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Antarctic Science 22(4), 399–407 (2010) & Antarctic Science Ltd 2010 doi:10.1017/S0954102010000210

‘Hitchhiker’ polynoid polychaetes in cold deep waters and theirpotential influence on benthic soft bottom food webs

STEFANO SCHIAPARELLI1, MARIA CHIARA ALVARO2, JEHNS BOHN3 and GIANCARLO ALBERTELLI1

1Dipartimento per lo Studio del Territorio e delle sue Risorse (Dip.Te.Ris.), Universita di Genova, C.so Europa 26,

Genova I-16132, Italy2Museo Nazionale dell’Antartide (MNA), Universita di Genova, Viale Benedetto XV n85, Genova I-16132, Italy

3Zoologische Staatssammlung Munchen, Munchhausenstrasse 21, Munchen D-81247, Germany

stefano.schiaparelli@unige.it

Abstract: We describe a new association for Antarctica, involving an holothuroid host, Bathyplotes

bongraini Vaney, 1914, and a parasitic polynoid polychaete, Eunoe opalina McIntosh, 1885, which lives on

the host body. Both species have never been recorded in the study area, the Ross Sea. The ecological

definition of this partnership is difficult to assess, being a mix of phoresis, protective association, parasitism

and, possibly, kleptocommensalism. Eunoe opalina emerges also as a true predator, ingesting several food

items that do not belong to the diet of Bathyplotes. We compare this association with analogous examples

known from shallow tropical environments as well as bathyal and abyssal depths. Given the conspicuous

similarities between the deep water and high latitude examples of this kind of association, a possible

common origin is hypothesized. Although the role of such a kind of parasitic relationships in Antarctic

communities remains to be fully evaluated, it seems evident that, at high latitudes, where trophic levels are

simplified and food webs do not have much redundancy, the impact of such a ‘multitasking’ predator-parasite as

E. opalina might be of a greater magnitude than its shallow water tropical counterpart.

Received 5 December 2009, accepted 4 March 2010

Key words: Antarctica, Holothuroidea, parasitism, Polychaeta, Ross Sea, ‘symbiotic’ association

Introduction

Marine ‘partnerships’ or ‘symbiotic’ associations (sensu De

Bary 1878) have only recently been recognized to play a very

important role in shaping marine communities, since they may

affect their structure to an extent as important as predation or

physical disturbance (Hay et al. 2004). In particular, parasitism

may increase connectance (links/species; Dunne et al. 2002)

and affect nestedness, chain length and linkage density of food

webs dramatically (Lafferty et al. 2006), and may play a major

role, with consequences that have still to be quantified, in most

marine environments.

Historically, the study of ‘symbioses’ has been focused on

reef communities, where these kind of partnerships are

widespread and abundant, whilst examples occurring in

temperate and cold areas, especially polar waters, have been

little studied. Nevertheless, in recent years, partnerships

involving Antarctic marine invertebrates have received

increasing interest with the result that a provisional list of

different associations occurring in this area now numbers

23–25 different examples, mainly shifted towards parasitism,

with polychaetes and molluscs being the commonest

symbionts (Schiaparelli et al. 2007 and unpublished data).

Among the polychetous annelids, the setting-up of close

associations with other marine invertebrates is a rather common

phenomenon at all latitudes (Martin & Britayev 1998),

especially in the case of Polynoidae. This family of 1666

species (Fauchald & Barnich 2009a), mainly of generalist

carnivores (Fauchald & Jumars 1979), also numbers several

examples of species living as ‘symbionts’ on different

invertebrate hosts (e.g. Pettibone 1982, 1993, Britayev et al.

2003). Among polychaetes, 55% of commensal polychaete

species belong to the Polynoidae (Martin & Britayev 1998).

In the Southern Ocean, Polynoidae are well represented

with about 82 species known (Fauchald & Barnich 2009b)

out of a total of 677 species of polychaetes described so far

for this area (RAMS 2009). For most of these polynoids,

however, no ecological data are available and to date only

Polynoe thouarellicola Hartmann-Schroder, 1989, has been

reported as a ‘commensal’, having been found in association

with gorgonians of the genus Thouarella (Hartmann-Schroder

1989).

