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Intertidal benthic communities associated with

the macroalgae Iridaea cordata and Adenocystis
utricularis in King George Island, Antarctica

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Intertidal benthic communities associated
with the macroalgae Iridaea cordata and
Adenocystis utricularis in King George
Island, Antarctica

Alberto Martín, Patricia Miloslavich,

Yusbelly Díaz, Ileana Ortega, Eduardo
Klein, Jesús Troncoso, Cristian Aldea &
Ana K. Carbonini
Polar Biology

ISSN 0722-4060

Polar Biol
DOI 10.1007/s00300-015-1773-1

1 23
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 Author's personal copy
Polar Biol
DOI 10.1007/s00300-015-1773-1

ORIGINAL PAPER

Intertidal benthic communities associated with the macroalgae

Iridaea cordata and Adenocystis utricularis in King George Island,
Antarctica
Alberto Martı́n1 • Patricia Miloslavich1,2 • Yusbelly Dı́az1 • Ileana Ortega1,3 •

Eduardo Klein1 • Jesús Troncoso4,5 • Cristian Aldea6,7 • Ana K. Carbonini1

Received: 18 December 2014 / Revised: 27 July 2015 / Accepted: 17 August 2015

Ó Springer-Verlag Berlin Heidelberg 2015

Abstract Antarctic benthos has been a main target in
Antarctic research, but very few quantitative studies have
been carried out in the littoral zone, which may be sea-
sonally covered by macroalgae. In this work, we studied
(1) cover and biomass of the macroalgae Iridaea cordata
and Adenocystis utricularis, and (2) composition of mac-
robenthic assemblage associated with these macroalgal
species at three locations at King George Island: Mare-
ograph Beach (1 M), Tank’s Bay (2R) and Ardley Bay
(3R). Iridaea cordata was collected by completely
detaching the algae from the substrate, while A. utricularis
was scraped. Adenocystis utricularis covered more than
80 % of the substrate at all locations, while coverage of
Iridaea cordata was below 53 % or absent (3R). Fresh
& Ileana Ortega
ileanaortega@gmail.com
biomass of I. cordata was 0.8–61.4 g/individual and
4.7–93.0 g/100 cm2 for A. utricularis. The assemblage
associated with both macroalgae differed significantly
between sites. The studied fauna was composed mainly of
amphipods, gastropods and bivalves. Species diversity was
higher in the community associated with A. utricularis. A
total of *27 ind/g DW were found associated with I.
cordata, while *112 ind/g DW were found associated
with A. utricularis. The most abundant groups associated
with I. cordata were amphipods at 1 M (57 %) and gas-
tropods at 2R (46 %). Both groups were responsible for the
dissimilarity between localities (62.50 %). The most
abundant groups associated with A. utricularis were the
gastropods at all localities reaching up to 82 % at 1 M.
This study provides a first baseline on the diversity and
abundance of benthic assemblages associated with inter-
tidal macroalgae in the southwest of King George Island.

1
Departamento de Estudios Ambientales, Universidad Simón Keywords Diversity
Macrobenthos
Macroalgae

Bolı́var, Valle de Sartenejas, Caracas, Estado Miranda 89000, Biomass
Amphipods
Gastropods
Venezuela
2
Australian Institute of Marine Science, Townsville, QLD,
Australia
Introduction
3
Programa de Pós-graduação em Oceanografia Biológica,
Universidade Federal do Rio Grande (FURG), Av Itália,
km 8, Campus Carreiros, Rio Grande, RS 96201-90, Brazil
Antarctic benthos has been one of the main targets in
4
Antarctic research (Arntz et al. 1994). In the last decades,
ECIMAT - Toralla Marine Sciences Station, University of
Vigo, 36331 Vigo, Spain
studies of Antarctic benthos have increased particularly
5
since the establishment of permanent research stations in
Departamento de Ecologı́a y Biologı́a Animal, Facultad de
Ciencias del Mar, Universidad de Vigo, Campus Lagoas
coastal zones and the introduction of scuba diving tech-
Marcosende, 36310 Vigo, Spain niques (Jazdzewski et al. 2001; Huang et al. 2007). The
6 Antarctic benthic fauna in general is known to be endemic
Laboratorio de Ecologı́a y Medio Ambiente, Instituto de la
Patagonia, Universidad de Magallanes, Avenida Bulnes, (Wakabara et al. 1990; Jazdzewski et al. 2001; Linse et al.
01890 Punta Arenas, Chile 2006; Fortes and Absalao 2011; De Broyer and Koubbi
7
Programa GAIA-Antártica, Universidad de Magallanes, 2014); however, very few studies have been carried out in
Punta Arenas, Chile the littoral and supralittoral zones and quantitative data on

