259. Lewis, D.B. Some aspects of the ecology of Fabricia sabella (Ehr.) (Annelida, Polychaeta). J. Linn. Soc. (Zool.) 1968, 47, 515–526.
260. Light, W.J. Extension of range for Manayunkia aestuarina (Polychaeta: Sabellidae) to British Columbia. J. Fish. Board Canada 1969,
26, 3088–3091.
261. Bagheri, E.; McLusky, D. Population dynamics of oligochaetes and small polychaetes in the polluted forth estuary ecosystem.
Neth. J. Sea Res. 1982, 16, 55–66.
262. Bick, A. Reproduction and larval development of Manayunkia aestuarina (Bourne, 1883) (Polychaeta, Sabellidae) in a coastal
region of the Southern Baltic. Helgoländer Meeresunters 1996, 50, 287–298.
263. Giangrande, A.; Gambi, M.; Micheli, F.; Kroeker, K. Fabriciidae (Annelida, Sabellida) from a naturally acidified coastal system
(Italy) with description of two new species. J. Mar. Biol. Assoc. UK 2014, 94, 1417.
264. Muus, B.J. The Fauna of Danish estuaries and lagoons: Distribution and ecology of dominating species in the shallow reaches
of the mesohaline zone. Medd. Danmarks Fisk. Havunders (n. ser.) 1967, 5, 1–316.
Diversity 2021, 13, 130 66 of 74
265. Lewis, D.B. Feeding and tube-building in the Fabriciinae (Annelida, Polychaeta). Proc. Linn. Soc. Lond. 1968, 179, 37–49.
266. Hartman, O. Fabricinae (Featherduster Polychaetous Annelids) in the Pacific. Pac. Sci. 1951, 5, 379–391.
267. Bartholomew, J.L.; Atkinson, S.D.; Hallett, S.L. Involvement of Manayunkia speciosa (Annelida: Polychaeta: Sabellidae) in the life
cycle of Parvicapsula minibicornis, a myxozoan parasite of Pacific salmon. J. Parasitol. 2006, 92, 742–748.
268. Alexander, J.D.; Hallett, S.L.; Stocking, R.W.; Xue, L.; Bartholomew, J.L. Host and parasite populations after a ten-year flood:
Manayunkia speciosa and Ceratonova (Syn Ceratomyxa) shasta in the Klamath River. Northwest. Sci. 2014, 88, 219–233.
269. Giangrande, A.; Gambi, M.C. The genus Perkinsiana (Polychaeta, Sabellidae) from Antarctica, with descriptions of the new spe-
cies P. milae and P. borsibrunoi. Zool. Scr. 1997, 26, 267–278.
270. Murray, J.; Watson, G.; Giangrande, A.; Licciano, M.; Bentley, M. Regeneration as a novel method to culture marine ornamental
sabellids. Aquaculture 2013, 410, 129–137.
271. Chughtai, I.; Knight-Jones, W.E. Burrowing into limestone by sabellid polychaetes. Zool. Scr. 1988, 17, 231–238.
272. Fonseca, E.A.; Dean, H.K.; Cortés, J. Non-colonial coral macro-borers as indicators of coral reef status in the South Pacific of
Costa Rica. Rev. Biol. Trop. 2006, 54, 101–115.
273. Licciano, M.; Stabili, L.; Giangrande, A. Clearance rates of Sabella spallanzanii and Branchiomma luctuosum (Annelida: Polychaeta)
on a pure culture of Vibrio alginolyticus. Water Res. 2005, 39, 4375–4384.
274. Licciano, M.; Terlizzi, A.; Giangrande, A.; Cavallo, R.A.; Stabili, L. Filter-feeder macroinvertebrates as key players in culturable
bacteria biodiversity control: A case of study with Sabella spallanzanii (Polychaeta: Sabellidae). Mar. Environ. Res. 2007, 64, 504–
513.
275. Stabili, L.; Schirosi, R.; Licciano, M.; Giangrande, A. The mucus of Sabella spallanzanii (Annelida, Polychaeta): Its involvement in
chemical defense and fertilization success. J. Exp. Mar. Biol. Ecol. 2009, 374, 144–149.
276. Giangrande, A.; Pierri, C.; Arduini, D.; Borghese, J.; Licciano, M.; Trani, R.; Corriero, G.; Basile, G.; Cecere, E.; Petrocelli, A. An
innovative IMTA System: Polychaetes, sponges and macroalgae co-cultured in a southern Italian in-shore mariculture plant
(Ionian Sea). J. Mar. Sci. Eng. 2020, 8, 733, 1–24.
277. Selim, S.A. New records of sabellid species (Polychaeta: Sabellinae) from the coastal Egyptian waters. Egypt J. Aquat. Res. 2008,
34, 108–128.
278. Giangrande, A.; Caruso, L.; Musco, L.; Licciano, M. Variability among Mediterranean populations of Sabella pavonina (Annelida:
Sabellidae). Ital. J. Zool. 2014, 81, 100–111.
279. Magalhães, W.F.; Bailey-Brock, J.H.; Tovar-Hernández, M.A. An abundant new genus and species of fan worms (Polychaeta:
Sabellidae) from Hawaii. Zootaxa 2020, 4763, 85–98.
280. Capa, M.; Nishi, E.; Tanaka, K.; Fujikura, K. First record of a Bispira species (Sabellidae: Polychaeta) from a hydrothermal vent.
Mar. Biodivers. Rec. 2013, 6, e68, doi:10.1017/S1755267213000468.
281. Amon, D.J.; Glover, A.G.; Wiklund, H.; Marsh, L.; Linse, K.; Rogers, A.D.; Copley, J.T. The discovery of a natural whale fall in
the Antarctic deep sea. Deep Sea Res. Part. II Top. Stud. Ocean. 2013, 92, 87–96.
282. Cordes, E.E.; Carney, S.L.; Hourdez, S.; Carney, R.S.; Brooks, J.M.; Fisher, C.R. Cold seeps of the deep Gulf of Mexico: Commu-
nity structure and biogeographic comparisons to Atlantic Equatorial belt seep communities. Deep Sea Res. Part. I Ocean. Res. Pap.
2007, 54, 637–653.
283. Sellanes, J.; Quiroga, E.; Neira, C. Megafauna community structure and trophic relationships at the recently discovered Con-
cepción methane seep area, Chile,∼ 36° S. ICES . Mar. Sci. 2008, 65, 1102–1111.
284. Goffredi, S.K.; Tilic, E.; Mullin, S.W.; Dawson, K.S.; Keller, A.; Lee, R.W.; Wu, F.; Levin, L.A.; Rouse, G.W.; Cordes, E.E. Metha-
notrophic bacterial symbionts fuel dense populations of deep-sea feather duster worms (Sabellida, Annelida) and extend the
spatial influence of methane seepage. Sci. Adv. 2020, 6, eaay8562.
285. Hutchings, P.; Murray, A. Taxonomy of the polychaetes from the Hawkesbury River and the Southern estuaries of New South
Wales, Australia. Rec. Aust. Mus. 1984, 36, 1–119.
286. Lardicci, C.; Castelli, A. Desdemona ornata Banse, 1957 (Polychaeta, Sabellidae, Fabricinae) New record in the Mediterranean Sea.
Oebalia 1986, 13, 195–201.
287. Castelli, A.; Galletti, C.; Lardicci, C. Structure of benthic communities of brackish-water microhabitats: Spatial and temporal
variations. MAP Tech. Rep. Ser. (UNEP) 1988, 22, 19–46.
288. Panagopoulos, D.; Nicolaidou, A. A population of Desdemona ornata Banse, 1957 (Polychaeta, Sabellidae) settled in a fully marine
habitat of the Mediterranean. Oebalia 1989, 16, 35–39.
289. Glasby, C.J.; Timm, T.; Muir, A.I.; Gil, J. Catalogue of non-marine Polychaeta (Annelida) of the World. Zootaxa 2009, 2070, 1–52.
290. Hossain, M.B.; Marshall, D.J. Benthic infaunal community structuring in an acidified tropical estuarine system. Aquat. Biosyst.
2014, 10, 1–12.
291. Hernández-Alcántara, P.; Cortés-Solano, J.D.; Medina-Cantú, N.M.; Avilés-Díaz, A.L.; Solís-Weiss, V. Polychaete diversity in
the estuarine habitats of Términos lagoon, Southern Gulf of Mexico. Mem. Mus. Vic. 2014, 71, 97–107.
292. Hsieh, H.L. Laonome albicingillum, a new fan worm species (Polychaeta, Sabellidae, Sabellinae) from Taiwan. Proc. Biol. Soc.
Wash. 1995, 108, 130–135.
