Field guide to calcareous tubeworms (Polychaeta, Serpulidae) of the Arctic Ocean

A.N. Severtzov Institute of Ecology and Evolution RAS
Australian Museum Research Institute
Akvaplan-niva
A.V. Rzhavsky, E.K. Kupriyanova, A.V. Sikorski
FIELD GUIDE TO CALCAREOUS
TUBEWORMS (POLYCHAETA,
SERPULIDAE) OF THE ARCTIC
OCEAN
KMK Scientific Press
Moscow 2018

A.V. Rzhavsky, E.K. Kupriyanova, A.V. Sikorski. Field guide to calcareous
tubeworms (Polychaeta, Serpulidae) of the Arctic Ocean. Moscow. KMK Scientific Press, 2018. 187 p.
The book is a taxonomic guide to serpulid polychaetes (including the subfamily Spirorbinae) of the Arctic Ocean. Taxonomic keys include 37 serpulid spesies
described and illustrated in detail. It starts with a description of serpulid morphology and includes a comprehensive glossary. Taxonomic treatment of species includes basic synonymy, references, and brief differential diagnoses. Information
is also available on species reproduction, geographical distribution, and habitats
in the Arctic Basin. Species illustrations are presented as light and scanning electron microscopy micrographs, photos of live specimens and line drawings. The
book is based on extensive (over 600 samples) material collected all over the
Arctic Ocean and deposited in Russia, Iceland, Germany, Norway, and Australia.
The guide is based on the same material as Rzhavsky et al. (2014) “Calcareous
tubeworms (Polychaeta, Serpulidae) of the Arctic Ocean”, but it has another concept and target user: it is a simplified and lavishly illustrated field guide for identification definition of calcareous tubeworms in the field and laboratory. Detailed
synonymy and taxonomic discussions are excluded.  This guide is intended for
undergraduate and graduate students, educators and naturalists as well as invertebrate zoologists, marine ecologists, and environmental consultants.
Cover photos F. Pleijel, A.V. Rzhavsky
Editor:
T.A. Britayev, A.N. Severtsov Institute of Ecology and Evolution RAS,
Moscow, Russia
Reviewers:
A.B. Tzetlin, Department of Invertebrate Zoology, M.V. Lomonosov Moscow
State University, Russia
N.E. Budaeva, P.P. Shirshov Institute of Oceanology Russian Academy
of Sciences, Russia
© KMK Scientific Press, 2018.
© Akvaplan-niva,  2018.
ISBN  978-5-6040493-7-2
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ACKNOWLEDGEMENTS
The authors greatly appreciate efforts of numerous colleagues and expedition staff who collected the material used in preparation of this book from
1880 to 2013 (see Table 1 in Rzhavsky et al., 2014). We thank the staff of the
Institutions and Museums where these collections are deposited for the opportunity to work with this material, especially G. N. Buzhinskaja and V. V.
Potin (Zoological Institute of the Russian Academy of Sciences, St. Petersburg, Russia), I. A. Jirkov (Department of Hydrobiology of Moscow State
University, Moscow, Russia), and D. L. Ivanov (Zoological Museum of Moscow State University, Moscow, Russia). Also we are grateful to the people
who provided photos: E. Wong (The University of Queensland, Brisbane,
Australia), R. Sanfilippo (Dipartimento di Scienze Geologiche, Sezione di
Oceanologia e Paleoecologia, Catania University, Catania, Italy), G. Rouse
(Scripps Institution of Oceanography, UCSD, La Jolla, CA, USA), H. A. ten
Hove (Netherlands Centre for Biodiversity Naturalis, Leiden, Netherlands),
P. Wirtz (Centro de Ciencias do Mar do Algarve Campus de Gambelas, Faro,
Portugal), F. Pleijel (University of Gothenburg).
Publication of this book and part of the research were supported by
Akvaplan-niva (Tromsø, Norway) and a grant from the Norwegian Research
Council (Project 233635/H30 “Environmental management of petroleum activities in the Barents Sea: Norwegian-Russian collaboration”).
