Swima (Annelida, Acrocirridae), holopelagic worms
from the deep Pacificzoj_727 663..678
KAREN J. OSBORN1*, STEVEN H. D. HADDOCK2 and GREG W. ROUSE1
1Scripps Institution of Oceanography, 9500 Gilman Drive, La Jolla, CA 92093-0202, USA
2Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039, USA
Received 16 September 2010; revised 3 December 2010; accepted for publication 16 December 2010
Two new species of Swima, a recently established genus of annelid worms, are introduced, one from deep water
off the North American West Coast and the other from the Philippines. The acrocirrid genus now contains three
named species, Swima bombiviridis, Swima fulgida sp. nov., and Swima tawitawiensis sp. nov. Swima are
holopelagic, occurring only in the water column, and thus far have only been observed below 2700 m. The worms
are relatively large, sometimes reaching over 30 mm in length and 5 mm in width. They have gelatinous bodies and
fans of long swimming chaetae, which are flattened into paddles in S. tawitawiensis sp. nov. Members of Swima
are distinguished from other swimming acrocirrids by their transparent bodies, single medial subulate branchiae,
and simple nuchal organs that do not skirt the bases of lateral subulate branchiae. Swima fulgida sp. nov. is
distinguished from other members of the genus by its darkly pigmented anterior gut, whereas S. tawitawiensis
sp. nov. is distinguished by possessing three subulate head appendages instead of just one and by the shape of
its noto- and neurochaetae. Swima species possess four pairs of elliptical, transformed segmental branchiae that
produce green bioluminescence when autotomized. These ‘bombs’ were observed in various states of regeneration
on a single individual. Swima are neutrally buoyant, often observed hanging immobile in the water column, and
are active, agile swimmers. Although not previously documented in the literature, these worms are not rare in the
deep water column. Since the worms were first noticed in 2001, they have been observed on more than half of the
Monterey Bay Aquarium Research Institute’s midwater remotely operated vehicle dives that went to sufficient
depth. The discovery of Swima underscores our lack of knowledge of deep pelagic fauna.
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678.
doi: 10.1111/j.1096-3642.2011.00727.x
ADDITIONAL KEYWORDS: Celebes Sea – Cirratuliformia – deep-sea – gelata – midwater – pelagic –
Swima bombiviridis – Swima fulgida sp. nov. – Swima tawitawiensis sp. nov.
INTRODUCTION
Increased access to deep water with research sub-
mersibles has enabled advances in our understanding
of deep-sea animal physiology and behaviour, as well
as new appreciation for the importance of gelatinous
animals in pelagic communities (Robison, Sherlock &
Reisenbichler, 2010). Direct observations have led to
the discovery of many previously unknown species
that were for so long missed because they were too
delicate to be successfully collected by nets or because
they could actively avoid capture (Haddock, 2004).
Use of submersibles allowed the recent discovery of
seven spectacular new species of swimming annelids
(Osborn et al., 2009).
The recently discovered swimming worms shared
features with both Flabelligeridae and Acrocirridae,
which are sister groups (Rouse & Fauchald, 1997;
Rouse & Pleijel, 2003; Osborn & Rouse, 2010). Under-
standing of the relationships amongst acrocirrids and
flabelligerids is still developing, with several efforts to
*Corresponding author. Current address: Department of
Invertebrate Zoology, National Museum of Natural History,
Smithsonian Institution, Washington D.C. 20052, USA.
E-mail: osbornk@si.edu
Zoological Journal of the Linnean Society, 2011, 163, 663–678. With 6 figures
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678 663
assess their evolutionary history (Rouse & Pleijel,
2003; Rousset et al., 2007; Osborn & Rouse, 2008;
Salazar-Vallejo, Carrera-Parra & Fauchald, 2008;
Osborn et al., 2009). Thus placement of the new species
required a phylogenetic study of Cirratuliformia,
focused primarily on Flabelligeridae and Acrocirridae
(Fig. 1; Osborn & Rouse, 2010). That study found that
all seven recently discovered swimming species formed
a clade (referred to hereafter as the ‘swimming clade’)
with Helmetophorus Hartman, 1978 and Chauvinelia
Laubier, 1974 and that clade belonged in Acrocirridae.
With the addition of Swima Osborn et al., 2009 and
Teuthidodrilus Osborn, Madin & Rouse, 2010, Acrocir-
ridae now probably consists of eight genera with just
over 40 known species whose members are primarily
small, thin benthic worms. The majority of the known
acrocirrids were collected from the seafloor, yet even
before the discovery of the seven swimming species
there was reason to believe certain acrocirrids could
swim.Helmetophorus rankiniHartman, 1978 and both
species of Chauvinelia Laubier, 1974, have long
chaetae, relatively fragile bodies, and were thought to
be demersal (capable of swimming up off the seafloor at
times; Hartman, 1978; Averincev, 1980; Kirkegaard,
1982). Additionally, the long capillary chaetae some-
times found in Acrocirrus are referred to as ‘swimming’
chaetae (Banse, 1969), although their ability to swim,
like that of Chauvinelia and Helmetophorus, is
unconfirmed. It is possible that some of these records
represent epitokous forms that transform for reproduc-
tive purposes.
The description of Swima bombiviridis Osborn
et al., 2009 (Fig. 2) and Teuthidodrilus samae Osborn
et al., 2010 confirmed the presence of holopelagic
species within Acrocirridae (Fig. 1) and provided the
third confirmed evolutionary origin of pelagicism
within Cirratuliformia (Poeobius, Burnette, Struck &
Halanych, 2005; Flota/Buskiella, Osborn & Rouse,
2008; Swima, Osborn et al., 2009). Here we describe
the two species most closely related to the type
species of Swima, S. bombiviridis, and restrict the
genus to these three species based on morphological
and molecular data. We also provide further informa-
tion on S. bombiviridis and notes on behaviour and
ecology of Swima.
MATERIAL AND METHODS
COLLECTIONS
Three specimens of Swima fulgida sp. nov. were
collected from deep water off central California over
the period 2004 to 2009 (Table 1). All in situ observa-
tions were made with the Monterey Bay Aquarium
Research Institute’s (MBARI’s) deep-diving remotely
operate vehicles (ROVs) Tiburon and Doc Ricketts,
which were equipped with a Panasonic high resolu-
tion, three-chip camera or an Ikegami HDL-40
camera attached to a Fujinon BERD HA 10 ¥ 5.2 lens.
Video was recorded on high-quality BetaCam and
high definition television tapes for subsequent analy-
sis, and these are housed in the video archive at
MBARI. Specimens were captured in 7.5 L detritus
samplers or with the high-flow suction sampler
(Robison, 1992). Both methods greatly reduce the
abrasion and crushing typical of collection in nets,
and also provide a way to collect the organism and its
surrounding water undisturbed. The relatively large
amount of native water collected with each organism
additionally serves to insulate the organism against
changes in water temperature and chemistry during
the trip to the surface. Upon recovery from such great
depth, animals were mostly unresponsive unless
pinched with forceps or when initially placed in isoos-
motic magnesium chloride. Specimens were photo-
graphed with a Nikon Coolpix 5000 as macro shots or
through a Nikon dissecting scope, prior to fixation.
Specimens were further imaged in the lab using a
Canon G9 fitted on a Leica MZ8 stereomicroscope.