293. Hsieh, H.L. Self-fertilization-a potential fertilization mode in an estuarine sabellid polychaete. Mar. Ecol. Prog. Ser. 1997, 147,
143–148.
294. Capa, M.; van Moorsel, G.; Tempelman, D. The Australian feather-duster worm Laonome calida Capa, 2007 (Annelida: Sabellidae)
introduced into European inland waters? Bioinvasions Rec. 2014, 3, 1–11, doi:10.3391/bir.2014.3.1.01.
Diversity 2021, 13, 130 67 of 74
295. Bonar, D.B. Feeding and tube construction in Chone mollis Bush (Polychaeta, Sabellidae). J. Exp. Mar. Biol. Ecol. 1972, 9, 1–18,
doi:10.1016/0022-0981(72)90002-0.
296. Fitzsimons, G. Feeding and tube building in Sabellastarte magnifica (Shaw) (Sabellidae: Polychaeta). Bull. Mar. Sci. 1965, 15, 642–
671.
297. Licciano, M.; Murray, J.M.; Watson, G.J.; Giangrande, A. Morphological comparison of the regeneration process in Sabella spal-
lanzanii and Branchiomma luctuosum (Annelida, Sabellida). Invertebr. Biol. 2012, 131, 40–51.
298. Jumars, P.A.; Dorgan, K.M.; Lindsay, S.M. Diet of worms emended: An update of polychaete feeding guilds. Ann. Rev. Mar. Sci
2015, 7, 497–520, doi:10.1146/annurev-marine-010814-020007.
299. Jones, M.L. On the Caobangiidae, a new family of the Polychaeta, with a redescription of Caobangia billeti Giard. Smithson. Contr.
Zool. 1974, 1–55, doi:10.5479/si.00810282.175.
300. Kuris, A.M.; Culver, C.S. An introduced sabellid polychaete pest infesting cultured abalones and its potential spread to other
California gastropods. Invertebr. Biol. 1999, 118, 391–403.
301. Ruck, K.R.; Cook, P.A. Sabellid infestations in the shells of South African molluscs: Implications for abalone mariculture. J.
Shellfish Res. 1998, 17, 693–699.
302. Kupriyanova, E.K.; Badyaev, A.V. Ecological correlates of Arctic Serpulidae (Annelida, Polychaeta) distributions. Ophelia 1998,
49, 181–193.
303. Kupriyanova, E.K.; Nishi, E.; ten Hove, H.A.; Rzhavsky, A.V. A review of life history patterns in serpulimorph polychaetes:
Ecological and evolutionary perspectives. Ocean. Mar. Biol. Ann. Rev. 2001, 39, 1–101.
304. Charles, F.; Jordana, E.; Amouroux, J.-M.; Gremare, A.; Desmalades, M.; Zudaire, L. Reproduction, recruitment and larval met-
amorphosis in the serpulid polychaete Ditrupa arietina (O.F. Muller). Estuar. Coast. Shelf Sci. 2003, 57, 435–443.
305. Goffredi, S.K.; Johnson, S.; Tunnicliffe, V.; Caress, D.; Clague, D.; Escobar, E.; Paduan, J.B.; Rouse, G.; Salcedo, D.L.; Soto, L.A.;
et al. Hydrothermal vent fields discovered in the Southern Gulf of California clarify role of habitat in augmenting regional
diversity. Proc. R. Soc. B Biol. Sci. 2017, 284, 20170817, doi:10.1098/rspb.2017.0817.
306. Kupriyanova, E.K.; Nishi, E.; Kawato, M.; Fujiwara, Y. New records of Serpulidae (Annelida, Polychaeta) from hydrothermal
vents of North Fiji, Pacific Ocean. Zootaxa 2010, 2389, 57–68, doi:10.11646/zootaxa.2389.1.3.
307. Vinn, O.; Kupriyanova, E.K.; Kiel, S. Systematics of serpulid tubeworms (Annelida, Polychaeta) from Cretaceous and Cenozoic
hydrocarbon-seep deposits in North America and Europe. Neues Jahrb. Geol. Paläontol. 2012, 265, 315–325.
308. Juniper, S.K.; Sibuet, M. Cold seep benthic communities in Japan subduction zones: Spatial organisation, trophic strategies and
evidence for temporal evolution. Mar. Ecol. Prog. Ser. 1987, 40, 115–126.
309. Olu, K.; Duperret, A.; Sibuet, M.; Foucher, J.-P.; Fiala-Médioni, A. Structure and distribution of cold seep communities along
the Peruvian Active Margin: Relationship to geological and fluid patterns. Mar. Ecol. Progr. Ser. 1996, 132, 109–125.
310. Segonzac, M.; Hekinian, R.; Auzende, J.; Francheteau, J. Recently discovered animal communities on the South East Pacific Rise
(17-19 S and the Eastern Microplaque Region). Cah. Biol. Mar. 1997, 38, 140–141.
311. López-González, P.; Rodríguez, E.; Gili, J.-M.; Segonzac, M. New records on sea anemones (Anthozoa: Actiniaria) from hydro-
thermal vents and cold seeps. Zool. Verh. 2003, 345, 215–243.
312. Sibuet, M.; Olu, K. Biogeography, biodiversity and fluid dependence of deep-sea cold-seep communities at active and passive
margins. Deep Sea Res. Part. II Top. Stud. Ocean. 1998, 45, 517–567.
313. Mak, P.; Huang, Z. The salinity tolerance of the serpulid polychaete, Hydroides elegans (Haswell, 1883), and its possible applica-
tions in bio-antifouling. The marine flora and fauna of Hong Kong and Southern China. Ecol. Morph. Behav. Phys. 1982, 1, 817–
823.
314. Knight-Jones, P. Behaviour, setal inversion and phylogeny of Sabellida (Polychaeta). Zool. Scr. 1981, 10, 183–202.
315. Dill, L.M.; Fraser, A.H.G. The worm re-turns: Hiding behavior of a tube-dwelling marine polychaete, Serpula vermicularis. Behav.
Ecol. 1997, 8, 186–193.
316. Pan, J.; Marcoval, M.A. Top-down effects of an exotic serpulid polychaete on natural plankton assemblage of estuarine and
brackish systems in the SW Atlantic. J. Coast. Res. 2014, 30, 1226–1235.
317. Jordana, E.; Charles, F.; Gremare, A.; Amouroux, J.-M.; Chretiennot-Dinet, M.-J. Food sources, ingestion and absorption in the
suspension-feeding polychaete, Ditrupa arietina (O. F. Muller). J. Exp. Mar. Biol. Ecol. 2001, 266, 219–236.
318. Bailey-Brock, J.H. Polychaetes from Fijian coral reefs. Pac. Sci. 1985, 39, 195–220.
319. Nishi, E. Serpulid polychaetes associated with living and dead corals at Okinawa Island, Southwest Japan. Publ. Seto Mar. Biol.
Lab. 1996, 36, 305–318.
320. Marsden, J.R. Coral preference behaviour by planktotrophic larvae of Spirobranchus giganteus corniculatus (Serpulidae: Poly-
chaeta). Coral Reefs 1987, 6, 71–74.
321. Hunte, W.; Conlin, B.E.; Marsden, J.R. Habitat selection in the tropical polychaete Spirobranchus giganteus. I. Distribution on
corals. Mar. Biol. 1990, 104, 87–92.
322. Marsden, J.R. Light responses of the planktotrophic larva of the serpulid polychaete Spirobranchus polycerus. Mar. Ecol. Prog. Ser.
1990, 58, 225–233.
323. Williams, G.B. The effect of extracts of Fucus serratus in promoting the settlement of larvae of Spirorbis borealis (Polychaeta). J.
Mar. Biol. Assoc. UK 1964, 44, 397–414.
324. Gee, J.M. Chemical stimulation of settlement in larvae of Spirorbis rupestris (Serpulidae). Anim. Behav. 1965, 13, 181–186.
325. Hartman, O. Catalogue of the polychaetous annelids of the world. Part II. Occ. Pap. Allan Hancock Found. 1959, 23, 355–628.
Diversity 2021, 13, 130 68 of 74
326. Darling, J.A.; Carlton, J.T. A framework for understanding marine cosmopolitanism in the Anthropocene. Front. Mar. Sci. 2018,
5, 1–293.
327. Hutchings, P.; Kupriyanova, E. Cosmopolitan polychaetes–fact or fiction? Personal and historical perspectives. Invertebr. Syst.
2018, 32, 1–9.
328. Briggs, J.C. Marine Zoogeography; McGraw-Hill: New York, NY, USA, 1974; pp. 1–475.
329. McClain, C.R.; Schlacher, T.A. On some hypotheses of diversity of animal life at great depths on the sea floor. Mar. Ecol. 2015,
36, 849–872.
