Polar Biology

, Volume 37, Issue 1, pp 73–88

Brittle stars from Southern Ocean (Echinodermata: Ophiuroidea)

Authors

    • Área de Zoología, Facultad de CienciasUniversidad de Extremadura
  • Pablo J. López-González
    • Biodiversidad y Ecología de Invertebrados Marinos, Departamento de Zoología, Facultad de BiologíaUniversidad de Sevilla
Original Paper

DOI: 10.1007/s00300-013-1411-8

Cite this article as:
Martín-Ledo, R. & López-González, P.J. Polar Biol (2014) 37: 73. doi:10.1007/s00300-013-1411-8

Abstract

The present biogeographic study on the ophiuroid fauna from the Southern Ocean (SO) contains an updated checklist, based on a compilation of all the published information provided for the Antarctic and sub-Antarctic regions as well as the information available in SCAR-MarBIN database. Faunal composition and geographical and bathymetric distribution are included. So far, 219 species have been recorded, of which 126 are endemic to the SO, 76 are exclusive to Antarctic waters, and 30 are exclusive to sub-Antarctic waters. This study corroborated the circumpolar and eurybathic character of the ophiuroid fauna of the SO, but some differences are discussed when considering shelf and deep-sea fauna in the whole SO, or in the Antarctic and sub-Antarctic regions separately. The biogeographic affinities of 17 areas considered in the SO are revised, based on a presence/absence datamatrix of the 219 species. This similarity analysis shows three main groups, two of them including sub-Antarctic areas and one for Antarctic areas. The faunal movement patterns between the main geographical connections have been based on historical site records of each species. These movements have a level of faunal exchange that exceeds that of other Antarctic benthic groups. Such movements are mainly from Antarctic and sub-Antarctic regions to the subtropical waters of South America, and from New Zealand and southern Australian waters to sub-Antarctic areas. In this context, the origin of the ophiuroid Antarctic fauna is discussed.

Keywords

AntarcticaBenthosOphiuroidsBiogeographyEndemismCircumpolarity

Introduction

Ophiuroids are one of the most important Southern Ocean (SO) benthic groups, due both to their biomass and to their diversity, being present from shallow to deep waters of the Antarctic and sub-Antarctic regions (Fell 1961; Fell et al. 1969; Dahm 1999; Brandt et al. 2007). The fact that benthos evolved in isolation and separated from other oceans since the Palaeocene, and the absence of durophagous predators has been suggested to be direct causes of their diversity (Clarke et al. 2004; Gili et al. 2006). Moreover, this isolation, along with extant ecological conditions in the Antarctic and sub-Antarctic regions, might be the origin of the biological characteristics of Antarctic ophiuroids, which they share with other Antarctic benthic organisms, such as the high number of brooding species (Mortensen 1936; Arnaud 1974) and their tendency to have opportunist feeding habits (Dearborn 1977; McClintock 1994).

The taxonomic study of the ophiuroid fauna of the SO started with the publication in 1843 of Neue Beiträge zur Kenntniss der Asteriden by the Germans Johannes Müller and Franz Hermann Troschel. In their publication, Müller and Troschel (1843) described the species Ophiolepis chilensis (now in Ophiophragmus), an ophiuroid collected by Rudolph Amandus Philippi in the coastal waters of the South of Chile, possibly in the archipelago of Chiloé (Bernasconi and D’Agostino 1977). Fifteen years later, Philippi himself described the first species found in both Antarctic and sub-Antarctic waters: Gorgonocephalus chilensis and Ophiactis asperula (see Philippi 1858). For over 168 years, there have been numerous studies from the first expeditions to sub-Antarctic waters conducted by Hassler, Gazelle and Challenger, to the epic Belgica, Scotia, Gauss, Pourquoi Pas? Aurora and Discovery during the so-called Heroic Age of Antarctic exploration. All of them led to the publication of the most important papers on SO ophiuroids: Studer (1876), Lyman (1875, 1882), Koehler (1901, 1908, 1912, 1922), Hertz (1927) and Mortensen (1936). The last species that has been described is Ophiacantha wolfarntzi Martín-Ledo, Sands and López-González, 2013 in the waters of the South Georgia Islands (Martín-Ledo et al. 2013).

The first biogeographic study of the ophiuroids from the SO was carried out by Studer (1885), who composed a list of 29 species distributed in South America [Magellan region and Falkland (Malvinas) Islands], Kerguelen arc islands and South Georgia. Ludwig (1899) compiled a total of 62 species, of which 19 were from New Zealand (which the author includes within the sub-Antarctic region). After the expedition Pourquoi Pas? Koehler (1912) composed a total of 105 species distributed in both the Antarctic and the sub-Antarctic regions, distinguishing between abyssal and littoral forms, and indicating those that were exclusive to each region. Hertz (1927) grouped the 89 species of ophiuroids that had been reported in waters under 60°S, according to three Antarctic regions (East, West and the waters of South Victoria Land), and distinguishing between shelf and deep-sea species. Fell (1961) made a biogeographic analysis of ophiuroid distribution, based on thermal and bathymetric tolerance patterns. Fell et al. (1969) compiled a list of 142 species with distribution in the Antarctic and sub-Antarctic regions, as well as of 36 species from the waters of adjacent regions (South Africa, Australia and New Zealand). Smirnov (1994) recorded a total of 93 species, 73 of which were endemic to Antarctic and sub-Antarctic shelf areas and made a biogeographic analysis of the species. Sands et al. (2012) recorded 57 species from West Antarctic sector of the SO. Other biogeographic studies that cover areas of the SO and their relationship with adjacent waters are those conducted by Fell (1947, 1953a, b), Dawson (1965, 1970) and O’Hara et al. (2011, 2012) for New Zealand and Australia waters, Castillo (1968), Jaramillo (1981), Dahm (1999) and Barboza et al. (2011) for the waters of South America.

In this paper, we present an updated inventory of 219 species of ophiuroids from the SO, discussing historical, biogeographic and diversity aspects. A comparative analysis of Antarctic and sub-Antarctic ophiuroid faunas is also included, reviewing the hypotheses that interpret their origin and biogeographic distribution.

