Polar Biol (2014) 37:859–877
DOI 10.1007/s00300-014-1487-9
ORIGINAL PAPER
Diversity, abundance and composition in macrofaunal molluscs
from the Ross Sea (Antarctica): results of fine-mesh sampling
along a latitudinal gradient
Stefano Schiaparelli • Claudio Ghiglione •
Maria Chiara Alvaro • Huw J. Griffiths •
Katrin Linse
Received: 2 August 2013 / Revised: 11 March 2014 / Accepted: 12 March 2014 / Published online: 26 March 2014
Springer-Verlag Berlin Heidelberg 2014
Abstract The Latitudinal Gradient Program (2002–2011)
aimed at understanding the marine and terrestrial ecosystems existing along the Victoria Land coast (Ross Sea), an
area characterized by strong latitudinal clines in environmental factors. During the program’s voyage of the Italian
RV ‘‘Italica’’ in 2004, a fine-mesh towed gear, the
‘‘Rauschert dredge’’, was deployed for the first time at 18
stations in four latitudinal distinct shelf areas between
*71S and *74S. The collected samples contained
undescribed species and new records for the Ross Sea from
a variety of different marine taxa. Here, we describe the
molluscan fauna and investigate evidences for latitudinal
effects on molluscan diversity, abundance and assemblage
composition. No significant latitudinal trends were detected: while diversity did not vary significantly with latitude,
species richness showed an apparent but non-significant
decrease with increasing latitude. Beta-diversity was found
to be high both within and between latitudinally distinct
shelf areas. A large fraction (*20 %) of the collected
molluscs corresponded to new species records for the Ross
Sea or undescribed species. Rarity in Antarctic molluscan
occurrences was confirmed, with singletons (i.e. species
represented by only a single individual) accounting for a
22 % and uniques (i.e. species occurring in one sample
S. Schiaparelli (&) C. Ghiglione M. C. Alvaro
Department of Earth, Environmental and Life Sciences
(DISTAV), University of Genoa, Genoa, Italy
e-mail: stefano.schiaparelli@unige.it
S. Schiaparelli C. Ghiglione M. C. Alvaro
Italian National Antarctic Museum (MNA) (Section of Genoa),
University of Genoa, Genoa, Italy
H. J. Griffiths K. Linse
British Antarctic Survey, Cambridge, UK
only) for a 43.5 % of the total presence. Our study of the
smaller macrofaunal benthic fraction showed that Antarctic
marine research still has far to go to have robust reference
baselines to measure possible changes in benthic communities, even in the case of the assumed well-known, wellsampled and well-studied group of Ross Sea shelf molluscs. We advocate the use of fine-mesh trawling gears for
routine sampling activities in future Antarctic expeditions
to assess the full marine biodiversity.
Keywords Antarctica Benthos Mollusca Ross Sea
Victoria Land coast Rauschert dredge
Introduction
In Antarctica, the Ross Sea sector is one of the better-known
areas due to the high number of scientific expeditions that
have been undertaken there since 1899, when during the
Southern Cross Expedition (1898–1900) men overwintered
for the first time on the Antarctic continent. This challenging
adventure opened the Ross Sea sector to a long series of other
scientific expeditions (i.e. the National Antarctic Expedition,
1901–1904; the British Antarctic Expedition, 1907–1909;
the British Antarctic Expedition, 1910–1913; the R.S.S
Discovery II, 1935–1937 and 1937–1939; the U.S Navy
Antarctic Expedition, 1947–1948; the Deep Freeze I,
1955–1956; the Deep Freeze II, 1956–1957; the Deep Freeze
III, 1957–1958; the Deep Freeze IV, 1958–1959; the Trans
Antarctic Expedition, 1956–1958; the Stanford University
Invertebrate Studies, 1958–1961; the New Zealand Oceanographic Institute, 1958–1960; the USAP Project,
1960–1961; the USAP Eltanin 27, 1967; and the USAP
Eltanin 32, 1968), which collected an impressive number of
scientific samples.
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860
After this initial phase of geographical and biological
exploration, including species description, there was a
progressive shift in research focus from large-scale biological sampling, aimed at species inventories and
descriptions, to the study of community assembly and
ecosystem functioning at the end of the 1960s. This change
was partly due to an increase in interest for ecological
disciplines, but also to the establishment of permanent
bases: McMurdo Station (built in 1955–1956) and Scott
Base (built in 1959), both located at *78S, and Mario
Zucchelli Station (built in 1985) located at *74S which
enabled sampling on a regular basis and ecological studies
related to the seasonal changes in environmental conditions
and the dynamics occurring at high latitudes (e.g. Dayton
et al. 1970; Dayton and Oliver 1977).
Thanks to all these recent and historical scientific
activities, resulting in a great number of stations sampled in
this region, the shelf fauna of the Ross Sea is considered to
be one the better sampled in the Southern Ocean (Clarke
et al. 2007; Griffiths et al. 2011).
Within this region and in general for Antarctica, one of
the best-studied taxa is the Phylum Mollusca, which is only
second to Arthropoda in terms of number of collection
records (De Broyer and Danis 2011). In fact, virtually all
scientific expeditions to the Ross Sea collected molluscan
specimens, forming an impressive amount of scientific
material which has accumulated on museum’s shelves
decade after decade since 1899.
In 1990, Dell, after having sorted, organized and classified a large part these mollusc samples, in an unprecedented effort which lasted for about 30 years (Dell
1990:1–2), published the volume ‘‘Antarctic Mollusca’’
(Dell 1990), a synthesis of the taxonomical and distributional knowledge of Antarctic molluscs, which embraced
almost all available samples collected at least until the end
of the 1970s. This book had a special focus on the Ross
Sea, due to the great number of samples collected in this
area and listed 193 species of shelled Mollusca, out of
which 43 were described as new (Dell 1990).
In later years, only few adjustments were made to the
number of species known for the Ross Sea, which
increased to 197 species (Griffiths et al. 2009), roughly
corresponding to *30 % of the total number of mollusc
species (n = 684) known for the Southern Ocean (Griffiths
2010).
All the above-cited sampling activities were performed
using a variety of sampling gears, ranging from grabs to
trawl nets, which should have assured the sampling of all
size classes. However, as Dell (1990) clearly stated in his
contribution, in all the studied Antarctic samples, there
always was an apparent lack of ‘‘microfauna’’ or smallsized macrofauna. Dell explained this was artefact of the
design of sampling activities and gears used, where most of
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Polar Biol (2014) 37:859–877
the sediment was probably washed away together with the
small-sized species (Dell 1990:264).
This was the state of the art until 2004, when a joint
Italian-New Zealand ship-based, large-scale sampling
campaign was performed in the Ross Sea under the Latitudinal Gradient Program framework (LGP, http://www.
lgp.aq/). Previously, for almost 40 years, no large-scale
benthic sampling activities occurred in the area and most
sampling was near shore oriented in the vicinity of permanent research stations.
The LGP was an international research project running
from 2002 to 2011, which aimed at understanding of the
complex ecosystems that exist along the Victoria Land
coast and the effects of environmental change on these
ecosystems (http://www.lgp.aq/). Along the natural gradient of the Victoria Land coast, in fact, environmental
factors such as solar radiation, temperature and sea-ice
cover vary with latitude (Berkman et al. 2005) and are
likely to affect the diversity and distribution of benthic
communities. Other environmental gradients such as depth
below sea level, height above sea level and distance from
the coast complicate the latitudinal gradient influence on
the coastal ecosystems (Cummings et al. 2010 and references therein). All these factors and gradients make the
Victoria Land coast one of the few natural latitudinal
gradients where it is possible to investigate the potential
effect of environmental parameter gradients on the benthic
communities.