330. Higgs, N.D.; Attrill, M. Biases in biodiversity: Wide-ranging species are discovered first in the deep sea. Front. Mar. Sci. 2015, 2,
61.
331. Giangrande, A.; Licciano, M. Factors influencing latitudinal pattern of biodiversity: An example using Sabellidae (Annelida,
Polychaeta). Biodiv. Conserv. 2004, 13, 1633–1646.
332. Banse, K. Beiträge zur kenntnis der gattungen Fabricia, Manayunkia und Fabriciola (Sabellidae, Polychaeta). Zool. Jahrb. (Abt. Syst.
Okol. Geogr. Tiere) 1956, 84, 415–438.
333. Bourne, A.G. On Haplobranchus, a new genus of Capitobranchiate annelids. J. Cell Sci. 1883, 23, 168–176.
334. Annenkova, N.P. Über Die Pontokaspischen Polychaeten. II. Die Gattungen Hypaniola, Parhypania, Fabricia und Manajunkia.
Ann. Mussée Zool. L’Academie des Sci. L’URSS, Leningrad 1928, 30, 13–20.
335. Day, J.H. The polychaete fauna of South Africa Part 8: New species and records from grab samplings and dreddings. Bull. Brit.
Mus. (Nat. Hist.) Zool. 1963, 10, 381–445.
336. Perkins, T.H. Revision of Demonax Kinberg, Hypsicomus Grube, and Notaulax Tauber, with a review of Megalomma Johansson
from Florida (Polychaeta: Sabellidae). Proc. Biol. Soc. Wash. 1984, 97, 285–368.
337. Knight-Jones, P.; Perkins, T.H. A revision of Sabella and Bispira and Stylomma. (Sabellidae: Polychaeta). Zool. J. Linn. Soc. 1998,
123, 385–467.
338. Knight-Jones, P.; Mackie, A.S. A revision of Sabellastarte (Polychaeta: Sabellidae). J. Nat. Hist. 2003, 37, 2269–2301.
339. Hartman, O. Abyssal polychaetous annelids from the Mozambique Basin off Southeast Africa, with a compendium of abyssal
polychaetous annelids from world-wide Areas. J. Fish. Res. Board Can. 1971, 28, 1407–1428.
340. Uschakov, P.V. Bathypelagic and deepwater forms of marine polychaetes from Kamchatka Area of the Pacific. Issled. Fauny
Morej USSR 1952, 3, 103–112.
341. Levenstein, R.Y. Polychaeta from deep water in the Bering Sea. Proc. Inst. Oceanol. USSR Acad. Sci 1961, 46, 147–178.
342. Levenstein, R.Y. Polychaeta. In Pacific Ocean. Biology. Deep-Sea Fauna; Zenkevitch, L.A., Ed.; Nauka: Moscow, Russia, 1969; pp.
52–62. (In Russian)
343. Belyaev, G.M. Hadal Bottom Fauna of the World Ocean; Institute of Oceanology, USSR Academy of Sciences: Moscow, Russia,
1972; pp. 1–199.
344. Belyaev, G.M. Glubokovodnye Okeanicheskie Zheloba i Ikh Fauna [Deep-Sea Oceanic Trenches and Their Fauna]; Nauka: Moscow, Rus-
sia, 1989; pp. 1–256. (In Russian)
345. Moore, J.P. Additional new species of Polychaeta from the North Pacific. Proc. Acad. Nat. Sci. Phil. 1906, 58, 217–260.
346. Moore, J.P. The Polychætous annelids Dredged by the U. S. S. “Albatross” off the Coast of Southern California in 1904. IV.
Spionidae to Sabellariidae. Proc. Acad. Nat. Sci. Phil. 1923, 7, 179–259.
347. Hartman, O. Deep-water benthic polychaetous annelids off New England to Bermuda and other North Atlantic Areas. Occ. Pap.
Allan Hancock Found. 1965, 28, 1–378.
348. Méndez, N. Trophic categories of soft-bottom epibenthic deep-sea polychaetes from the Southeastern Gulf of California (Mex-
ico) in relation with environmental variables. Pan Am. J. Aquat. Sci. 2013, 8, 299–311.
349. Zibrowius, H. Review of Serpulidae (Polychaeta) from depths exceeding 2000 meters. In Essays on Polychaetous Annelids in
Memory of Dr. Olga Hartman; Reish, D.J., Fauchald, K., Eds.; Allan Hancock Press: Los Angeles, CA, USA, 1977; pp. 289–306.
350. Kirkergaard, J.B. Benthic Polychaeta from depths exceeding 6000 m. Galathea Rep. 1956, 2, 63–78.
351. Paterson, G.L.; Glover, A.G.; Froján, C.R.B.; Whitaker, A.; Budaeva, N.; Chimonides, J.; Doner, S. A Census of abyssal poly-
chaetes. Deep Sea Res. Part. II Top. Stud. Ocean. 2009, 56, 1739–1746.
352. Kupriyanova, E.K. Deep-water Serpulidae (Annelida, Polychaeta) from the Kurile-Kamchatka Trench. 2. Genera Bathyditrupa,
Bathyvermilia and Protis. Zool. Zhurnal 1993, 72, 21–28.
353. Kupriyanova, E.K. Deep-water Serpulidae (Annelida, Polychaeta) from the Kurile-Kamchatka Trench. 1. Genus Hyalopomatus.
Zool. Zhurnal 1993, 72, 145–152.
354. Sanfilippo, R. New species of Hyalopomatus Marenzeller, 1878 (Annelida, Polychaeta, Serpulidae) from Recent Mediterranean
deep-water coral mounds and comments on some congeners. Zoosystema 2009, 31, 147–161.
355. Kupriyanova, E.K.; Bailey-Brock, J.; Nishi, E. New records of Serpulidae (Annelida, Polychaeta) collected by R/V “Vityaz” from
bathyal and abyssal depths of the Pacific Ocean. Zootaxa 2011, 2871, 43–60, doi:10.11646/zootaxa.2871.1.3.
356. Kupriyanova, E.K.; Vinn, O.; Taylor, P.D.; Schopf, J.W.; Kudryavtsev, A.B.; Bailey-Brock, J. Serpulids living deep: Calcareous
tubeworms beyond the abyss. Deep Sea Res. Part. I Ocean. Res. 2014, 90, 91–104, doi:10.1016/j.dsr.2014.04.006.
357. Kupriyanova, E.K.; Nishi, E. New records of the deep-sea Nogrobs grimaldii (Serpulidae: Annelida). Mar. Biodivers. Rec. 2011, 4,
e74.
358. Rouse, G.W.; Kupriyanova, E.K. Laminatubus (Serpulidae, Annelida) from Eastern Pacific hydrothermal vents and methane
seeps, with description of two new species. Zootaxa 2021, 4915, 1–27.
Diversity 2021, 13, 130 69 of 74
359. Thorp, C.H.; Pyne, S.; West, S.A. Hydroides ezoensis Okuda, a fouling serpulid new to British coastal waters. J. Nat. Hist. 1987, 21,
863–877.
360. Zibrowius, H. A propos des pretendud “Recifs de Serpulidae” de l’lle Rousse, Corse (Mediterranee Nord-Occidentale). Mesogee
1991, 50, 71–74.
361. Zibrowius, H. Assessing scale and impact of ship-transported alien fauna in the Mediterranean? In Alien Marine Organisms
Introduced by Ships in the Mediterranean and Black Seas; Briand, F., ed.; CIESM Workshop Monographs: Monaco, France, 2002;
Volume 20, pp. 62–68.
362. Lewis, J.A.; Watson, C.; Harry, A. Establishment of the Caribbean serpulid tubeworm Hydroides sanctaecrucis Krøyer [in] Mörch,
1863, in Northern Australia. Biol. Invasions 2006, 8, 665–671.
363. Giangrande, A.; Licciano, M.; Pagliara, P.; Gambi, M.C. Gametogenesis and larval development in Sabella spallanzanii (Poly-
chaeta: Sabellidae) from the Mediterranean Sea. Mar. Biol. 2000, 136, 847–861.
364. Read, G.; Inglis, G.; Stratford, P.; Ahyong, S. Arrival of the alien fanworm Sabella spallanzanii (Gmelin, 1791) (Polychaeta: Sabel-
lidae) in two New Zealand harbours. Aquat. Invasions 2011, 6, 273–279, doi:10.3391/ai.2011.6.3.04.
365. Çinar, M.E. Alien polychaete species worldwide: Current status and their impacts. J. Mar. Biol. Assoc. UK 2013, 93, 1257–1278,
doi:10.1017/S0025315412001646.