Materials and methods

For this bibliographic study, over a hundred bibliographic references describing or reporting ophiuroid species present in the SO, as well as different works on the biogeography and ecology of ophiuroids, have been revised. We also took into account the records from SCAR-MarBIN database made by an expert in the taxonomy of ophiuroids (Igor Smirnov, ZIN). The diversity and biogeographic patterns in the SO of this zoological group have been explored with the purpose of comparison in concordance with previous works carried out on other benthic Antarctic organisms, and on benthos in general, such as those by Clarke and Crame (1989, 1992), Arntz et al. (1994, 2005, 2006), Brandt (1999), Munilla (2001), López-González and Williams (2002), Clarke and Johnston (2003), Clarke et al. (2004), Gili et al. (2006), Linse et al. (2006), Smith et al. (2006), Rodríguez et al. (2007), Brandt et al. (2007), Barnes and Griffiths (2008), Munilla and Soler (2009), Primo and Vázquez (2009), Griffiths et al. (2009), Griffiths (2010), O’Loughlin et al. (2010) and De Broyer and Danis (2010).

In this study, the SO is considered to extend from SOs of the Subtropical Front to the coasts of the Antarctic continent (Deacon 1982; Rodríguez et al. 2007). The Antarctic region extends from the coastal waters of the continent to the Antarctic Polar Front, including Bouvet Island, while the waters of the sub-Antarctic region are those located between the Subtropical Front and the Antarctic Polar Front (Hedgpeth 1969, 1970; Dell 1972). According to previous studies (Munilla 2001; Clarke and Johnston 2003; Linse et al. 2006; Rodríguez et al. 2007), we consider the limit of continental shelf fauna is at 1,000-m depth.

Within each region (Antarctic or sub-Antarctic), the following biogeographic areas were established:
  • Antarctic region: A = Amundsen Sea; B = Bellingshausen Sea; Bo = Bouvet Island; E = East Antarctic zone (from Dronning Maud Land to Victoria Land); P = Antarctic Peninsula and islands (South Shetland included); R = Ross Sea; S = Scotia Sea (including the Scotia Arc island: South Georgia, South Sandwich, South Orkneys); W = Weddell Sea.

  • Sub-Antarctic region: AC = sub-Antarctic New Zealand islands (Auckland and Campbell); Ar = Argentine coast (to 40°S) and Falkland (Malvinas) Islands; C = Crozet Island; Ch = Chilean coast (to 40°S); HM = Heard and McDonalds Islands; K = Kerguelen Islands; M = Macquarie Island (Macquarie Ridge included); MP = Marion and Prince Edwards Islands; SOA = Southern Ocean Atlantic sector; SOI = Southern Ocean Indian sector; SOP = Southern Ocean Pacific sector; T = Tristan da Cunha group (Gough included).

We summarised all the species recorded in each of these areas in a presence/absence matrix, which was later analysed with PRIMER v6 (Clarke and Gorley 2006). Faunistic similarities were established by using the Bray–Curtis index (Bray and Curtis 1957). Subsequently, relations between areas were illustrated by dendrograms (Cluster).

Bathymetric information was considered in both directions. Firstly, considering bathymetric segments (e.g. 0–1,000, 0–2,000, 0–3,000), in which the total number of species present and those exclusive for that segment were take into account. Secondly, in order to explore and quantify a stenobathic or eurybathic behaviour in the two main bathymetric zones [shelf (0–1,000 m) and deep (1,001–6,000 m)] at the different regions, the following formulation, as a stenobathic–eurybathic index (Bruno David, pers. comm.), was calculated for each species:
$${\text{S}} - {\text{E index}} = \left[ {{\text{Difference in meters between the deepest and the shallowest known records}}/{\text{the deepest known record}}} \right] \times 100.$$
The S–E indices are expressed in percentages and vary from values close to 0 (when the bathymetric distributional range of a species is narrow) to others close to 100 (when the bathymetric distributional range of a species is wide). Values of all species based on S–E index were plotted by classes (e.g. 0–9, 10–19, 20–29) in order to know the main trends of shelf and deep fauna in the SO, Antarctic and sub-Antarctic regions.

Results

The geographical distribution, bathymetry and references of all the species considered in this study are shown in the Online Resource 1. The 219 species of ophiuroids present in the SO represent 10.6 % at a global scale. The total number of ophiuroid species is 2,064, which belong to 270 genera (Stöhr et al. 2012). Regarding the specific and generic richness of each of the 11 ophiuroid families present in the SO (Fig. 1), two families (Ophiuroidea 22 gen. and Ophiacanthidae 14 gen.) represent 56.3 % of the diversity of genera in the SO. These families also represent 63 % (with 101 spp. and 37 spp., respectively) of the total number of species in the SO. The family Amphiuridae stands out: with only 4 genera, it represents 38 species (17.4 %) of the SO. The 11 families are present in the sub-Antarctic region, while the families Asteronychidae, Euryalidae and Ophiodermatidae have no representatives in the Antarctic region. There are no endemic families to the SO.
https://static-content.springer.com/image/art%3A10.1007%2Fs00300-013-1411-8/MediaObjects/300_2013_1411_Fig1_HTML.gif
Fig. 1