In 2004, two parallel LGP voyages, i.e. RV ‘‘Tangaroa’’
TAN0402 BioRoss and ‘‘Italica’’ ‘‘Latitudinal Gradient
Program’’, sampled along the Victoria Land coast collecting new records of molluscs from the Ross Sea which
accounted for a *20 % of the total of species found
(Schiaparelli et al. 2006).
During the RV ‘‘Italica’’ expedition, the fine-meshed
‘‘Rauschert dredge’’ was deployed for the first time on the
shelf of the Ross Sea (Rehm et al. 2006). The ‘‘Rauschert
dredge’’ (Lörz et al. 1999), like the ‘‘Brenke-sled’’ (Brenke
2005), belongs to the category of ‘‘fine-mesh towed gears’’,
i.e. those having mesh sizes B500 lm and are specifically
designed to retain epibenthic specimens of small size. The
use of fine-mesh towed gears has progressively increased in
recent years, especially in the Atlantic sector of the
Southern Ocean (e.g. Linse 2006; Schrödl et al. 2011),
allowing a considerable increase in the knowledge of
species distribution and occurrence, especially for deep-sea
taxa (Kaiser et al. 2013 and references therein), but had
never previously been used in the Ross Sea. More recently,
a ‘‘Brenke-sled’’ was used in the Ross Sea during the RV
‘‘Tangaroa’’ TAN0802 in 2008 (Lörz et al. 2013).
To date, several papers have been published based on
the material collected by this dredge during the 2004 RV
‘‘Italica’’ research voyage. In general, they focus on
Polar Biol (2014) 37:859–877
861
Peracarida (Rehm et al. 2007), with specific studies on
Isopoda (Choudhury and Brandt 2007, 2009; Choudhury
et al. 2011) and Cumacea (Rehm and Heard 2008),
including descriptions of few species and subspecies.
Molluscs, although not being numerically dominant in
the ‘‘Rauschert dredge’’ samples (they accounted only for a
9.6 % in abundance and 4.2 % in biomass; Rehm et al.
2006), were represented mostly by small-sized specimens,
i.e. to the size fraction that was considered by Dell (1990)
to be ‘‘lacking’’. This small macrobenthic fraction had a
great potential of including new species records as well as
undescribed species. Following the targets of the Latitudinal Gradient Program, here, we present the small macromolluscan fauna of the Victoria Land Area and
investigate any effect of latitude on this group for diversity,
abundance and assemblage composition.
Materials and methods
Study area and sample processing
In the Austral summer 2004, during the 19th PNRA Antarctic expedition on board, the RV ‘‘Italica’’, a ‘‘Rauschert
dredge’’, was deployed between Cape Adare (*71S) and
Terra Nova Bay (*75S) at eighteen stations with depths
varying from 84 to 515 m (Fig. 1; Table 1).
The ‘‘Rauschert dredge’’ was equipped with a net of
500-lm mesh size and an opening width of 0.5 m (Lörz
et al. 1999). The dredge was towed at a mean velocity of 1
knot (1,852 km/h) and calculated haul distances ranged
from 59 to 575 m (Table 1 and Rehm et al. 2006).
The collected material was sieved on board through a
500-lm mesh, preserved in 90 % pre-cooled ethanol and
kept at -25 C for later DNA extraction. A DNA barcoding activity on this material is currently underway
within the research program BAMBi (Barcoding of Antarctic Marine Biodiversity, 2010/A1.10) funded by the
Italian National Antarctic Research Program (PNRA)
(Ghiglione et al. 2013). In the laboratory, all living specimens were sorted under a stereomicroscope and, whenever
possible, classified down to the species level. Minute species were photographed using an ESEM (Leo Stereoscan
440). Dead shells, i.e. the thanatocoenosis, were not taken
into account in the present study, which refers only to live
collected specimens.
Data analysis
Species richness was evaluated within and between each of
the four latitudinal sampling areas (i.e. *71S, *72S,
*73S and *75S), called latitudinal bins from here on.
Firstly, individual-based interpolation (rarefaction) and
Fig. 1 Victoria Land coast where the 2004 RV ‘‘Italica’’ voyage took
place with the sampled areas of Cape Adare, Cape Hallett, Coulman
Island and Cape Russell. Position of sampling stations is marked with
black circles. Stations’ coordinates are reported in Table 1
extrapolation curves for all the stations sampled at each of
the four latitudinal bins considered were compared, using
the method proposed by Colwell et al. (2012). Secondly,
species richness was compared between latitudinal bins by
combining together all the samples within a bin and calculating sample-based interpolation (rarefaction) and
extrapolation curves, based on incidence data from reference samples (Colwell et al. 2012). Uncertainty of estimations is reported in terms of unconditional confidence
intervals (at 95 %) under the multinomial model (for
Individual-based interpolation/extrapolation curves) or
under the Bernoulli product model (for the sample-based
interpolation/extrapolation curves) (Colwell et al. 2012).
The non-overlap of 95 % confidence intervals was used as
the indication of statistical difference (Colwell et al. 2012;
Gotelli and Ellison 2013). Rarefaction and extrapolation
analyses were conducted using the on-line resource iNEXT
(Hsieh et al. 2013), which is based on R-statistical language (http://www.r-project.org). In sample-based rarefaction analysis, the Coulman Island data were not included
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862
Polar Biol (2014) 37:859–877
Table 1 Rauschert dredge stations of the Victoria Land Transect Cruise (Ross Sea, Antarctica)
Station
Date
North–South
Position
Latitude (S)
Longitude (E)
Depth (m)
Haul length (m)
Sediment
Cape Adare
A1
15/02/2004
7115.50
17041.90
515
358
Sand with few pebbles and stones
A2
14/02/2004
7117.30
17039.20
421
298
Sand and gravel
A3
14/02/2004
7118.7
0
0
17029.2
305
257
Sand
A4
14/02/2004
7118.40
17028.90
230
376
Sand and pebbles
A5
15/02/2004
7118.70
17025.50
119
59
Cape Hallett
Hout1
09/02/2004
7215.70
17024.80
458
375
Mud and pebbles
Hout2
11/02/2004
7217.5
0
0
17029.4
353
375
Sandy mud and stones
Hout4
12/02/2004
7218.50
17026.80
235
194
Sand
Hin2
10/02/2004
7216.90
17012.20
391
186
Coarse sand and small gravel
Hin3
16/02/2004
7217.00
17013.10
316
194
Muddy sand with stones
Hin4
16/02/2004
7217.10
17014.00
196
169
Mud and sand
16/02/2004
7217.2
0
0
17017.9
84
113
Small gravel
18/02/2004
7324.50
17023.20
474
375
Mud and small gravel
18/02/2004
7322.7
0
17006.90
410
153
Mud and pebbles
20/02/2004
7443.20
16413.10
366
192
Sand with gravel and stones
R2
21/02/2004
7449.0
0
0
16418.1
364
575
Fine sand
R3
20/02/2004
7449.30
16411.50
330
565
Rock, sand, mud and pebbles
R4
20/02/2004
7449.30
16411.50
208
97
Hin5
Sand with pebbles and stones
Coulman Island
C1
C2
Cape Russell
SMN
Rock, mud and large stones
Sediment data from Rehm et al. (2006)
in calculations due to the inadequacy of the sample size
(i.e. only two sites were available), following Gotelli and
Ellison (2013, 467).
Beta-diversity (i.e. species turnover) between samples
and between latitudinal bins was evaluated by considering
incidence data and partitioning pairwise gamma diversity
into additive components by following the SDR simplex
methodology (Podani and Schmera 2011). The additive
absolute components of gamma diversity for sites (species
shared, beta-diversity or species turnover, richness difference, richness agreement, species replacement, nestedness)
were graphically reported in ternary plots (e.g. Fig. 5), and
their percentage values reported in tables (e.g. Table 4).