366. Morais, P.; Reichard, M. Cryptic invasions: A review. Sci. Total Environ. 2018, 613, 1438–1448.
367. Chapman, J.W.; Carlton, J.T. A test of criteria for introduced species: The global invasion by the isopod Synidotea laevidorsalis
(Miers, 1881). J. Crust. Biol. 1991, 11, 386–400, doi:10.2307/1548465.
368. Wolff, W.J. Non-Indigenous marine and estuarine species in the Netherlands. Zool. Med. Leiden 2005, 79, 1–116.
369. Patti, F.; Gambi, M. Phylogeography of the invasive polychaete Sabella spallanzanii (Sabellidae) based on the nucleotide sequence
of internal transcribed spacer 2 (ITS2) of nuclear rDNA. Mar. Ecol. Prog. Ser. 2001, 215, 169–177.
370. Ahyong, S.T.; Kupriyanova, E.; Burghardt, I.; Sun, Y.; Hutchings, P.A.; Capa, M.; Cox, S.L. Phylogeography of the invasive
Mediterranean fan worm, Sabella spallanzanii (Gmelin, 1791), in Australia and New Zealand. J. Mar. Biol. Assoc. UK 2017, 97, 985–
991, doi:10.1017/S0025315417000261.
371. Pabis, K.; Krodkiewska, M.; Cebulska, K. Alien freshwater polychaetes Hypania invalida (Grube 1860) and Laonome calida Capa,
2007 in the Upper Odra River (Baltic Sea catchment area). Knowl. Manag. Aquat. Ecosyst. 2017, 418, 46.
372. Boltachova, N.; Lisitskaya, E.; Frolenko, L.; Kovalev, E.; Barabashin, T. The finding of polychaete Laonome calida Capa, 2007
(Annelida: Sabellidae) in the Southeast Sea of Azov. Russ. J. Biol. Invasions 2017, 8, 303–306.
373. Tamulyonis, A.Yu.; Gagaev, S.Yu.; Stratanenko, E.A.; Zuyev, Yu.A.; Potin, V.V. Invasion of the Polychaeta Laonome xeprovala
Bick & Bastrop, 2018 (Sabellidae, Polychaeta) into the estuary of the Luga and Khabolovka Rivers (Luga Bay, Gulf of Finland).
Russ. J. Biol. Invasions 2020, 11, 148–154, doi:10.1134/S2075111720020113.
374. Tovar-Hernández, M.A.; Yáñez-Rivera, B.; Bortolini-Rosales, J.L. Reproduction of the invasive fan worm Branchiomma bairdi
(Polychaeta: Sabellidae). Mar. Biol. Res. 2011, 7, 710–718, doi:10.1080/17451000.2010.547201.
375. Roman, S.; Perez-Ruzafa, A.; Lopez, E. First record in the Western Mediterranean Sea of Branchiomma boholense (Grube, 1878)
(Polychaeta: Sabellidae), an alien species of Indo-Pacific origin. Cah. Biol. Mar. 2009, 50, 241–250.
376. Arias, A.; Giangrande, A.; Gambi, M.C.; Anadón, N. Biology and new records of the invasive species Branchiomma bairdi (An-
nelida: Sabellidae) in the Mediterranean Sea. Mediterr. Mar. Sci. 2013, 10,162–171.
377. Ramalhosa, P.; Camacho-Cruz, K.; Bastida-Zavala, R.; Canning-Clode, J. First record of Branchiomma bairdi McIntosh, 1885 (An-
nelida: Sabellidae) from Madeira Island, Portugal (Northeastern Atlantic Ocean). Bioinvasions Rec. 2014, 3, 235–239,
doi:10.3391/bir.2014.3.4.04.
378. Cepeda, D.; Rodríguez-Flores, P. First record of the invasive worm Branchiomma bairdi (Annelida: Sabellidae) in the Balearic Sea
(Western Mediterranean). J. Mar. Biol. Assoc. UK 2018, 98, 1955–1963.
379. Del Pasqua, M.; Schulze, A.; Tovar-Hernández, M.A.; Keppel, E.; Lezzi, M.; Gambi, M.C.; Giangrande, A. Clarifying the taxo-
nomic status of the alien species Branchiomma bairdi and Branchiomma boholense (Annelida: Sabellidae) using molecular and mor-
phological evidence. PLoS ONE 2018, 13, e0197104, doi:10.1371/journal.pone.0197104.
380. Hewitt, C.L.; Campbell, M.L.; Thresher, R.E.; Martin, R.B.; Boyd, S.; Cohen, B.F.; Currie, D.R.; Gomon, M.F.; Keough, M.J.; Lewis,
J.A.; et al. Introduced and cryptogenic species in Port Phillip Bay, Victoria, Australia. Mar. Biol. 2004, 144, 183–202,
doi:10.1007/s00227-003-1173-x.
381. Zenetos, A.; Çinar, M.E.; Pancucci-Papadopoulou, M.A.; Harmelin, J.G.; Furnari, G.; Andaloro, F.; Bellou, N.; Streftaris, N.;
Zibrowius, H. Annotated list of marine alien species in the Mediterranean with records of the worst invasive species. Mediterr.
Mar. Sci. 2005, 6, 63–118, doi:10.12681/mms.186.
382. Gravili, C.; Belmonte, G.; Cecere, E.; Denitto, F.; Giangrande, A.; Guidetti, P.; Longo, C.; Mastrototaro, F.; Moscatello, S.; Petro-
celli, A. Nonindigenous species along the Apulian Coast, Italy. Chem. Ecol. 2010, 26, 121–142.
383. Giangrande, A.; Montanaro, P.; Castelli, A. On some Amphicorina (Polychaeta, Sabellidae) species from the Mediterranean coast,
with the description of A. grahamensis. Ital. J. Zool. 1999, 66, 195–203.
384. Zenetos, A.; Gofas, S.; Verlaque, M.; Çinar, M.E.; Garcia Raso, J.E.; Bianchi, C.N.; Morri, C.; Azzurro, E.; Bilecenoglu, M.; Froglia,
C.; et al. Alien species in the Mediterranean Sea by 2010. A contribution to the application of European Union’s Marine Strategy
Framework Directive (MSFD). Part I. Spatial distribution. Mediter. Mar. Sci. 2010, 11, 381, doi:10.12681/mms.87.
385. Faasse, M.A.; Giangrande, A. Description of Bispira polyomma n. sp. (Annelida: Sabellidae): A probable introduction to the Neth-
erlands. Aquat. Invasions 2012, 7, 591–598.
Diversity 2021, 13, 130 70 of 74
386. Capa, M.; Murray, A. A taxonomic guide to the fanworms (Sabellidae, Annelida) of Lizard Island, Great Barrier Reef, Australia,
including new species and new records. Zootaxa 2015, 4019, 98, 98–167, doi:10.11646/zootaxa.4019.1.8.
387. Khedhri, I.; Tovar-Hernández, M.A.; Bonifácio, P.; Ahmed, A.; Aleya, L. First report of the invasive species Branchiomma bairdi
McIntosh, 1885 (Annelida: Sabellidae) along the Tunisian Coast (Mediterranean Sea). Bioinvasions Rec. 2017, 6, 139–45.
388. Abdelnaby, F. Alien polychaete species and the first record of Branchiomma bairdi (McIntosh, 1885) from the Suez Canal and the
Mediterranean coast of Egypt. Egypt. J. Aquat. Biol. Fish. 2020, 24, 13–32.
389. Knight-Jones, P.; Knight-Jones, W.; Ergen, Z. Sabelliform Polychaetes, mostly from Turkey’s Aegean coast. J. Nat. Hist. 1991, 25,
837–858.
390. Çinar, M.E. Polychaetes from the coast of Northern Cyprus (Eastern Mediterranean Sea), with Two new records for the Medi-
terranean Sea. Cah. Biol. Mar. 2005, 46, 143–160.
391. Keppel, E.; Tovar Hernández, M.A.; Ruiz, G.M. First record and establishment of Branchiomma coheni (Polychaeta: Sabellidae)
in the Atlantic Ocean and review of non indigenous species of the genus. Zootaxa 2015, 4058, 4, 499–518.
392. Tovar-Hernández, M.A.; Dean, H.A. New gregarious sabellid worm from the Gulf of California reproducing by dpontaneous
fission (Polychaeta, Sabellidae). J. M. Biol. Assoc. UK 2014, 94, 935–946, doi:10.1017/S0025315414000186.
393. Bianchi, C. Serpuloidea (Annelida, Polychaeta) Delle Lagune Costiere Laziali e Campane. Annali del Museo Civico di Storia Nat-
urale di Genova 1983, 84, 231–243.