In the present contribution, we describe an Antarctic

association from the Ross Sea involving the polychaete

Eunoe opalina McIntosh, 1885 (Phyllodocida: Polynoidae)

and the holothurian Bathyplotes bongraini Vaney, 1914

(Holothuroidea: Synallactidae), which have never been

reported in association before, probably due to the well

known bias of destructive sampling, as trawling or

dredging, which may separate symbionts and hosts.

The partnership between polynoids and holothuroids has

been previously reported from shallow tropical waters,

where it has been extensively studied from an ecological

point of view (Britayev & Zamishliak 1996, Britayev et al.

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1999, Britayev & Lyskin 2002, Lyskin & Britayev 2005),

and for Californian temperate shallow water communities

(e.g. Dimock & Davenport 1971). A few more scattered

examples involving these partners have been described for

the deep waters of the Atlantic Ocean (e.g. Wesenberg-

Lund 1941, Kirkegaard & Billet 1980). In each of these

examples different species of polynoids and holothuroids

are involved, establishing relationships which only partially

overlap, if their ecological traits are taken into account.

Here we describe the southernmost case of such an

association, the first one for Antarctica, and review the

available literature comparing this example with the tropical

shallow water and deep water, non-Antarctic, counterparts.

The possible ecological role of these ‘symbiotic’ associations,

generally overlooked in deep waters environments, is

discussed in the light of the potential influence they may

have on benthic soft bottom food webs.

Methods

Polychaetes and holothurians were collected by two

different cruises in the Antarctic waters by the RV

Tangaroa. The first one took place in the Ross Sea, from

January–March 2004, sampling between 658S and 758S and

from 65–1570 m. The second one occurred between

February and March 2008, sampling from 668S and 768S

and from 150–3553 m. Both cruises used Orange Roughy

Trawls, Beam Trawls and dredges.

Immediately after collection, samples were carefully

observed and polychaetes photographed in situ on the

Table I. List of sampling stations in the Balleny Islands and in the Ross Sea areas.

Cruise St. Site Holothuroid species Latitude S Longitude E Depth (m) Date

BioRoss Cruise 218 Balleny Islands Bathyplotes bongraini 67815'13'' 164852'30'' 348 03/03/04

(TAN0402) (Sturge)

BioRoss Cruise 249 Balleny Islands Bathyplotes bongraini 66833'30'' 163801'04'' 555 05/03/04

(TAN0402) (Young)

IPY-CAML Cruise 56 Ross Sea shelf Bathyplotes bongraini 75837'58'' 169850'59'' 531 14/02/08

(TAN0802)

IPY-CAML Cruise 169 Ross Sea shelf Laetmogone sp. 71823'03'' 174844'07'' 2202 25/02/08

(TAN0802)

Fig. 1. Different views of the association

between Bathyplotes bongraini and

Eunoe opalina. a. B. bongraini

specimen photographed in situ

(Tangaroa 2008 Cruise, station 56).

b. Ventral view of a freshly collected

B. bongraini specimen carrying

E. opalina next to its mouth, between

the fields of tube feet. c. Particular

showing the cephalic end of

B. bongraini with E. opalina lying into

its ‘niche’ in the host tegument. The

polychaete ventral side is in direct

contact with the holothurian’s one.

d. E. opalina specimen: ventral view

(left) and dorsal view (right).

400 STEFANO SCHIAPARELLI et al.

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host, in order to document their exact position on the

holothuroid. After fixation in 70% ethanol, every specimen

of E. opalina was dissected and its stomach isolated.

Stomachs were then dipped for half a day in a solution of

1% Rose Bengal, rinsed three times in water and their

contents extracted, dehydrated in increasing alcohol

concentrations (80%–90%–100%) and placed on a glass

slide for microscope examination. The dominance method

(Holden & Raitt 1974) was adopted to quantify the

abundance of food items.

As regards the host, B. bongraini, skin fragments from

three different parts (oral zone, central zone, anal zone) of

the holothurian body were cut both from dorsal and ventral

sides. Ossicles of the body wall were then obtained by

digesting the tissue with the proteolitic enzyme Tripsina

(Tiago et al. 2005). The ossicles were then rinsed in distilled

water, dehydrated and mounted on a glass slide with Eukitt.

SEM observations of chaetae, polychaete stomach content

and holothuroid skin and ossicles were performed with a

Leica Stereoscan 440, after dehydratation of samples with

HMDS (hexamethyldisilazane) (Nation 1983).