The above analyses were performed with the software
SYN-TAX 2000, and ternary plots were produced using its
module ‘‘Non-hierarchical clustering’’ (Podani 2001).
The program PRIMER 6 (Plymouth Marine Laboratory)
(Clarke and Gorley 2005) was used to calculate diversity
indices. For each sampling station, we calculated: the
abundance (N), the number of species (S), the ShannonWiener diversity index (H0 ) (in log10) and the Pielou’s
evenness (J0 ). Although Shannon-Wiener H0 is not the best
performing available index for measuring biodiversity
(Buckland et al. 2011), we preferred to keep using this one
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in order to allow comparisons with published literature
(e.g. Rehm et al. 2007, cfr. Table 5 and Schiaparelli et al.
2006, cfr. Fig. 2). H’ and Simpson’s values were averaged
per latitudinal bins and compared by one-way parametric
ANOVA. Homogeneity of variances was tested with
Bartlett’s test and normality checked with the Shapiro test.
When necessary, a post hoc Tukey’s HSD test was used to
evidence differences between latitudes. Post hoc comparisons were made using the ‘‘agricolae’’ package in R.
Abundance and composition
Due to the different lengths of hauls, number of individuals
were standardized to 1,000 m2 hauls (Table 2; Fig. 7)
according to (Rehm et al. 2007) in order to allow comparisons between hauls and with published literature (e.g.
numbers of Peracarida: Table 2 in Rehm et al. 2007).
Possible differences between groups of stations, due to
depth and latitude, were studied with multivariate techniques. Abundances in each sample were standardized by
total and then transformed by square root to down weight
the contribution of most abundant species, or, alternatively,
presence/absence data were used. Bray-Curtis similarity
coefficients were calculated between stations and displayed
Polar Biol (2014) 37:859–877
863
Fig. 2 Box-plot of H’ and
Simpson’s diversity indices at
the four considered areas
by non-metric multidimensional scaling (nmMDS). Oneway ANOSIM was then used to test for the factor ‘‘depth’’,
with pre-defined levels: ‘‘1’’ (0–100 m), ‘‘2’’ (101–200 m),
‘‘3’’ (201–300 m), ‘‘4’’ (301–400 m), ‘‘5’’ (401–500 m),
‘‘6’’ ([501 m) and the factor ‘‘latitude’’, with subjectively
chosen levels: ‘‘1’’ (stations between 71S and 72S), ‘‘2’’
(between 72S and 73S), ‘‘3’’ (between 73S and 74S),
‘‘4’’ (between 74S and 75S). In the multivariate analyses,
we excluded 14 specimens, which were not determinable
due to the small dimensions or the lack of morphological
characters (Tritonia spp., Toledonia sp. juv., Pseudokellya
sp. juv., Opisthobranchia indet.). All Solenogastres were
sorted into 7 OTUs (operational taxonomic units) and
included in this form in the analyses. Species, which were
not classified to the specific level, were indeed included in
the multivariate analyses and reported at the level of genus
or family. Multivariate analyses were performed with the
software PRIMER 6 (Plymouth Marine Laboratory)
(Clarke and Gorley 2005).
Taxonomy
The choice of the right specific name, for several taxa, has
been problematic due to the fact that, for several groups,
there are no recent taxonomic revisions available. Moreover, there is an apparent state of flux at the family level for
several taxa, following results from recent molecular
studies (e.g. Bouchet et al. 2011) and different interpretations given by different authors (e.g. Engl 2012). In the
latest comprehensive review of Antarctic Mollusca (Engl
2012), for example, there are several affiliations at the
family level, which do not reflect those currently in use and
reported in the World Register of Marine Species
(WORMS) (www.marinespecies.org, last search 30 July
2013). In Engl (2012), for example, the genera Brookula
Iredale, 1912; Lissotesta Iredale, 1915; and Leptocollonia
Powell, 1951 are all placed in Turbinidae, a family characterized by heavily calcified opercula. Of these species,
only Leptocollonia has a calcareous operculum and belong
to Collonidae (as correctly reported in WORMS), while
Brookula and Lissotesta are considered Seguenzioidea with
unassigned family in WORMS and do not have a calcareous operculum. This instability at the family would have
made, in many cases, any choice of a family assignment
arbitrary. Due to this uncertainty, in this study, we have
decided to refrain from any taxonomic revision. For supraspecific classifications, we adhered to WORMS while,
for the specific affiliations, we have followed (unless differently stated in notes) the classification of Engl (2012),
since it is based in most cases on direct comparison with
type materials.
The classes Gastropoda, Bivalvia and Monoplacophora
were classified by S. Schiaparelli; Solenogastres, Polyplacophora and Scaphopoda by K. Linse. The complete list of
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864
Polar Biol (2014) 37:859–877
Table 2 Abundance of Mollusca along the Victoria Land coast (Ross Sea, Antarctica)
Station
Gastropoda
N
Bivalvia
N*1,000 m
-2
N
Monoplacophora
N*1,000 m
-2
N
-2
N*1,000 m
Solenogastres
Polyplacophora
-2
N
N*1,000 m
N
N*1,000 m
Scaphopoda
-2
N
N*1,000 m-2
Cape Adare
A1
18
100.56
0
0
0
0
5
27.93
0
0
0
0
A2
70
469.80
64
429.53
0
0
39
261.74
0
0
0
0
0
A3
515
4,007.78
26
202.33
0
0
15
116.73
0
0
0
A4
3,885
20,664.89
132
702.13
0
0
46
244.68
0
0
0
0
A5
58
1,966.10
6
203.39
0
0
1
33.90
0
0
0
0
0
41
218.67
0
0
18
96
0
0
2
0
0
Cape Hallett
Hout1
0
10.67
Hout2
18
96
35
186.67
3
16.00
39
208
0
Hout4
197
2,030.93
63
649.48
35
360.82
383
3,948.45
4
41.24
0
0
Hin2
76
817.20
0
0
0
0
21
225.81
1
10.75
4
43.01
Hin3
403
4,154.64
173
1,783.51
0
0
99
1,020.62
2
20.62
1
10.31
Hin4
398
4,710.06
61
721.89
0
0
69
816.57
1
11.83
0
0
Hin5
57
1,008.85
91
1,610.62
0
0
136
2,407.08
1
17.70
0
0
0
Coulman Island
C1
1
5.33
34
181.33
0
0
0
0
0
0
15
C2
81
1,058.82
467
6,104.58
0
0
29
379.08
0
0
51
666.67
80
770.83
11
114.58
0
0
34
354.17
0
0
0
0
17.39
Cape Russell
SMN
74
R2
28
97.39
86
299.13
0
0
5
R3
31
109.73
17
60.18
0
0
0
55
5,965
1,134.02
16
1,323
329.90
0
38
0
10
949
R4
Total
1
3.48
1
3.48
0
0
0
0
0
206.19
0
10
0
0
74
0
N = number of specimens collected per station; N*1,000 m-2 = number of specimens per station standardized to 1,000 m2
species and their distributional data occurrences (available
through ANTOBIS, the geospatial component of SCARMarBIN) are reported in Ghiglione et al. (2013).
Results
Diversity
Almost, all the species collected by the ‘‘Rauschert
dredge’’ were very small (generally not exceeding 3 mm)
and belong to families that are known to include minute
species. Only very few individuals were juveniles of species which attain larger sizes when adult (e.g. Limopsis
marionensis).
From the 18 sampled stations, 8,359 living specimens of
molluscs belonging to 161 species were obtained (Table 2).