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 Author's personal copy
density and biomass are very scarce (Gambi et al. 1994).
With expanded sampling efforts, some studies have shown
a great diversity of certain marine groups surrounding the
Antarctic continent, increasing the number of endemic
species. Antarctic endemism may be associated with its
isolation and climate change over an evolutionary time
scale. Despite this relative isolation, recent evidence sug-
gests some degree of connectivity between the Antarctic
and South American faunas (Fortes and Absalao 2011).
The prevalence of ice cover, the abrasive action of ice
floes or ice foot, and the reduction in incoming solar
radiation during the polar winter has led to the assumption
that the Antarctic intertidal fauna is scarce or even absent.
Seasonal changes of salinity caused by the summer ice melt
and runoff with terrestrial sediments as well as high UV
irradiation in the austral summer are thought to be addi-
tional reasons for the poorly populated intertidal habitats in
Polar regions (Bick and Arlt 2013). Disturbance has long
been recognized as an integral part of ecosystems as its
frequency and magnitude are critical in shaping community
structure and its biodiversity. In rocky shores, there are
many physical and biological factors operating at different
scales to determine community structure. For example, at a
local scale, desiccation limits the distribution of many
organisms in the high intertidal zone, while competition
and predation have shown to be important in the lower
subtidal zones. At a regional scale, the community struc-
ture is highly influenced by salinity and wave exposure,
while at a larger scale, temperature and biogeographical
factors play key roles (Ingólfsson 2005; Pabis and Sicinski
2010). In the Antarctic, the benthic community structure
has been proposed to be shaped by ice disturbance along
with biological interactions such as herbivory, competition,
predation and food availability (Jazdzewski et al. 2001;
Momo et al. 2008). The absence of ice in large areas of the
coast during austral summer allows the development of a
diverse intertidal community of algae and invertebrates
which is very dynamic in terms of succession even in the
most stable substrates due to frequent disturbances (Barnes
et al. 1996; Pugh and Davenport 1997; Sicinski et al. 2011).
Due to the high impact of ice in the Antarctic coastal
zone, it has been proposed that species diversity in the
littoral zone is low in shallow areas and increases with
depth (Echeverria and Paiva 2006). In the intertidal zone,
the ice foot can have a thickness of some meters and persist
for much of the year (Barnes and Conlan 2007). In areas
where ice impact is lower, macroalgal growth can be
observed. These macroalgae host a community of gas-
tropods, bivalves and crustaceans among other inverte-
brates (Jazdzewski et al. 2001). Further in depth,
biodiversity patterns may become more complex, even if
not necessarily related to depth as reported for bivalve and
gastropod species for the South Shetland Islands to
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Bellingshausen Sea area (Aldea et al. 2008). Cryptic spe-
cies are also an important feature of Antarctic intertidal
communities and may be very diverse and abundant
(Shabica 1972; Stockton 1973; Barnes et al. 1996; Waller
et al. 2006; Waller 2008; Bick and Arlt 2013). For these,
the ice foot is probably the most important source of dis-
turbance limiting colonization.
Knowledge of the benthic community associated with
macroalgae is limited to a few geographic areas. In the
Antarctic Peninsula, Amsler et al. (2015) studied the
abundance and diversity of gastropods associated with
subtidal macroalgae reporting abundances of up to 38
individuals per 100 g fresh weight of alga regardless of
algal species or site. In the South Shetland Islands, there
are some studies on the taxonomy and the local and
regional distribution of macroalgae (Weykam et al. 1996;
Farı́as et al. 2002), but knowledge of the fauna associated
with these macroalgae is limited to some localities in King
George Island, like Admiralty Bay, Potter Cove and Ade-
laide Island (Jazdzewski et al. 1986, 1991, 1992, 2001;
Broitman et al. 2001; Quartino et al. 2008a). In the subti-
dal, zonation patterns of the benthic communities from
some Antarctic and Subantarctic areas are well known
(Aldea et al. 2008; Saiz et al. 2013), and some quantitative
data from subtidal habitats and shallow sublittoral mac-
robenthos are available at a local scale (Bone 1972; Bre-
gazzi 1972a, b; Richardson and Whitaker 1979; Jazdzewski
et al. 2001; Huang et al. 2007).
Seaweeds are an important source of energy for herbi-
vores, as well as an important source of organic matter for
detritivores and suspension feeders in shallow areas of the
Antarctic littoral (Quartino et al. 2008a, b; Oliveira et al.
2009). In Admiralty Bay seaweed beds cover about 30 %
of the bottom surface, thereby constituting an estimated
74,000 tons of fresh biomass (Zielinski 1990; Nedzarek
and Rakusa-Suszczewski 2004). The morphological com-
plexity of macroalgae is one of the parameters that shape
the epifaunal community. However, the relationship
between the morphological complexity of the macroalgae
with abundance, richness and structure of the associated
faunal assemblage is not simple nor follows a general
pattern as it may also be influenced by other species-
specific attributes of the seaweed (Veiga et al. 2014). In
addition, habitat availability and complexity also play an
important role in shaping the diversity and abundance
patterns of epifaunal communities (Cacabelos et al. 2010;
Torres et al. 2015).
The macroalgal species Iridaea cordata and Adenocystis