Some parapodia were removed from specimens and
examination via differential interference contrast
on a Leica DMR compound microscope with a Nikon
Coolpix 4300. Parapodia were then prepared for scan-
ning electron microscope imaging by transfer through
buffer and fresh water rinses and an ethanol dehy-
dration series before air drying and mounting.
Chaetae were viewed with an FEI Quanta 600 scan-
ning electron microscope.
Figure 1. Ninety-five per cent majority rule consensus
tree from Bayesian analyses of five concatenated genes
[18S, 28S, 16S, cytochrome oxidase I (COI) and cyto-
chrome b (cytb)] from cirratuliform annelids, showing
Swima as part of Acrocirridae (Osborn & Rouse, 2010).
Support indicated as posterior probabilities,
bootstraps from the maximum likelihood analysis and
from the parsimony analysis. Asterisks indicate 1.0 or
100% support.
664 K. J. OSBORN ET AL.
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
T
ab
le
1.
Sp
ec
im
en
,
co
lle
ct
io
n,
an
d
ac
ce
ss
io
n
nu
m
be
rs
.A
ll
ar
e
ho
lo
ge
no
ph
or
es
(P
le
ije
l
et
al
.,
20
08
)
vo
uc
he
r
ac
ce
ss
io
n
an
d
ty
pe
de
si
gn
at
io
n
(m
ol
ec
ul
ar
ID
no
.)
C
ol
le
ct
io
n
da
te
L
oc
al
it
y
C
ol
le
ct
io
n
de
pt
h
(m
)
18
S
28
S
16
S
C
O
I
C
yt
b
F
ix
at
iv
e
S
w
im
a
bo
m
bi
vi
ri
di
s
SI
O
B
IC
A
12
82
ho
lo
ty
pe
(P
B
51
)
7.
iv
.0
5
36
°1
9.
80
′N
,
12
2°
53
.9
9′
W
30
54
G
Q
42
21
43
G
Q
42
21
44
F
J9
44
50
6
F
J9
44
52
7
F
J9
44
54
0
G
lu
ta
ra
ld
eh
yd
e
SI
O
B
IC
A
12
81
pa
ra
ty
pe
(P
B
44
)
5.
vi
.0
5
36
°4
3.
98
′N
,
12
3°
41
.9
3′
W
37
44
F
J9
44
49
3
F
J9
44
51
6
F
J9
44
50
5
F
J9
44
52
6
F
J9
44
53
9
G
lu
ta
ra
ld
eh
yd
e
n/
a
(P
B
39
)
22
.ii
i.0
5
36
°1
9.
80
′N
,
12
2°
53
.9
9′
W
31
87
F
J9
44
49
5
–
F
J9
44
50
8
F
J9
44
52
9
F
J9
44
54
2
n/
a
SI
O
B
IC
A
12
83
pa
ra
ty
pe
(P
9)
28
.x
i.0
7
35
°5
0.
42
′N
,
12
2°
40
.1
3′
W
30
19
F
J9
44
49
4
F
J9
44
51
7
F
J9
44
50
7
F
J9
44
52
8
F
J9
44
54
1
G
lu
ta
ra
ld
eh
yd
e
SI
O
B
IC
A
12
84
pa
ra
ty
pe
(P
B
42
)
5.
vi
.0
5
36
°4
3.
98
′N
,
12
3°
41
.9
3′
W
37
44
F
J9
44
49
6
F
J9
44
51
8
F
J9
44
50
9
F
J9
44
53
0
F
J9
44
54
3
G
lu
ta
ra
ld
eh
yd
e
SI
O
B
IC
A
16
34
pa
ra
ty
pe
(P
31
)
21
.ix
.0
5
36
°1
9.
80
′N
,
12
2°
53
.9
9′
W
34
42
–
–
–
G
Q
33
86
64
–
F
or
m
al
in
SI
O
B
IC
A
16
35
pa
ra
ty
pe
(P
26
)
20
.ix
.0
5
36
°1
9.
80
′N
,
12
2°
53
.9
9′
W
33
25
–
–
–
G
Q
33
86
62
–
95
%
et
ha
no
l
SI
O
B
IC
A
16
36
pa
ra
ty
pe
(P
30
)
2.
x.
06
35
°3
7.
99
′N
,
12
2°
44
.0
0′
W
27
32
–
–
–
G
Q
33
86
66
–
G
lu
ta
ra
ld
eh
yd
e
SI
O
B
IC
A
16
37
pa
ra
ty
pe
(P
25
)
2.
xi
.0
7
36
°1
9.
39
′N
,
12
2°
54
.1
8′
W
34
11
–
–
–
G
Q
33
86
67
–
95
%
et
ha
no
l
SI
O
B
IC
A
16
38
pa
ra
ty
pe
(P
28
)
26
.ii
.0
9
35
°0
7.
61
′N
,
12
2°
55
.6
0′
W
36
00
–
–
–
G
Q
33
86
65
–
95
%
et
ha
no
l
n/
a
(P
23
)
22
.v
i.0
6
36
°2
0.
08
′N
,
12
2°
55
.0
0′
W
33
33
–
–
–
G
Q
33
86
68
–
n/
a
n/
a
(P
24
)
23
.v
i.0
6
36
°2
0.
08
′N
,
12
2°
55
.0
0′
W
32
47
–
–
–
G
Q
33
86
63
–
n/
a
SI
O
B
IC
A
16
76
pa
ra
ty
pe
(P
27
)
26
.ii
.0
9
35
°0
7.
61
′N
,
12
2°
55
.6
0′
W
36
00
–
–
–
G
Q
33
86
61
–
95
%
et
ha
no
l
S
w
im
a
fu
lg
id
a
sp
.
n
ov
.
SI
O
B
IC
A
12
85
ho
lo
ty
pe
(P
B
32
)
7.
x.
04
35
°4
6.
38
′N
,
12
2°
50
.2
4′
W
32
67
F
J9
44
49
7
–
–
F
J9
44
53
1
F
J9
44
54
4
G
lu
ta
ra
ld
eh
yd
e
SI
O
B
IC
A
12
86
pa
ra
ty
pe
1
(P
1)
22
.v
i.0
6
36
°2
0.
08
′N
,
12
2°
55
.0
0′
W
34
78
F
J9
44
49
8
F
J9
44
51
9
F
J9
44
51
0
F
J9
44
53
2
F
J9
44
54
5
G
lu
ta
ra
ld
eh
yd
e
SI
O
B
IC
A
16
75
pa
ra
ty
pe
2
(P
29
)
26
.ii
.0
9
35
°0
7.
61
′N
,
12
2°
55
.6
0′
W
36
25
–
–
–
G
Q
33
86
60
–
95
%
et
ha
no
l
S
w
im
a
ta
w
it
a
w
ie
n
si
s
sp
.
n
ov
.
N
M
A
04
37
ho
lo
ty
pe
(P
13
)
6.
x.
07
4°
58
.0
0′
N
,
12
0°
14
.6
1′
E
28
36
F
J9
44
49
9
F
J9
44
52
0
F
J9
44
51
1
F
J9
44
53
3
F
J9
44
54
6
F
or
m
al
in
G
en
B
an
k
nu
m
be
rs
in
bo
ld
in
di
ca
te
pr
ev
io
us
ly
un
pu
bl
is
he
d
se
qu
en
ce
s.
F
ix
at
io
n
m
et
ho
ds
ar
e
in
di
ca
te
d
fo
r
th
e
an
te
ri
or
po
rt
io
n
of
ea
ch
ty
pe
sp
ec
im
en
.