These comprised of 5,965 specimens of Gastropoda (113
species; 72 % of the total species richness), 1,323 specimens of Bivalvia (36 species; 22.4 % of the total), 949
specimens of Solenogastres (7 species; 4.3 % of the total),
74 specimens of Scaphopoda (3 species; 1.9 of the total),
38 specimens of Monoplacophora (1 species; 0.6 % of the
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total) and 10 specimens of Polyplacophora (1 species;
0.6 % of the total). Thirty-one species (3 Bivalvia, 7 Solenogastres, 1 Polyplacophora, 2 Scaphopoda, 18 Gastropoda corresponding to a total of 1,090 specimens) were
assigned to the genus or family level only for a variety of
reasons and were treated as OTUs (operational taxonomic
units).
Thirty-five species were present as singletons
(21.74 % of the total number of species), i.e. found with
a single specimen, and 13 species as doubletons (8.07 %
of the total), i.e. found with two specimens only. Seventy
species (43.48 % of the total) were uniques, i.e. occurring in a single station only, and 35 (21.74 % of the
total) were duplicates, i.e. occurring at two stations only.
Diversity indexes (H0 log10) showed a general constancy
across the sampling stations, with values comprised
between 0.7 and 1.14 (Table 3; Fig. 2). Parametric
ANOVA showed no statistically significant differences
between group means, for the considered latitudinal bins,
of H0 values (F (3, 14) = 1.54, p = 0.247) while, for
Simpson’s index, parametric ANOVA indicated the existence of statistically significant differences (F (3,14) =
3.75, p = 0.036). Post hoc comparisons (Tukey’s HSD test
Polar Biol (2014) 37:859–877
865
Table 3 Diversity equitability indexes of the 18 Rauschert dredge stations: S = Total species, N = Total individuals, d = Margalef’s index,
J0 = Pielou’s evenness, H0 = Shannon’s index, 1 - k0 = Simpson’s index
Sample
S
N
d
J0
H0 (log10)
1 - k0
A1
8
128
1.442
0.8882
0.8021
0.8116
A2
24
1,161
3.259
0.763
1.053
0.8701
A3
29
4,327
3.344
0.6146
0.8988
0.805
A4
54
21,612
5.31
0.55
0.9528
0.8107
A5
19
2,203
2.338
0.8549
1.093
0.8899
Hout1
12
325
1.902
0.7737
0.835
0.7942
Hout2
Hout4
18
51
507
7,031
2.73
5.645
0.8107
0.6415
1.018
1.095
0.8686
0.8119
Hin2
23
1,097
3.143
0.8278
1.127
0.8966
Hin3
52
6,990
5.761
0.7399
1.27
0.9099
Hin4
30
6,260
3.317
0.6189
0.9142
0.7599
Hin5
25
5,044
2.815
0.5657
0.7908
0.7335
C1
12
267
1.969
0.6839
0.7381
0.7267
C2
50
8,209
5.437
0.6172
1.049
0.751
SMN
20
1,240
2.668
0.7758
1.009
0.8544
R2
28
421
4.468
0.7627
1.104
0.8598
R3
17
170
3.116
0.9059
1.115
0.9125
R4
33
1,670
4.312
0.8962
1.361
0.9364
with significance level at 0.05) indicated that the mean
value of Simpson’s diversity index was not statistically
different between Cape Adare and Cape Hallett, but differed from those of Coulman Island and Terra Nova Bay.
Species Richness evaluated through individual-based
interpolation (rarefaction) and extrapolation curves
(Fig. 3) showed clusters of curves having largely overlapping unconditional confidence intervals (at 95 %) at
Cape Adare, Cape Hallett and Terra Nova Bay areas.
Only at Coulman Island and Terra Nova Bay area did
some of the sampled stations showed markedly different
values (i.e. with not overlapping confidence intervals) of
species richness. At Coulman Island, station C2 almost
doubled the richness of station C1, while at Terra Nova
Bay, station R4 did not overlapped with the cluster
formed by the others.
Sample-based interpolation (rarefaction) and extrapolation curves for incidence data showed a cluster of curves
with overlapping 95 % confidence intervals (Fig. 4), which
indicate that the three latitudes do not statistically differ. It
is worth remembering, however, that the number of samples available per latitudinal bin is limited and only Cape
Adare–Cape Hallett areas satisfy the recommended
threshold (i.e. the availability of at least 5 samples) for this
kind of analyses (Gotelli and Ellison 2013, 467).
Beta-diversity, calculated as the sum of species
replacement and richness difference (Podani and Schmera
2011), was found to be high at all sites but that of
Terra Nova Bay, the area also having the lowest species
richness (although not statistically significant, Fig. 4),
where beta-diversity and richness agreement appear to be
more balanced (Fig. 5; Table 4). At all latitudes, with the
exception of Coulman Island, only two sampling stations
were performed (and thus the result are less informative),
the similarity always showed percentage values lower
than those of species replacement or richness difference
(Table 4).
Abundance and composition
The relative abundance of species within the six mollusc
classes varied at each sampling station. In general, Gastropoda and Bivalvia are dominant, while at same places
Solenogastres represented *50 % of the number of species
present, e.g. stations Hout4 and Hin5 (Fig. 6).
Out of the 161 species found, two exceeded 1,000
individuals (in non-standardized data), i.e. Onoba turqueti
(Lamy, 1905) (1,668 individuals) and Powellisetia deserta
(E.A. Smith, 1907) (1,060), while other 12 species were
found with more than 100 individuals which are, in order of
decreasing abundance: Eatoniella kerguelenensis (E.A.
Smith, 1907) (971 ind.), Solenogastra sp. 3 (701 ind.),
Thyasira debilis (Thiele, 1912) (568 ind.), Anatoma euglypta (Pelseneer, 1903) (510 ind.), Onoba gelida (E.A.
Smith, 1907) (279 ind.), Onoba kergueleni (E.A. Smith,
1875) (241 ind.), Microdiscula vanhoeffeni Thiele, 1912
123
866
Polar Biol (2014) 37:859–877
Fig. 3 Individual-based
interpolation (rarefaction) and
extrapolation curves for all the
stations sampled at the four
areas considered: Cape Adare
(*71S, stations A1, A2, A3,
A5), Cape Hallett (*72S,
stations Hin2, Hin3, Hin4,
Hout1, Hout2, Hout4), Coulman
Island (*73S, stations C1 and
C2) and Terra Nova Bay
(*75S, stations R2, R3, R4,
SMN). Shaded (or coloured in
the on-line version) areas
represent 95 % unconditional
confidence intervals under the
multinomial model
Fig. 4 Sample-based interpolation (rarefaction) and extrapolation for
incidence data from reference samples corresponding to Cape Adare
(*71S, stations A1, A2, A3 and A5 combined), Cape Hallett
(*72S, stations Hin2, Hin3, Hin4, Hout1, Hout2 and Hout4
combined) and Terra Nova Bay (*75S, stations R2, R3, R4,
SMN). Coulman Island (*73S) stations (i.e. C1 and C2) were not
included in this analysis. Shaded (or coloured in the on-line version)
areas represent 95 % unconditional confidence intervals under the
Bernoulli product model
(218 ind.), Adacnarca nitens Pelseneer, 1903 (137 ind.),
Lissotesta minutissima (E.A. Smith, 1907) (108 ind.),
Solenogastra sp. 4 (104 ind.), Melanella antarctica
123
(Strebel, 1908) (102 ind.) and Lissarca notorcadensis
Melvill & Standen, 1907 (101 ind.).
