Introduction
Across the world's marine habitats, from young to old, tropics to poles and shores to deep trenches, echinoid echinoderms (sea urchins) are a common and important component of seabed communities. They can be voracious grazers so that high abundance and biomass often results in them playing a major role in structuring benthic communities (Tuya et al. Reference Thompson and Riddle2004 and references therein). They are particularly abundant and ecologically pivotal in kelp forests but also on the nearshore shelf around Antarctica, where they are often the most obvious megafauna. The first specimens were collected during the voyage of HMS Challenger in 1873–76 and most of the Antarctic and sub-Antarctic species were described in the first decades of the twentieth century (David et al. Reference David, Magniez, Villier, De Wever, Fèrd and David2005a). In the Southern Ocean, the regular urchin Sterechinus neumayeri frequently dominates the shallows and a wide variety of species including pencil and burrowing urchins frequent the shelf, slope, abyssal plains and trenches (e.g. Brockington et al. Reference Brockington, Clarke and Chapman2001, Mooi et al. Reference Mooi, David, Fell and Choné2004, David et al. Reference David, Magniez, Villier, De Wever, Fèrd and David2005a, Reference David, Choné, Festeau, Mooi and De Ridder2005b, Brandt et al. Reference Brandt, De Broyer, De Mesel, Ellingsen, Gooday, Hilbig, Linse, Thomson and Tyler2007a, Palma et al. Reference Néraudeau, Crame and Kooser2007).
The dominance of S. neumayeri in the zone accessible to sampling has made it one of the principal model species for studies of Antarctic benthos (e.g. Pearse & Giese Reference Palma, Poulin, Silva, San Martin, Munoz and Diaz1966, Bosch et al. Reference Bosch, Beauchamp, Steele and Pearse1987, Brey & Gutt Reference Brey and Gutt1991, Brey et al. Reference Brey, Pearse, Basch, McClintock and Slattery1995, Tyler et al. Reference Tuya, Boyra, Sanchez-Jerez, Barbera and Haroun2000, Brockington & Peck Reference Brockington and Peck2001, Cox & Halanych Reference Cox and Halanych2005, Linse et al. Reference Kaiser and Brandt2006a, Brockington et al. Reference Brockington, Peck and Tyler2007). However, with the exception of a few other species, e.g. Abatus cordatus (Schatt & Féral Reference Schatt and Féral1991, Reference Rehm, Thatje, Arntz, Brandt and Heilmayer1996, Poulin & Féral Reference Poulin, Palma and Féral1995) or A. ingens (Thomson & Riddle Reference Tatiàn, Antacli and Sahade2005), other studies of Antarctic and sub-Antarctic echinoids have simply documented their importance in the composition of macrobenthic assemblages (e.g. Arnaud et al. Reference Arnaud, Lopez, Olaso, Ramil, Ramos-Espla and Ramos1998, Ramos Reference Quale, Peck, Peat, Ellis-Evans and Harrigan1999, Barnes & Brockington Reference Barnes and Brockington2003, Rehm et al. Reference Ramos-Esplà, Càrcael and Varela2006, Griffiths et al. Reference Elner and Vadas2008) or their diversity of reproductive modes (e.g. Poulin et al. Reference Pena Cantero2002, Chenuil et al. Reference Chenuil, Hault and Féral2004, Pearse & Lockhart Reference Pearse and Giese2004 and references therein). Even then such studies have already shown this taxon to provide powerful insight into differences between evolutionary and ecological success and glacial versus interglacial selective pressures (Poulin et al. Reference Pena Cantero2002).
The extreme physical disturbance around Antarctica (poor fossilization conditions) and rarity of rock uncovered by ice (few areas of exposed fossils) combine to produce a very poor record of faunal change through time in the Southern Ocean. With strong calcified tests and spines, the Echinoidea have one of the better fossil records of the region, from the Cretaceous to the Holocene (e.g. Hotchkiss Reference Hilbig, Gerdes and Montiel1982, Blake & Aronson Reference Blake and Aronson1998, Néraudeau et al. Reference Mortensen2000, BAS Fossil database - Griffiths, personal communication 2007). Their large size, ease of sampling with benthic trawls and ease of identification makes them an ideal group to investigate current and past biodiversity patterns around Antarctica and what underlies them. Some recent studies have assembled species lists for a few markedly different localities, such as the eastern Weddell Sea, Deception Island, the Ross Sea and along the coast adjacent to Victoria Land (see Jacob Reference Jacob, Terpstra and Brey2001, Lovell & Trego Reference Lockhart, O'Loughlin, Tutera, David, Guille, Feral and Roux2003, Chiantore et al. Reference Chiantore, Guidetti, Cavallero, De Domenico, Albertelli and Cattaneo-Vietti2006, De Domenico et al. Reference David, Choné, Mooi, De Ridder, Wägele and Sieg2006). The database of Southern Ocean echinoids assembled by David et al. (Reference David, Magniez, Villier, De Wever, Fèrd and David2005a), one of the best for any Antarctic taxa, still reveals major gaps in the geographic and bathymetric distributions of many species.
Probably the single most interesting region within the Southern Ocean for marine biogeographic and evolutionary links between the Antarctic and a neighbouring continent is the Scotia Arc. It encompasses islands (and thus shelf areas) of widely different ages and isolation levels and is the only semi-continuous shelf and slope link to a temperate region. It has become an important focus for many research programmes on benthos including the Spanish Antártida 8611 (Ramos Reference Quale, Peck, Peat, Ellis-Evans and Harrigan1999), German LAMPOS (Arntz & Brey Reference Arntz and Brey2003), international IBMANT (Arntz & Rios Reference Arntz and Rios1999, Arntz et al. Reference Arntz, Lovrich and Thatje2005a, Reference Arntz, Thatje, Gerdes, Gili, Gutt, Jacob, Montiel, Orejas and Teixido2005b) and British BIOPEARL (Linse Reference Linse, Griffiths, Barnes and Clarke2008) scientific cruises. In the current study we investigate the echinoids living on seven island slopes. We sampled from the continental shelf to the upper continental slope around all the major archipelagos of the Scotia Arc and report the most comprehensive geographic and bathymetric surveys to date for a region of the Southern Ocean. Furthermore, we examine the contribution that echinoids make to Antarctic benthic richness through their considerable associated commensal fauna.