P
os
te
ri
or
ti
ss
ue
cl
ip
s
w
er
e
fr
oz
en
in
liq
ui
d
ni
tr
og
en
or
fix
ed
an
d
pr
es
er
ve
d
in
95
%
ch
ill
ed
et
ha
no
l
th
en
us
ed
fo
r
ge
no
m
ic
D
N
A
ex
tr
ac
ti
on
C
O
I,
cy
to
ch
ro
m
e
ox
id
as
e
I;
C
yt
b,
cy
to
ch
ro
m
e
b;
n/
a,
no
t
ap
pl
ic
ab
le
.
SWIMA, HOLOPELAGIC ACROCIRRIDS 665
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
666 K. J. OSBORN ET AL.
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
The only specimen of Swima tawitawiensis sp. nov.
was observed and collected from the deep water
column of the Celebes Sea in October of 2007 by the
ROV Max Rover Global Explorer operated off the
Research Vessel Hydrographer Presbitero. The speci-
men was damaged during collection but retained
characters sufficient to distinguish the specimen from
its congeners.
Specimens of Swima were recovered in varying
conditions and preserved using several methods
(70 or 95% ethanol, 2% sodium cacodylate buffered
glutaraldehyde, 4–20% formalin, or frozen in liquid
nitrogen).
DNA SEQUENCING
Specimens of both S. fulgida sp. nov. and S. bom-
biviridis have variable morphology with respect to
head appendages, presence of gametes and gonopores,
visibility of branchial scars, possession of digitiform
branchiae, buccal organ morphology, and general
body form; thus, as many specimens as possible were
sequenced for a fragment of the mitochondrial cyto-
chrome oxidase I (COI) gene to determine if there
were one or multiple species present. Genomic DNA
was extracted from specimens using a Qiagen DNeasy
tissue kit (Valencia, CA, USA). Approximately 650
base pairs of the mitochondrial COI gene were ampli-
fied using universal primers HCO2198 and LCO1490
(Folmer et al., 1994). Twenty-five-microlitre reactions
were carried out using either Illustra PuReTaq
Ready-To-Go PCR beads (GE Healthcare, Uppsala,
Sweden) or Promega GoTaq Green (Madison, WI,
USA). Amplification profile: five cycles of 94 °C for
30 s, 45 °C for 90 s, 72 °C for 60 s, 30 cycles of 94 °C
for 30 s, 51 °C for 90 s, 72 °C for 60 s, initial denatur-
ation at 94 °C for 60 s and final extension at 72 °C for
5 min.
PCR products were sequenced directly after spin
column purification (Ultrafree-DA columns, Millipore,
Billerica, MA, USA) following the manufacturer’s pro-
tocols. All sequencing was carried out using the same
primers that were used in the amplification. Sequenc-
ing was carried out by Advanced Studies in Genomics,
Proteomics and Bioinformatics at the University
of Hawaii at Manoa using Applied Biosystems
BigDye terminator chemistry and an ABI 3730XL
sequencer. Sequences have been deposited in
GenBank (Table 1).
PHYLOGENETIC ANALYSES
Sequences were aligned with MUSCLE 3.6 (Edgar,
2004) using default settings and proof-read by eye
in MacClade v.4.04 OS X (Maddison & Maddison,
2000). Third codon positions were not removed from
analyses because no evidence of saturation was
found with COI following the Xia et al. (2003)
test implemented in DAMBE (Xia and Xie, 2001).
Flabelligeridae were used as the outgroup for
this analysis examining the relationships within
Acrocirridae because they are the sister group of the
Acrocirridae (Rouse & Fauchald, 1997; Rouse &
Pleijel, 2003; Osborn & Rouse, 2010). The complete
alignment is available from K. J. O. or at TreeBase
(http://www.treebase.org/treebase-web/home.html).
Bayesian analyses of the data sets were conducted
using MrBayes 3.1.2 (Huelsenbeck & Ronquist, 2001).
Standard procedures based on MODELTEST 3.5
(Posada & Crandall, 1998) were implemented in
PAUP* 4.0b10 to select the most appropriate model.
The relative fit of models was assessed by the Akaike
information criterion (AIC). Smaller values of AIC
are preferred (Akaike, 1974; Posada & Crandall,
2001) and the general time reversible + proportion
invariant + gamma (GTR+I + G) represented the
optimal model. Partitions were unlinked in all analy-
ses. Each Markov chain, three heated and one cold,
was started from a random tree and all four chains
were run simultaneously for five to 60 million gen-
erations, with trees being sampled such that the
resulting data set from each run contained at least
10 000 data points after burn-in. AWTY (Wilgen-
busch, Warren & Swofford, 2004) was used to deter-
mine if a sufficient number of generations had been
completed for posterior probabilities to stabilize, as
Figure 2. Compilation of figures reproduced with permission from description of Swima bombiviridis (Osborn et al.,
2009) with the addition of C. Images A, B, and D taken from live animals. A, ventral view of holotype anterior with inset
detailing elliptical branchiae scars, digitiform branchiae, and nephridiopore papillus. B, dorsal view of paratype, showing
grooved palps, chaetal fans, at least six attached ‘bombs’, transparent body with gut and gonads visible through body wall,
gelatinous sheath, and yellow, clavate papillae projecting through the gelatinous sheath. Photo credit, © Casey Dunn
2007. C, illustration of A showing location of features: lollipop-shaped papillae (lp), gonopores (gp), gonads (g), digitiform
branchiae (db), medial subulate branchia (sb), and nephridia (n), nephridiopore papillus (np), and elliptical branchiae
scars (1–4 inset). D, ventral view of posterior end showing interramal lollipop-shaped papillae and posterior gut loops. E,
parapodium showing notochaetae on right and neurochaetae on left, two interramal lollipop-shaped papillae, and
fragments of the gelatinous sheath. F, light micrograph of distal portion of a chaeta. G, scanning electron micrograph of
shaft of a chaeta. H, scanning electron micrograph of distal tip of a chaeta. Scale bars: A = 4 mm, G and H = 2 mm.
!
SWIMA, HOLOPELAGIC ACROCIRRIDS 667
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
well as to determine the amount of required burn-in
before inference from the Markov chain Monte Carlo
(MCMC) data set was made. Repeated analyses con-
verged on similar parameter estimates.
RESULTS AND DISCUSSION
The swimming clade (Fig. 1) contains acrocirrids with
six distinct morphologies (Swima, Helmetophorus,
Chauvinelia, horned/Tiburon bombers, Teuthidodri-
lus, and Juanita worm). Distinctiveness of each
morphology-based group (Swima, Teuthidodrilus,
horned/Tiburon bombers, and Juanita worm were
available for molecular analyses) was also observed in
sequence data. A well-supported group of three
species was recovered within the more inclusive clade
originally designated as Swima (Osborn et al., 2009).
This less inclusive clade (Swima sensu stricto) con-
tained the type species, S. bombiviridis, and two
other morphologically similar species, which are
described here. Swima is here restricted to S. bom-
biviridis, S. fulgida sp. nov., and S. tawitawiensis sp.
nov., which formed a well-supported clade in all
molecular analyses (Figs 1, 3). Their transparent
body, thick gelatinous sheath, the form of their nuchal
organs as a simple ridge with no more than a
single 180° bend, small ‘bombs’ (elliptical branchiae,
largest less than half width of body), and possession
of a medial subulate branchia distinguish them
from all known acrocirrids, including the as-yet-
undescribed demersal species (Osborn & Rouse,
2010).