Richness of species and genera of the ophiuroid families presented in the SO

Among the 64 ophiuroid genera present in the SO (23.7 % of the total number worldwide), 38 are from the Antarctic region, 52 are present in the sub-Antarctic region, and 26 are common to both regions. There are 11 genera exclusive to the SO, 9 of which are endemic to the Antarctic region (Astrochlamys, Astrohamma, Ophioplexa, Ophiodaces, Ophiomages, Euvondrea, Ophiolebella, Ophiosparte and Ophioperla). All of them—except for Astrochlamys, which has 2 species—are monotypic. One genus is exclusive to the sub-Antarctic region (Ophioparva), besides being monotypic. In addition, there is a genus which is common to both regions (Ophionotus, with 3 species). The genus Ophiosteira, which so far was considered endemic to the Antarctic region (Smirnov 1994), now includes one species from Ecuadorian waters (Ophiosteira koehleri A.H. Clark, 1917), which was not accounted for in this study. The two genera with the highest number of species in the SO are Amphiura (27 spp.) and Ophioplinthus (24 spp.). The genus Ophioplinthus is the most diversified in the Antarctic region, with 20 species, 14 of which are endemic; in the sub-Antarctic region, the most diversified genus is Amphiura, with 20 species, 3 of which are endemic. The genera Ophiacantha, Ophiura and Amphiura are the only ones, which are present in all the areas analysed of the two regions of the SO. The area with the greatest diversity is the Scotia Sea, with 30 genera, followed by the East Antarctic zone, with 29 genera. In sub-Antarctic waters, the areas with the greatest diversity are Chilean coast with 22 genera and Kerguelen Island with 21 genera. On the other hand, with reference to the richness of species per geographic region and area (Table 1), 76 species (58 % of a total of 131 spp.) are endemic to the Antarctic region, if we take each area separately, endemicity is relatively low, and therefore, there is a broad distribution of species. There are 51 circumpolar species (23.3 % of the total number of species in the SO), a species being considered circumpolar when it has been recorded in at least three widely separated areas. In the sub-Antarctic region, there are 136 species, 30 of which (22.1 %) are endemic, being the Chilean coast area (to 40°S) the one which presents the greatest number of exclusive species (11 spp.). The Antarctic and sub-Antarctic regions share 48 species (21.9 %), 20 of which (9.1 %) have not been found outside the Subtropical Front. According to these data, 57.5 % (126 spp.) of ophiuroid species present in the SO (Antarctic and sub-Antarctic regions) are exclusively from this biogeographic region, which means 6.1 % of the total number of ophiuroid species worldwide.
Table 1

Species richness from geographic area

Species in the world (according to Stöhr et al. 2012)

2,064

Species in the SO (endemic)

219 (126)

Species reported in Antarctic waters (endemic)

131 (76)

Species reported in sub-Antarctic waters (endemic)

136 (30)

Common species in Antarctic and sub-Antarctic waters (endemic)

48 (20)

Antarctic circumpolar species

51

Species reported in and out of Antarctic and/or sub-Antarctic waters

92

Endemicity of species from Antarctic zones (76 spp.)

 

 Amundsen Sea

0

 Bellingshausen Sea

4

 Bouvet Island

0

 East Antarctic zone

11

 Antarctic Peninsula and South Shetland

1

 Ross Sea

3

 Scotia Sea

8

 Weddell Sea

1

 Endemic species common in two or more Antarctic zones

44

Endemicity of species from sub-Antarctic zones (30 spp.)

 

 Sub-Antarctic New Zealand Islands (Auckland and Campbell)

1

 Crozet Island

0

 Heard and McDonalds Islands

0

 Kerguelen Islands

4

 Macquarie Island

0

 Marion and Prince Edwards Islands

3

 Argentine coast (to 40°S) and Falkland Islands

3

 Chilean coast (to 40°S)

11

 Southern Ocean Atlantic sector

1

 Southern Ocean Indian sector

3

 Southern Ocean Pacific sector

0

 Tristan da Cunha group

2

 Endemic species common in two or more sub-Antarctic zones

2

The area with the highest diversity (see Tables 1, 2 comparatively) is the East Antarctic zone, with 85 species recorded (64.9 % of the species of Antarctic waters), 37 of which are not circumpolar and 11 are endemic. In second place is the Scotia Sea with 74 species (56.5 %). In sub-Antarctic waters, the areas with the greatest species diversity are Chilean coast with 35 species recorded (25.7 % of the species of sub-Antarctic waters) followed by Kerguelen Island with 32 species (23.5 %). The most common species in areas of the SO are Gorgonocephalus chilensis, Astrotoma agassizii, Ophiacantha antarctica, Ophiacantha vivipara, Ophiolimna antarctica, Ophioleuce regulare, Amphiura eugeniae, Amphiura joubini and Ophioceres incipiens. The endemic species of the Antarctic region with the broadest distribution are Astrochlamys bruneus, Ophiocten dubium, Ophiocten megaloplax, Ophiosteira antarctica, Ophionotus victoriae, Ophiura rouchi, Ophioplinthus gelida, Ophioplinthus brevirima, Ophioplinthus wallini and Ophioperla koehleri. The species present in the sub-Antarctic region (and not recorded in the Antarctic region) with the widest geographic expansion are Asteronyx loveni, Amphiura (Amphiura) magellanica and Amphipholis squamata.
Table 2

Number of species recorded in each area (in bold) and common species between different areas

Antarctic region

S

74

                

P

50

65

               

B

27

25

36

              

A

17

18

15

22

             

R

35

39

24

18

50

            

W

44

45

25

16

37

65

           

E

48

48

27

19

42

54

85

          

Bo

7

6

4

2

5

7

6

7

         

Sub-Antarctic region

Ar

19

16

10

6

11

15

16

2

31

        

Ch

13

10

8

4

6

8

10

2

15

35

       

K

18

13

8

6

13

12

17

1

11

10

32

      

C

13

8

8

6

10

9

12

1

7

8

12

17

     

MP

12

8

6

3

7

9

13

1

6

7

13

8

24

    

HM

11

9

7

3

8

7

9

1

8

7

16

6

8

17

   

AC

3

3

1

1

3

3

3

0

3

4

3

1

3

1

24

  

M

7

6

4

3

7

6

9

0

6

5

5

4

3

1

9

28

 

T

1

0

1

0

0

2

3

0

3

4

2

1

1

0

2

4

16

  

S

P

B

A

R

W

E

Bo

Ar

Ch

K

C

MP

HM

AC

M

T

  