Materials and methods
Study area
Specimens of regular and irregular Echinoidea were collected during the scientific cruise JR 144 (BIOPEARL) of RRS James Clark Ross around the Scotia Arc in 2006. Our sample localities included the Falkland Trough (FT) and six areas south of the Polar Front (Table I). In the South Shetland Islands (SH) we sampled at Deception Island (DI) and Livingston Island (LI) and to the north-east of these at Elephant Island (EI) and Powell Basin (PB). East from there we sampled the southernmost of the South Sandwich Islands (SSI) - Southern Thule Island and finally adjacent to South Georgia (SG) and Shag Rocks (SR) at the northernmost limit of the polar frontal zone. For brevity throughout this study we refer to other localities in the region using the abbreviations: Adelie Land (AD), Antarctic Peninsula (AP), Bellingshausen Sea (BS), Bouvet Island (BI), Cape Horn/ Magellan Region (CH/MR), Davis Sea (DS), Dronning Maud Land (DM), Falkland Islands (FI), Kerguelen Islands (KI), Lazarev Sea (LS), eastern Weddell Sea (E-WS), western Weddell Sea (W-WS), Ross Sea (RS), and South Orkney Islands (SO). Within the Scotia Arc are islands with widely varying degrees of isolation and age, and some of the volcanos have even had considerable eruptions within the last few decades (Smellie et al. Reference Schatt and Féral1998).
Table I. Station list of JR 144 BIOPEARL containing echinoids.
Sampling
Benthic samples were taken by two different types of bottom trawls; Agassiz trawl (AGT) and rough bottom otter trawl (RBOT) at 24 stations between depths of 91–1045 m (Table I). When the samples reached the deck, echinoids were separated by hand from other taxa and into families. Of each species collected three specimens were fixed in 96% ethanol, and further specimens of each species were frozen at -20°C. Identities were later established to species level following literature keys.
Morphometric and biomass analysis
Measurements of test length, width and height were made on each individual or each species using digital Vernier callipers to accuracy levels of 1 mm. In total 273 regular (cidaroid and temnopleurid) and irregular (spatangoid and holasteroid) specimens from 24 locations were measured (Table II). Population size spectra and shape variability (ratios of length, width and height measurements) were compared within and between species and locations. In cidaroid specimens all spines were removed before mass measurements for comparability between specimens as some had either incomplete numbers of spines or epibionts on the spines. Dry mass and ash free dry mass measurements were obtained exclusively from frozen samples. Only the tests of species represented by at least 10 individuals were ashed to obtain ash free dry mass measurements as intact representatives of each species were considered as rare and valuable reference material.
Table II. Echinoid species per station.
Our definitions were as follows,
Wet mass (WM): individuals were unfrozen and pressed onto tissue paper to remove excess moisture for 30 seconds. Their wet mass was then determined to accuracies of 0.001 g.
Dry mass (DM): individuals were oven dried at 60°C for 24 hours in pre-weighed tin foil receptacles. Specimens were allowed to cool to ambient temperature. Thereafter specimens were again measured to accuracies of 0.001 g.
Ash-free dry mass (AFDM): dried individuals were placed in a furnace at 480°C for 24 hours in pre-weighed tin receptacles. Specimens were allowed to cool to ambient temperature in a desiccator containing silica gel. Thereafter specimens were transferred to a microbalance (Satorius MC210P) and the ash measured to accuracies of 0.001 g. The ash mass was then subtracted from the previously recorded DM for each specimen to yield the AFDM to accuracies of 0.001 g.
Despite masses being recorded to 0.001 g accuracy, we only report these to 0.1 g levels due to inherent inaccuracies, such as variation in gut contents across individuals.
Epibiont analysis
Specimens of every species from every site were examined for epifaunal colonists. Up to 24 individuals of each species were studied for attached macrofauna using a binocular microscope. In most cases at least some spines had been lost during the process of being trawled, brought to the surface and landed on the ship's deck. Where a species was represented by many individuals at a site, the most intact specimens were examined. On the echinoids with epifauna (cidaroid species), the colonists were identified to the lowest possible taxonomic level, in most cases species. Each epifaunal species was scored as abundant (present on all specimens examined), occasional (present on < all but > 1 individual) or rare (present on just 1 individual).
Results
Echinoidea were present, sometimes abundant but rarely a dominant component of most shelf trawls at locations around the Scotia Arc. Echinoids were rarely present in any of the continental slope trawls (~1000 or 1500 m depths) but at the Southern Thule site (deep sea) echinoids were only found at 1000 m. Otherwise echinoids were absent from some study depths at some locations but only at South Georgia did they dominate the benthos (Table II). In total 13 species of regular urchins (Fig. 1a) and 10 species of irregular urchins (Fig. 1b) were found. These collections greatly extended the distribution and depth ranges, by thousands of km and hundreds of metres respectively, for several species.
Fig. 1. Distributions of echinoids collected during the BIOPEARL cruise a. regular echinoids, b. irregular echinoids.
Distribution and biometrics of Scotia Arc echinoid species
Where our data extend the depth, test size and/or geographic distribution ranges of echinoid species or the epibiont taxa known from them we show this information in bold. General information for echinoid species on distribution, depth, size and ecology was taken from David et al. (Reference David, Magniez, Villier, De Wever, Fèrd and David2005a) and our new findings were added.