Swima s.s. differed from other sequenced acrocir-
rids by 16–25% uncorrected pairwise COI distance
(18S 0.7–18%, 28S 3–13%, 16S 11–36%, and cyto-
chrome b (cytb) 16–30%; see Osborn & Rouse, 2010,
for all additional sequencing protocols) and flabel-
ligerids by 18–30% uncorrected pairwise COI distance
(18S 11–20%, 28S 15–36%, 16S 23–36%, and cytb
25–33%). Swima bombiviridis, S. fulgida sp. nov., and
S. tawitawiensis sp. nov. differed from each other by
14–16% uncorrected pairwise COI distance, from the
other members of the swimming clade by 17–22%,
and from other acrocirrids by 19–23%. Within-species
distances were less than 3% for COI. Six unique
haplotypes were present amongst the 13 specimens of
S. bombiviridis sequenced for COI with a single hap-
lotype being dominant (7 of 13 specimens). Each of
the three specimens of S. fulgida sp. nov. had a
unique COI haplotype.
Figure 3. Ninety per cent majority rule consensus cytochrome oxidase I (COI) gene tree from Bayesian analyses of
cirratuliform annelids, showing Swima as part of Acrocirridae and support for Swima monophyly. Unsupported branches
were collapsed. Support indicated as posterior probabilities. Asterisks indicate 1.0 or 100% support.
668 K. J. OSBORN ET AL.
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
SYSTEMATICS
SWIMA OSBORN ET AL., 2009
Type species: Swima bombiviridis Osborn et al., 2009
Diagnosis (emended): Swimming acrocirrids with
thick gelatinous sheath penetrated throughout by
long, clavate papillae. Body transparent. One or more
lollipop-shaped, inter-ramal papillae projecting well
beyond gelatinous sheath. With more than 30 long
(more than body width) chaetae per parapodium.
Eyes absent. Head not retractable. Nuchal organs
just posterior to palps as simple, slightly raised cili-
ated ridges making no more than single 180° bend,
not curving around bases of subulate branchiae.
Possessing single, medial subulate branchia either
individually or as part of a single row of subulate
branchiae immediately posterior to palps and anterior
to segmental branchiae, not easily lost. Sometimes
with single row of more than 30 digitiform branchiae
just posterior to subulate branchiae. Nephridiopores
as papillae on second achaetous segment. Four pairs
of segmental branchiae modified as ellipsoid, biolumi-
nescent structures, the second of which is attached to
basal portion of nephridiopore papillae. Segmental
branchiae small (largest less than half width widest
body), easily lost, leaving obvious circular scars.
Remarks: Photos for the type species (S. bombiviridis,
Fig. 2) are reproduced from Osborn et al. (2009:
supplement), with permission, to represent the char-
acters of the genus and for comparison to the species
described here. Swima shares the following features
with other Acrocirridae: several achaetous anterior
segments (Figs 2A, C, 4E, 5B, 6E), shape of prosto-
mium, presence of nephridiopores near second bran-
chiae (Figs 2C, 5B, 6F), gonads in three or fewer
anterior segments (Figs 2C, 4E, 5A, 6G), four pairs or
fewer of branchiae that are easily lost, and simple,
spinous notochaetae (Figs 2E–H, 4G–H, 5F–H, 6B).
Swima differs from Macrochaeta Grube, 1850, Acro-
cirrus Grube, 1873, Flabelligella Hartman, 1965, and
Flabelligena Gillet, 2001 in general body form
(Fig. 2A), the absence of eyes, and presence of more
than 30 chaetae per parapodium (Figs 2E, 4A, 6C).
Swima differs from Flabelliseta incrusta Hartman,
1978 in the shape of the notopodial papillae, by pos-
sessing notochaetae, and by not adhering sediment
particles to their gelatinous sheath. Swima is similar
to Helmetophorus rankini Hartman, 1978 and Chau-
vinelia (consisting of Chauvinelia biscayensis Laubier,
1974 and Chauvinelia arctica Averincev, 1980),
sharing with them the nature of their buccal
organ and possibly the ability to swim, although the
latter is unconfirmed in Chauvinelia and Helmetopho-
rus. Members of Swima differ from members of
Helmetophorus and Chauvinelia by lacking a cephalic
hood and elongate achaetous anterior segments, pos-
sessing a medial subulate branchia, having simple,
not convoluted nuchal organs, and in general body
size. Swima and Chauvinelia further differ from Hel-
metophorus by possessing lollipop-shaped interramal
papillae (Figs 2D, 4C) and more than 30 chaetae per
parapodium. Although the papillae drawn by Glasby
& Fauchald (1991) from the types suggest Helmeto-
phorus’s interramal papillae are lollipop-shaped,
examination of the type material indicates that they
are not because they lack the extremely bulbous,
granular appearing, solid distal tips. Instead, Helme-
tophorus has flaccid, nongranular, moderately
bulbous distal tips on their clavate interramal
papillae.
Analysis of molecular sequences (Figs 1, 3) shows
that Swima forms a well-supported clade distinct
from all previously known acrocirrids and flabel-
ligerids available for these analyses. Helmetophorus,
Chauvinelia, Flabelliseta, and Flabelligella were
unavailable for genetic analyses, but as detailed
above, they are distinguishable from Swima based on
morphology. Helmetophorus and Chauvinelia are the
most likely of these missing taxa to form a clade with
Swima, but their morphology clearly distinguishes
them from Swima as outlined above.
SWIMA FULGIDA SP. NOV.
Green bomber sp. 1 (Osborn et al., 2009), shining
bomber (Osborn & Rouse, 2010).
Common name: Shining bomber
Type material: Holotype, collected off the central coast
of California 7.x.2004 at 3267 m over a bottom depth
of 3546 m by K. J. O. and S. H. D. H., deposited
at the Benthic Invertebrate Collection of Scripps
Institution of Oceanography (SIO BIC A1285;
35°46.38′N, 122°50.24′W). Two female paratypes
collected by K. J. O. (SIO BIC A1286, 22.vi.2006, at
3478 m, 36°20.08′N, 122°55.00′W, undetermined live
length; A1675, 26.ii.2009, at 3625 m, 35°7.61′N,
122°55.60′W, > 30 mm).
Diagnosis: Member of Swima with a darkly pigment
anterior gut and buccal organ. Possessing single,
subulate, medial branchia, thick, transparent gelati-
nous sheath penetrated throughout by narrow clavate
papillae, simple noto- and neurochaetae, and three
achaetous anterior segments supporting ellipsoid,
bioluminescence-producing, derived branchiae that
are less than 1.2 mm in length.
SWIMA, HOLOPELAGIC ACROCIRRIDS 669
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
670 K. J. OSBORN ET AL.
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
Etymology: Named for the shining or gleaming (fulgi-
dus) bioluminescence produced by the four pairs of
ellipsoid, segmental branchiae. Feminine.
Holotype description: Body transparent, 27 chaeti-
gers, 29 mm live body length, distinct parapodial
lobes, numerous long chaetae, posterior half smoothly
tapered, broadest segments after chaetiger 3
(Fig. 4A). Thick gelatinous sheath through which
narrow, clavate, yellow (in life) papillae, extend
(Fig. 4B). Papillae especially numerous on para-
podia and dorsum of anterior segments. Pygidium
unadorned.