Antarctic region

Sub-Antarctic region

For abbreviations see Fig. 3 caption

The records of the 219 species of ophiuroids from the SO have been analysed in order to identify potential tendencies in bathymetric distribution (see Table 3). In summary, the shelf waters (0–1,000 m) harbour the greatest number of species, as well as the greatest percentage of species restricted to a specific bathymetric range when compared with the deep segment here considered (1,001–6,000 m). This happens to both endemic and non-endemic species in the Antarctic and sub-Antarctic regions. The number of endemic species is higher in Antarctic than in sub-Antarctic regions, with the same trends, being higher in shelf than in deep bottoms, also valid for species exclusive of the respective depth segments considered. As for the species present in deep waters (>1,000 m), their presence is higher in the waters of the sub-Antarctic region (66.9 %) than in the Antarctic region (57.3 %). If we only take into consideration the species that are situated exclusively at depths exceeding 1,000 m, the percentage decreases sharply in both regions (16 % in the Antarctic region and 8.1 % in the sub-Antarctic region). On a global scale, in the SO, the species present in deep waters exceed half of the total number (58 %), and if we consider only the exclusive ones, the percentage falls to 13.2 %. In general, the number of deep-sea species in the range 1,001–3,000 is higher than in the deeper segment 3,001–6,000; however, the number of species exclusive to that range is equal (endemic Antarctic) or often higher in the 3,001–6,000 than in 1,001–3,000 m depth.
Table 3

Number of SO ophiuroids species related to depth

 

Reported Southern Ocean

Endemic Southern Ocean

Reported Antarctica

Endemic Antarctic

Reported sub-Antarctica

Endemic sub-Antarctic

Common

Total species

219

126

131

76

136

30

48

Depth range

 0–100

90 (10)

45 (8)

56 (5)

24 (5)

64 (5)

10 (3)

30 (0)

 0–1,000

190 (92)

105 (74)

110 (56)

61 (44)

125 (45)

27 (23)

45 (9)

 0–3,000

208 (169)

117 (106)

122 (96)

71 (62)

132 (103)

28 (27)

46 (30)

 0–6,000

219 (216)

126 (124)

131 (128)

76 (75)

136 (134)

30 (30)

48 (46)

 101–1,000

188 (53)

104 (45)

110 (34)

61 (29)

123 (22)

26 (14)

45 (3)

 1,001–3,000

116 (7)

44 (5)

67 (4)

27 (4)

87 (3)

5 (1)

37 (0)

 3,001–6,000

50 (12)

20 (8)

35 (9)

14 (4)

33 (5)

3 (2)

18 (2)

 1,001–6,000

127 (29)

53 (21)

75 (21)

32 (15)

91 (11)

7 (3)

39 (3)

Between parenthesis, number of species exclusive of that depth range

In reference to the behaviour of the stenobathic–eurybathic index along the ophiuroid species in the SO (Fig. 2a), there is a marked tendency to the eurybathy, being the segments 90–100 and 80-89 % the best represented (42 and 14.2 % of the total species, composed mainly by non-endemic species), followed by the most strict stenobathic segment, 0–9 % (11.9 % of the total species, all endemic species). The remaining segments (from 10–19 to 70–79 %) do not reach 6.5 % each.
https://static-content.springer.com/image/art%3A10.1007%2Fs00300-013-1411-8/MediaObjects/300_2013_1411_Fig2_HTML.gif
Fig. 2

Stenobathic–eurybathic index (S–E index). Distribution of SO ophiuroid species along segments of the S–E index, from the most stenobathic (0–9 %) to the most eurybathic (90–100 %). A total species; B species exclusively distributed between 0 and 1,000 m depth; C species exclusively distributed between 1,001 and 6,000 m depth

If the two main bathymetric distributional ranges (0–1,000 and 1,001–6,000 m) are taken in consideration for the whole SO, a similar tendency can be observed in the shallowest range (Fig. 2b); the 90–100 % segment reaches up to 29 % of the total species (being similar the number of endemic and non-endemic species), but the next most important segment is the most strict stenobathic one (0–9 % in S–E index) reaching a 20.7 % of the total species in SO (being all endemic), and in the intermediate segments (excluding the 80–90 %), the index oscillates under 8 % of the species.

The deepest range (Fig. 2c) is mainly characterised by the dominance of stenobathic species (0–29 % in S–E index) that accumulates more than 70 % of the species exclusive to this bathymetric range, being most of the species endemic (18 of 21). None species with a S–E index higher than 80 % was found.

If we consider this analysis in the two main regions here compared, Antarctica and sub-Antarctica, we can observe a similar tendency in Antarctic region in all three above described cases (Fig. 3a–c). There are slight differences in some percentages, but in general, they follow the same trends. It is worthy to mention that in the deepest waters, none species with a S–E index higher that 70 % was found, being these bottoms again dominated by the stenobathic and endemic species, mainly in the range 0–29 % of this index.
https://static-content.springer.com/image/art%3A10.1007%2Fs00300-013-1411-8/MediaObjects/300_2013_1411_Fig3_HTML.gif
Fig. 3

Stenobathic–eurybathic index (S–E index). Distribution of Antarctic ophiuroid species along segments of the S–E index, from the most stenobathic (0–9 %) to the most eurybathic (90–100 %). A total species; B species exclusively distributed between 0 and 1,000 m depth; C species exclusively distributed between 1,001 and 6,000 m depth

However, the behaviour in the sub-Antarctic was much more accented; for the total number of species (Fig. 4a), it was widely dominated by eurybathic species (90–100 and 80–89 % categories, reaching 52.9 and 12.9 % of the species, respectively), being eminently non-endemic species (82 of 89 species in the combined segment). The strictest stenobathic species (0–9 % in S–E index) was the third most important category, represented by a 11 % of the species and mainly composed by endemic species (14 of 15 spp.). In the case of the 0–1,000-m depth range (Fig. 4b), the most noticeable is the significative increment of non-endemic species in the most eurybathic category 90–100 % (15 of 18 species). For the deepest sub-Antarctic bathymetric range (1,001–6,000), a 27.3 % of the species were strictly stenobathic (0–9 % in S–E index), all of them endemic, while the remaining species were present from 10 to 79 % of the index, and all of them were non-endemic species.
https://static-content.springer.com/image/art%3A10.1007%2Fs00300-013-1411-8/MediaObjects/300_2013_1411_Fig4_HTML.gif
Fig. 4

Stenobathic–eurybathic index (S–E index). Distribution of sub-Antarctic ophiuroid species along segments of the S–E index, from the most stenobathic (0–9 %) to the most eurybathic (90–100 %). A total species; B species exclusively distributed between 0 and 1,000 m depth; C species exclusively distributed between 1,001 and 6,000 m depth