- Distribution
SH (LI 1437 m, EI 884–990 m)
- Depth
884–1437 m
- Size
up to 45 mm horizontal diameter, holotype: 29.3 mm in diameter, 16.9 mm height
- Remarks
Two specimens of Aporocidaris cf eltaniana were collected at 884–990 m at Elephant Island, the shallowest the species has been reported to date.
- Distribution
off CH/MR (30–641 m), FI (124–509 m), SG (13–45 m)
- Depth
13–641 m
- Size
up to 35 mm horizontal Ø (previous 31 mm Ø)
- Remarks
The specimens, collected on the shelf in the Falkland Trough, resemble Austrocidaris spinulosa in their overall morphology, though their primary spines have more barbs than is typical. Our specimens showed very little variation in shape but some in mass to length and wet mass was approximately 2.5x dry mass (Figs 2a & 3).
- Epibiota
They were densely colonized by a diverse range of epibionts, many of which have never been reported either as commensal on echinoids or even other fauna. Their primary spines were colonized by Annelida (6 polychaete species), Bryozoa (15 cheilostome and 2 cyclostome species), Cnidaria (1 hydroid species), Crustacea (1 isopod species), Mollusca (1 bivalve species), Porifera (2 demosponge species), Foraminfera and foliculinid Protozoa.
- Distribution
SH (EI 192–745 m), SO (284–302 m), E-WS (569–624 m, 587–746 m, 350–602 m), RS (589–714 m, 1225–1240 m), BS (350 m, 100–600 m)
- Depth
100–1240 m
- Size
44 mm horizontal Ø (previous 40 mm Ø)
- Remarks
Wet mass was about 3x dry mass.
- Epiobiota
Jacob (Reference Jacob, Terpstra and Brey2001) reported a diverse epifauna from the spines of this species, consisting of spirorbid polychaetes, bryozoans, the bivalve Lissarca notorcadensis, Holothuroidea, and the sponge Jophon radiatus. This study found representatives of all known epibiont groups and recorded serpulid annelids and Foraminfera for the first time.
- Distribution
SH (LI 199–209 m, EI 199–200 m), SO (232–506 m), E-WS (399–462 m, 294–746 m, 302–531 m), DS (540 m), RS (190–375 m, 184–320 m, 256–384 m, 238–340 m, 408–565 m, 344–357 m)
- Depth
184–746 m
- Size
up to 65 mm in diameter
- Remarks
This is the first record of C. gigantea for the South Shetland Islands. Our specimens showed little variation in shape or mass to length. Typically wet mass was about 5x dry mass but two large individuals of similar dry mass did have quite different wet masses (Figs 2b & 3).
- Epibiota
The known epifauna consists of the bivalve L. notorcadensis, the sponge J. radiatus and bryozoans (Jacob Reference Jacob, Terpstra and Brey2001) while this study also found Annelida (1 spirorbid and 1 serpulid species), Chordata (1 ascidian species) and Foraminifera.
- Distribution
AP (450–670 m), SH (LI 32–750 m, EI 73–1230 m), SO (232–662 m), SSI (148–201 m), W-WS (31–704 m), E-WS (498–509 m, 193–898 m, 185–423 m), DM (207–216 m, 300 m), DS (220 m, 219 m), AL (293–329 m), RS (64–836 m)
- Depth
31–1230 m
- Size
50 mm diameter, up to 70 mm diameter
- Remarks
The following epibiotic groups are previously known to occur on this species: foraminiferans, sponges, polychaetes, bivalves, brachiopods, bryozoans, small crinoids and holothurians.
- Distribution
SO (506 m), E-WS (270–509 m, 294–305 m, 301–403 m), DM (200–450 m), DS (450–530 m), KI (250–450 m)
- Depth
23–650 m
- Size
30–40 mm diameter
- Remarks
This is the first record for the species from the South Orkney Islands. Height at size varied more than length to width and typically wet mass was 2.6x dry mass but one specimen had anomalously low mass for its size (Figs 2c & 3).
- Epibiota
Despite being small, C. nutrix was host to a diverse array of epibionts on the primary spines including Annelida, Bryozoa, Cnidaria and Foraminifera.
- Distribution
SH (EI 199–267 m), SO (232–239 m), E-WS (233–406 m, 437–810 m), DS (442–598 m) AL (278–651 m)
- Depth
199–810 m
- Size
71 mm diameter
- Remarks
As in C. nutrix, height varied more than width in its relation to length. Mass to length ratio varied little and wet mass to dry mass ratios (Figs 2d & 3) were similar to C. nutrix and Austrocidaris cf spinulosa.
- Epibiota
No epibionts were known from this species but we found a polychaete, crustacean, echinoderm, bivalve and foraminfera.
- Distribution
FI (339–357 m), SH (LI 160–500 m, EI 192–1120 m), SO (232–761–1012 m), SSI (148–201 m), SG (75–686 m), SR (160–467 m), W-WS (203–512 m, 400 m), E-WS (498–624 m, 587–1353 m, 602–617 m)
- Depth
75–1353 m
- Size
typically 50 mm diameter, but up to 62 mm diameter
- Remarks
We established new depth records for three sites in this widely occurring species. Length to width varied very little but height to length varied considerably (Figs 2e & 3). Wet mass was ≥ 4x dry mass.
- Epibiota
Prior to this study only L. notorcadensis was known as a spine epibiont of this echinoid species but the current study found at least 13 species on 14 specimens. Epibionts included Bryozoa, Crustacea, Echinodermata, Porifera and Foraminifera.
- Distribution
SH (LI 199–209 m), E-WS (64–423 m, 893–898 m, 210–233 m, 390–396 m), LS (200–300 m), DS (202 m)
- Depth
64–898 m
- Size
typically 40–50 mm diameter, up to 52 mm diameter
- Remarks
This is the first record of C. spinosa from the South Shetland Islands and even western Antarctica. Of the cidaroid echinoids, this species varied most in height to length, such that no relationship was evident while the mass/test length relationships were less variable (Figs 2f & 3).