Results

Both cruises together provided a total of 86 specimens of

B. bongraini which carried 26 specimen of E. opalina.

Since we found only one polychaete per holothurian, the

estimated infestation rate is about 30% of the holothuroid

population. Due to logistic restrictions, the evaluation of

the infestation rate has been possible only in selected

stations (see Table I) and, therefore, the distribution of this

association may be much wider than herein considered.

Both species are here reported for the first time in the

Ross Sea. Bathyplotes bongraini (Fig. 1a) was previously

known from western Antarctica (Weddell Sea, between

Fig. 2. Position of the polychaete on the

host. a. Depression dug by Eunoe

opalina into Bathyplotes bongraini

skin, clearly visible only after

polychaete removal and whose

dimensions perfectly fit with

polychaete size. b. SEM micrographs

of tissue sample belonging to an

intact portion of B. bongraini body

wall (Scale bar: 50 mm). c. SEM

micrographs of healing tissue sample

corresponding to the inner part of the

depression (Scale bar: 50 mm); arrows

show the partially exposed spines of

B. bongraini body wall ossicles.

d. B. bongraini skin section: intact

portion of the holothuroid body wall

(above) and inner part of the

depression dug by the polychaete

(below). e. Typical 4-armed crosses

ossicle with a central spine vertical to

the plane of the arms, belonging to

the body wall of B. bongraini.

Fig. 3. Eunoe opalina food items quantified with the dominance

method (Holden & Raitt 1974).

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245–465 m; Antarctic Peninsula, 250 m) and eastern

Antarctica (Prydz Bay, 120–768 m; off Kemp Land,

603 m) (O’Loughlin 2002, O’Loughlin et al. 2009), while

E. opalina was known for the Antarctic Peninsula and the

Scotia Ridge (Fauchald 2009).

In all the cases we have examined, E. opalina (Fig. 1d)

was exclusively found on the host’s ventral side, mainly

next to the mouth of the holothuroid, between tube feet

fields (Fig. 1b & c) (in one case only it was on the opposite

side), where it was lying in a depression excavated into the

holothurian tegument. This cavity remained clearly visible

even after polychaete removal, perfectly fitting the worm’s

shape and size (Fig. 2a).

SEM observation of the host’s tissue samples, taken from

an intact portion of the holothurian body (Fig. 2b) and from

the inner part of the depression dug by the polychaete

(Fig. 2c), respectively, showed the presence of a different skin

texture in the two areas. It is clear that the polychaete activity

has somehow removed part of the tegument, almost exposing

(Fig. 2c, arrows) the 4-armed crosses ossicles (Fig. 2e), typical

of B. bongraini tegument, that emerged beneath the thin,

perhaps healing, tissue. Where the tegument is intact, the

ossicles do not protrude and are completely embedded.

The stomach content analysis of seven polychaetes

(dominance method, according to Holden & Raitt 1974)

(Fig. 3) allowed the identification of a variety of prey items

(Fig. 4a), as: ossicles of Bathyplotes (14%) and other

holothuroid species (Echinocucumis sp.) (28%) (Fig. 4d),

bivalves (71%), foraminiferans (42%), benthic (42%) and

planktic (28%) diatoms, ophiuroids (100%), chaetae of

errant polychaetes (28%), microcrustaceans fragments

(Fig. 4b & c) belonging to Cumacea (57%) and to

Leptostraca (28%) and nematodes (57%).

Discussion

Representatives of most marine phyla are known to live in

close association with echinoderms, establishing different

typologies of partnerships, ranging from phoresis to parasitism

(e.g. Barel & Kramers 1977, Jangoux 1987a, 1987b).

Among echinoderms, Holothuroidea harbours the highest

number of symbionts, reaching a total of 145 species

belonging to ten different Phyla (Jangoux 1987b, table I,

p. 223). These associated organisms may live inside the

holothuroid body, as in fishes (Carapidae) and crabs

(Pinnotheriodae), or outside and/or transdermically, as in

the case of bivalves (Galeommatoidea) and gastropods

(Eulimidae) (Waren 1983, Jangoux, 1987a, Ng & Manning

2003, Middelfart & Craig 2004, Parmentier & Vanderwalle

2005). On the whole, it has been estimated that, in temperate

and tropical waters, about 40 different species of holothuroids

are the hosts in 50 recognized cases of ‘symbioses’ involving

polychaetes (Martin & Britayev 1998).