Head consists of prostomium, peristomium, and
three achaetous segments possessing what is inter-
preted here as three forms of branchiae (Fig. 4B, E,
but see Variation). Prostomium limited to tissue
posterior to palps supporting a pair of low, ciliated,
oblique ridge-like nuchal organs (shown in paratype 1
Fig. 5C). No eyes. Grooved frontal peristomial palps
transparent to yellow in life, tapered, coiling tips,
long, reaching at least sixth chaetiger (Fig. 4A). Peris-
tomium surrounds prostomium completely. Buccal
organ anteroventrally located, unarmed, bilobed,
forming eversible lateral lips. Lateral lips with dark
pigment, purple-brown in life, inner lobe transparent
to purple-brown in life (Fig. 4B). Slight ridge found
posterior to nuchal organs (anterior to digitiform and
medial branchiae) possibly indicating a segment
margin (Fig. 4B). Three forms branchiae: (1) single,
long (reaches to fourth chaetiger), tapered/subulate,
medial projection interpreted here as branchia, trans-
parent to white (Fig. 4B) peristomial or on segment 1;
(2) more than 40, fine, digitiform respiratory bran-
chiae present across lateral and dorsal surface
segment 1 or 2 in tightly packed, single row, yellow in
life (Fig. 4B); and (3) three pairs elliptical lobe-like
branchiae on achaetous anterior segments (posterior
to all other forms branchiae) and one pair on chaeti-
ger 1 (referred to colloquially as ‘bombs’ because they
burst into light when dropped by animal; Fig. 4E, F).
Segmentally occurring, elliptical, lobe-like branchiae
greenish-yellow in life, autofluorescent, produce green
bioluminescence when detached, often autotomized,
0.7 to 1.1 mm in length (Fig. 4E). All elliptical bran-
chiae detached from holotype during collection,
examination, and/or storage. Scars from detached
elliptical branchiae distinguishable in live and pre-
served specimen as slightly raised rings thickened
tissue, four pairs: one slightly ventral from lateral
midline just posterior to digitiform branchiae, one
posterior on medial half of nephridiopore papillae, one
posterior to nephridiopore papillus at lateral midline,
one posterior to chaetae on first notopodium (shown
in paratype 1 Fig. 5B).
Chaetigers similar along body. Noto- and neuropo-
dial lobes form continuous, nearly smooth parapo-
dium (Fig. 4H) with more fine papillae relative to rest
of body surface. One to four, white to brown, clavate
papillae with rounded bulbous tips and narrow bases
(‘lollipop’-shaped) found between noto- and neuropo-
dial lobes, projecting well beyond gelatinous sheath,
tips solid (Fig. 4C). Noto- and neurochaetae indistin-
guishable except by position, simple, with no articu-
lations (Fig. 4D, G, shown in paratype 1 Fig. 5F).
High magnification reveals fine whorls of spines
making distal tips appear segmented (Fig. 4D, G,
shown in paratype 1 Fig. 5G), bases appear striated.
Distal edge of spinous whorls project as frayed edges
on worn and longest chaetae (Fig. 4D, shown in
paratype 1 Fig. 5H). Chaetigers 4–6 each with a pair
of gonopores, low, hollow papillae at ventral base of
neuropodia (Fig. 4E, F).
Internal anatomy visible through transparent body
wall and gelatinous sheath (Fig. 4A, shown in
paratypes Fig. 5A, D). Ventral nerve cord with two
paired, fused ganglia in each segment, diverge just
posterior to peristomium to surround buccal organ,
fused again just posterior to palp attachment points
(Fig. 4E, shown in paratypes Fig. 5A, D). Single pair
of large, anterior, semitransparent nephridia reaching
second chaetiger, largely lying in ventral part of
coelum, overlapping each other in ventral portions of
first and second chaetigers, folding back anterodor-
sally, then narrowing, with each nephridium leading
to a lateral nephridiopore (shown in paratype 2
Figure 4. Swima fulgida sp. nov. holotype. Images A, B and E taken of live animal. A, whole animal dorsal view (pins
holding animal down should not be confused with structures on the animal). B, dorsal view of anterior showing yellow
digitiform branchiae (db), palps (p), medial subulate branchia (sb), dark pigmented lateral lips of buccal organ, and body
papillae as small yellow dots on dorsum. C, ventral view of lollipop-shaped papillae on chaetigers 15 and 16. D, scanning
electron micrograph of distal tip of chaeta. E, ventral view of anterior showing the buccal organ, double ventral nerve cord,
three autotomized ‘bombs’ (green) and two attached (right side on first chaetiger, left side on one anterior segments and
one recently autotomized) and gonad in early development at the posterior margins of chaetigers 4 and 5. F, illustration
of image in E showing location of features. Abbreviations: b, bombs or elliptical branchiae; db, digitiform branchiae; g,
gonad; gp, gonopore; lp, lollipop-shaped papillae; np, nephridiopore papilla; p, palp; vn, ventral nerve cord. G, light
micrograph of tip of neurochaetae from seventh chaetiger, showing whorls of fine spines. H, seventh chaetiger, notochaetae
seen above and neurochaetae below. Scale bars: A = 4 mm, D = 10 mm, E = 1 mm.
!
SWIMA, HOLOPELAGIC ACROCIRRIDS 671
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
Fig. 5D–E). Gut running from buccal organ straight
for one-third body length (approximately to chaetiger
10) after which a wide, single loop is formed. Gut in
this loop portion broadens (to at least one quarter
body width) and continues back to approximately
chaetiger 20 before narrowing and turning anterior.
Gut continues anterior to near first loop then folds
rearward and continues directly to pygidium. Foregut
(region anterior to the first loop) darkly pigmented,
appearing black through body wall, expandable to
near body width (Fig. 4A, E, shown in Paratypes
Fig. 5A, D, E). Heart body and dorsal blood vessel
first distinguishable just posterior to digitiform bran-
chiae, extends through anterior one-third of body
until apparently merging with anterior-most dorsum
of broadened portion of gut (shown in paratype 2
Figure 5. Swima fulgida sp. nov. paratype 1 (A–C, F–H) and paratype 2 (D–E), images A, B, D taken from live
animals. A, ventral view, whole animal. Dark pigmented foregut and coils of orange midgut are visible through the
transparent body wall. B, dorsal view, anterior. C, illustration showing location of features visible in B. Grey arrows
indicate left elliptical branchiae scars; black arrow indicates right nuchal organ. The bases of the palps, the medial
subulate branchia (sb), nuchal organs, and nephridiopore papillus (np) are visible. D, ventral view, anterior. E, illustration
showing location of features visible in C. Developing gonads indicated by arrows; posterior fold of the left nephridia (n),
and dorsal blood vessel (bv) visible. F, light micrograph of notochaetae, stitched compilation of four images. G, light
micrograph of shaft of chaeta. H, scanning electron micrograph of shaft of chaeta. Scale bars: A = 5 mm, D = 1 mm,
F = 0.4 mm, H = 10 mm.
672 K. J. OSBORN ET AL.
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
Fig. 5D, E). Gonads form at posterior margin of cha-
etigers 4–6 (shown in paratype 2 Fig. 5D, E).
Variation: The two paratypes had 27 and more than
28 chaetigers (specimen incomplete), respectively.
Each was more than 30 mm total body length when
alive. Swima are particularly prone to distortion
when injured and to preservation artefacts. If speci-
mens were not completely relaxed prior to fixation,
they contracted dramatically during initial fixation.