- Epibiota
Jacob (Reference Jacob, Terpstra and Brey2001) reported Bryozoa, the bivalve L. notorcadensis, holothuroidea, and the sponge J. radiatus to occur as epibionts of C. spinosa. In addition Hétérier et al. (Reference Hedgpeth2004) found Annelida, Cnidaria and Foraminifera. In total the current study found 10 specimens supported at least 18 epibiont species, of which foliculinid Protozoa are new reports.
- Remarks
Three species of the genus Sterechinus were found around the Scotia Arc. Examination of live specimens of the Sterechinus species found (listed below) revealed no epibiota on any specimen of any species. The specimens collected during this expedition are used for a comparative study on the calcium carbonate uptake in shell and test building taxa from temperate and polar regions and are not considered further in this study. Their distribution details are listed below.
- Distribution
FI (103–430–509 m), SR (177–199 m), SG (13–970 m), BI (320–471 m) MI (300–500 m)
- Depth
13–970 m
- Size
up to 80 mm diameter
- Distribution
circum-Antarctic
- Depth
32–2012 m
- Size
typically 50 mm diameter, but up to 80 mm diameter
- Distribution
circum-Antarctic
- Depth
0–810 m
- Size
typically 30 mm diameter, but up to 70 mm diameter
- Distribution
off CH/MR (1–10 m, 1–250 m), FI (1–242 m)
- Depth
1–250 m
- Size
25–40 mm diameter
- Epibiota
None found.
- Distribution
SH (LI 160–500 m, EI 19–28 m), SO (11–761 m), SR (3742–3806 m), SG (11–970 m), BI (20–60 m), DS (219 m), AL (20–46 m), off CH/MR (174 m)
- Depth
11–3806 m
- Size
max length up to 50 mm.
- Remarks
The two specimens found were almost at the maximum size recorded (Table III).
- Epibiota
Mortensen (Reference Mooi, Constable, Lockhart and Pearse1951) noted commensal bivalves, especially in the marsupial and on the peristome spines but no bivalves or other associated epibiont species were found on the two specimens collected in this study.
- Distribution
W-WS (246–500 m), SH (LI 160–670 m, EI 20–769 m), SO (150–235 m)
- Depth
20–769 m
- Size
max length in males up to 43 mm, max length in females up to 51 mm.
- Remarks
This study extends the biogeographic distribution of this species to the South Orkney Islands. There is minor variability in shape, both in length to width and to height (Fig. 2 g). We found wet mass to be an unreliable predictor of dry mass (or AFDM, see Fig. 3).
- Epibiota
None known.
- Distribution
SH (LI 199–209 m, EI 199–482 m), SO (150–235 m), DS (333–761 m, 202 m), AL (46 m, 20–30 m), RS
- Depth
20–761 m
- Size
length typically 60–70 mm can reach up to 88 mm
- Remarks
This study extends the biogeographical distribution of this species to the South Shetland and South Orkney islands, therefore a representative specimen is figured (Fig. 4a & b). More variability in length to height than vs width (Fig. 2 h). Wet mass measurements showed two distinct patterns possibly male and female, but this was less obvious in dry mass (Fig. 3). The samples of A. ingens we found were very large south of Livingston Island (> 60 mm length) whereas those around Powell Basin and South Georgia were small (< 46 mm). North of Livingston Island nearly the entire range of A. ingens were found (25–72 mm). Lockart et al. (Reference Livermore, Hillenbrand, Meredith and Eagles1994) report brooding with up to 149 juveniles in Prydz Bay. In the current collection only two specimens carried young in their marsupia.
- Epibiota
None known.
- Distribution
SH (LI 30–92 m, EI), SO (240–257 m), W-WS (51–70 m), DS (8 m, 431 m), AL (35–73 m, 20–46 m, 0–30 m), RS (44–184 m, 13–631 m)
- Depth
8–631 m
- Size
length typically 45 mm but females can reach 67 mm
- Remarks
First species record for the South Orkney Islands (two specimens). Size measurements for the specimens of A. shackletoni collected are given in Table III.
- Epibiota
None known.
- Distribution
BS (300–600 m), SH (LI 70–592 m, EI 174–1230 m), SO (232–1012 m), W-WS (137–512 m, 400 m), E-WS (270–462 m, 193–2012 m, 391–623 m), DS (219 m), DS South (474–500 m), RS
- Depth
70–2012 m
- Size
about 50 mm length
- Remarks
Two specimens resembling Amphipneustes cf lorioli were collected in the southern slope of the South Orkney Islands, the deepest recorded for this location. Size measurements for the specimens of A. cf lorioli collected are given in Table III.
- Epibiota
No epibiota known.
- Distribution
SH (LI 199–209 m), E-WS (399–462 m, 352–1353 m, 406–531 m), DS (532–536 m, 442–598 m, 202–659 m), AL (278–651 m)
- Depth
199–1353 m
- Size
up to 71 mm length (previous known 50–60 mm length)
- Remarks
This is the first record for the South Shetland Islands. The single specimen is the largest example of A. rostratus known (Table III).
- Epibiota
No epibiota known.
- Distribution
SH (LI 199–202–670, EI 192–745 m), SO (150–232–239 m), W-WS (246–320 m), E-WS (270–462 m, 442–1353 m), LS (207–216 m)
- Depth
150–1353 m
- Size
up to 85 mm length (typically 55–60 mm lengths, females up to 77 mm)
- Remarks
At both the South Shetland and South Orkney islands we found B. chesheri shallower than has been recorded in the past. Their sizes are shown in Table III and include one specimen which is the largest ever reported.
- Epibiota
No epibiota known.