394. Arvanitides, C. Polychaete fauna of the Aegean Sea: Inventory and new information. Bull. Mar. Sci. 2000, 66, 73–96.
395. Simboura, N.; Nicolaidou, A. The Polychaetes (Annelida, Polychaeta) of Greece: Checklist, distribution and ecological charac-
teristics. Monographs on Marine Sciences, Ser. 4; National Center for Marine Research: Athens, Greece, 2001; pp. 1–115.
396. Licciano, M.; Giangrande, A.; Gambi, M.C. Reproduction and simultaneous hermaphroditism in Branchiomma luctuosum (Poly-
chaeta, Sabellidae) from the Mediterranean Sea. Invertebr. Biol. 2002, 121, 55–65.
397. Mastrototaro, F.; Petrocelli, A.; Cecere, E.; Matarrese, A. Non indigenous species settle down in the Taranto Seas. Biogeographia
2004, 25, 47–54.
398. Çinar, M.E.; Bilecenoglu, M.; Öztürk, B.; Can, A. New records of alien species on the Levantine coast of Turkey. Aquat. Invasions
2006, 1, 84–90.
399. El Haddad, M.; Capaccioni Azzati, R.; García-Carrascosa, A.M. Branchiomma luctuosum (Polychaeta: Sabellidae): A non-indige-
nous species at Valencia Port (Western Mediterranean Sea, Spain). Mar. Biodivers. Rec. 2008, 1, e61,
doi:10.1017/S1755267207006604.
400. Giangrande, A.; Licciano, M. Revision of the species of Megalomma (Polychaeta, Sabellidae) from the Mediterranean Sea, with
the description of M. messapicum n. sp. Ital. J. Zool. 2008, 75, 207–217, doi:10.1080/11250000801913124.
401. Tanduo, V.; Golemaj, A.; Crocetta, F. Citizen-science detects the arrival and establishment of Branchiomma luctuosum (Grube,
1870) (Annelida: Polychaeta: Sabellidae) in Albania. Biodivers. Data J. 2020, 8, e54790.
402. de Matos Nogueira, J.M.; Rossi, M.C.S.; López, E. Intertidal species of Branchiomma Kolliker and Pseudobranchiomma Jones (Pol-
ychaeta: Sabellidae: Sabellinae) occurring on rocky shores along the state of Sao Paulo, Southeastern Brazil. Zool. Stud. 2006, 45,
586–610.
403. Hartmann-Schröder, G. Teil 8. Die Polychaeten der Subtropisch-Antiborealen Westküste Australiens (Zwischen Cervantes im
Norden und Cape Naturliste im Suden). Mitt. Hamb. Zool. Mus. Inst. 1982, 79, 51–118.
404. Ceberio, A.; Martínez, J.; Aguirrezabalaga, F. Presencia de Desdemona ornata Banse, 1957 (Polychaeta, Sabellidae) en las costas
de La Península Ibérica, Golfo de Vizcaya. Munibe 1998, 50, 37–41.
405. Smith, P.; Perrett, J.; Garwood, P.; Moore, G. Two additions to the UK marine fauna: Desdemona ornata Banse, 1957 (Polychaeta,
Sabellidae) and Grandidierella japonica Stephensen, 1938 (Amphipoda, Gammaridea). Newsl. Porcupine Mar. Nat. Hist. Soc. 1999,
2, 8–11.
406. Çinar, M.E.; Dagli, E.; Açik, S. Annelids (Polychaeta and Oligochaeta) from the Sea of Marmara, with descriptions of five new
species. J. Nat. Hist. 2011, 45, 2105–2143.
407. Carvalho, S.; Pereira, P.; Pereira, F.; de Pablo, H.; Vale, C.; Gaspar, M.B. Factors structuring temporal and spatial dynamics of
macrobenthic communities in a eutrophic coastal lagoon (Óbidos Lagoon, Portugal). Mar. Environ. Res. 2011, 71, 97–110.
408. Faasse, M. Dispersal of the invasive tubeworms Desdemona ornata and Pseudopolydora paucibranchiata to the Netherlands (Poly-
chaeta: Sedentaria). Nederl. Faun. Med. 2016, 46, 49–56.
409. McArthur, M. Systematics and Introduced Status of Euchone (Polychaeta: Sabellidae) in Port Phillip Bay, and the Feeding Biol-
ogy of Euchone limnicola. Bachelor’s Thesis, Victoria University of Technology, Melbourne, Australia, 1997.
410. Guyonnet, B.; Borg, D. Premier signalement de l’espèce introduite Euchone limnicola Reish, 1959 (Polychaeta: Sabellidae) sur ses
Côtes Françaises de la Mer du Nord (Grand Port Maritime de Dunkerque). Cah. Nat. Observat. Mar. 2015, 4, 15–23.
411. Dane, L Morphological and Genetic Variation in the Cryptic Species Complex Myxicola infundibulum (Polychaeta, Sabellidae),
and its Introduction to Australia. Master’s Thesis, University of Melbourne, Melbourne, Australia 2008.
412. Keppel, E.; Ruiz, G.; Tovar–Hernández, M. Re-description of Parasabella fullo (Grube, 1878) (Polychaeta: Sabellidae) and diag-
nostic characteristics for detection in California. Eur. Zool. J. 2020, 87, 105–115.
413. Currie, D.; McArthur, M.; Cohen, B. Exotic Marine Pests in the Port. of Geelong, Victoria. Report 8; Marine and Freshwater Resources
Institute: Queenscliff, Australia, 1998; pp. 1–57.
414. Coles, S.L. Historical and recent introductions of non-indigenous marine species into Pearl Harbor, Oahu, Hawaiian Islands.
Mar. Biol. 1999, 135, 147–158.
Diversity 2021, 13, 130 71 of 74
415. Eldredge, L.G.; Smith, C.A. Guidebook of Introduced Marine Species in Hawaii; Bishop Museum Technical Report 21; Bishop Mu-
seum: Honolulu, Hawaii, USA, 2001.
416. Coles, S.; Eldredge, L.G. Nonindigenous species introductions on coral reefs: A need for information. Pac. Sci. 2002, 56, 191–209.
417. Culver, C.S.; Kuris, A.M.; Beede, B. Identification and Management of the Exotic Sabellid Pest in California Cultured Abalone; Califor-
nian Sea Grant College System: La Jolla, CA, USA, 1997.
418. Moore, J.D.; Juhasz, C.I.; Robbins, T.T.; Grosholz, E.D. The introduced sabellid polychaete Terebrasabella heterouncinata in Cali-
fornia: Transmission, methods of control and survey for presence in native gastropod populations. J. Shellfish Res. 2007, 26, 869–
876.
419. Moreno, R.A.; Neill, P.E.; Rozbaczylo, N. Native and non-indigenous boring polychaetes in Chile: A threat to native and com-
mercial mollusc species. Rev. Chil. Hist. Nat. 2006, 79, 263–278.
420. Dittmann, S.; Rolston, A.; Benger, S.N.; Kupriyanova, E.K. Habitat Requirements, Distribution and Colonisation of the Tubeworm
Ficopomatus Enigmaticus in the Lower Lakes and Coorong; Report for the South Australian Murray-Darling Basin Natural Resources
Management Board; Department of Environment and water: Adelaide, Australia, 2009; pp. 1–99.
421. Grosse, M.; Pérez, R.; Juan-Amengual, M.; Pons, J.; Capa, M. The elephant in the room-first record of invasive gregarious species
of serpulids (Calcareous Tube Annelids) in Majorca (Western Mediterranean). Sci. Mar. 2021, in press.
422. Assis, J. de; Alonso, C.; Christoffersen, M.L. First record of Ficopomatus uschakovi (Pillai, 1960) Serpulidae (Polychaeta: Annelida)
for the Western Atlantic. Rev. Nord. Biol. 2008, 19, 51–58.
423. Bastida-Zavala, R.; García-Madrigal, S. First record in the Tropical Eastern Pacific of the exotic species Ficopomatus uschakovi
(Polychaeta, Serpulidae). ZooKeys 2012, 238, 45–55.
424. Liñero-Arana, I.; Díaz-Díaz, Ó. Presencia del poliqueto exótico Ficopomatus uschakovi (Polychaeta: Serpulidae) en Venezuela:
Descripción y comentarios sobre su distribución. Interciencia 2012, 37, 234–237.
425. Arteaga-Flórez, C.; Fernández-Rodríguez, V.; Londoño-Mesa, M.H. First record of the polychaete Ficopomatus uschakovi (Pillai,
1960) (Annelida, Serpulidae) in the Colombian Caribbean, South America. Zookeys 2014, 371, 1–11.