Additionally, when specimens were injured they often
contracted around the injury site. The degree of
buccal organ lateral lobe eversion varied amongst
preserved specimens.
Palps were easily dislodged from specimens during
handling leaving obvious scars. Palps varied in length
relative to body length. The length of the single,
medial branchia also varied in length relative to
body length. Digitiform branchiae were not easily
lost from the holotype and left obvious scars when
they were. Digitiform branchiae were absent from
both paratypes genetically confirmed to belong to the
species. Elliptical branchiae were easily autotomized,
even during the gentlest collection, and were often
found on the floor of the sampling device upon recov-
ery of the ROV or were detached during laboratory
examination. As no specimens were recovered with all
elliptical branchiae attached, it was not possible to
determine if more than one pair can be attached to a
single segment at one time, but this seems unlikely
based on the scars. Various sized elliptical branchiae,
ranging from 0.6–1.2 mm in longest dimension,
were found on a single individual. Smaller ‘bombs’
were nearly spherical whereas larger branchiae were
ellipsoidal.
Paratype 1 with obvious gonopores only on chaeti-
ger 6 and developing gonads in the right posterior
margin of chaetiger 4 and left posterior margin of
chaetigers 4–6 (Fig. 5A). Paratype 2 with developing
gonads in chaetigers 4–6 (Fig. 5D), obvious gonopores
only in chaetiger 5. Oocytes in female up to 0.5 mm in
diameter.
Remarks: Swima fulgida sp. nov. is most similar to S.
bombiviridis. The presence of dark pigment on the
foregut and lateral lips of the buccal organ, as well as
the differences found in COI and cytb sequences
clearly separate the two species. Additionally, speci-
mens of S. fulgida sp. nov. tend to be larger than
those of S. bombiviridis and are broadest after the
third chaetiger, unlike S. bombiviridis, which tapers
from the head and first chaetiger. Swima fulgida sp.
nov. has fewer prominent interramal lollipop-shaped
papillae than S. bombiviridis. See Remarks below for
comparison to S. tawitawiensis sp. nov.
It cannot be determined at this time if the struc-
tures referred to here as subulate and digitiform
branchiae are peristomial or segmental. Unlike
other branchiae known in acrocirrids and flabel-
ligerids (Spies, 1975), these structures are not easily
detached. The digitiform branchiae were not lost from
the two paratypes by handling or damage to the
specimen; they were absent. Absence of digitiform
branchiae was also observed in S. bombiviridis where
specimens were observed with numerous long, few
short, or absent digitiform branchiae. Pulling on both
digitiform and subulate branchiae of both live and
dead specimens resulted in breakage of the structure
at various positions along their lengths and left
ragged, torn edges. This contrasts with the removal of
palps and elliptical lobe-like branchiae, which always
come away from the body at the base and leave a
regular, sealed scar.
The spherical tips of the lollipop-shaped papillae
found in S. bombiviridis and S. fulgida sp. nov. should
not be confused with the balloon-like tips of the
notopodial papillae of Flabelliseta incrusta. The tips
of the lollipop-shaped papillae are solid, with a granu-
lar outer appearance whereas the balloon-shaped
papillae are described as hollow with a smooth outer
surface.
Ecology: Swima fulgida sp. nov. was found off of
the central California coast at 3267–3625 m depth,
from 30–340 m above the seafloor. Similar animals
were observed via ROV but not collected (identifica-
tion unconfirmed) off the Oregon coast (45°24.02′N,
126°43.00′W), as well as the Gulf of California
(24°18.99′N, 109°11.95′W) by K. J. O. Animals were
not observed on the seafloor although they were some-
times observed within sight of it via the ROV. The
proximity to the seafloor at great depth, ability to
swim, and delicate body are probably the reasons why
this species was only recently discovered.
Animals were observed hanging horizontally in the
water column with the dorsal surface uppermost
and the palps hanging forward and downward over
the buccal organ, which typically projects anteroven-
trally. Swima fulgida sp. nov., like others in the clade,
swims by lateral undulation of the body coupled with
expansion on the power stroke and contraction on the
recovery stroke of the chaetal fans. Observations of
parapodia removed from the animal suggest that
this expansion and contraction of chaetal fans can be
attributed to passive mechanical mechanisms, not
requiring musculature. Swimming was observed to be
both forward and rearward, which was difficult to
distinguish unless the ROV was completely still and
camera zoomed in enough to identify the anterior end.
Animals were seldom observed in situ in close enough
detail to determine the direction of their initial
SWIMA, HOLOPELAGIC ACROCIRRIDS 673
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
674 K. J. OSBORN ET AL.
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
swimming when disturbed, but in the instances
where it was possible, it was consistently rearward.
This is consistent with the direction of escape swim-
ming observed in other Swima species. A rearward
escape response is also consistent with use of anteri-
orly located, autotomizable, bioluminescent decoys by
removing the bulk of the body away from the released
body part or decoy.
Specimens were recovered in various conditions
and possessed from two to eight elliptical branchiae of
various sizes. The first pair of elliptical branchiae
differed slightly from all other pairs in that the first
pair was always smaller than, or the same size as, the
smallest bomb found on an individual. The second to
fourth bombs varied in size; this was assumed to be
because of regeneration of previously autotomized
bombs. Manual stimulation of animals at any point
along the body or head resulted in release of a bomb
or two, which immediately produced green biolumi-
nescence. Further stimulation would result in release
of additional bombs if available. Bioluminescence was
seen as a steady glow from bombs that had been
autotomized. Bombs that were separated from the
animal could be triggered to produce light again by
gently squeezing them with forceps. The glow of an
individual bomb lasted several seconds.
SWIMA TAWITAWIENSIS SP. NOV.
Common name: Orange bomber
Type material: Holotype, and only specimen, collected
from the Celebes Sea off Tawi-Tawi, Philippines
(4°58.00′N, 120°14.16′E), x.2007 at 2836 m by ‘Explor-
ing the Inner Space of the Celebes Sea 2007 Expedi-
tion’ using ROV Max Rover Global Explorer operated
from R/V Hydrographer Presbitero. Body severed into
two pieces when recovered from ROV (anterior frag-
ment, head to chaetiger 5, posterior fragment, 27
chaetigers and pygidium; Fig. 6A). The specimen is
deposited at the National Museum of the Philippines
(NMA 0437, Table 1).
Diagnosis: Swima with nuchal organs forming
oblique lines, each with medial end curved into
U-shape. Three equally long, subulate branchiae just
posterior to nuchal organs, one medial, with smooth
sides, two lateral with 90° projection one-third to
one-half distance from base. Notochaetae broad and
flattened with a fine, spinous tip. Compound neuro-
chaetae with short (barely as long as the medial
element is wide), straight, round in cross section,
spinous distal element and broad flattened medial
element.
Etymology: Named after the location where it was
collected, Tawi-Tawi, Philippines. The locality name
is simplified and the adjectival ending -ensis is added.
Holotype description: Body transparent (Fig. 6A).
Chaetigers with distinct parapodial lobes and numer-
ous long chaetae, posterior body smoothly tapered
(Fig. 6A), with gelatinous sheath through which
narrow, short, clavate papillae extend. Gelatinous
sheath mostly peeled from body, visible as shreds
around bases of chaetae. Total preserved body length
greater than 45 mm (anterior fragment 15 mm, pos-
terior fragment 30 mm) and 6 mm widest width.
Pygidium unadorned.