- Distribution
SH (EI 199–621 m), SSI (4680–5651), E-WS (1353 m), 60°S 100°E (3607 m)
- Depth
199–5651 m
- Size
37 mm length, up to 61 mm
- Remarks
All five specimens of G. affinis collected were smaller than the reported sizes and with 20–28 mm test length similar in size (Table III).
- Epibiota
No epibiota known.
- Distribution
off CH/MR (115 m), FI (74–595 m), SH (EI 91 m), SO (211–221 m), SG (13–45 m), MI (45–570 m)
- Depth
13–595 m
- Size
78 mm length
- Remarks
The current study extends the known range of the species to both the South Orkney and South Shetland islands. Shape is fairly variable (Fig. 2i) as is length to dry mass (Fig. 3). Wet mass was a poor predictor of dry mass and was highly variable.
- Epibiota
No epibiota known.
- Distribution
SSI (1033–1045 m), DS (442–598 m, 1600 m)
- Depth
442–1600 m
- Size
44–55 mm
- Remarks
This species is one of the least known Antarctic echinoderms. Confirmed distributions of this species are only known from two sites in the Davis Sea (David et al. Reference David, Magniez, Villier, De Wever, Fèrd and David2005a). A record from the Weddell Sea appeared doubtful to David et al. (2005a). They stated “It is possible that one specimen, collected in the WS by the RV Polarstern and identified as P. aff hispida by De Ridder et al. (Reference De Ridder, Lawrence, Jangoux and Lawrence1992), may be P. aurorae.” Because their specimen was different from typical P. aurorae they did not wish to suggest the dramatic change in its geographic distribution. The three specimens collected during the current cruise were clearly identified as P. aurorae by their test morphology and distinct colour (Fig. 4c & d) and extend the species biogeographic range thousands of kilometres beyond its previous confirmed find. Size measurements for the specimens of P. aurorae are given in Table III.
Table III. Individual size measurements of the rare irregular echinoid species.
Cidaroid epifauna
No epifauna were found on any of the species of irregular echinoids, or regular echinoids of the family Echinidae, at any of the sites or depths they were found. Most cidaroid echinoids had epifauna, mainly on their large primary spines, but also elsewhere. These cidaroid echinoids had considerable biodiversity associated with them, including eight phyla of animals as well Foraminifera and foliculinid protists (Table IV). Of the 51 faunal species (representing 10 classes) found on cidaroids all but seven were identified to genus level and most to species. By far the most rich epifaunal taxon was the Phylum Bryozoa, Class Gymnolaemata and the least the ascidians just represented by one species on one echinoid individual. Bryozoans and foraminiferans were the only taxa present as epifauna on every cidaroid species and recorded from every site.
Table IV. Echinoid epibionts. Abbreviations: (x) - number of analysed echinoid specimens, • - abundant, ⊗⊗ - occasional, ○ - rare.
The most colonized individual was an Austrocidaris cf spinulosa from the Falkland Trough, which had 16 macrofaunal species attached. This species had the richest epifauna both in terms of average (6.5 ± 1.4 species) per individual and in total (Table IV). Meaningful comparisons of richness between cidaroid species, sites and depths were difficult because of such unequal sample sizes. ANOVA revealed no significant differences between echinoid species or sites (F4,3 < 2.4, P > 0.056). There were, however, significant differences between the sample depths (F2 = 27.8, P > 0.001). The shallowest sample depths (160–200 m) were the richest with 4.89 (± 0.48, n = 38) epifaunal species per individual compared to 0.79 (± 0.19, n = 25) at 500 m and 0.43 (± 0.3, n = 7) at 1000 m. Thus there was an order of magnitude decrease in epifaunal richness from the shallow continental shelf to the continental slope.
Discussion
What we know about the sea floor of the Southern Ocean suggests that the macrofauna there is rich, can be abundant and much of it lives nowhere else (Arntz et al. Reference Arntz, Brey and Gallardo1994, Reference Arntz, Gutt, Klages, Battaglia, Valencia and Walton1997, Brandt et al. Reference Brandt, De Broyer, De Mesel, Ellingsen, Gooday, Hilbig, Linse, Thomson and Tyler2007a). In the shallows, the depth for which we know by far the most, echinoids are typically very abundant and ecologically important, not dissimilar to elsewhere in the world (Andrew et al. Reference Andrew, Agatsuma, Ballesteros, Bazhin, Creaser, Barnes, Botsford, Bradbury, Campbell, Dixon, Einarsson, Gerring, Hebert, Hunter, Hur, Johnson, Juinio-Menez, Kalvass, Miller, Moreno, Palleiro, Rivas, Robinson, Schroeter, Steneck, Vadas, Woodby and Xiaoqi2002, Jacob et al. Reference Hotchkiss and Craddock2003). Unlike elsewhere at most shallow localities around Antarctica this abundance is represented by the same single species. However, 74 echinoid species are known from the Southern Ocean (David et al. Reference David, Magniez, Villier, De Wever, Fèrd and David2005a) of which we found nearly a third in 38 trawl samples or 50 500 mReference Andrew, Agatsuma, Ballesteros, Bazhin, Creaser, Barnes, Botsford, Bradbury, Campbell, Dixon, Einarsson, Gerring, Hebert, Hunter, Hur, Johnson, Juinio-Menez, Kalvass, Miller, Moreno, Palleiro, Rivas, Robinson, Schroeter, Steneck, Vadas, Woodby and Xiaoqi2 within a small region, the Scotia Arc. The single species so dominant in abundance in the shallows and in the scientific literature, Sterechinus neumayeri, was found in just a single shelf sample. Few if any epibiotic species have ever been reported associated with S. neumayeri, so in the shallows echinoids are neither species rich nor harbourers of richness. The current study shows that the shelves around the Scotia Arc are both rich in species numbers of echinoids and their associated fauna but also that unlike the shallows they rarely dominate there.
What does echinoid distribution tell us about Southern Ocean benthos?