To date, the best known association between a

polychaete and its holothuroid host is that of the polynoid

Fig. 4. SEM micrographs of Eunoe

opalina stomach content. a. Overview

of the main food items (Scale bar:

100 mm). b,c. Particular of

microcrustacean fragments.

d. Echinocucumis sp. ossicle

(Scale bar: 20 mm).

402 STEFANO SCHIAPARELLI et al.

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Gastrolepidia clavigera Schmarda, 1861, a shallow water

‘polyxenous’ species from the Indo-West Pacific region,

which is known to live on 13 different holothuroids of the

families Stichopodidae and Holothuriidae (Martin &

Britayev 1998). Gastrolepidia clavigera has been studied

in detail from an ecological point of view and, therefore,

represents a good reference example to be compared with

E. opalina, the most ‘extreme’ case of such a kind of

relationship, occurring in the cold Antarctic waters.

The first macroscopic difference between these two

polychaetes is that E. opalina was found in only one

specimen per host, always placed ventrally next to the

mouth of the holothurian’s body, where it lies in a deep

depression produced by the polychaete itself. Gastrolepidia

clavigera may be present with up to four specimens per host,

usually living on the holothurian dorsal side (Britayev &

Zamishliak 1994, 1996, Britayev et al. 1999) where they may

form temporary depressions that disappear after polychaete

removal (Britayev & Zamishliak, 1996). Gastrolepidia

clavigera is also known to crawl into the mouth or cloaca of

the holothurian host in case of threats (Britayev & Zamishliak

1994, 1996), a behaviour not observed in E. opalina, although

it has to be taken into account the fact that no in vivo long-term

observations are available for this species.

A comparison between the stomach contents of the two

polychaetes reveals that both species have a wide variety of

food items, which almost perfectly overlaps from a

qualitative point of view, including: holothuroid ossicles,

crustacean fragments, multicellular and unicellular algae,

chaetae and jaws of polychaetes (other than G. clavigera

or E. opalina), detritus, foraminifera and fragments of

the shells of bivalves (Britayev & Lyskin 2002 for

G. clavigera; present data for E. opalina, Fig. 3).

Unfortunately, it is not possible to make a direct,

quantitative comparison of food items due to the different

methodologies used but some very important differences

can be highlighted about the origin of the holothuroid

ossicles found in the stomachs. In G. clavigera, the stomach

content analysis clearly indicates that the polychaete

feeds on the skin of the host from which it has been

collected (Britayev & Lyskin 2002). Eunoe opalina

contains B. bongraini ossicles and another distinctive kind

of ossicles, clearly not belonging to the host species. These

ossicles fall within the morphological range of the genus

Echinocucumis and may belong to a not yet described species

(O’Loughlin, personal communication 2009).

This finding opens several scenarios, the most obvious one

being that of a host switch of E. opalina during its lifetime.

However, considering the size of the known Echinocucumis

species, which are really small holothurians, almost comparable

to E. opalina in average size, a permanent association with this

holothuroid genus can be excluded. The possibility that these

ossicles could already be present in the sediment as loose items

and that these are passively ingested by the polychaete during

its feeding activity seems highly improbable, as these have

been found in quantities in the stomachs and always in very

good condition (not damaged, etched or worn). Most

interestingly, the same ossicle type was also found in

stomachs of E. opalina specimens from the Weddell Sea

(unpublished data). It is therefore possible that E. opalina

undertakes opportunistic predation on other holothuroid species

(i.e. Echinocucumis), if these are somehow detected by the

polychaete during the host’s grazing activity on the bottom.

The fact that Echinocucumis ossicles have been found in

E. opalina stomachs both from the Ross Sea and the Weddell

Sea, possibly indicates that the environmental settings in which

B. bongraini specimens is found are very similar, despite the

Fig. 5. Eunoe opalina parapodia and chaetae. a. Right

parapodium, posterior view (Scale bar: 500 mm). b. Left

parapodium, posterior view (Scale bar: 500 mm). c. Particular

of distally dentate neurochaetae (Scale bars: 100 mm).