Head consists of prostomium, peristomium, at least
three achaetous segments possessing two forms of
branchiae, not retractable (Fig. 6F). Prostomium is
tissue posterior to palps supporting nuchal organs.
Nuchal organs raised ciliated ridges forming oblique
lines with medial ends curved into U-shape (Fig. 6F,
H). No eyes. Peristomium surrounds prostomium
completely. Grooved frontal palps transparent to
orange in life, tapered, coiling at tips, reaching to first
chaetiger (Fig. 6E). Buccal organ anteroventrally
Figure 6. Swima tawitawiensis sp. nov. holotype. A, ventral view of posterior portion and twisted laterodorsal view
of anterior portion upon recovery from the remotely operated vehicle. Arrow indicates an attached bomb. B, scanning
electron micrograph of notochaeta tip; inset, differential interference light micrograph of several notochaetae. C,
parapodium with notochaetae on right and neurochaetae on left. D, scanning electron micrograph of neurochaeta tip;
inset, differential interference light micrograph of neurochaeta. E, dorsolateral view, anterior fragment of the preserved
specimen showing palps, subulate branchiae (sb indicates left lateral branchia), peeled away gelatinous sheath around
bases of chaetae, and the outgrowths of body wall supporting the two posterior-most elliptical branchiae scars (arrows).
F, right lateral view of head. G, ventral view anterior fragment of preserved specimen showing gonads in chaetigers 4–5
(arrows), posterior fold of left nephridium (n), buccal organ, coiled palps, shape of the left lateral subulate branchia (sb),
and the dark gut wall. H, illustration of image in F showing location of features. Abbreviations: 2, second elliptical
branchia scar on nephridiopore papillus; bo, buccal organ; lsb, lateral subulate branchia; msb, medial subulate branchia;
n, nephridium; np, nephridiopore papillus; nu, nuchal organ; p, palp. Scale bars: B = 50 mm, C = 1 mm, D = 20 mm, and
E = 3 mm.
!
SWIMA, HOLOPELAGIC ACROCIRRIDS 675
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
located, unarmed, bilobed, forming eversible lateral
lips, inner lobe transparent to black (Fig. 6G). Slight
ridge found posterior to nuchal organs and anterior to
row subulate branchiae, indicating segment margin
(Fig. 6F). Two branchial forms: (1) single row of three
equally long (to second segment), subulate, transpar-
ent to white, single medial with smooth sides, lateral
pair with 90° projection one-third to one-half distance
from base (Fig. 6E–H), and (2) elliptical branchiae.
Photograph taken immediately after collection shows
an elliptical branchia attached to the right nephrid-
iopore papillus (Fig. 6A), no elliptical branchiae
retained with preserved specimen. Branchial scars
lateral, first slightly ventral of lateral midline just
posterior to row subulate branchiae, second on medial
half of nephridiopore, third and fourth on following
achaetous segments on saclike projections of body
wall (Fig. 6E). Branchial scars found in the same
locations and identical to those in S. bombiviridis and
S. fulgida sp. nov. except the fourth, which is located
on an additional achaetous segment instead of on first
chaetiger. Elliptical branchiae yellow-green in life.
Large projection supporting fourth elliptical branchia
scar on left (Fig. 6E top arrow).
Chaetigers undifferentiated into thoracic and
abdominal. Noto- and neuropodial lobes form single,
nearly smooth projection (Fig. 6C). One to four
clavate papillae lollipop-shaped, found between noto-
and neuropodial lobes (Fig. 6C). Notochaetae simple
with smooth body, no articulations, broad and flat,
paddle-like, narrow abruptly to fine point at distal tip
(Fig. 6B). Neurochaetae compound, with broad, flat
medial element, cylindrical distal element (Fig. 6D).
High magnification reveals fine whorls of spines
making distal tips noto- and neurochaetae appear
segmented (Fig. 6B, D), bases appear striated under
high magnification. Chaetigers 4–5 with developing
gonads, gonopore low, broad papilla just posterior to
right fifth neuropodium.
Internal anatomy visible through transparent body
wall and gelatinous sheath. Ventrally located double
nerve cord with two pairs fused ganglia per segment,
diverge just posterior to peristomium to surround
buccal organ, fused again just posterior to palp
attachment. Single pair of large anterior, semitrans-
parent nephridia reaching back to fifth chaetiger,
ventrally orientated from lateral origin, folding back
anteriorly, then narrowing to lead to lateral nephrid-
iopores (Fig. 6F). Gut running from buccal organ
straight for one-third body length, coiled in mid-
region, straight in posterior region. Anterior gut
black, expandable to near body width (Fig. 6E). Heart
body and dorsal blood vessel extend through anterior
one third of body. Gonads ventral in chaetigers 4–5
(Fig. 6G), chaetiger 6 severely damaged so unknown if
contained gonads as well.
Remarks: This species is most similar to S. fulgida sp.
nov. and S. bombiviridis and is sister to the former
based on DNA sequence data (Figs 1, 3). Swima tawi-
tawiensis sp. nov. possesses a pair of lateral subulate
branchiae, which is absent in both other species
(Fig. 6F). We suggest that the medial subulate and the
lateral projections are branchiae because of the large
afferent and efferent blood vessels that run their
length and originate from just anterior to the heart
body. These structures possess no obvious sensillae.All
three projections appear to originate from a single
achaetous segment because a slight ridge of tissue
connects them (Fig. 6F). Horned and Tiburon bombers,
Chauvinelia spp. and Helmetophorus rankini have
similar subulate structures, but possess multiple rows
or segments of them, each row possessing various
numbers of projections. Each of those species also
possesses convoluted nuchal organs that wind along
the bases of the subulate branchiae, further distin-
guishing them from S. tawitawiensis sp. nov.
The broad, flattened notochaetae and compound
neurochaetae further differentiate S. tawitawiensis
sp. nov. from S. fulgida sp. nov. and S. bombiviridis
and the other members of the swimming clade, as do
the less pronounced interramal lollipop-shaped papil-
lae and U-shaped medial end of the nuchal organs.
Swima tawitawiensis sp. nov. and S. fulgida sp. nov.
share a darkly pigmented foregut. The posterior-most
pair of elliptical branchiae scars of S. tawitawiensis
sp. nov. is not on the first chaetiger as found in the
other two Swima species, but instead they lie on an
additional achaetous segment. The body-wall projec-
tions supporting the small ring-like scars where the
elliptical branchiae were attached also differentiate S.
tawitawiensis sp. nov. from the other two Swima
species.
There was variation from one side of the specimen
to the other with respect to the form of the posterior-
most elliptical branchia scars; this appears to be an
abnormal enlargement of the tissue because nothing
of the sort was found on the other side of the animal
or on any specimens of the closely related species S.
fulgida sp. nov. and S. bombiviridis. No digitiform
branchiae were found on the holotype but they might
be expected to occur on additional specimens of this
species considering the variation found in the other
Swima species.
In all Swima species, the broadened and coiled
region of the midgut is always the first portion of the
body to deteriorate upon collection (possibly because
of release of digestive enzymes when damaged or
dying). The gut of S. tawitawiensis sp. nov. is presum-
ably coiled similar to that of S. fulgida sp. nov. and S.
bombiviridis, but this could not be determined from
the specimen because the body wall was severely
damaged, with the gut spilled out.
676 K. J. OSBORN ET AL.
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
Ecology: Found in the Celebes Sea at 2836 m depth
within 30 m of the seafloor. Animals were not
observed on the seafloor. The specimen was dead upon
recovery and not checked for bioluminescence.