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CONTENTS
Acknowledgments .............................................................................................3
Contents .............................................................................................................4
Introduction .......................................................................................................6
General morphology ..........................................................................................7
Methodological remarks .................................................................................. 17
- Recommendations for identification of non-spirorbins ............................17
- Recommendations for identification of spirorbins....................................18
Glossary ...........................................................................................................20
The former subfamilies “Serpulinae” and “Filograninae”
- Key to non-spirorbins based on tube morphology ....................................24
- Key to non-spirorbins based on specimen morphology ............................32
- Genus Apomatus .......................................................................................38
- Apomatus globifer...................................................................................40
- Genus Bathyvermilia................................................................................. 42
- Bathyvermilia eliasoni ............................................................................ 44
- Bathyvermilia islandica ..........................................................................46
- Genus Chitinopoma ..................................................................................48
- Chitinopoma serrula ...............................................................................50
- Genus Ditrupa...........................................................................................52
- Ditrupa arietina ......................................................................................54
- Genus Filograna .......................................................................................56
- Filograna implexa ..................................................................................58
- Genus Hyalopomatus ................................................................................60
- Hyalopomatus claparedii........................................................................62
- Genus Hydroides .......................................................................................64
- Hydroides norvegica...............................................................................66
- Genus Metavermilia .................................................................................. 68
- Metavermilia arctica............................................................................... 70
- Genus Placostegus ....................................................................................72
- Placostegus tridentatus...........................................................................74
- Genus Protis.............................................................................................. 76
- Protis akvaplani ......................................................................................78
- Protis arctica .......................................................................................... 80
- Genus Protula ........................................................................................... 82
- Protula tubularia ....................................................................................84
- Genus Serpula ...........................................................................................86
- Serpula vermicularis...............................................................................88
- Genus Spirobranchus ................................................................................90
- Spirobranchus triqueter ..........................................................................92
Spirorbinae
- Key to spirorbins.......................................................................................94
- Tribe Circeini .......................................................................................... 108
- Genus Circeis .......................................................................................... 108
- Circeis armoricana ............................................................................... 110
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- Circeis spirillum ................................................................................... 112
- Genus Paradexiospira ............................................................................ 114
- Subgenus Paradexiospira ....................................................................... 114
- Paradexiospira (Paradexiospira) violacea .......................................... 116
- Subgenus Spirorbides ............................................................................. 118
- Paradexiospira (Spirorbides) cancellata .............................................. 120
- Paradexiospira (Spirorbides) vitrea .....................................................122
- Tribe Januini ...........................................................................................124
- Genus Janua ...........................................................................................124
- Janua heterostropha .............................................................................126
- Tribe Pileolariini ..................................................................................... 128
- Genus Bushiella ...................................................................................... 128
- Subgenus Bushiella ................................................................................. 129
- Bushiella (Bushiella) barentsii .............................................................130
- Bushiella (Bushiella) evoluta................................................................ 132
- Bushiella (Bushiella) verruca ............................................................... 134
- Subgenus Jugaria....................................................................................136
- Bushiella (Jugaria) acuticostalis .......................................................... 138
- Bushiella (Jugaria) granulata ..............................................................140
- Bushiella (Jugaria) kofiadii .................................................................. 142
- Bushiella (Jugaria) quadrangularis .....................................................144
- Bushiella (Jugaria) similis.................................................................... 146
- Genus Pileolaria ..................................................................................... 148
- Pileolaria ex.gr. berkeleyana ................................................................150
- Genus Protoleodora ................................................................................152
- Protoleodora gracilis............................................................................154
- Protoleodora uschakovi ........................................................................156
- Tribe Spirorbini .......................................................................................158
- Genus Spirorbis ......................................................................................158
- Subgenus Spirorbis .................................................................................158
- Spirorbis (Spirorbis) corallinae ............................................................160
- Spirorbis (Spirorbis) inornatus .............................................................162
- Spirorbis (Spirorbis) rupestris ..............................................................164
- Spirorbis (Spirorbis) spirorbis ..............................................................166
- Spirorbis (Spirorbis) tridentatus ...........................................................168
References .....................................................................................................170
Index ..............................................................................................................181
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INTRODUCTION
Serpulidae are obligatory sedentary polychaetes inhabiting calcareous tubes.