Echinoids are typically large, obvious and fairly easily identifiable animals for which a comprehensive database and identification guide to Southern Ocean species has been established (David et al. Reference David, Magniez, Villier, De Wever, Fèrd and David2005a). There can be few taxa that will better reveal how well we know the Southern Ocean fauna. At a family level our findings were as might be expected. Most Antarctic echinoid species known are representatives of two dominant families, the Schizasteridae (22 species known) and Cidaroidae (15 species known) (David et al. Reference David, Magniez, Villier, De Wever, Fèrd and David2005a). So it was in our Scotia Arc shelf samples, these two families being represented by nine species each. The Echinidae, typically the most abundant but not species-rich, Antarctic family dominated the total numbers of specimens but were represented by just three species.
The current study of continental shelf and slope depths found 23 species at seven geographical localities. None of the 23 species we found were new to science - all were clearly identifiable as known species. At the next scale down, the number of echinoid species found represent a substantial proportion of the total. As 14 species have previously only been reported much deeper than we sampled (Brandt et al. Reference Brandt, De Broyer, De Mesel, Ellingsen, Gooday, Hilbig, Linse, Thomson and Tyler2007a), the 23 samples we report here comprise more than 38% of the known shelf and slope echinoids we could have expected to find. Either the Scotia Arc is disproportionately rich or disproportionably well sampled or both. Evidence of other scientific cruise paths and studies of other taxa suggests the Scotia Arc is both amongst the best studied of Antarctic regions and also very rich in species (e.g. Tatiàn et al. Reference Smellie, Morris, Leat and Turner2005, Ramos-Esplà et al. Reference Ramos2005, Hilbig et al. Reference Hétérier, De Ridder, David, Rigaud, Heinzeller and Nebelsick2006, Linse et al. Reference Linse, Barnes and Enderlein2006b, Clarke et al. Reference Clarke, Griffiths, Linse, Barnes and Crame2007, Primo & Vazquez Reference Poulin and Féral2007, Barnes & Griffiths Reference Barnes and Griffiths2008). At a finer scale, for many of the echinoid species we found, the localities, depths or sizes were new. For eight (~35%) of these, this was the first record of the species in the areas we found them in - the next nearest localities where they had previously been found were hundreds to thousands of kilometres away. Three species were found in shallower water than previously reported and four at larger sizes than previously known. Thus status of the echinoid species we found was changed by this study despite our sample protocol taking only single samples at each depth, focussing on the most sampled depth range, in one of the more sampled regions and the taxon being one of the most obvious and well known. In contrast to the Scotia Arc, sampling less well-known regions, such as the Amundsen Sea, should almost certainly increase known geographic and bathymetric ranges as well as unearthing new species.
Only two (28.6%) of the nine families but 27 (54%) of the 50 species known to occur within the Scotia Arc were not found by our sampling regime. Considering the small size of our sample areas and lack of replicates at each depth this very high ‘find rate’ suggests echinoid species are both fairly common and ubiquitous within the areas in which they occur. This certainly contrasts with patterns shown by some other taxa (e.g. isopod crustaceans, which appear to be highly patchy: equivalent sampling would only capture a tiny proportion of species at a given locality (Kaiser et al. Reference Jacob2007)). These two taxa seem to represent examples of opposite extremes of distribution, but we suggest that it is the echinoids which are unusual. Scientific sampling expeditions around the Scotia Arc have generally found both low proportions of e.g. ascidians, bryozoans, polychaetes, molluscs or other taxa known to occur in an area and often new species of each (Ramos Reference Quale, Peck, Peat, Ellis-Evans and Harrigan1999, Arntz & Brey Reference Arntz and Brey2003, López-Fe Reference Lovell and Trego2005, Linse Reference Linse, Griffiths, Barnes and Clarke2008).
Southern Ocean biogeography
Despite being one of the less speciose classes in Antarctica (Clarke & Johnston Reference Clarke and Johnston2003), investigations of echinoid distribution can be particularly useful at elucidating Southern Ocean biogeography. Ease of identification makes literature data more reliable, most of their reproductive patterns are known, their fossil record is relatively (for the Southern Ocean) good and it is unlikely many new species will be found. Because the reproductive strategies of most Antarctic echinoids are known (Poulin et al. Reference Pena Cantero2002, Pearse & Lockhart Reference Pearse and Giese2004, David et al. Reference David, Magniez, Villier, De Wever, Fèrd and David2005a), distributions can be linked to apparent dispersal ability and thus how marine habitats in Antarctic have been colonized. The opportunity for a locality to be colonized and its subsequent diversity is dependent on geographic isolation and geological age of the locality. A strong fossil record, such as in the echinoids (Hotchkiss Reference Hilbig, Gerdes and Montiel1982, Néraudaeu et al. 2000), is particularly important around Antarctica where there have been massive oceanographic and climatic changes (e.g. Barrett Reference Barrett2001, Matsumoto et al. Reference Massin and Hétérier2001, Mackensen Reference López-Fe, Moyano, Cancino and Wyse-Jackson2004, Livermore et al. Reference Linse2004, Reference Livermore, Eagles, Morris and Maldonado2007, Maldonado et al. Reference Mackensen2006) but there are poor preservation conditions. The current knowledge in Antarctic echinoid biogeography is summarized in David et al. (Reference David, Magniez, Villier, De Wever, Fèrd and David2005a, Reference David, Choné, Festeau, Mooi and De Ridder2005b) and is publicly available in the SCAR MarBIN database (http://www.scar-marbin.be). Of the nine echinoid species for which the current study extends the known ranges, four are noteworthy (Fig. 5). With the exception of Abatus curvidens, all seem to be widely distributed around the Southern Ocean, supporting an old notion of Antarctic species being circumpolar (Hedgpeth Reference Hayward1969, Clarke & Johnston Reference Clarke and Johnston2003). Echinoids are probably now one of the best examples of this concept, which has not proved so true in other taxa examined in detail (see Peña Cantero Reference Pearse and Lockhart2004, Allcock Reference Allcock2005, Collins & Rodhouse Reference Collins and Rodhouse2006, Linse et al. Reference Linse, Barnes and Enderlein2006b, Barnes & Griffiths Reference Barnes and Griffiths2008).