Based on the frequencies, if we explore chi-square test, we observe that there is no significant difference in S–E index distribution of ophiuroids between Antarctic and sub-Antarctic regions (p > 0.05). If we consider each area separately, there is significant difference between shallow and deep waters in the Antarctic region (p < 0.05), but no significant difference is found for the same bathymetric comparison for sub-Antarctic waters (although the obtained value is relatively close to significant value, p = 0.171). When analysing the S–E index distribution in deep waters species, we have not found significant difference between the two areas of the SO (Antarctica vs. sub-Antarctica, p > 0.05), and neither on shallow waters level, although the value can be considered in the proximities of the limit (p = 0.082). By focusing only on endemic species, we have only significant differences between shallow and deep waters in the Antarctic region (p < 0.05). Although for the comparisons Antarctic versus sub-Antarctic in total species and when only considering shallow species, p values are relatively close to the limits (p = 0.115 and 0.085, respectively). If we observe only non-endemic species, the significant differences appears between shallow versus deep species in both Antarctic and sub-Antarctic regions (p = 0.023 and 0.012, respectively).

When the distribution of the S–E index in all the previously commented cases is relativised to percentages of their respective total number of species, a higher number of significant differences can be found. For the total number of species, there are not only differences in the Antarctic versus sub-Antarctic comparison. The same occurs when only endemic species are considered. However, for those non-endemic species, there are only significant differences in the comparisons of Antarctic (shallow vs. deep species) and sub-Antarctica (shallow vs. deep species). A summary of the significant differences obtained in all these comparisons is showed in Table 4.
Table 4

Summary of chi-square significant differences obtained when considering all reported species (endemic and non-endemic), only the endemic species or only non-endemic species at the different geographical areas and bathymetric ranges compared

 

Total number of species

Only endemic species

Only non-endemic species

 

Freq.

%

Freq.

%

Freq.

%

Geographical areas and bathymetric ranges

 ANT vs. sub-ANT (all depths)

NO

NO

NO (p = 0.115)

NO

NO

NO

 ANT, shallow vs. deep

YES

YES

YES

YES

YES

YES

 Sub-ANT, shallow vs. deep

NO (p = 0.171)

YES

NO

YES

YES

YES

 Shallow, ANT vs. sub-ANT

NO (p = 0.082)

YES

NO (p = 0.085)

YES

NO

NO

 Deep, ANT vs. sub-ANT

NO

YES

NO

YES

NO

NO

Freq. = when considering the number of species in each S–E index case. % = when considering the percentage of species with respect to the total in each geographic and bathymetric range [all depths, shallow (0–1,000) and deep (1,001–6,000)]. When the obtained p is relatively close to 0.05, that value is indicate

The ophiuroid fauna present in the Antarctic region (presence–absence data of the 219 species present in the SO) clearly differs from sub-Antarctic areas (Fig. 5). Although Bouvet Island is supposed to belong to the Antarctic region, the analysis considers it as an isolated unit at both similarity levels of comparison here considered (20 and 50 %). The remaining Antarctic zones are in the group IV (at 20 % of similarity level) with other sub-Antarctic zones. Most of the Antarctic zones are better defined when considering a 50 % level of similarity, where they are included in the groups 5 and 6. The group 5 includes Ross, Weddell Seas, Eastern Antarctic, Scotia Sea and Antarctic Peninsula, while the group 6 includes Bellingshausen and Amundsen Seas.
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Fig. 5

Similarity of Antarctic and sub-Antarctic zones (Bray–Curtis Index, group average), based on presence–absence data. Antarctic region: A = Amundsen Sea; B = Bellingshausen Sea; Bo = Bouvet Island; E = East Antarctic zone (from Dronning Maud Land to Victoria Land); P = Antarctic Peninsula and islands (South Shetland included); R = Ross Sea; S = Scotia Sea (including the Scotia Arc island: South Georgia, South Sandwich, South Orkneys); W = Weddell Sea. Sub-Antarctic region: AC = Sub-Antarctic New Zealand islands (Auckland and Campbell); Ar = Argentine coast (to 40°S) and Falkland (Malvinas) Islands; C = Crozet Island; Ch = Chilean coast (to 40°S); HM = Heard and McDonalds Islands; K = Kerguelen Islands; M = Macquarie Island (Macquarie Ridge included); MP = Marion and Prince Edwards Islands; T = Tristan da Cunha group (Gough included)

The sub-Antarctic region is much more heterogeneous than the Antarctic region, and the zones here considered are part of three of the four group identified at 20 % level of similarity (groups I, II and IV), and eight of the eleven groups identified at 50 % level of similarity (groups 1, 2, 3, 7, 8, 9,10, and 11). Group I (identified at 20 % similarity) only includes Tristan da Cunha (T), being Amphiura dacunhae and Ophiactis seminuda two examples of exclusive ophiuroid species. Groups II and IV include more than a single sub-Antarctic zone. Ophiacantha otagoensis and Ophiactis hirta are species unifying group II (AC-M zones), while the complex group IV act as a umbrella for Antarctic and sub-Antarctic zones, being Ophiacantha pentactis, Ophionotus hexactis and Amphiura gaussi examples of exclusive species of this group.

As mentioned above, grouping at 50 % similarity are much more heterogeneous, identifying until eleven units. All sub-Antarctic zones are isolated, with the exception of the group 11, where Kerguelen (K) and Heard and McDonalds Islands (HM) are grouped.

In reference to the distribution of ophiuroid species throughout the major biogeographic zones of the SO here considered, among the 219 species recorded in the SO, there are 92 species (42 %) with a distribution that extends beyond the Subtropical Front. Among the 131 species listed in the Antarctic region, there are 35 (26.7 %) which are also recorded outside the SO, going beyond the Polar Front and the Subtropical Front. Among the 136 species listed in sub-Antarctic waters, there are 85 (62.5 %) that extend beyond the limits of the Subtropical Front.

Discussion

The discoveries of Antarctic and sub-Antarctic ophiuroid species were made during the last 168 years, thanks to more than 50 different expeditions to the SO. Two opposite moments are the most outstanding: on the one hand, the Heroic Age of Antarctic exploration, when the great biodiversity of Antarctic benthos was discovered, and on the other hand, the negative influence of the First and Second World Wars. Taxonomic and faunistic studies reemerged later in the 1980s and continued for the next three decades, mainly providing further additional data about the distribution and biology of species already known, rather than identifying new taxa.