They share the presence of a radiolar crown and division of the body into
thoracic and abdominal regions. Their thorax is flanked by lateral thoracic
membranes and the border between thorax and abdomen is marked by chaetal
inversion, the chaetal arrangement where thoracic uncini switch from ventral
to dorsal in the abdomen, while the chaetae switch from dorsal in the thorax
to ventral in the abdomen. Traditionally the family Serpulidae was divided
into three subfamilies: Spirorbinae, Serpulinae, and Filograninae (e.g., Rioja,
1923; Fauvel, 1927). Pillai (1970) elevated the Spirorbinae to the family status. Later, a number of authors (e.g., ten Hove, 1984; Smith, 1991;
Kupriyanova, 2003; Kupriyanova et al., 2006), based on the results of phylogenetic analyses of morphological and molecular data, concluded that
spirorbins are monophyletic and nested inside the Serpulidae. Kupriyanova’s
(2003) results of morphology-only analyses placed Spirorbinae as a sister
group to Serpulinae. However, the results of analyses of both molecular (Lehrke
et al., 2007; Kupriyanova et al., 2009) and combined morphological and molecular data (Kupriyanova et al., 2006) indicate that neither Serpulinae nor
Filograninae are monophyletic and that Spirorbinae is a sister group to a clade
containing mostly “filogranins” and some “serpulins”. Therefore, the rank of
the spirorbids has been lowered to the subfamily and all six former spirorbids
sub-families are now placed at tribal ranks (Rzhavsky et al., 2013). Moreover, the traditional subfamilies Serpulinae and Filograninae have been abandoned pending revision and re-formulation as a result of a nearly comprehensive combined phylogenetic analysis (Kupriyanova et al., in prep.).
The Arctic Ocean, smallest of the world’s oceans, centres approximately
on the North Pole, covers much of the Arctic and washes upon northern North
America and Eurasia. It is connected to the Pacific Ocean by the Bering Strait
and to the Atlantic Ocean through the Greenland Sea and Labrador Sea, and is
sometimes regarded as an estuary of the Atlantic Ocean. A number of opinions exists regarding the exact borders of the Arctic Oean. Here we accept the
opinion of Makkaveev (2005) that the line separating the Atlantic and Arctic
Oceans goes along the entrance to Hudson Strait and through Davis Strait
along 70°N from Baffin Island to the west coast of Greenland; then through
the Denmark Strait from Cape Brewster on the east coast of Greenland to the
Reydinupyur Point on the west coast of Iceland and along the Icelandic northern coast to Gerpir Point on the east. From Iceland the demarcation line goes
to the Faroe Islands, passes north of Shetland Islands and then along 61°N to
the Norwegian coast. The border of Arctic and Pacific Oceans passes through
the Bering Strait from Cape Dezhnev to Cape Prince of Wales.
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GENERAL MORPHOLOGY
The description of serpulid morphology (including that of spirorbins) below is more detailed than one would need to identify only Arctic serpulids.
However, this additional information may be useful for understanding of terminology used in other papers on serpulid taxonomy. The most comprehensive review of the serpulid morphology (excluding spirorbins) accompanied
by numerous illustrations (ten Hove, Kupriyanova 2009).
Tubes. Serpulid tubes are composed of crystalline calcium carbonate (calcite, aragonite, or both) interspersed with a mucopolysaccharide matrix. The
adult tube is secreted by glands located on the collar and tube additions are
molded by the collar folds when the worm is in the feeding position. Tubes
are usually chalky (opaque) white with rough or more or less smooth surface
or white with smooth shining (porcellaneous) surface; rarely tubes may be
completely or partially semitransparent because of the thin wall. Completely
transparent tubes are termed vitreous.
Although tubes are mostly white, they may be completely or partly pink,
bluish, orange purple, mustard, or even white with dark-brown transverse stripes.
In spirorbins with vitreous tubes the inner tube lining or body of live specimens
may be visible through tube walls, thus making the tubes appear coloured.