The abundances of individuals, standardized to
1,000 m2 hauls (Fig. 7), show a dominance of infaunal
groups such as Bivalvia and Scaphopoda in muddy areas
(i.e. station C2; Table 1). Epifaunal groups such as Solenogastres, Monoplacophora and Polyplacophora dominate
in station Hout4 (sandy bottom; Table 1), while Gastropoda dominate at station A4 (sand and pebbles; Table 1).
The multivariate analysis of the assemblage structures
(MDS plots) show an apparent separation of northernmost
stations (Cape Adare and Cape Hallett, respectively, white
triangles and squares in Figs. 8, 9) from southernmost ones
(Coulman Island and Cape Russell, respectively, black
triangles and squares in Figs. 8, 9) either for the plot
referred to ‘‘latitude’’ with all classes combined (squareroot transformed data) (Fig. 8) or for plot where only
Bivalvia and Gastropoda have been taken into account
(Fig. 9). However, ANOSIM analyses show the existence
of a very slight significant difference (at 0.1 %) for the
factor ‘‘latitude’’ when square-root transformed data for all
classes are considered (Table 5). No statistically significant
distinctions can be found for the factor ‘‘depth’’ or for
presence/absence data for both factors (Table 5) (MDS
plots not reported).
Polar Biol (2014) 37:859–877
867
Fig. 5 Ternary plots (Podani
and Schmera 2011) showing the
additive components of gamma
diversity for Cape Adare, Cape
Hallett, Terra Nova Bay and the
whole data set. Data from
Coulman Island (2 stations
only) are only reported in
Table 4. Smaller ternary plots at
the centre of the figure report
the single components evaluated
(species shared, beta-diversity
or species turnover, richness
difference, richness agreement,
species replacement,
nestedness) of the gamma
diversity
Table 4 Percentage statistics from SDR simplex analysis
Additive
Cape Adare
Cape Hallett
Coulman Island
Cape Russell
Total area
Similarity (S)
23.0196
22.4421
16.9811
29.3501
18.9140
Species replacement (R)
31.2392
41.4365
11.3208
45.9922
47.0673
Richness difference (D)
45.7412
36.1214
71.6981
24.6577
34.0187
Beta-diversity (R ? D)
76.9804
77.5579
83.0189
70.6499
81.0860
Richness agreement (R ? S)
54.2588
63.8786
28.3019
75.3423
65.9813
Taxonomical remarks and new records
Although further work will be necessary to refine the
classifications of about a 18 % of species (which could be
either new species or known ones but not easily classifiable
due to unavailability of proper iconography in the literature), the remaining 82 % was represented by: (1) new
records for the Ross Sea (*12 % of the total number of
species) (Figs. 10, 11; Table 6); (2) new species (*6 % of
the total); and (3) species already reported in the literature
for the Ross Sea (*64 % of the total).
Many of the new records are remarkable for a variety of
reasons. For example, Tjaernoeia michaeli Engl, 2002
(Fig. 9d) represents not only the first record for the Ross
Sea but also the second one after the species description
(Engl, 2002). Another species, the monoplacophoran Micropilina arntzi Warén and Hain, 1992 (Fig. 10f), was
collected in a total of 38 specimens, 35 of which in a single
station (Hout4) showing an ‘‘aggregated distribution’’ as it
was already previously observed in the Weddell Sea
(Warén and Hain 1992). The family Newtoniellidae, which
was not treated by Dell (1990), is present in our samples
with two new records for the Ross Sea: Cerithiella seymouriana (Strebel, 1908) (Fig. 9e) and Eumetula dilecta
Thiele, 1912 (Fig. 9f). E. dilecta seems to be a rather
variable species, and some of our specimens were only
tentatively referred to this taxon and reported as E. cf. dilecta (Fig. 9g). Other notable new records for the Ross Sea
are Trilirata sexcarinata Warén & Hain, 1996 (Fig. 9l),
Pleurotomella deliciosa (Thiele, 1912) (Fig. 9j, k), Onoba
egorovae Numanami, 1996 (Fig. 9h) and Onoba paucilirata
(Melvill and Standen, 1912) (Fig. 9i). Omalogyra burdwoodiana (Strebel, 1908) (Fig. 9m) could be considered as
an ‘‘expected’’ new record, since Omalogyridae, at all
123
868
Polar Biol (2014) 37:859–877
Fig. 6 Relative abundance
(number of species) of the six
mollusc classes in each
sampling station
latitudes, can be obtained only when the smallest sediment
fraction is examined.
Lissotesta similis (Thiele, 1912) is here reported as a
new record since our specimens (Fig. 9c) perfectly match
the ‘‘syntype 7’’ of this species figured by Engl (2012,
plate 26, Fig. 8a). Dell (1990) reports another Lissotesta
for the Ross Sea, i.e. L. liratula (Pelseneer, 1903) (Dell
1990, Figs 165–166). These two species, indeed, are very
similar and might represent the same taxon, but Dell’s L.
liratula has a morphology and sculpture that do not completely fit our one. Engl (2012) considers the original
description and the drawing of the holotype of Lissotesta
liratula too poor to decide if the two taxa are conspecific or
not. Given this state of uncertainty, we have preferred to
use the taxon L. similis due to the more similar appearance
of our material with the type material, rather than to refer it
to the form figured by Dell (1990). The minute species
belonging to Brookula were unexpectedly found just with
13 specimens, which were assigned to 3 different species:
B. strebeli (Powell, 1951), B. pfefferi (Powell, 1951)
(Fig. 9a) and B. cf. argentina Zelaya, Absalão and Pimienta, 2006 (Fig. 9b). Of these species, only B. strebeli
(Powell, 1951) was previously reported for the Ross Sea by
Dell (1990) who cited it as B. antarctica (now a synonym
of B. strebeli).
The classification of the species belonging to the Diaphanidae genus Toledonia Dall, 1902 has been problematic since nobody dealt with this group after Dell (1990),
even in the case of monographic contributions dedicated to
Antarctic molluscs (e.g. Hain 1990; Aldea and Troncoso
2010). In our samples, besides six Toledonia species
already known for the Ross Sea, two species were
123
determined at the generic level only. One can be confidently considered new and two others represent new
records for the area. These latter two are Toledonia palmeri
Dell, 1990, which is known only from the Antarctic Peninsula in shallow water (Fig. 10a), and T. cf. perplexa Dall,
1902 (Fig. 10b), which is reported for the Magellanic area
only. T. palmeri has rather distinctive shell forms which, at
least on a morphological base, makes the assignment of our
specimen to this taxon straightforward. Two other opisthobranchs represent important findings for the Ross Sea.
The first one, Philine alata Thiele, 1912 (Fig. 10d, e),
although being a rather common species at King George
Island and along the Scotia Arc (Engl 2012), has never
been previously collected in the Ross Sea. It is possible that
this species was confounded with the similar P. apertissima
E.A. Smith, 1902, which abounds in the Ross Sea (Schiaparelli, unpublished data). The second one, Prodoridunculus gaussianus Thiele, 1912 (Fig. 10c), is a taxon that
will certainly require more study, but the affiliation herein
proposed is based on the presence of two rather unique
characters: (1) the presence of elevated tubercles on the
notum and (2) a series of ‘‘indentations’’ on the notum
edge, apparently due to the presence of spicules. Thiele
(1912), in the unique figure provided with the description
of this species, figures (Tafel XIX, Fig. 5) show a similar
feature in the edge of the notum. Within Bivalvia, one
Propeamussiidae, Cyclochlamys gaussianus (Thiele, 1912)
(Fig. 10g, h) and one Cyclochlamydidae, Cyclochlamys
pteriola (Melvill and Standen, 1907) (Fig. 10i, j) can be
considered new records for the Ross Sea. C. gaussianus has
a distinctive prodissoconch with coarse longitudinal ribs
(Fig. 10h), a feature already documented in the literature
Polar Biol (2014) 37:859–877
869
diameter of the prodissoconch, which allowed the exclusion of other known forms. This is the case of Limatula
ovalis (Fig. 10k–n), which does have a prodissoconch of
about 320 lm, while the other similar species, L. hodgsoni
and L. simillima have smaller prodissoconchs (Hain and
Arnaud 1992).