During the past three decades, there have been a number of scientific contributions to our knowledge of the biodiversity of the SO (see Griffiths 2010; De Broyer and Danis 2010). However, this tendency has not necessarily been reflected in our knowledge of the biodiversity of ophiuroids. It has been suggested that the state of knowledge of Antarctic echinoderms is really good (Clarke and Johnston 2003; Griffiths 2010). However, in combination with the lack (or insufficient number) of taxonomists, not all areas have been sampled with the same effort, Bouvet Island and the Bellingshausen and Amundsen Seas are poorly sampled, as well as several Antarctic and sub-Antarctic deep-sea areas (Griffiths 2010). Therefore, our knowledge of Antarctic ophiuroids, as suggested by Pawson (1994), for all Antarctic echinoderms, is still fragmentary.

Dearborn et al. (1990) gave an approximate number of 150 ophiuroid species in the SO (below 45°S). Later Clarke and Johnston (2003) estimated 119 species (for these studies, the SO was strictly considered as the Antarctic region with its limit at the Polar Front). Stöhr et al. (2012) estimated 126 species in the Antarctic region. As already mentioned, the SO is currently considered in a broader sense, including the Antarctic and sub-Antarctic regions, with the Subtropical Front as a boundary. The ophiuroid diversity of the SO (219 spp.) is partly determined by its biotic conditions, which, although originally presumed to be hard, are really rather favourable (Smith et al. 2006) thanks to the trophic and reproductive plasticity that ophiuroids (and echinoderms in general) exhibit (O’Loughlin et al. 2010; O’Hara et al. 2011). The originality of the ophiuroid fauna from the SO is also evidenced by the great number of endemic species, reaching 57.5 % of the total ophiuroid fauna. Such endemism decreases at genus level (17.2 %). There are no endemic families of ophiuroids in the SO. This pattern is similar to other SO benthic groups such as isopods, shell-less gastropods, bivalves, cheilostomes bryozoans, sea anemones and pycnogonoids (Brandt 1999; Linse et al. 2006; Barnes and Griffiths 2008; Rodríguez et al. 2007; Munilla and Soler 2009). This level of endemism is proposed to be caused by long evolutionary isolation (Clarke and Crame 1989; Clarke et al. 2004) and by the fact that a part of the species comes from common ancestors of the Mesozoic Gondwana (Gili et al. 2006). As a result, there would have been enough time (or selective pressures) for speciation and formation of different genera, but not enough for diversification at a level that today would be recognised with the category of family (Linse et al. 2006).

As happens with other benthic groups of the Antarctic region, eurybathic species are widely represented among the ophiuroids, if we take all SO species into consideration, eurybathic ophiuroid species predominate (72.6 % of the total, if we consider those species with a S–E index >50 %, approximately half of these species are endemic) as compared with stenobathic species (27.4 % of the total, if we consider those species with a S–E index <50 %, approximately 86.6 % of these species are endemic) (see Fig. 3a). This eurybathic distribution pattern has been observed in some benthic groups (see Brey et al. 1996; Brandt et al. 2007), while pycnogonids do not seem to follow this trend (43.6 %) (Munilla 2001).

Cold shelf waters of the Antarctic region and deep ocean waters have been demonstrated to be similar (Gage and Tyler 1991), and therefore, fauna might move across shelf, slope and ocean floor areas, more frequently in interglacial periods (Brey et al. 1996; Thatje et al. 2005). Brey et al. (1996) suggested that eurybathy arose when the conditions in the Antarctica were considerably different. These authors found no significant differences in bathymetric ranges when comparing Antarctic and European species. Such differences would have allowed us to establish a correlation between Antarctic ophiuroids’ tendency to eurybathy and the changes which occurred in glacial and interglacial cycles.

The Antarctic region seems to manifests itself as an entity, as it has a large number of endemic species and, to a lesser extent, exclusive genera, although the latter causes a higher degree of divergence in its fauna. The Circumpolar Current seems to be the main route for the spreading of Antarctic ophiuroids and is also responsible for the high level of species with circumpolar distribution. However, poor sampling effort could also be the cause of the apparent isolation of Bouvet Island both from other Antarctic areas and from sub-Antarctic ones (Arntz et al. 2006), and therefore, further faunistic studies are needed in this area, in order to specify its biogeographic affinity. Sub-Antarctic areas are in general much more heterogeneous from a faunistic point of view.

As already mentioned, the affinities for Tristan da Cunha, Auckland-Campbell Islands and Macquarie Island are unclear (see Fig. 5). However, finding common species for Tristan da Cunha (Table 2: 3 and 4 spp. with South American areas (Ar and Ch, respectively), 2 spp. with the Auckland-Campbell Islands and 4 spp. with Macquarie Island) and ignoring the widespread species that do not define a biogeographic zonation (such as Ophiopleura inermis, Amphipholis squamata, Ophiactis abyssicola and Ophiomusium lymani), we can see that their faunistic connections are better defined. Hence, Ophiomyxa vivipara links Tristan da Cunha to the sub-Antarctic area of South America (Ar and Ch) and South Africa, Amphiura (Amphiura) capensis relates it to South Africa, while it is Amphiura (Amphiura) magellanica, a sub-Antarctic circumpolar species, which would seem to approximate Tristan da Cunha to the Auckland-Campbell Islands and Macquarie. However, they could happen to be morphological but not biological species, and they would simply alter the results and conclusions of this analysis. Therefore, the faunistic connections of Tristan da Cunha, as suggested by Mortensen (1941) and Fell et al. (1969), are between the most proximate littoral areas, such as South America and South Africa.