ANTARCTIC SYMBIOTIC POLYNOID EUNOE OPALINA 403

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distance between the two areas, and have almost the same

species composition.

Although belonging to different genera, it is clearly evident

that G. clavigera and E. opalina are adapted to live in

association with holothuroids, both showing morphological

peculiarities linked to their symbiotic mode of life. As

documented by Britayev & Zamishlyak (1994), G. clavigera

has specially designed attaching structures, called ‘ventral

sucker-like lobes’. These features have probably evolved to

enable the adherence of the polychaete to several hosts,

accounting for the potentially different ‘tegument properties’

encountered from time to time. In contrast, E. opalina does

not have these structures, but shows distally dentate spines

(Fig. 5a–c), known to occur in other symbiotic polynoids

(Martin & Britayev 1998).

In summary, G. clavigera is a ‘polyxenous’ polychaete

with several host species, while E. opalina is a ‘monoxenous’

polychaete, always associated with B. bongraini. On the other

hand, it is clear that E. opalina has a wider prey range

including other holothurian species with which no ‘symbiotic’

partnerships are established.

From an ecological point of view, these differences are

rather intriguing and might be possibly related to the

ecosystems in which these associations have been established,

and not only to the taxonomic and morphological differences

between the two symbionts.

The latitudinal and bathymetric distribution of the

documented associations involving polynoids and holothuroids

show that most of them occur in the Northern Hemisphere,

at intermediate latitudes and on the continental shelf

(shallower than 200 m, Fig. 6a).

The relationship between E. opalina and B. bongraini,

even if it occurs between 348–555 m depth (Fig. 6b),

should be considered in the category of shelf examples, as

it is known that the Antarctic continental shelf is much

deeper than other continental shelves, due to the weight of

the ice cap (Anderson 1999). On the other hand, it is also

known that most Antarctic species are extremely eurybathic

and recolonized the shelf only when it again became

available after ice retreat during interglacials (Brey et al.

1996).

Several similarities between Antarctic and deep water

representatives of ‘symbiotic’ associations involving

polynoids and holothurians species can also be highlighted.

For example, the presence of a ‘scar’ on the host’s ventral

body wall clearly resembles what has already been described

for the polychaetes Harmothoe bathydomus Ditlevsen, 1917

and Eunoe laetmogonensis Kirkegaard & Billet, 1980,

respectively associated with the holothuroids Bathyplotes

natans (Sars, 1868) and Laetmogone violacea Theel, 1879

(Wesenberg-Lund 1941, Kirkegaard & Billet 1980), both

occurring in deep Atlantic waters (800–3200 m). The first

Fig. 6. Latitudinal and bathymetric distribution of the

documented associations involving polynoid polychaetes and

holothuroids worldwide distributed. Northern and southern

latitude values have been combined. a. Shelf water records

(0–200 m). b. Deepwater records (200–3700 m).

Fig. 7. Specimen of Oneirophanta mutabilis, carrying a

‘symbiotic’ polychaete, photographed at 3356 m in the

Monterey Canyon, California (28/08/2005, Tiburon Dive 889:

40.948N; 127.488E, MBARI courtesy, & 2005 MBARI).

Distance between the two laser beam points is 30 cm.

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example, in particular, is remarkable not only for the

similarities with the Antarctic case, but also because the

partners involved in the association are another Bathyplotes

species and a polychaete that, although now included in

Harmothoe, a genus closely allied to Eunoe, has been

considered indistinguishable from E. opalina by Ditlevsen

(1917, p. 26).

It is therefore possible that these two deep water polynoid-

holothuroid associations share a common origin with the

Antarctic one. The disjointed, bipolar distribution could be

explained in the light of the ‘thermohaline expressway’

hypothesis, according to which some Antarctic species could

have spread into deep water basins outside Antarctica,

by following the increased production of cold, hyperhaline

water masses during glacial cycles (Strugnell et al. 2008).

Independent information on phylogenetic relationships of both

polynoids and holothuroids would be required to test this

hypothesis but, unfortunately, no such studies are yet available.