Discussion
Fig. 7 Abundance of individuals (standardized to 1,000 m2 hauls)
(principal Y axis) and number of species (secondary Y axis)
(Aldea and Troncoso 2010, Fig. 221). C. pteriola, although
similar to the previous species, has no spiny processes and
a completely different microsculpture of prodissoconch
and teloeoconch (Fig. 10j) formed by fine radial lyrae.
Some of the new records were classified taking into
account specific ‘‘indirect’’ morphological features, e.g. the
In recent years, the Scientific Committee on Antarctic
Research (SCAR) has addressed the necessity for baseline
information and long-term monitoring of the Antarctic
environment (Turner et al. 2009), while the Committee for
the Conservation of Antarctic Marine Living Resources
(CCAMLR) has started a bioregionalization program for
the Southern Ocean (Grant et al. 2006). In both cases,
precise distributional data of species are required in order
to develop meaningful models and consistent comparisons
across different spatial and temporal scales.
In this direction, several projects, above all the Census
of Antarctic Marine Life (CAML) (Schiaparelli et al.
2012), have helped in achieving such invaluable information by assessing what is already known and what are the
gaps that still exist. Most of this information is now also
freely and permanently available through a coordinated
network of databases such as the Antarctic Biodiversity
Information Facility (ANTABIF, www.antabif.aq).
Such an increase in knowledge of Antarctic marine life
is unprecedented in the history of Antarctic research
(Kaiser et al. 2013) and the new SCAR new program
‘‘AntEco’’ (State of the Antarctic Ecosystem) will have,
amongst other tasks, that of analysing spatial patterns of
both terrestrial and marine Antarctic species and develop
bio-physical models based on the data obtained so far.
One of the principal variables used in these studies is
species richness, which is an elusive quantity to measure,
its perception being confounded by a variety of factors as
well as by the scale, extent and grain size examined in a
study (Rahbek 2005). Moreover, the comparison of species
richness between sites is also a not straightforward task, as
biased results can be produced if specific methods, such as
rarefaction, are not taken into account (Gotelli and Colwell
2001; Gotelli and Ellison 2013).
In Antarctica, amongst the favourite groups of invertebrates used to explore spatial patterns in diversity and
richness are the Mollusca (e.g. Clarke et al. 2007). The use
of this Phylum as a model taxon is partly due to the large
amount of distributional information available compared
with other taxa, which also made necessary the creation of
a dedicated database for Antarctic species, the Southern
Ocean Mollusc Database (SOMBASE, Griffiths et al.
2003). The importance of molluscs relies in the fact that,
123
870
Polar Biol (2014) 37:859–877
Fig. 8 MDS plot for factor
latitude of the complete dataset
(all classes included)
Fig. 9 MDS plot for factor
latitude, for Bivalvia and
Gastropoda only
Table 5 ANOSIM analysis for factors depth and latitude; in bold the unique statistically significative p
All classes combined
Global R
Only Gastropoda and Bivalvia
p (%)
Global R
p (%)
Depth (H-transformed data)
0.18
9.4
0.232
5.6
Latitude (H-transformed data)
0.447
0.1
0.278
1.5
Depth (presence–absence data)
0.175
12.6
0.202
6.8
Latitude (presence–absence data)
0.29
1.3
0.2111
3.6
unlike polychaetes or arthropods, whose bodies soon decay
after death, a mollusc’s empty shell is informative of the
presence of a species in an area, even though this was not
collected alive. Mollusc tanatocoenoses (i.e. dead assemblages) can sometimes mirror the original biocoenosis due
to their high fidelity (e.g. Carthew and Bosence 1986), but
in biodiversity studies, these two fractions, i.e. the living
and the dead one, have to be dealt with separately.
123
Unfortunately, in the historical literature where the main
focus was species inventory, this distinction was only seldom made explicit and distributional data of both living
and dead mollusc accumulated producing the large amount
of information we have available today. Regrettably, as a
consequence, at least a fraction of the historical distributional data used in biogeographical studies is based on
records of dead shells (Schiaparelli, unpublished).
Polar Biol (2014) 37:859–877
871
Fig. 10 New records of micromolluscs (Gastropoda) collected by the
‘‘Rauschert dredge’’ in the Ross Sea during the Latitudinal Gradient
Program (LGP) voyage on board the RV ‘‘Italica’’. a Brookula
pfefferi (scale bar 200 lm), b Brookula cf. argentina (scale bar
500 lm), c Lissotesta similis (scale bar 200 lm), d Tjaernoeia
micaeli (scale bar 200 lm), e Cerithiella seymouriana (scale bar
1 mm), f Eumetula dilecta (scale bar 1 mm), g Eumetula cf. dilecta
(scale bar 1 mm), h Onoba egorovae (scale bar 500 lm), i Onoba
paucilirata (scale bar 500 lm), j Pleurotomella deliciosa (scale bar
500 lm), k Pleurotomella deliciosa protoconch detail relative to
j figure (scale bar 200 lm), l Trilirata sexcarinata (scale bar
500 lm), m Omalogyra burdwoodiana (scale bar 200 lm)
Despite the considerable amount of data about Antarctic
molluscs and notwithstanding the ‘‘contamination’’ of
distributional data with records of dead shells, rarefaction
curves of species richness plotted against number of sampling locations, still do not show any sign of levelling-off
both for Gastropoda and Bivalvia, suggesting that a complete the inventory of molluscs from Antarctic waters is yet
to be accomplished (Clarke et al. 2007, Fig. 8).
Given this, it would be not surprising to find ‘‘unexpected’’ new records, not only in the historically most
neglected areas, where constraints linked to perennial ice
cover represent a severe logistic limiting factor for sampling, but also in the more well known ones such as the
Ross Sea shelf. For this area, Dell (1990) reported 144
species of Gastropoda (increased to 150 in Griffiths et al.
2009), 42 species of Bivalvia, 3 species of Polyplacophora
and 4 species of Scaphopoda. Schiaparelli et al. (2006)
studying the samples obtained in the framework of two
2004 research voyages done in the Ross Sea under the LGP
framework, where ‘‘standard’’ sampling gears (i.e. grabs,
dredges, trawls) were deployed, found 99 species of Gastropoda, 37 species of Bivalvia, 4 species of Polyplacophora and 2 species of Scaphopoda, with a *20 % of
species that did not overlapped with the list by Dell (1990)
and were considered new records.
In the new data set studied here, always collected during
the 2004 RV ‘‘Italica’’ expedition but with a ‘‘Rauschert
dredge’’ (which was not included in Schiaparelli et al.