utricularis have been associated with subtidal and shallow
rocky shores (0–5 m) and intertidal pools with tempera-
tures over 1 °C, low-to-medium salinities and high solar
radiation conditions (Quartino et al. 2008a, b). Iridaea
cordata is frequently found on the drift. Small specimens
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are also common in rocky pools, cracks and crevices in the
lower inter-tidal zone. The thallus is often clathrate,
greenish to red, with a blade that may reach up to 35 cm in
length. The holdfast is a flat disk with a flat stipe of 1–4 cm
in length (Boraso 2013). Adenocystis utricularis is a very
common species throughout Admiralty Bay and is found
either growing epiphytically on larger algae, especially
Desmarestia spp., or in pools, crevices and clefts protected
from ice scouring at the intertidal zone. Its morphology and
size may vary a great deal with depth and water movement
(Oliveira et al. 2009). The tallus is hollow, shaped like a
bladder and with a solid crust filled with liquid. The stipe is
short and the holdfast is small (Boraso 2013).
In this work we evaluate the cover and biomass of the
macroalgae Iridaea cordata and Adenocystis utricularis,
the dominant algal species found near the Uruguayan
General Artigas Antarctic Base at King George Island, as
well as their associated macrobenthic diversity and
abundance.
Materials and methods
Samples of I. cordata and A. utricularis were obtained at
three sites between February 7 and 9, 2009 at: (1) Ardley
Bay (3R) in front of the Bellingshausen Station (-62.1984,
-58.9542 l), (2) the beach near the oil deposits of the
Bellingshausen Station (Tank’s Bay) (2R) (-62.1972,
-58.9368) and (3) Mareograph Beach (1 M) near the
Uruguayan General Artigas Antarctic Base (62.1883,
-58.9048) (Fig. 1). Macroalgal cover at each site was
quantified with 50 9 50 cm randomly placed quadrats
(n = 20) subdivided into 100 squares. To obtain the
associated benthic fauna, the macroalgae were collected
manually in each site during low tide from randomly
placed quadrats of 10 9 10 cm in which only one indi-
vidual alga was present. Given the morphological differ-
ences between both algal species, I. cordata was collected
by detaching the complete algae from the substrate, while
A. utricularis was collected by scraping the quadrat sur-
face. A total of 22 samples were collected for each species.
Each macroalgal sample was placed in a plastic bag and
fixed in 10 % formaldehyde diluted in seawater. In the
laboratory, each sample was gently stirred to detach the
associated fauna. Once detached, the algae were removed
from the bag and their fresh and dry weight measured
(0.1 g precision scale). Animals were then sieved through a
500-lm Tyler sieve. The macrobenthos was separated into
taxonomic groups, and the amphipods, bivalves and gas-
tropods were identified to species level. For storage, all
animals were preserved in ethanol 70 %.
Macrobenthic density was standardized to individuals per
gram of algal dry weight (ind/g DW). Mean total abundance
between sites was compared through an ANOVA, and total
abundance of the different taxonomic groups between sites
was compared through a PERMANOVA. To visualize these
data, an nMDS was performed using the Bray Curtis index,
on log ?1 transformed data (Clarke and Gorley 2006). The
relative contribution of each taxon to the dissimilarity
between sites was assessed with SIMPER analysis, included
in PRIMER 6.0 (Clarke and Gorley 2006). Biodiversity of
each locality was assessed by studying the relative contri-
bution of each species (taxa) of amphipods and mollusks on
each type of algae. A PERMANOVA using all the species
abundances was carried out to test if there were differences
between localities and the sampling method used for each
macroalga.
Results
Substrate cover by A. utricularis varied from 71 to 81 % in
Mareograph Beach, from 14 and 100 % at Tank’s Bay, and
from 32 and 96 % at Ardley Bay. This macroalga was
dominant in the supralittoral, and in some quadrats, its
cover reached 100 %. The average cover of I. cordata was
between 4 and 53 % at Mareograph Beach and between 0
and 20 % at Tank’s Bay. Iridaea cordata was not found at
Ardley Bay. Fresh biomass of I. cordata varied between
0.8 and 61.4 g/individual, while the fresh biomass of A.
utricularis varied between 4.7 and 93.0 g/100 cm2.
Abundance of associated invertebrates
Abundance of macroinvertebrates associated with these
macroalgae was very high. A total of 35,308 individuals
with an average of 111.6 ± 75.1 ind/g DW were obtained
in association with A. utricularis samples from the three
sites: 80.64 ± 47.18 ind/g DW in Tank’s Bay, 92.8 ±
50.8 ind/g DW in Mareograph Beach and 161.5 ±
93.6 ind/g DW in Ardley Bay. Macrobenthic abundance
associated with I. cordata was lower with a total count of
7908 individuals (26.91 ± 21.25 ind/g DW) from the two
sites in which this macroalga was found: 31.00 ±
14.48 ind/g DW in Tank’s Bay and 22.65 ± 24.23 ind/
g DW in Mareograph Beach (Table 1). Due to limitations
in taxonomic expertise, only bivalves, gastropods and
amphipods were identified to species level (and a few only
to genus). The rest of the specimens were not identified and
are deposited at the Museo de Ciencias Naturales Univer-
sidad Simón Bolı́var, available for examination and inter-
institutional loan. The taxonomic groups represented in the
samples were amphipods, polychaetes, gastropods,
bivalves, platyhelminthes, copepods, isopods, oligochaetes,
nematodes, ostracods, sipunculids, acari and tanaids. The
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Fig. 1 Location of sampling stations in King George Island, Antarctic. 1 Ardley Bay (3R), 2 Tank’s Bay (2R), 3 Mareograph Beach (1 M). The
enlarged area represents the black rectangle in the inset reference map