Thus, the present analysis based on the distribution of the ophiuroid fauna looks similar to the biogeographic affinities shown by studies focused on other benthic groups such as shell-less gastropods and bivalves (Linse et al. 2006), sea anemones (Rodríguez et al. 2007), bryozoans (Barnes and Griffiths 2008) and pycnogonids (Munilla and Soler 2009), and supports the biogeographical model for the SO developed by Hedgpeth (1969). In general, this study supports a biogeographic differentiation of Antarctic and sub-Antarctic regions, as well as the circumpolar nature of its fauna (Hedgpeth 1971; Arntz et al. 1994; Clarke and Johnston 2003; Griffiths et al. 2009). The Polar Front and, to a lesser extent, the Subtropical Front are the geographic discontinuities that, to a large degree, impede exchange with bordering benthic faunas (Clarke 2003; Clarke et al. 2004), thus delimiting the SO as a biogeographic system clearly differentiated from adjacent oceans. However, the idea of defining marine ecoregion after species and environmental parameters distribution instead of the a priori geographical delimitation of areas will surely improve or, at least, complement our knowledge on the distributional pattern of SO fauna in the nearest future (Spalding et al. 2007).

However, to what extent has the apparent isolation of the SO been broken? Ophiuroid fauna (data based on 92 species with a distribution that exceeds the geographic boundaries of the SO) shows relatively high exchange rates. Such rates are higher than those of other benthic taxa showing very low exchange rates, as in the case of sponges, asteroids (Clarke 2003), sea anemones (Rodríguez et al. 2007) and ascidians (Primo and Vázquez 2009). Other zoological groups, such as polychaete annelids (Montiel et al. 2005) and scleractinian corals (Cairns 1982), exhibit a higher degree of exchange on both sides of the aforementioned biogeographic boundaries (Polar and Subtropical Fronts).

From the point of view of those species of ophiuroids which in their distribution cross the Subtropical Front, there can be four basic movement patterns conditioning the distribution areas of the species and that, in part, could explain the origin of the ophiuroid fauna of the SO. Such movement patterns would be as follows:

1. Between the SO and the subtropical waters of South America. Antarctic and/or sub-Antarctic species migrating to lower latitudes. The subtropical species of the Atlantic coast such as Amphioplus albidus, Amphiura crassipes and Ophioplocus januarii seem to have marked their distribution limits in the southern waters of the convergence zone of the Subtropical Front. The most southern records of these species are in the San Matías Gulf (Bernasconi and D’Agostino 1977; Bartsch 1982; Martínez 2008), so they have not been considered as species of the SO in this study. On the Pacific coast, the limit of cold waters is on the coasts of Valdivia (39°S) (see Castillo 1968). Thus, the ophiuroid fauna is exclusively austral from Tierra de Fuego to Valdivia. However, further north, although species are prevailingly austral, there is a transition zone between Valdivia and Talcahuano (36°S) (Castillo 1968; Jaramillo 1981) where we found warm water species such as Ophiactis kroyeri and Amphioplus magellanicus, which have not been included in this inventory.

Sub-Antarctic and subtropical areas were connected through the continental shelf and coastal currents, such as that of the Falkland (Malvinas) Islands (Martínez 2008). And, between the Antarctic and sub-Antarctic areas, connection would be via the Scotia Arc (Fell et al. 1969; Jaramillo 1981; Smirnov 1994; Dahm 1999; Manso 2010; Barboza et al. 2011). The same connection has been suggested for other benthic groups (Arntz et al. 2005), such as some species of pennatulaceans (López-González and Williams 2002), polychaetes (Montiel et al. 2004), bryozoans (Moyano 2005; Barnes 2006), sea anemones (Rodríguez et al. 2007), pycnogonids (Fry and Hedgpeth 1969; Munilla and Soler 2009) and sponges (Downey et al. 2012). Although considering the bathymetric range of some of the aforementioned species (see Online Resource 1), there could have been a connection via deep waters.

2. Between New Zealand, southern Australia and the sub-Antarctic region. Although migration occurred in both directions, the movement made by species from New Zealand and southern Australia to waters of the sub-Antarctic islands of Campbell, Auckland and Macquarie is apparently slightly more intense; this faunistic connection had been previously pointed out in several studies (Mortensen 1924; Fell 1953a, b; Dawson 1965, 1970; O’Hara 1998; O’Hara et al. 2012). As already mentioned, ophiuroids could have moved across the shelf of New Zealand to the Auckland and Campbell Islands and across Macquarie Ridge to Macquarie Island. For the species with disjunctive distribution such as Ophiomitrella conferta and sub-Antarctic circumpolar species as Amphiura (Amphiura) magellanica, the movement could have been via the Antarctic Circumpolar Current (ACC), which would have acted as a vector from the sub-Antarctic area of South America or from the islands of the Kerguelen arc. However, these hypotheses might be biased, due to the lack of reliable information on the distribution of these species, or to the existence of cryptic species. Considering the bathymetric range of some of the species mentioned, the connection could have occurred via deep waters.

The ACC seems to be the main dispersive and homogenising mechanism of SO ophiuroid fauna, serving directly to epiplanctonic larvae or indirectly to adults, which is especially important for viviparous species distribution, as they raft on macrophytes (Mortensen 1924; Fell 1953a, 1962; Arnaud 1974; Smirnov 1994; O’Hara 1998; Hunter and Halanych 2008; Sands et al. 2012). The importance of the ACC as a vector for benthic species distribution has also been suggested for other groups of echinoderms (Fell 1953a, 1962), molluscs (Helmuth et al. 1994; Linse et al. 2006), isopods (Brandt 1999), pycnogonids (Fry and Hedgpeth 1969; Munilla 2001) and polychaetes (Montiel et al. 2005). In addition, the discovery of planktonic larvae attributed to Astrotoma agassizii (see Heimeier et al. 2010)—a species traditionally considered to be viviparous (Bernasconi 1965; Bartsch 1982; Monteiro and Tommasi 1983)—whether it is a dual reproductive mechanism (oviparous–ovoviviparous) or a result of cryptic species divergence, might open new ways to interpret the dispersion of Antarctic viviparous ophiuroids.

3. Between the SO and South Africa. Species migrating to lower latitudes. The species Amphiura (Amphiura) capensis migrates to higher latitudes of Tristan da Cunha and is a viviparous species that, as suggested by Mortensen (1941), has been transported by the Benguela Current, by rafting on macrophytes. As for other species such as Astrophiura permira and Ophiernus quadrispinus, there is insufficient data to identify movements in their distribution.