Spirorbins live in small spiral (hence the name) tubes 1.5–4 (up to 8) mm
in coil diameter. Normally the spirals are flat, but the distal parts may be
uncoiled and raised above the substrate, whorls being positioned on top of
each other or attached to the substrate, not forming a spiral. Spirorbin tubes
may be coiled clockwise (sinistral) or counter clockwise (dextral). Most species show only one coiling direction, but tubes of some Spirorbis coil in either
direction. Rarely, some Circeini and Januini (most of which are dextral) have
specimens with opposite coiling directions. Dextral forms have never been
recorded for typically sinistral species.
In other serpulids the tube shape is variable and coiling, when present, is
irregular. Most tubes are attached by at least the proximal older parts and
some tubes are attached to the substrate throughout their entire length. Notable exceptions are the free-living Ditrupa (one species is known from the
Arctic) and some deep-sea taxa.
Serpulid tubes are usually circular or sub-circular in external cross-section. Longitudinal keels usually do not change the tube cross-section, but
some species may have triangular, quadrangular, pentangular or even
octangular cross-sections. Within a single tube changes may occur from trapezoidal to multiangular or from triangular respectively trapezoidal/semi-circular to circular.
The external ornamentation (sculpture) of the tube surface typically consists of longitudinal and transverse elements. A single major prominent keel
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(often termed longitudinal ridge in spirorbins) or several identical keels may
be present.  The major keel may be supplemented by secondary ones. The
keels may either be sharp or smooth, high or low, straight or wavy, or in the
form of longitudinal rows of denticles.
Transverse tube ornamentation in spirorbins may be presented by growth
lines (transverse striations) or rarely by transverse ridges (e.g., see KnightJones E.W. et al., 1974, fig. 2d; Knight-Jones P. et al., 1979, fig. 7B(a)). In
non-spirorbins transverse sculpturing includes subtle growth striations, more
distinct incomplete ridges or complete circular growth rings, and large flaring
anteriorly directed peristomes that might be smooth or denticulate.
A combination of numerous longitudinal keels and transverse ridges may
form characteristic honey-comb structures as e.g., in Metavermilia arctica
Kupriyanova, 1993d. Sculpturing may differ between the free distal and attached proximal parts of a tube. Tube surface may also be completely or partially pitted by numerous alveoli, that may completely perforate tube keels in
Neodexiospira spp. Tabulae or transverse tube elements may partition the
oldest parts of the tube as response to tube damage in some serpulids (e.g.,
Spirobranchus). Attached parts of the tubes often form flattened peripheral
flanges and may also contain alveolar structures.
Genera such as Salmacina and Filograna (formerly Filograninae) build
characteristic aggregations (often incorrectly termed colonies) made of numerous branching tubes. These aggregations are a result of both asexual budding and gregarious larval settlement; they are different from the aggregations resulting from gregarious larval settlement only.
Morphological structures used for embryo incubation. All spirorbins
have lecithotrophic larvae and incubate their embryos either inside their tubes
or in opercular brood chambers. The methods of embryo brooding have been
used to subdivide spirorbins into 6 subfamilies (now tribes).
Tube brooding: 1) Embryos positioned freely in the abdominal faecal
groove – Paralaeospirini (Fig. 1A); 2) Embryo positioned in a sac fixed to the
thorax or to the abdomen by an epithelial stalk – Romanchellini (Fig. 1B); 3)
Embryos adhering to each other and directly to the internal tube wall – Circeini
(Fig. 1C); 4) Embryo string attached posteriorly to the internal tube wall by a
filament – Spirorbini (Fig. 1D). Opercular brooding: 1) Embryos brooded in
the re-usable brood chamber formed by invagination of the operculum –
Pileolariini (Fig. 1E); 2) Embryos brooded in a cuticular brood chamber formed
outside the distal part of the operculum, a new chamber is formed for each
brood – Januini (Fig. 1F-G). Only the species of the Spirorbini, Circeini,
Pileolariini and Januini are found in the Arctic.
While many non-spirorbin serpulids are free-spawners with feeding larvae, some brood embryos inside the tube (e. g., Filograna), in various tube
ovicells (Chitinopoma), inside the radiolar crown, in pockets of the thoracic
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Figure 1. Embryo incubation in Spirorbinae. À – Paralaeospirini; B –
Romanchellini; C – Circeini; D – Spirorbini; E – Pileolariini; F, G – Januini. A –
from Knight-Jones P., Walker (1972), B-E from Knight-Jones P., Vine (1972), F,
G – from Okuda, 1934.
membranes, and in a gelatinous mass near the tube mouth (Protula), etc. (see
Kupriyanova et al. (2001) for details).