Deep water polynoid-holothuroid partnerships might be

much more common and widespread than believed. Using

images collected during deepwater ROV surveys, we were

able to document two further examples. The first one refers

to a specimen of Oneirophanta mutabilis Theel, 1879,

photographed at 3356 m, off Monterey (California), with a

polynoid moving on its body (Fig. 7). This record increases

the maximum known depth limit for a polynoid associated

with an holothuroid (the previous deepest record was of

3136 m for H. bathydomus, Ditlevsen 1917), and adds a new

host record in this kind of association. A further example is

that of Laetmogone sp. (probably an undescribed species,

O’Loughlin personal communication 2009), photographed

at 2202 m in the Ross Sea. This latter species carried an

undetermined polynoid whose cephalic end was clearly

inserted within the holothuroid tentacles crown (Fig. 8).

A precise, strict definition of the relationship between

E. opalina and B. bongraini is not possible, as it appears to

be a mix of phoresis (the polychaete is carried by the host),

protective association (the polychaete is also protected from

predators by its host), parasitism (the polychaete removes and

ingests host skin and ossicles) and kleptocommensalism (due

to the possibility that some of the preys are removed from the

host mouth as documented in Fig. 8). Nevertheless, it is clear

from the variety of food items collected, and from the removal

of host tegument, that the polychaete may have both a

detrimental effect on its host and a negative impact on other

bottom dwelling invertebrates living in the same environment.

Considering the formula to calculate Connectance,

corrected to include parasites (C 5 L0/F(F 1 P), where

C 5 connectance, L0 5 number of links, F 5 free living

species and P 5 parasite species) (see Lafferty et al. 2006

for details), it emerges that the presence of E. opalina in the

loop determines an increase of connectance from 0.25

(holothuroid-detritus chain with a single link, where

detritus is contemplated as a ‘non-phylogenetic category’,

Dunne et al. 2002) to 0.33 (detritus-B. bongraini-E. opalina

chain, with two links), in accordance to what is expected

when parasites are included in food webs (Lafferty et al.

2006). Interestingly, if we take into account the double role

of E. opalina, that can be considered simoultaneously a free

living species (F) and a parasite (P), by including in the

calculation also the food items (i.e. bivalves, ophiuroids

and the other holothuroid species) which are not part of the

B. bongraini diet, the number of total links rises to five and

the connectance decreases to 0.16.

Given the major role that parasites have been demonstrated

to play on complex food webs in general (Lafferty et al.

2006), and in the light of the above calculations, it is

reasonable to suppose that in Antarctica, where trophic levels

are simplified, no ‘modern’ predators exist (Aronson & Blake

2001) and food webs do not have much redundancy, the

impact of such a ‘multitasking’ predator-parasite as E. opalina

might be even of a greater magnitude, deeply affecting

Connectance and other food web features.

Further studies dedicated to the quantification of the

effects that the ‘symbiotic’ interactions may have in

Antarctica, will enable some of the hypotheses proposed

here to be tested and will contribute to our understanding of

the ecological constraints which affect invertebrates living

at high latitudes.

Acknowledgements

We would like to acknowledge the crew of the Tangaroa

expeditions ‘BioRoss TAN0402’ and ‘IPY-CAML

TAN0802’ for logistic support during both cruises. A

particular acknowledgement is due to Anne Nina Loerz

Fig. 8. Undetermined specimen of Laetmogone sp. carrying a

symbiotic polychaete, photographed in situ at 2202 m in the

Ross Sea (IPY-CAML Cruise, TAN0802, st. 169). The head

of the polychaete (arrow) is clearly inserted within the

holothuroid oral tentacle crown. This behaviour could be

interpreted as kleptocommensalism, with the polychaete possibly

stealing food items before the holothuroid swallow them.

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(NIWA) and Sadie Mills (NIWA) for collaboration during the

cruises. We are indebted to the New Zealand Ministry of

Fisheries (MFish) and NIWA (Wellington) for the financial

support of the cruises and related study activities. We are

extremely grateful to MBARI (www.mbari.org) for the

permission to use the picture from the Tiburon Dive 889,

and to Mark O’Loughlin (Marine Biology Section, Museum

Victoria) for the useful commentaries and suggestions. Geoff

Read (NIWA, Wellington) kindly provided the E. opalina

classification. Gaia Magioncalda and Sylvie de Sousa Pereira

contributed to laboratory analyses. Two anonymous reviewers

are acknowledged for useful comments on the manuscript.

This paper is a contribution to the multinational Latitudinal

Gradient Project and contribution #28 to the Census of

Antarctic Marine Life (CAML).

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