4. Immigrant species, which could have entered the SO through deep waters. This seems to be the main entry route for ophiuroid invaders, although the method of their dispersion in deep waters is unknown, unless it could be by directly moving across the ocean floor (Fell et al. 1969). It has also been mentioned as an entry route for other groups of benthic invertebrates (Brandt et al. 2007; Griffiths 2010), pycnogonids (Fry and Hedgpeth 1969; Munilla 2001), molluscs (Hain 1990), tanaidaceans (Brandt 1999), amphipods (Clarke and Crame 1992; Brandt 1999), pennatulaceans (López-González and Williams 2002) and sea anemones (Rodríguez et al. 2007).

As the number of ophiuroid species present in the SO and also found on the other side of the Subtropical Front (42 %) is higher than the species of SO also present on both sides of the Polar Front (22 %), it is possible to consider the Subtropical Front as a more permissive barrier than the Polar Front for species with wide distribution, facilitating exchange with adjacent oceans. The waters of the sub-Antarctic region constitute a buffer zone between the ophiuroid fauna of neighbouring oceans and the waters of the Antarctic region, as has been proposed for other benthic organisms.

The two evolutionary forces that have determined the distribution of the biota in the Southern Hemisphere are dispersion and vicariance (Sanmartín and Ronquist 2004). The origin of the diversity of Antarctic and sub-Antarctic ophiuroids—as that of other benthic groups—is also subject to these forces that led to a multiple origin; through deep waters, by transport with the help of ocean currents, and through bridges connecting the shelf areas of New Zealand and the Scotia Arc. These three types suggest an exogenous origin of part of the diversity of Antarctic and/or sub-Antarctic ophiuroids, having their origin in the adjacent oceans and the waters of New Zealand, Australia and South America.

By vicariance, as a result of the rupture of Gondwana, the fragmentation of Gondwana and the subsequent geographic and thermal isolation of the Antarctica, due to the formation of the Drake Passage, caused the extinction of the durophagous and the prevalence of certain benthic groups, including echinoderms (Clarke et al. 2004; Gili et al. 2006; Bowden et al. 2010). Therefore, a pool of species derived from them by vicariant speciation, as a result of the separation caused by the rupture (Rogers 2007), would form part of the current ophiuroid fauna. Examples of this possible origin could be the species of the genus Ophiosteira with six species known at global scale, five of which were distributed in the continental shelf of Antarctic region and one of them in the coasts of Ecuador. Another example could be the genus Ophiogona, which has four species, one with Antarctic and sub-Antarctic distribution (O. doederleini), two with sub-Antarctic distribution (O. laevigata and O. tenella) and one from South America (O. rugosa). Other evidence of the hypothesis of the existence of a pool of Gondwana species that evolved after isolation has been reported among gastropods (Clarke 1990), isopods (Brandt 1991, 1999), octocorals (López-González and Gili 2001; Gili et al. 2006), pycnogonids (Munilla 2001; Munilla and Soler 2009), sponges (Gili et al. 2006) and sea anemones (Rodríguez et al. 2007).

Considering the high level of endemism of the ophiuroid fauna in the Antarctic region, the question is to what extent this isolation has been a source of diversity and dispersion possibilities towards sub-Antarctic waters and adjacent oceans (“Evolutionary incubator” by Watling and Thurston 1989). Probably, Antarctic waters have been a speciation pump for the genus Ophioplinthus, since of the 35 species at a global scale (Martynov and Litvinova 2008), 23 are present in the waters of the SO and 18 of them are endemic (14 exclusive to Antarctic waters, 2 to sub-Antarctica waters and 2 of them are endemic to both regions).

Antarctic waters are considered to be a hotspot for different groups of echinoderms (O’Loughlin et al. 2010), a phenomenon that is being endorsed by recent discoveries of cryptic species in ophiuroids (Hunter and Halanych 2008, 2010), as well as in other groups of echinoderms (O’Loughlin et al. 2010). Their origin can be explained by the allopatric speciation, which would have been caused by the isolation provoked by the Polar Front, as well as by the isolation in the areas of refuge of the insular habitats, which appeared during the Late Cenozoic glacial cycles, due to the expansion and retraction of the ice (Clarke and Crame 1989, 1992; O’Loughlin et al. 2010).

To learn more about the diversity, geographical and bathymetric distribution of the fauna of these Polar areas, greater efforts should be made to complete the existing inventories. This is particularly necessary for the areas with low sampling effort, especially in the Bellingshausen and Amundsen Seas, Bouvet Island and in numerous abyssal areas in the SO. Finally, the better knowledge on the distribution of ophiuroid species (in combination with the correct understanding of the environmental, biotic and abiotic, conditions which finally model the distributional patterns of the species) will surely permit to interpret how historical and present events define the faunistic composition of marine invertebrates in the SO.

Acknowledgments

The authors would like to express their gratitude to the cruise leader and steering committee of the R/V Polarstern ANT XXIII/8 and ANT XXIX/3 cruises, especially Julian Gutt and Enrique Isla, who kindly facilitated the work on board and allowed us to collaborate in this Antarctic Program. PJL-G takes this opportunity to extend our thanks to the officers and crew, of the R/V Polarstern and many colleagues on board during the ANT XXIII/8 cruise for their help during the sampling period on board. Support for this study was partially provided by the Spanish CICYT projects CLIMANT (POL2006-06399/CGL), ECOWED (CTM2012-39350-C02-01) and SCAR-MarBIN mini-grant to Chester Sands (British Antarctic Survey), which enabled RML’s stay in BAS for the study of specimens. We would like to thank Igor Smirnov (Zoological Institute of Russian Academy of Sciences) for their kind assistance during the preparation of the present work. Special thanks to Elena Zaikina for providing assistance to RML. Thanks to the Editors of PB and three anonymous referees whose criticisms have improved the first versions of this manuscript. Special thanks are also addressed to Bruno David (Université de Bourgogne, Dijon) for his constructive comments during the participation of PJL-G in the ANT XXIX/3 Polarstern cruise (January–March, 2013), and for his suggestions to use the stenobathic and eurybathic data in the form here described as a source of comparative information. Mr. Tony Krupa is thanked for reviewing the English version of the final manuscript of this paper.

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