Table 1 Densities (ind/g DW)

Locality Adenocystis utricularis Iridaea cordata
of macrobenthic organisms
associated with the macroalgae Min Max Average Min Max Average
Adenocystis utricularis and
Iridaea cordata for the sampled Ardley Bay 14.8 335.8 161.5 ± 93.0 – – –
sites Mareograph Beach 31.0 238.5 92.8 ± 50.8 2.0 110.0 22.7 ± 24.2
Tank’s Bay 23.6 234.0 78.0 ± 48.3 6.5 76.0 29.1 ± 17.1

most abundant groups associated with I. cordata were the
amphipods (44.29 %) and the gastropods (34.82 %), while
for A. utricularis the most abundant group was the gas-
tropods (58.46 %). Macrobenthic density in A. utricularis
was much higher than in I. cordata for all sampled beaches.
For A. utricularis, the highest average density was found in
Ardley Bay, which was almost twofold in comparison with
the other sites, while for I. cordata the average value was
relatively similar between sites (Table 2).
The three most abundant groups in all samples were
Amphipoda (11 species), Gastropoda (8 species) and
Bivalvia (5 species). Within the amphipods, the most
abundant species associated with A. utricularis were Or-
chomenella (Orchomenella) ultima (47.24 %) and
Paramoera edouardi (41.15 %), while the most abundant
species associated with I. cordata was Gondogeneia
antarctica (94.30 %). Within the mollusks the most
abundant species were the gastropod Laevilitorina
antarctica (63.29 % in A. utricularis and 46.92 % in I.
cordata) and the bivalve Mysella subquadrata (25.38 % in
A. utricularis and 12.68 % in I. cordata).
The highest average densities of the amphipods P.
edouardi and O. ultima on A. utricularis were observed in
Ardley Bay (10.45 ± 38.75 and 19.10 ± 24.29 ind/g DW,
respectively), being these values more than tenfold in
comparison with Mareograph beach. The lowest density
values for P. edouardi were observed at Mareograph beach
(1.27 ± 2.69 ind/g DW), while the lowest values for O.
ultima were observed at Tank’s Bay (0.06 ± 0.16 ind/
g DW). The average density of G. antarctica on I. cordata