123
872
Polar Biol (2014) 37:859–877
Fig. 11 New records of micromolluscs (Gastropoda Opisthobranchia, Bivalvia and Monoplacophora) collected by ‘‘Rauschert dredge’’ in
the Ross Sea during the Latitudinal Gradient Program (LGP) voyage
on board the RV ‘‘Italica’’. a Toledonia palmeri (scale bar 500 lm),
b Toledonia cf. perplexa (scale bar 500 lm), c Prodoridunculus
gaussianus (scale bar 200 lm), d Philine alata ventral view (scale
bar 1 mm), e Philine alata dorsal view (scale bar 1 mm), f Micropilina arntzi (scale bar 200 lm), g Cyclochlamys gaussianus (scale
bar 500 lm), h Cyclochlamys gaussianus protoconch detail relative
to g figure (scale bar 100 lm), i Cyclochlamys pteriola (scale bar
1 mm), j Cyclochlamys pteriola protoconch detail relative to i figure
(scale bar 100 lm), k Limatula ovalis dorsal view (scale bar 1 mm),
l Limatula ovalis ventral view (scale bar 1 mm), m Limatula ovalis
protoconch detail relative to k, l figures (scale bar 200 lm),
n Limatula ovalis (scale bar 200 lm)
2006), other new records were found and have to be added
to the Ross Sea list of species. These account for another
18 % of new findings divided into a 6 % of new species
and a 12 % of new records.
This means that by considering the present data plus
Schiaparelli et al. (2006) and Griffiths et al. (2009), even
though we adopt a ‘‘conservative’’ approach, i.e. by
excluding the species with an ‘‘uncertain’’ status (*18 % of
123
Polar Biol (2014) 37:859–877
873
Table 6 New records for the Ross Sea and their occurrences at the studied stations
A2
A3
A4
Hout1
Hout2
Hout4
Hin3
Hin5
•
R3
R4
•
•
•
Cyclochlamys pteriola (Melvill & Standen, 1907)
•
•
•
•
•
Eumetula dilecta Thiele, 1912
•
•
•
•
•
Lissotesta similis (Pelseneer, 1903)
•
•
Micropilina arntzi Warén & Hain, 1992
•
•
Omalogyra burdwoodiana Strebel, 1908
•
Onoba egorovae Numanami, 1996
Onoba paucilirata (Melvill and Standen, 1912)
•
•
•
•
Philine alata Thiele, 1912
•
•
Pleurotomella deliciosa Thiele, 1912
•
Prodoridunculus gaussianus Thiele, 1912
•
Tjaernoeia micaeli Engl, 2002
•
Toledonia cf. perplexa Dall, 1902
Toledonia palmeri Dell, 1990
SMN
•
Cerithiella similis (Strebel,1908)
Limatula ovalis (Thiele, 1912)
C2
•
Brookula pfefferi Powell, 1951
Brookula cf. argentina Zelaya, Absalao & Pimenta, 2006
Cyclochlamys gaussiana (Thiele, 1912)
C1
•
Trilirata sexcarinata Warén & Hain, 1996
the total, see results), the overall number of new records of
molluscs for the Ross Sea collected during the two LGP
voyages undertaken in 2004 corresponds to 51 species of
gastropods, 5 species of bivalves and one monoplacophoran.
All these new findings (those reported in Schiaparelli
et al. 2006 and present data) were achieved thanks to
specific sampling strategies: (1) the deployment of a variety of different gears (i.e. grab, sledge and trawl net) in the
same area during the RV ‘‘Tangaroa’’ 2004 voyage
(Schiaparelli et al. 2006), a strategy that maximized the
opportunities of collecting species with a different catchability and (2) the use of a ‘‘Rauchert dredge’’ with a small
mesh size during the RV ‘‘Italica’’ 2004 voyage (present
data), which allowed to obtain samples of the size that was
under-represented in historical samples (Dell 1990).
The ‘‘Rauschert dredge’’, analogously to all other towed
gears, is not a quantitative method such as grabs or cores.
This clearly limits the statistics that can be done, as there is
no way to obtain a ‘‘true’’ number of individuals, due to
sampling effect. Although it is possible to standardize, i.e.
reporting abundances to 1,000 m2 hauls (Rehm et al.
2007), this allows only limited comparisons, and other
methods such as rarefaction have to be used.
On the other hand, it is evident that the new records and
the great amount of specimens found in the ‘‘Rauschert
dredge’’ samples are a consequence of the design of the
gear which enables a high sampling performance and
allows to retain the smallest size fraction of the macrofauna
•
•
•
•
which was only seldomly studied before in the Ross Sea
(Dell 1990).
It is well known that the use of a different mesh size, i.e.
a smaller one, can strongly affect the outcomes of a study
(e.g. Bachelet 1990; Tanaka and Leite 1998; Gage et al.
2002) and that several diversity indices are sensitive both
to rare species and to fluctuations in the numbers of
specimens per species that characterize each size fraction
of a sample (Buckland et al. 2011). For example, Shannon’s H0 generally increases with the decrease of the mesh
size until the threshold of 0.5 mm, then it gives a variable
response at smaller mesh sizes (Gage et al. 2002). Besides
this fact, the variety of sampling gears deployed and the
different protocols adopted even between the two 2004
LGP voyages make the comparisons of diversity indices
even more complicated.
In our samples, H0 values between northernmost and
southernmost areas were not found to be statistically different (Fig. 2). Instead, the Simpson index, a more robust
diversity measure (Buckland et al. 2011), was found to not
to differ between Cape Adare and Cape Hallett, which,
however, differed from Coulman Island and Terra Nova
Bay (Fig. 2). Indeed, no latitudinal trends in diversity are
evident in our data: Terra Nova Bay (the southernmost
station) showing higher values of the Simpson index, Cape
Adare and Cape Hallett (the northernmost sites) intermediate ones and Coulman Island (which is almost in the
middle of the Ross Sea) the lowest values.
123
874
Although species richness is constrained by sampling
effort, regardless the considered spatial scale of observation (Clarke et al. 2007; Clarke 2008), sound comparisons
can be made using rarefaction methods (Gotelli and Ellison
2013). In our samples, species richness, evaluated through
this method, analogously to diversity, was found not to
statistically differ in the three main areas considered
(Fig. 4, Coulman Island excluded, see ‘‘Materials and
methods’’). Here again, although the differences are not
statistically relevant, no linear latitudinal trends are evident
indeed: the northernmost site (Cape Adare) showed intermediate richness values, the southernmost one (Terra Nova
Bay) the lowest and the intermediate site (Cape Hallett) the
highest.
The high values of beta-diversity (81.1 %) that characterize the whole data set (Table 4; Fig. 5, right lower
corner) indicate a high rate of substitution of species
between large areas as well as between replicates, suggesting the presence of a high degree of patchiness
amongst habitats along the Victoria Land coast. Some of
the species also showed a very circumscribed distribution
(such as the case of the rare monoplacophoran Micropilina
arntzi) and the high number of singletons (21.74 %) and
uniques (43.48 %) confirms the elevated habitat
heterogeneity.
Present data are in apparent contrast from what was
observed by Schiaparelli et al. (2006), where a cline in
diversity was found, with a higher diversity in the Northern
Ross Sea and a lower one in the Southern Ross Sea, and by
Clarke et al. (2007, cfr. Fig. 4), where an apparent cline of
richness residuals versus plotted latitude was observed. In
Schiaparelli et al. (2006), however, much coarser latitudinal groups and ‘‘larger’’ macrofaunal species were taken
into account: there, for example, the ‘‘north Ross Sea’’
corresponded to data from Cape Adare (71S) and Cape
Hallett (72S) pooled together, while the latitudinal bins
here considered have a finer resolution and the latitudes
71S and 72S were analysed separately.
Concordantly, the multivariate analyses performed did
not resulted in any robust latitudinal patterns. In fact, only
the data combined for all classes together after a square
root transformation show a slightly significant value of
R (at p \ 0.1 %) for the factor latitude.
However, these findings have to be interpreted with
caution, as it is known that by varying the grain size and
extent of an analysis, contrasting results may be obtained
(e.g. Rahbek 2005). It should also be considered that all the
analyses here performed are based on a total of 18 sampling stations only and that, for some latitudes, only very
few samples were available: 5 stations at 71S, 7 at 72S, 2
only at 73S and 4 at 74S (Table 1). This paucity of
samples per latitudinal bin did not allow for meaningful
statistical tests: rarefaction analyses were limited by the
123
Polar Biol (2014) 37:859–877
availability of only two sampling stations at Coulman
Island and multivariate analyses by the low number of
possible permutations.