Body. The body of non-spirorbin serpulids is bilaterally symmetrical even
in animals that live in spirally coiled tubes. The thorax bears notopodial chaetae (dorsally) and neuropodial uncini (ventrally), whereas in the abdomen
the position of chaetae and uncini is reversed, that is, the abdomen appears to
be turned 180° relative to the thorax. Unlike torsion of molluscs, this chaetal
inversion does not affect internal organs of the animal; it only affects the
insertion of the chaetae. Both thorax and abdomen are facing the substrate by
the dorsal side (bearing notochaetae in thorax and uncini in abdomen). Spirorbin
bodies are always asymmetrical and curved in the direction of the tube’s coil;
their abdomen is turned by approximately 90° relative to the thorax (e.g., see
Knight-Jones P., Fordy, 1979, fig. 1, 3). The thoracic region of spirorbins is
turned to the substrate by the dorsal side (bearing notochaetae), while the
abdomen faces the substrate laterally. Therefore, it is impossible to use such
common terms as “dorsal” and “ventral”, “right side” and “left side” for
spirorbin morphology. Instead, the terms “facing the substrate” and “facing
away from substrate”, “convex side” and “concave side” are used.
9

Body colour. Serpulids are often very brightly coloured (red, pink, orange, brown, blue, greenish, yellow, or flesh-coloured). However, the
colouration is of taxonomic little value because colour fades in preservatives,
particular in alcohol, and may also be a subject to significant interspecific
variability. The only exception is the genus Spirorbis where body colour is
used as a taxonomic character.
In some Pileolariini, the posterior part of thorax and achaetigerous zone
on the side facing the substrate has iridescent crystalline red, pink, purple
patches that normally maintain their colour after fixation, although sometimes change to dark brown or almost black. These patches are likely not
epithelial pigments but a secretion of some glands; they are located on top of
the epithelium and can be easily removed by a preparation needle.
The radiolar crown. The crown, used for feeding and respiration, with
each radiole bearing rows of paired ciliated pinnules, is a distinct feature of
serpulids. The radioles are attached to paired lobes located laterally on both
sides of the mouth. The bases of the radioles in some serpulids are joined by
an inter-radiolar membrane. Such a membrane is always absent in spirorbins.
In all spirorbins and most small remaining serpulids, radioles are arranged in
two semi-circles when in feeding position outside the tube. Spiralled radiolar
arrangement occurs when the ventral margins of the radiolar lobe continue to
grow, adding radioles and spiralling along the inner margin of the crown. In
some large serpulids, especially in the large species of the genus Spirobranchus,
the crown is a pair of beautiful spiralled cones.
Operculum. A modification of the distal part of a radiole, the operculum,
serving as a tube plug, is present in most serpulids and always in spirorbins.
Some serpulid taxa are non-operculate, (e.g., Protula), although normally
operculate genera may include non-operculate species (e.g., Spirobranchus)
and normally non-operculate genera may include operculate species (e.g.,
Protis). The opercular structure has been considered one of the most important taxonomic characters.
In non-spirorbin serpulids and all tube-brooding spirorbins, opercular structure remains essentially the same throughout adult life. Opercular structure
varies from soft vesicular (e.g., Apomatus) or spoon-shaped (e.g., Filograna)
to very elaborate. The operculum mostly consists of a basal bulbous part (ampulla) and a distal part often reinforced with chitinous endplate. The chitinous endplates may be additionally reinforced by calcareous deposits, sometimes with non-movable spines (e.g., Spirobranchus). In the genus
Metavermilia a range of opercular shapes is found, from a soft spherical to a
complex multi-tiered chitinous structure. The funnel-shaped opercula of
Hydroides and Serpula are composed of numerous radii and covered with a
thickened cuticle. While the operculum in species of Serpula is a simple funnel, it is armed with a distal verticil of chitinous spines in Hydroides.
10