426. Zibrowius, H. Les espèces Méditerrannéennes du genre Hydroides (Polychaeta Serpulidae). Remarques sur le prétendu poly-
morphisme de Hydroides uncinata. Téthys 1971, 2, 691–746.
427. Zibrowius, H. Introduced invertebrates: Examples of success and nuisance in the European Atlantic and in the Mediterranean.
Introduced species in European coastal waters. Ecosyst. Res. Rep. 1994, 8, 44–49.
428. Cohen, A.N.; Harris, L.H.; Bingham, B.L.; Carlton, J.T.; Chapman, J.W.; Lambert, C.C.; Lambert, G.; Ljubenkov, J.C.; Murray,
S.N.; Rao, L.C. Project Report for the Southern California Exotics Expedition. A Rapid Assessment Survey of Exotic Species in
Sheltered Coastal WatersCalifornia Department of Fish and Game, Sacramento CA State Water Resources Control Board, Sac-
ramento CA National Fish and Wildlife Foundation: San Francisco, CA, USA, 2002; pp. 1–37.
429. Carlton, J.T.; Eldredge, L.G. Marine bioinvasions of Hawaiʻi; Bernice, P., Eds.; Bishop Museum Press: Honolulu, HI, USA, 2009;
pp. 1–202.
430. Pettengill, J.; Wendt, D.; Schug, M.D.; Hadfield, M. Biofouling likely serves as a major mode of dispersal for the polychaete
tubeworm Hydroides elegans as inferred from microsatellite loci. Biofouling 2007, 23, 161–169.
431. Gruet, Y.; Hèral, M.; Robert, J.M. Premières observations sur l’introduction de la faune associée au naissain d’huîtres Japonaises
Crassostrea gigas (Thunberg), importé sur la Côte Atlantique Française. Cah. Biol. Mar. 1976, 17, 173–184.
432. Zibrowius, H. Introduction du polychete Serpulidae Japonais Hydroides ezoensis sur la Cote, Atlantique Frnacoise et remarques
sur la propagation d’autre espeies de Serpulidae. Tethys 1978, 8, 141–150.
433. Hayes, K.; Sliwa, C.; Migus, S.; McEnnulty, F.; Dunstan, P. National Priority Pests: Part II Ranking of Australian Marine Pests.
In An. independent report undertaken for the Department of Environment and Heritage by CSIRO Marine Research; Australian Govern-
ment Department of the Environment and Heritage: ACT, Australia, 2005; pp. 1–106.
434. Ferrario, J.; Minchin, D. Spread of the non-indigenous serpulid Hydroides sanctaecrucis Krøyer in Mörch, 1863 in the Pacific
Ocean: A new record from Taiwan. Bioinvasions Rec. 2017, 6, 33–38.
435. Lee, A.L., Dafforn, K.A., Hutchings, P.A., Johnston, E.L. Reproductive strategy and gamete development of an invasive fan-
worm, Sabella spallanzanii (Polychaeta: Sabellidae), a field study in Gulf St Vincent, South Australia. PloS ONE, 2018, 13, 7,
e0200027.
436. Clapin, G.; Evans, D.R. The status of the introduced marine fanworm Sabella spallanzanii in Western Australia: A preliminary
investigation. Cent. Res. Introd. Mar. Pests Tech. Rep. 1995, 2, 1–34.
437. Yee, A.; Mackie, J.; Pernet, B. The distribution and unexpected genetic diversity of the non-indigenous annelid Ficopomatus
enigmaticus in California. Aquat. Invasions 2019, 14, 250–266, doi:10.3391/ai.2019.14.2.06.
438. Oliva, M.; De Marchi, L.; Sanches, M.V.; Pires, A.; Cuccaro, A.; Baratti, M.; Chiellini, F.; Morelli, A.; Freitas, R.; Pretti, C. Atlantic
and Mediterranean populations of the widespread serpulid Ficopomatus enigmaticus: Developmental responses to carbon nano-
tubes. Mar. Pollut. Bull. 2020, 156, 111265.
439. Zibrowius, H. Serpulidae (Annelida Polychaeta) de l’Ocean Indien arrives sur des Coques de Bateaux a Toulon (France, Medi-
terranee). Rapports et Proces Verbaux des Reunions Commission Internationale pour l’Exploration Scientifique de la Mer Mediterranee
Monaco 1979, 25–26, 133–134.
440. Ben-Eliahu, M.N. Red Sea serpulids (Polychaeta) in the Eastern Mediterranean. Ophelia Suppl. 1991, 5, 515–528.
441. Zenetos, A.; Çinar, M.E.; Crocetta, F.; Golani, D.; Rosso, A.; Servello, G.; Shenkar, N.; Turon, X.; Verlaque, M. Uncertainties and
validation of alien species catalogues: The Mediterranean as an example. Estuar. Coast. Shelf Sci. 2017, 191, 171–187.
Diversity 2021, 13, 130 72 of 74
442. Streftaris, N.; Zenetos, A. Alien marine species in the Mediterranean-the 100 ‘worst invasives’ and their impact. Mediterr. Mar.
Sci. 2006, 7, 87–118.
443. Dürr, S.; Watson, D.I. Biofouling and antifouling in aquaculture. Biofouling 2010, 12, 267–287.
444. Wang, J.; Huang, Z. Fouling polychaetes of Hong Kong and adjacent saters. Asian Mar. Biol. 1993, 10, 1–12.
445. Mohan, P.C.; Aruna, C. The biology of serpulid worms in relation to biofouling. In Recent Developments in Biofouling Control;
Thompson, M.F., Nagabhushanam, R., Sarojini, R., Fingerman, M., Eds.; Oxford & IBH Publishing Company: New Delhi, India,
1994; pp. 59–64.
446. Fitridge, I.; Dempster, T.; Guenther, J.; De Nys, R. The impact and control of biofouling in marine aquaculture: A review. Bio-
fouling 2012, 28, 649–669.
447. Schloesser, D.W.; Malakauskas, D.M.; Malakauskas, S.J. Freshwater polychaetes (Manayunkia speciosa) near the Detroit River,
Western Lake Erie: Abundance and life-history characteristics. J. Great Lakes Res. 2016, 42, 1070–1083.
448. Read, G.B.; Gordon, D.P. Adventive occurrence of the fouling serpulid Ficopomatus enigmaticus (Polychaeta) in New Zealand.
N. Z. J. Mar. Freshw. Res. 1991, 25, 269–273, doi:10.1080/00288330.1991.9516478.
449. Probert, P.K. First record of the introduced fouling tubeworm Ficopomatus enigmaticus (Polychaeta: Serpulidae) in Hawke Bay,
New Zealand. N. Z. J. Zool. 1993, 20, 35–36, doi:10.1080/03014223.1993.10423240.
450. Pernet, B.; Barton, M.; Fitzhugh, K.; Harris, L.; Lizárraga, D.; Ohl, R.; Whitcraft, C. Establishment of the reef-forming tubeworm
Ficopomatus enigmaticus (Fauvel, 1923) (Annelida: Serpulidae) in Southern California. Bioinvasions Rec. 2016, 5, 13–19,
doi:10.3391/bir.2016.5.1.03.
451. Heiman, K.W.; Micheli, F. Non-native ecosystem engineer alters Estuarine communities. Integr. Comp. Biol. 2010, 50, 226–236.
452. Ulman, A.; Ferrario, J.; Forcada, A.; Seebens, H.; Arvanitidis, C.; Occhipinti-Ambrogi, A.; Marchini, A. Alien species spreading
via biofouling on recreational vessels in the Mediterranean Sea. J. Appl. Ecol. 2019, 56, 2620–2629.
453. Secretaría de Medio Ambiente y Recursos Naturales, Estados Unidos Mexicanos. Acuerdo por el que se Determina la Lista de
las Especies Exóticas Invasoras Para México; Secretaría de Medio Ambiente y Recursos Naturales: Ciudad de México, Mexico,
2016.
454. Mackie, G.L.; Qadri, S.U. A polychaete, Manayunkia speciosa, from the Ottawa River, and Its North American distribution. Canad.
J. Zool. 1971, 49, 780–782.
455. Stocking, R.W.; Bartholomew, J.L. Distribution and habitat characteristics of Manayunkia speciosa and infection prevalence with
the parasite Ceratomyxa shasta in the Klamath River, Oregon–California. J. Parasitol. 2007, 93, 78–88.
456. Piazzolla, D.; Cafaro, V.; Mancini, E.; Scanu, S.; Bonamano, S.; Marcelli, M. Preliminary investigation of microlitter pollution in
low-energy hydrodynamic basins using Sabella spallanzanii (Polychaeta: Sabellidae) tubes. Bull. Environ. Contam. Toxicol. 2020,
104, 345–350.