ACKNOWLEDGEMENTS
We would like to thank Bruce Robison of the
Monterey Bay Aquarium Research Institute for ship
time made available for observation and collection of
several specimens. Thanks go to Larry Madin of
Woods Hole Oceanographic Institution, the science
party, and crew aboard the R/V Hydrographer Pres-
bitero for their work in the Celebes Sea, for the
foresight to collect, photograph, and preserve for mor-
phology and molecular work the single specimen of S.
tawitawiensis considered here. Thanks go to the crew
of the R/V Western Flyer, the pilots of the ROVs
Tiburon and Doc Ricketts, and the MBARI video lab
staff for their dedication to deep-sea exploration. We
also thank Cynthia Claxton (UC Irvine) for advice
regarding Latin usage and form, although any errors
are the sole responsibility of the authors. Evelyn
York’s expertise on the SEM was much appreciated.
Scripps Institution of Oceanography funded K. J. O.
and G. W. R. and the University of California Presi-
dent’s Postdoctoral Fellowship supported K. J. O. The
David and Lucile Packard Foundation provided
funding to the Monterey Bay Aquarium Research
Institute. The National Geographic Society, National
Oceanic and Atmospheric Administration, and Woods
Hole Oceanographic Institution provided funding for
the Celebes Sea Expedition.
REFERENCES
Akaike H. 1974. New look at statistical model identification.
IEEE Transactions on Automatic Control 19: 716–723.
Averincev VG. 1980. Chauvinelia arctica, sp. n. (Acrocir-
ridae, Polychaeta) from the Canadian plain. Issledovaniya
fauny morei. Zoologicheskii Institut Akademii Nauk USSR
25: 57–62.
Banse K. 1969. Acrocirridae n. fam. (Polychaeta Sedentaria).
Journal of the Fisheries Research Board of Canada 26:
2595–2620.
Burnette AB, Struck TH, Halanych KM. 2005. Holopelagic
Poeobius meseres (‘Poeobiidae,’ Annelida) is derived from
benthic flabelligerid worms. Biological Bulletin 208: 213–
220.
Edgar RC. 2004. MUSCLE: multiple sequence alignment
with high accuracy and high throughput. Nucleic Acids
Research 32: 1792–1797.
Folmer O, Black M, Hoeh R, Lutz R, Vrijenhoek R. 1994.
DNA primers for amplification of mitochondrial cytochrome
c oxidase subunit I from metazoan invertebrates. Molecular
Marine Biology and Biotechnology 3: 294–299.
Gillet P. 2001. Flabelligena amoureuxi new genus, new
species (Polychaeta, Acrocirridae) from Crozet Islands
(Indian Ocean). Bulletin of Marine Science 68: 125–131.
Glasby CJ, Fauchald K. 1991. Redescription of Helme-
tophorus rankini Hartman, 1978 (Polychaeta: Helme-
tophoridae) and its transfer to the Flabelligeridae.
Proceedings of the Biological Society of Washington 104:
684–687.
Grube AE. 1850. Die Familien der Anneliden. Archiv für
Naturgeschichte, Berlin 16: 249–364.
Grube AE. 1873. Die Familie der Cirratuliden. Jahres-
Bericht der Schlesiche Gesellschaft fuer vaterlandische
Cultur, Breslau 50: 59–66.
Haddock SHD. 2004. A golden age of gelata: past and future
research on planktonic ctenophores and cnidarians. Hydro-
biologia 530/531: 549–556.
Hartman O. 1965. Deep-water benthic polychaetous annelids
off New England to Bermuda and other North Atlantic
areas. Occasional Papers of the Allan Hancock Foundation
28: 1–378.
Hartman O. 1978. Polychaeta from the Weddell Sea quad-
rant, Antarctica. Antarctic Research 26: 124–223.
Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian
inference of phylogenetic trees. Bioinformatics 17: 754–
755.
Kirkegaard JB. 1982. The Polychaeta of West Africa Part I.
Sedentary species. Atlantide Report 5: 7–117.
Laubier L. 1974. Chauvinelia biscayensis gen. sp. nov., un
Flabelligeridae (Annélide Polychète Sédentaire) aberrant de
l’étage abyssal du Golfe de Gascogne. Bulletin de la Société
Zoologique de France, Paris 99: 391–399.
Maddison DR, Maddison WP. 2000. Macclade. Sunderland,
MA: Sinauer Associates.
Osborn KJ, Haddock SHD, Pleijel F, Madin LP, Rouse
GW. 2009. Deep-sea, swimming worms with luminescent
‘bombs’. Science 325: 964.
Osborn KJ, Madin LP, Rouse GW. 2010. The remarkable
Squidworm is an example of discoveries that await in deep,
pelagic habitats. Biology Letters 7: 449–453.
Osborn KJ, Rouse GW. 2008. Multiple origins of pelagicism
within Flabelligeridae (Annelida). Molecular Phylogenetics
and Evolution 49: 386–392.
Osborn KJ, Rouse GW. 2010. Phylogenetics of Acrocirridae
and Flabelligeridae (Cirratuliformia, Annelida). Zoologica
Scripta 40: 204–219.
Pleijel F, Jondelius U, Norlinder E, Nygren A, Oxelman
B, Schander C, Sundberg P, Thollesson M. 2008. Phy-
logenies without roots? A plea for the use of vouchers in
molecular phylogenetic studies. Molecular Phylogenetics
and Evolution 48: 369–371.
Posada D, Crandall KA. 1998. Modeltest: testing the model
of DNA substitution. Bioinformatics 14: 917–918.
Posada D, Crandall KA. 2001. Selecting the best-fit model of
nucleotide substitution. Systematic Biology 50: 580–601.
Robison BH. 1992. Midwater research methods with
MBARI’s ROV. Marine Technology Society Journal 28:
32–39.
SWIMA, HOLOPELAGIC ACROCIRRIDS 677
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678
Robison BH, Sherlock RE, Reisenbichler KR. 2010. The
bathypelagic community of Monterey Canyon. Deep-Sea
Research II 57: 1551–1556.
Rouse GW, Fauchald K. 1997. Cladistics and polychaetes.
Zoologica Scripta 26: 139–204.
Rouse GW, Pleijel F. 2003. Problems in polychaete system-
atics. Hydrobiologia 496: 175–189.
Rousset V, Pleijel F, Rouse GW, Erséus C, Siddall ME.
2007. A molecular phylogeny of annelids. Cladistics 23:
41–63.
Salazar-Vallejo SI, Carrera-Parra LF, Fauchald K. 2008.
Phylogenetic affinities of the Flabelligeridae (Annelida,
Polychaeta). Journal of Zoological Systematics and Evolu-
tionary Research 46: 203–215.
Spies RB. 1975. Structure and function of the head in fla-
belligerid polychaetes. Journal of Morphology 147: 187–207.
Wilgenbusch JC, Warren DL, Swofford DL. 2004. AWTY:
a system for graphical exploration of MCMC convergence in
Bayesian phylogenetic inference. Available at http://
ceb.csit.fsu.edu/awty
Xia X, Xie Z. 2001. DAMBE: Data analysis in molecular
biology and evolution. Journal of Heredity 92: 371–373.
Xia XH, Xia Z, Salemi M, Chen L, Wang Y. 2003. An index
of substitution saturation and its application. Molecular
Phylogenetics and Evolution 26: 1–7.
678 K. J. OSBORN ET AL.
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 663–678