It is likely that only the analysis of a much wider data set
corrected for the sampling effort (e.g. as in Clarke et al.
2007) where only presence–absence data are taken into
account for all the known Ross Sea sampling stations with
molluscs (*700 collecting sites; Schiaparelli unpublished)
could possibly allow us to understand if a real latitudinal
cline or pattern in diversity exists along Victoria Land
(Schiaparelli et al. in preparation).
Besides the uncertainty that may derive from the low
number of samples available in this study, our results are
nevertheless in agreement with those of Cummings et al.
(2010) who found a similar, nonlinear pattern in diversity
along the Victoria Land coast by studying cores obtained
from grab samples collected during the RV ‘‘Italica’’ 2004
voyage. Here, a significant correlation between both
number of individuals and taxa with sediment phaeophytin
concentration across locations indicated a strong linkage
between benthos and seafloor productivity (Cummings
et al. 2010). In this study, neither latitude nor depth was
good predictors of macrofaunal community composition
and, overall, there were no indications of simple patterns in
Ross Sea benthic assemblage composition (Cummings
et al. 2010).
Although the grab stations studied by Cummings et al.
(2010) and the Rauschert ones studied here are geographically close to each other, it is not possible to use Cummings et al. (2010) phaeophytin and sediment data for our
samples due to the fact that a towed gear, when deployed,
may collect samples from multiple different communities
(e.g. having a different organic content). Consequently,
there is no way to find a direct correspondence between
species/specimens abundances and other variables, as it is
possible with a core from a grab sample. In spite of this, for
some areas such as Cape Adare, both gastropod species
richness and abundance of individuals in our samples show
a striking proportionality to the phaeophytin content in the
sediments as reported in Cummings et al. (2010) (compare
Fig. 7 this study with Fig. 2b of Cummings et al. 2010). At
this site, the highest numbers of molluscs are gastropods
such as Onoba turqueti, Powellisetia deserta, Eatoniella
kerguelensis, Anatoma euglypta, Microdiscula vanhoeffeni
and Onoba kegueleni, all microdetritivores that could be
potentially considered indicators of high organic content
and, due to the above correspondence, of phaeophytin.
Besides the above limitations in statistical analyses, it is
clear that a survey done with a ‘‘Rauschert dredge’’ gives
access to a size fraction which is species rich, but usually
neglected in standard surveys (where larger mesh sizes are
used) and is rewarding in terms of new findings. No other
gear using the same mesh size, i.e. grabs and corers whose
Polar Biol (2014) 37:859–877
samples are generally sieved on small mesh sizes, would
have enabled a similar collection of species and specimens
due to the very limited area of the bottom sampled at each
deployment.
All these new findings in the small fraction mirror what
are already known for the tropics, where about 33.5 % of
the molluscs species have an adult size comprised between
0.4 and 4.1 mm and macromolluscs (i.e. those species
which are larger than 41 mm) do account for just 8 % of
the total fauna (Bouchet et al. 2002). If we adopt Bouchet’s
criterion of size division for our samples (Bouchet et al.
2002), 110 species out of 161 (68.5 %) have a dimension
lower or equal to 4.1 mm. In order to obtain similar results
in terms of number of sampled specimens and species, it
would have been necessary to deploy a grab for an unfeasibly large number of stations/replicates, due to the low
densities that shelf molluscs generally have in grab samples
(Schiaparelli, unpublished). However, the time demand for
such an effort would have been unattainable under standard
sampling conditions, especially operating at high latitudes
with the well-known logistic constraints.
A similar success in sampling with the ‘‘Rauschert
dredge’’ during the 2004 expedition is mirrored by the
finding of several new species and new distributional records
also in other groups. For example, in Isopoda, the 56 % of
the recorded species are new to science and 75 species
represent new records (Choudhury and Brandt 2009).
Unfortunately, few other data sets about molluscs collected by a ‘‘Rauschert dredge’’ are available in the literature, e.g. for the Scotia Arc (Polarstern voyage ANT XIX/
5: 16 ‘‘Rauschert Dredge’’ stations; Linse et al. 2003) and
Bouvet Island (Polarstern voyage ANT XXI/2: with 4
‘‘Rauschert Dredge’’ stations; Linse 2006). However, direct
comparisons of numbers of new records or ratios between
different mollusc classes are prevented for different reasons. In Linse et al. (2003), the taxonomic resolution is still
at a coarse level since the source is a post voyage data
report, and in Linse (2006), a mesh size of 1.5 mm was
used, which is three times larger than the one used in the
Ross Sea in the present study. Mesh sizes of 500 lm have
been instead widely used to sieve grab samples (e.g. Arnaud et al. 2001; Troncoso et al. 2007), but the different
sampling methods adopted (qualitative vs quantitative)
prevents a meaningful comparison of sampling performance between the two studies.
In the present study, the greatest bottleneck was the
great amount of laboratory time and ‘‘scientist-hours’’
necessary to sort and classify the studied 8,359 living
specimens of molluscs found in the samples. This task took
months to be accomplished, often requiring crosschecking
of large numbers of specimens in order to achieve consistent division into OTUs or species across samples. This
kind of workflow shows similar constraints to those found
875
by researchers working in tropical forest areas (e.g. Lawton
et al. 1998).
In this phase, straightforward diagnoses were often
hampered by the nearly non-existent imagery for these
minute species. In order to classify this minute fauna,
understand intraspecific variability in shell features, as well
as select more robust characters that would allow a ‘‘firstpass’’ discrimination of forms, a large use of SEM images
was necessary. This great iconographic effort lead us to
document a variety of unknown features such as larval
shells, opercula and other morphological features, which
will make future classification easier.
It is auspicated that, given the high efficiency of sampling of the ‘‘Rauschert dredge’’, more standardized protocols (i.e. use of the same mesh size of 0.5 mm) could be
established and applied by different research groups in
order to compare, in the future, mollusc assemblages from
different Antarctic areas.
It is expected that even more species will be added in the
near future when samples from the less sampled slope and
abyssal areas of the Ross Sea are added. In this regard, it is
necessary to point out that in the Ross Sea more than 90 %
of the seafloor is deeper than 1,000 m (Griffiths 2010), and
most of the stations studied so far rarely exceed 500 m
depth.
The NIWA ‘‘IPY-CAML’’ voyage (TAN0802) held in
the Ross Sea in 2008 during the International Polar Year
(2007–2008) sampled deeper water strata in the Ross Sea
(i.e. down to 3,490 m) using a ‘‘Brenke-sled’’. These
samples, which are currently under study (Schiaparelli
et al. unpublished), will allow the refinement of our
knowledge of the Ross Sea mollusc fauna and will probably reduce the sampling bias due to the limited number of
deep water stations available so far.
Acknowledgments The authors are grateful to crew of RV ‘‘Italica’’ for their help and efficiency during the 19th expedition in the Ross
Sea, Antarctica. We are indebted to Peter Rehm for the sampling of
the ‘‘Rauschert dredge’’ molluscs. We thank the NIWA (National
Institute of Water and Atmospheric Research) and the Italian National
Antarctic Program (PNRA) for funding and logistic support. We are
indebted to Anne-Nina Lörz (NIWA) and two anonymous referees for
their comments and suggestions, which greatly improved the MS.
This is CAML contribution #162, PNRA project BAMBi (2010/
A1.10) contribution#5 and part of the integrated output from the
SCAR-AntEco Science Programme.
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