457. Gopalakrishnan, S.; Thilagam, H.; Raja, P.V. Comparison of heavy metal toxicity in life stages (spermiotoxicity, egg toxicity,
embryotoxicity and larval toxicity) of Hydroides elegans. Chemosphere 2008, 71, 515–528.
458. Thilagam, H.; Gopalakrishnan, S.; Vijayavel, K.; Raja, P.V. Effluent toxicity test using developmental stages of the marine poly-
chaete Hydroides elegans. Arch. Environ. Contam. Toxicol. 2008, 54, 674–683.
459. Vijayaragavan, S.; Raja, P.V. The toxic effects of phorate on early embryonic stages of sedentary polychaete Hydroides elegans
(Haswell, 1883). J. Basic Appl. Zool. 2018, 79, 45.
460. Bellante, A.; Piazzese, D.; Cataldo, S.; Parisi, M.G.; Cammarata, M. Evaluation and comparison of trace metal accumulation in
different tissues of potential bioindicator organisms: Macrobenthic filter feeders Styela plicata, Sabella spallanzanii, and Mytilus
galloprovincialis. Environ. Toxicol. Chem. 2016, 35, 3062–3070.
461. Giangrande, A.; Licciano, M.; Del Pasqua, M.; Fanizzi, F.P.; Migoni, D.; Stabili, L. Heavy metals in five Sabellidae species (An-
nelida, Polychaeta): Ecological implications. Environ. Sci. Pollut. Res. 2017, 24, 3759–3768.
462. Xie, Z.-C.; Wong, N.C.; Qian, P.-Y.; Qiu, J.-W. Responses of polychaete Hydroides elegans life stages to copper stress. Mar. Ecol.
Prog. Ser. 2005, 285, 89–96.
463. Gopalakrishnan, S.; Thilagam, H.; Raja, P. Toxicity of heavy metals on embryogenesis and larvae of the marine sedentary pol-
ychaete Hydroides elegans. Arch. Environ. Contamin. Toxicol. 2007, 52, 171–178.
464. Ross, K.E.; Bidwell, J.R. A 48-h larval development toxicity test using the marine polychaete Galeolaria caespitosa Lamarck (Fam.
Serpulidae). Arch. Environ. Contamin. Toxicol. 2001, 40, 489–496.
465. Giangrande, A.; Cavallo, A.; Licciano, M.; Mola, E.; Pierri, C.; Trianni, L. Utilization of the filter feeder polychaete Sabella. Aquac.
Int. 2005, 13, 129–136.
466. Licciano, M.; Stabili, L.; Giangrande, A.; Cavallo, R.A. Bacterial accumulation by Branchiomma luctuosum (Annelida: Polychaeta):
A tool for biomonitoring marine systems and restoring polluted waters. Mar. Environ. Res. 2007, 63, 291–302.
467. Pierri, C.; Fanelli, G.; Giangrande, A. Experimental co-culture of low food-chain organisms, Sabella spallanzanii (Polychaeta,
Sabellidae) and Cladophora prolifera (Chlorophyta, Cladophorales), in Porto Cesareo area (Mediterranean Sea). Aquac. Res. 2006,
37, 966–974.
468. Stabili, L.; Licciano, M.; Giangrande, A.; Longo, C.; Mercurio, M.; Marzano, C.N.; Corriero, G. Filtering Activity of Spongia offic-
inalis var. adriatica (Schmidt) (Porifera, Demospongiae) on bacterioplankton: Implications for bioremediation of polluted sea-
water. Water Res. 2006, 40, 3083–3090.
469. Stabili, L.; Licciano, M.; Lezzi, M.; Giangrande, A. Microbiological accumulation by the Mediterranean invasive alien species
Branchiomma bairdi (Annelida, Sabellidae): Potential tool for bioremediation. Mar. Pollut. Bull. 2014, 86, 325–331.
Diversity 2021, 13, 130 73 of 74
470. Stabili, L.; Licciano, M.; Giangrande, A.; Gerardi, C.; De Pascali, S.A.; Fanizzi, F.P. First insight on the mucus of the annelid
Myxicola infundibulum (Polychaeta, Sabellidae) as a potential prospect for drug discovery. Mar. Drugs 2019, 17, 396.
471. Soto, D. Integrated Mariculture: A Global Review Food and Agriculture Organization of the United Nations (FAO): Rome, Italy, 2009.
472. Stewart, B.; Davies, B. Effects of macrophyte harvesting on invertebrates associated with Potamogeton pectinatus L. in the Marina
Da Gama, Zandvlei, Western Cape. Trans. R. Soc. S. Africa 1986, 46, 35–49.
473. Joyce, C.B.; Vina-Herbon, C.; Metcalfe, D.J. Biotic variation in coastal water bodies in Sussex, England: Implications for saline
lagoons. Estuar. Coast. Shelf Sci. 2005, 65, 633–644.
474. Davies, B.; Stuart, V.; De Villiers, M. The filtration activity of a serpulid polychaete population (Ficopomatus enigmaticus (Fauvel)
and its effects on water quality in a coastal marina. Estuar. Coast. Shelf Sci. 1989, 29, 613–620.
475. Licciano, M.; Watson, G.J.; Murray, J.M.; Giangrande, A. Evidence of regenerative ability in Myxicola infundibulum (Annelida,
Sabellida): Evolutionary and systematic implications. Invertebr. Biol. 2015, 134, 48–60, doi:10.1111/ivb.12077.
476. Bely, A.E. Distribution of segment regeneration ability in the Annelida. Integr. Comp. Biol. 2006, 46, 508–518.
477. Prentiss, N.K.; Tyler, M.S.; Dean, D.A. Morphological and histological investigation of the regeneration in Myxicola infundibulum
(Montagu, 1808) (Sabellida, Annelida). Mar. Biol. Assoc. UK 2017, 97, 1155–1165.
478. Nicol, J. The giant nerve-fibres in the central nervous system of Myxicola (Polychaeta, Sabellidae). Q. J. Micros. Sci. 1948, 3, 1–45.
479. Roberts, M.B.V. The Rapid response of Myxicola infundibulum (Grube). J. Mar. Biol. Assoc. U.K. 1962, 42, 527–539.
480. Gilbert, D. Axoplasm architecture and physical properties as seen in the Myxicola giant axon. J. Physiol. 1975, 253, 257–301.
481. Barry, J.F.; Turner, M.J.; Schloss, J.M.; Glenn, D.R.; Song, Y.; Lukin, M.D.; Park, H.; Walsworth, R.L. Optical magnetic detection
of single-neuron action potentials using quantum defects in diamond. Proc. Natl. Acad. Sci. USA 2016, 113, 14133–14138.
482. Purschke, G. Annelida: Basal groups and Pleistoannelida. In Structure and Evolution of Invertebrate Nervous Systems; Schmidt-
Rhaesa, A., Harzsch, S., Purschke, G., Eds.; Oxford University Press: Oxford, UK, 2016; pp. 254–312.
483. Schauf, C.; Davis, F.A.; Marder, J. Effects of carbamazepine on the ionic conductances of Myxicola giant axons. J. Pharmacol. Exp.
Ther. 1974, 189, 538–543.
484. Nedved, B.T.; Hadfield, M.G. Hydroides elegans (Annelida: Polychaeta): A model for biofouling research. In Marine and Industrial
Biofouling; Flemming, H-S., Sriyutha Murthy, P., Venkatesan, R., Cooksey, K., Eds.; Springer Series on Biofilms: Los Angeles,
CA, USA, 2008; Vol 4, pp. 203–218.
485. Hadfield, M.G. The D.P. Wilson Lecture. Research on settlement and metamorphosis of marine invertebrate larvae: Past, present
and future. Biofouling 1998, 12, 9–29.
486. Hadfield, M.G. Biofilms and marine invertebrate larvae: What bacteria produce that larvae use to choose settlement sites. Ann.
Rev. Mar. Sci 2011, 3, 453–470.
487. Qian, P.-Y. Larval settlement of polychaetes. Hydrobiologia 1999, 402, 239–253.
488. Hadfield, M.G.; Nedved, B.T.; Wilbur, S.; Koehl, M. Biofilm cue for larval settlement in Hydroides elegans (Polychaeta): Is contact
necessary? Mar. Biol. 2014, 161, 2577–2587.
489. Shikuma, N.J.; Antoshechkin, I.; Medeiros, J.M.; Pilhofer, M.; Newman, D.K. Stepwise metamorphosis of the tubeworm Hy-
droides elegans is mediated by a bacterial inducer and MAPK Signaling. Proc. Natl. Acad. Sci. USA 2016, 113, 10097–10102.