Fig. 2. Test height and width relationships with test length in the regular echinoids a.Austrocidaris aff. spinulosa, b.Ctenocidaris gigantea, c.C. nutrix, d.C. rugosa, e.C. speciosa, and f.C. spinosa, and the irregular echinoids g.Abatus curvidens, h.A. ingens and i.Tripylaster philippi.
Fig. 3. Mass relationships with test length in regular and irregular echinoids for a. wet mass (WM), b. dry mass (DM), and c. ash free dry mass (AFDM).
Fig. 4. Specimens of a. & b.Abatus ingens Kœhler, 1926 and c. & d.Pourtalesia aurorae Kœhler, 1926. a, b. BAS 06-273-13, c. BAS 06-744-02, d. BAS 06-744-03. Scale bar 10 mm.
Fig. 5. Biogeographical distributions of echinoid species with new records. Known distribution records are marked in black filled-in labels, new records in open labels.
Of the species where we extended the ranges, only Tripylaster philippi occurs north and south of the Polar Front. Geographic distribution ranges crossing the Polar Front are known for a further 23 echinoids species, especially for deep sea species of the families Pourtalesidae and Urechinidae. Of shelf species, six species of Schizasteridae, five species of Cidaridae, three species of Echinidae and the arbaciid Arbacia dufresnii (Blainville, 1825) show cross-Polar Front distributions. Previously all records of T. philippi were Magellan or sub-Antarctic but our findings make it clear that it is a high-Antarctic species as well. The echinoids represent one of the best taxa to establish fairly reliable current range estimates and thus monitor Antarctic marine biological responses to climate change. Elsewhere in the world range extensions and distributional changes have been one of the most obvious signals of regional warming (Walther et al. 2002). The Scotia Arc is both a centre for warming (Quale et al. Reference Primo and Vazquez2002, Convey Reference Convey, Bergstrom, Convey and Huiskes2006) and the only shelf/slope link of the Southern Ocean to areas north of the Polar Front; this makes it the obvious place to look for organismal changes and invasions.
With one exception all new records we found were on the shelves of the South Shetland and South Orkney archipelagos. This is surprising as these islands are amongst the best-sampled areas in the Southern Ocean (e.g. Ramos Reference Quale, Peck, Peat, Ellis-Evans and Harrigan1999, Arntz & Brey Reference Arntz and Brey2003, Arntz et al. Reference Arntz, Thatje, Gerdes, Gili, Gutt, Jacob, Montiel, Orejas and Teixido2005b). In the Southern Ocean only in the Ross Sea has a similar intensity of sampling been reported at species level (Chiantore et al. Reference Chiantore, Guidetti, Cavallero, De Domenico, Albertelli and Cattaneo-Vietti2006, De Domenico et al. Reference David, Choné, Mooi, De Ridder, Wägele and Sieg2006). The only echinoid we found on the slopes of the geologically young, isolated island of Southern Thule, South Sandwich Islands, was the deep-water species P. aurorae. A priori our expectation was that any echinoids at such a location would be those either with planktotrophic larvae (i.e. wide and fast dispersers) or deeper species colonizing up the slope from the surrounding abyssal plains. Our finding of P. aurorae, only the third confirmed record for this species, is interesting as its previously confirmed closest location was thousands of kilometres away in the Davis Sea.
Bathymetry and Antarctic benthos
The current study reports 19 trawls sampled at both shelf and slope depths. However the area sampled was 19.631 mReference Andrew, Agatsuma, Ballesteros, Bazhin, Creaser, Barnes, Botsford, Bradbury, Campbell, Dixon, Einarsson, Gerring, Hebert, Hunter, Hur, Johnson, Juinio-Menez, Kalvass, Miller, Moreno, Palleiro, Rivas, Robinson, Schroeter, Steneck, Vadas, Woodby and Xiaoqi2 from 160–500 m compared with 30.870 mReference Andrew, Agatsuma, Ballesteros, Bazhin, Creaser, Barnes, Botsford, Bradbury, Campbell, Dixon, Einarsson, Gerring, Hebert, Hunter, Hur, Johnson, Juinio-Menez, Kalvass, Miller, Moreno, Palleiro, Rivas, Robinson, Schroeter, Steneck, Vadas, Woodby and Xiaoqi2 at 1000–1500 m. Whilst the shelf samples yielded 19 species the slope samples, despite the greater area, contained just four. The greater supply of organic matter to the shelf makes such a result unsurprising, especially considering echinoids are often primary consumers, but also grazing generalists and deposit feeders (De Ridder & Lawrence Reference De Domenico, Chiantore, Buongiovanni, Ferranti, Ghione, Thrush, Cummings, Hewitt, Kroeger and Cattaneo-Vietti1982). However, just because each species is more abundant, and therefore more likely to be sampled on the shelf does not necessarily mean the shelves are richer in echinoids. It seems likely that with increasing depth proportionally greater areas need to be sampled to reach asymptote. This is supported by the fact that we found a smaller proportion of the echinoid species known to live below 1000 m depth than the proportion of those known to live on the shelf despite sampling 64% more of the deeper area. Antarctic benthos is known to be more eurybathic than fauna at most other locations (Brey et al. Reference Brey, Dahm, Gorny, Klages, Stiller and Arntz1996). This varies between groups (Hilbig et al. Reference Hétérier, De Ridder, David, Rigaud, Heinzeller and Nebelsick2006, Kaiser & Brandt Reference Kaiser, Barnes and Brandt2007). The echinoid species reported here are quite eurybathic, their mean depth range being 1241 m (± 245 m) and only one of these has a known depth range of < 500 m. All but Aporocidaris eltaniana occur on the continental shelf yet nearly all these echinoid species occur deeper than 750 m. That the current study only found three incidences of species occurring outside previously known depth ranges suggests that the pattern of echinoid bathymetric occurrence is probably fairly robust.