490. Vijayan, N.; Lema, K.A.; Nedved, B.T.; Hadfield, M.G. Microbiomes of the polychaete Hydroides elegans (Polychaeta: Serpulidae)
across its life-history stages. Mar. Biol. 2019, 166, 19.
491. Toonen, R.J.; Pawlik, J.R. Foundations of gregariousness. Nature 1994, 370, 511–512.
492. Toonen, R.J.; Pawlik, J.R. Settlement of the gregarious tube worm Hydroides dianthus (Polychaeta: Serpulidae): Cues for gregar-
ious settlement. Mar. Biol. 1996, 126, 725–733.
493. Toonen, R.; Pawlik, J. Settlement of the gregarious tube worm Hydroides dianthus (Polychaeta: Serpulidae). I. gregarious and
nongregarious settlement. Mar. Ecol. Prog. Ser. 2001, 224, 103–114, doi:10.3354/meps224103.
494. Kenny, N.J.; Shimeld, S.M. Additive multiple k-mer transcriptome of the keelworm Pomatoceros lamarckii (Annelida; Serpulidae)
reveals annelid trochophore transcription factor cassette. Dev. Genes Evol. 2012, 222, 325–339.
495. Barton-Owen, T.B.; Szabó, R.; Somorjai, I.M.; Ferrier, D.E. A revised spiralian homeobox gene classification incorporating new
polychaete transcriptomes reveals a diverse TALE class and a divergent hox gene. Genome Biol. Evol. 2018, 10, 2151–2167.
496. Szabó, R.; Ferrier, D.E.K. Cell proliferation dynamics in regeneration of the operculum head appendage in the annelid Poma-
toceros lamarckii. J. Exp. Zool. Part. B Mol. Dev. Evol. 2014, 322, 257–268.
497. Szabó, R.; Ferrier, D.E. Another biomineralising protostome with an msp130 gene and conservation of msp130 gene structure
across Bilateria. Evol. Dev. 2015, 17, 195–197.
498. San Chan, V.B.; Li, C.; Lane, A.C.; Wang, Y.; Lu, X.; Shih, K.; Zhang, T.; Thiyagarajan, V. CO2-driven ocean acidification alters
and weakens integrity of the calcareous tubes produced by the serpulid tubeworm, Hydroides elegans. PLoS ONE 2012, 7, e42718.
499. Lane, A.C.; Mukherjee, J.; Chan, V.B.; Thiyagarajan, V. Decreased pH does not alter metamorphosis but compromises juvenile
calcification of the tube worm Hydroides elegans. Mar. Biol. 2013, 160, 1983–1993.
500. Díaz-Castañeda, V.; Cox, T.E.; Gazeau, F.; Fitzer, S.; Delille, J.; Alliouane, S.; Gattuso, J.-P. Ocean acidification affects calcareous
tube growth in adults and reared offspring of serpulid polychaetes. J. Exp. Biol. 2019, 222, jeb196543.
501. Wabnitz, C. From Ocean to Aquarium: The Global Trade in Marine Ornamental Species; UNEP/Earthprint: Cambridge, UK, 2003.
502. Murray, J.M.; Watson, G.J.; Giangrande, A.; Licciano, M.; Bentley, M.G. Managing the marine aquarium trade: Revealing the
data gaps using ornamental polychaetes. PLoS ONE 2012, 7, e29543.
503. Bybee, D.R.; Murray, J.M. Polychaetes. Mar. Ornam. Spec. Aquacult. 2017, 1, 565–579.
Diversity 2021, 13, 130 74 of 74
504. Bybee, D.R.; Bailey-Brock, J.H.; Tamaru, C.S. Larval development of Sabellastarte spectabilis (Grube, 1878) (Polychaeta: Sabelli-
dae) in Hawaiian waters. Sci. Mar. 2006, 70, 279–286, doi:10.3989/scimar.2006.70s3279.
505. Bybee, D.R.; Bailey-Brock, J.H.; Tamaru, C.S. Evidence for sequential hermaphroditism in Sabellastarte spectabilis (Polychaeta:
Sabellidae) in Hawai’i. Pac. Sci. 2006, 60, 541–547, doi:10.1353/psc.2006.0025.
506. Bybee, D.R.; Bailey-Brock, J.H.; Tamaru, C.S. Gametogenesis and spawning periodicity in the fan worm Sabellastarte spectabilis
(Polychaeta: Sabellidae). Mar. Biol. 2007, 151, 639–648, doi:10.1007/s00227-006-0504-0.
507. Murray, J.M. Regeneration and Reproduction in Sabella pavonina (Savigny): Developing a Novel Method to Culture Marine
Ornamental Sabellids. Ph.D. Thesis, University of Portsmouth, Portsmouth, UK, 2010.
508. Dávila-Jiménez, Y.; Tovar-Hernández, M.A.; Simōes, N. The social feather duster worm Bispira brunnea (Polychaeta: Sabellidae):
Aggregations, morphology and reproduction. Mar. Biol. Res. 2017, 13, 782–796.
509. Alalykina IL, Polychaeta. A review of the deep-sea benthic polychaetes along the NW Pacific. In Biogeographical Atlas of the Deep
NW Pacific Fauna; Pensoft Publishers: Sofia, Bulgaria, 2020; pp. 175–212.
510. Gunton, L.M.; Kupriyanova, E.K.; Alvestad, T.; Avery, L.; Blake, J.A.; Biriukova, O.; Böggemann, M.; Borisova, P.; Budaeva, N.;
Burghardt, I.; Capa, M.; Georgieva, M.N.; Glasby, C.; Hsueh, P.W.; Hutchings, P.; Jimi, N.; Kongsrud, J. A.; Langeneck, J.;
Meißner, K.; Murray, A., Nikolic, M., Paxton, H., Ramos, D., Schulze, A., Sobczyk, E., Watson, C., Wiklund, H.; R.S.;
Zhadan, A.; Zhang, J. Annelids of the eastern Australian abyss collected by the 2017 RV ‘Investigator’voyage. ZooKeys 2021,
1020, 1–198.
511. Simon, C. The wonderful world of worms. Quest 2014, 10, 32–34.
512. Ippolitov, A.; Rzhavsky, A. Tube morphology, ultrastructures and mineralogy in recent Spirorbinae (Annelida; Polychaeta;
Serpulidae). I. General introduction. Tribe Paralaeospirini. Invertebr. Zool. 2014, 11, 293–314.
513. Sigvaldadóttir, E.; Mackie, A.S. Prionospio steenstrupi, P. fallax and P. dubia (Polychaeta, Spionidae): Re-evaluation of identity
and status. Sarsia 1993, 78, 203–219.
514. Martin, D.; Britayev, T.A.; San Martín, G.; Gil, J. Inter-population variability and character description in the sponge-associated
Haplosyllis spongicola complex (Polychaeta: Syllidae). In Advances in Polychaete Research; Springer: Dordrecht, The Netherlands,
2003; pp. 145–162.
515. ten Hove, H.A.; M. J. Jansen-Jacobs, A. Revision of the genus Crucigera (Polychaeta; Serpulidae); a proposed methodical ap-
proach to serpulids, with special reference to variation in Serpula and Hydroides. In Proceedings of the First International Polychaete
Conference; Hutchings, P.A., Ed.; Linnean Society of New South West: Sydney, Australia, 1984; pp. 143–180.
516. Watanabe, M.E. The evolution of natural history collections: New research tools move specimens, data to center stage. Bioscience
2019, 69, 163–169.
517. Annenkova, N.P. Polychaeta of the North Japan Sea and their horizontal and vertical distribution. USSR Hydrobiological Ex-
pedition in 1934 to the Japan Sea. Trudy Daln. Filiala Akademii Nauk SSSR 1938, 1, 81–230. (In Russian)
518. Oug, E.; Bakken, T.; Kongsrud, J.A. Original specimens and type localities of early described polychaete species (Annelida) from
Norway, with particular attention to species described by O. F. Müller and M. Sars. Mem. Mus. Vic. 2014, 71, 217–236,
doi:10.24199/j.mmv.2014.71.17.
519. Montagu, G. Testacea Brittanica or Natural History of British Shells, Marine, Land and Fresh-Water, Including the Most Minute: Sys-
tematically Arranged and Embellished with Figures. Part II; White: London, UK, 1803; pp. 293–606.
520. von Siebold, C.T. Bericht Über die Leistungen in der Naturgeschichte der Würmer, Zoophyten und Protozoen Während der
Jahre 1845, 1846 und 1847. Arch. Naturgesch. 1850, 16, 351–468.