Size and biomass
As with bathymetry, the state of knowledge on maximum sizes in Antarctic echinoids seems to be fairly good. Our measurements of echinoid specimens generally lay within the size ranges reported by Jacob (Reference Jacob, Terpstra and Brey2001) and David et al. (Reference David, Magniez, Villier, De Wever, Fèrd and David2005a). Antarctic echinoids may grow very slowly (Brockington Reference Brockington2001), especially at larger size/age, so increases in 8–9 mm of test diameter that we report for Ctenocidaris spinosa, A. rostratus and B. chesheri may have significant implications for their lifespan. It is likely that even this small increase in diameter of nearly 1 cm might mean these species live decades more than previously thought. However, we appreciate that site and food availability differences could account for significant differences in growth characteristics (David & Laurin 1991, Mespoulhé & David Reference Matsumoto, Lynch-Stieglitz and Anderson1992).
Echinoids can often be the major component of shelf biomass and representatives of the Echinidae can fill ROV film of benthos or trawls from Antarctic shelves (e.g. Barry et al. Reference Barry, Grebmeier, Smith and Dunbar2003, Cranmer et al. Reference Cranmer, Ruhl, Baldwin and Kaufmann2003). However, of the 38 trawls in the current study, only one was dominated by echinoids suggesting that our view of them as a dominant group based on super-abundance in the shallows is rarely the case at depth. Most regular echinoids showed straightforward increases in mass with increasing test length, though strangely C. spinosa showed negligible increase in mass with length (Fig. 2). Echinoid contribution to biomass can be reported as simple wet mass, but we found this to be highly variable between species. Relationships between dry mass and ash free dry mass were more robust but whilst cidaroid species were typically ~17% tissue mass, irregular species varied from 17.7% (A. curvidens) to 11.2% and 8.9% (A. ingens and T. phillipi respectively). It is clear both that meaningful estimates of echinoid contributions to biomass need to involve identifications to species level and that irregular species show considerable intraspecific variability.
Echinoid associated biodiversity
In tropical and temperate seas, echinoids are often associated with changing levels of biodiversity through their grazing activities. Keystone roles in mediating biodiversity (see Elner & Vadas Reference De Ridder, David and Larrain1990) are unlikely in the Antarctic as most species occur below the depth of macroalgae and ice scour is pivotal in the shallows (see David et al. Reference David, Magniez, Villier, De Wever, Fèrd and David2005a, Barnes & Conlan Reference Barnes and Conlan2007). However, whilst most echinoids, such as Echinidae or Schizasteridae, are rarely fouled by epibionts, the Cidaroid families carry a variety of taxa (Jacob Reference Jacob, Terpstra and Brey2001, David et al. Reference David and Laurin2003, Hétérier et al. Reference Hedgpeth2004, Massin & Hétérier Reference Maldonado, Bohoyo, Galindo-Zaldivar, Hernandez-Molina, Jabaloy, Lobo, Rodriguez-Fernandez, Surinach and Vazquez2004). A variety of animal externa from pycnogonan legs to brachiopod shells can be important, particularly with increasing depth because of the rarity of hard surfaces (Barnes & Clarke Reference Barnes and Clarke1995). The biodiversity associated with our study cidaroid species is greater (at all taxonomic levels) known to the authors, than has ever been previously described on any other Antarctic organism externa. Such cidaroid associated biodiversity declined considerably with depth but is probably quite important at all depths. Firstly, the 70 cidaroids examined represent only a relatively small amount of surface area, yet had 10 classes and 51 benthic species associated with it (Table IV). Representatives of up to eight phyla had been previously reported from a study of two species of Antarctic cidaroids, but were not identified beyond phylum level (Hétérier et al. Reference Hedgpeth2004). Some of the associated species in the current study are otherwise very rare. For example Escharoides torquata found on N. mortenseni at Elephant Island had only previously been found at a single site at South Georgia (Hayward Reference Griffiths, Linse and Barnes1995). Secondly, there was little overlap in epibiota between different cidaroid specimens suggesting other specimens would contribute further to local biodiversity. Third, many of the species, which occurred as cidaroid epibiota, were not otherwise found in those trawls or even areas (BIOPEARL unpublished data). Many such species only or mostly occur as epibiota (Barnes & Clarke Reference Barnes and Clarke1995). For trawls of the BIOPEARL cruise in which cidaroids were present, echinoid associated fauna was (on average) > 38% of the total number of species recorded, clearly a significant contribution to total biodiversity of a local area. In addition in a number of trawls the epibionts of cidaroids were a major proportion of all the sessile (and even total) species found. Finally most of the epibiota were sessile without planktotrophic larvae and thus with limited powers of dispersal. Being attached to mobile echinoids increases possibilities for dispersal and so colonization of this component of biodiversity.
In summary, this study provides results on the geographic distributions of echinoid species, including ranges extensions in nine species, on their test size and biomass relationships and on their associated epibiont biodiversity. Our data enhances the knowledge on biogeography and biodiversity patterns in the Antarctic benthos and shows the need for more, internationally co-operative research to establish a comprehensive picture of the biodiversity of shelf, slope and deep sea habitats of the Southern Ocean.
Acknowledgements
The authors are grateful to the captain, officers and crew of RRS James Clarke Ross who enabled us to collect the samples for this study as well as to our joint colleagues on the cruise who helped sorting samples on deck. We thank C. De Ridder and J. Bohn for their constructive reviews that have led to an improved manuscript. This paper is a contribution to British Antarctic Survey core project BIOPEARL, and linked with the SCAR EBA programme.