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Table 2 Average density (ind/g DW) ± standard deviation of macrobenthos associated with the macroalgae Adenocystis utricularis and Iridaea
cordata at the three localities in King George Island (DW = dry weight)
Adenocystis utricularis Iridaea cordata
Tank’s Bay Mareograph Beach Ardley Bay Tank’s Bay Mareograph Beach

Amphipods 9.32 ± 12.41 1.67 ± 2.82 34.26 ± 31.01 11.32 ± 10.07 12.55 ± 19.05
Polychaetes 2.05 ± 5.63 1.18 ± 2.67 1.40 ± 1.57 0.64 ± 0.99 0.77 ± 1.17
Gastropods 52.67 ± 43.84 76.51 ± 40.57 59.93 ± 38.72 13.89 ± 9.17 4.65 ± 5.07
Bivalves 1.61 ± 2.57 4.43 ± 4.96 63.91 ± 48.55 4.03 ± 5.79 2.63 ± 5.36
Platyhelminthes 0.91 ± 0.79 1.28 ± 1.12 1.41 ± 2.12 0.76 ± 0.59 0.32 ± 0.89
Copepods 11.53 ± 14.82 4.01 ± 7.70 0.10 ± 0.17 0.03 ± 0.08 1.26 ± 2.54
Isopods 0.04 ± 0.13 0.05 ± 0.09 0.01 ± 0.04 0.04 ± 0.1 0.04 ± 0.11
Oligochaetes 0.14 ± 0.27 2.83 ± 3.91 0.41 ± 0.81 – –
Nematodes – 0.05 ± 0.24 0.06 ± 0.16 – –
Ostracods 0.73 ± 2.18 0.62 ± 2.16 0.02 ± 0.07 0.02 ± 0.08 0.33 ± 1.09
Sipunculids 0.03 ± 0.13 – – – –
Acari 0.02 ± 0.08 0.03 ± 0.06 – – –
Tanaids – 0.01 ± 0.03 – – –
N.I. 1.60 ± 6.56 0.08 ± 0.16 0.02 ± 0.12 0.26 ± 0.57 0.23 ± 0.46

Table 3 Average density (ind/g DW) of amphipods associated with the macroalgae Adenocystis utricularis and Iridaea cordata at the three
localities in King George Island
Adenocystis utricularis Iridaea cordata
Ardley Bay Mareograph Beach Tank’s Bay Mareograph Beach Tank’s Bay
Average SD Average SD Average SD Average SD Average SD
density density density density density

Ampithoe kergueleni 0.03 0.09 – – – – – 0.02 0.08

Bovallia gigantea – – – – – – 0.02 0.05 0.04 0.11
Eurymera monticulosa 0.02 0.07 – – 0.03 0.13 – – – –
Gitanopsis sp. – – 0.02 0.05 – – 0.01 0.05 – –
Gondogeneia antarctica 4.56 12.61 0.12 0.23 0.25 0.81 11.24 17.12 10.88 9.95
Heterophoxus videns 0.02 0.08 0.00 0.02 – – – – – –
Ischyrocerus camptonyx 0.01 0.06 – – 0.08 0.17 0.36 0.73 0.02 0.05
Jassa sp. – – – – – – 0.06 0.23 – –
Oradarea sp. – – – – – – 0.08 0.21 – –
Orchomenella 19.10 24.29 0.22 0.55 0.06 0.16 – – – –
(Orchomenella) ultima
Paramoera edouardi 10.45 10.36 1.27 2.69 8.75 11.79 0.43 1.58 0.32 0.62
Probolisca ovata 0.03 0.07 0.03 0.07 0.14 0.40 0.19 0.53 0.04 0.09
Quadrimaera sp. – – – – – – – – 0.01 0.03
Wandelia crassipes – – – – – – 0.00 0.01 – –
N.I. 0.04 0.19 – – 0.01 0.05 0.02 0.12 – –

was similar between both sites (*11 ind/g DW) (Table 3).
For the mollusks, on the macroalgae A. utricularis, average
densities of L. antarctica were higher in Mareograph Beach
(68.42 ± 38.75 ind/g DW), while for M. subquadrata the
highest value was found in Ardley Bay (63.46 ±
48.42 ind/g DW). On I. cordata, average densities of L.
antarctica were higher in Tank’s Bay (10.56 ± 8.28 ind/
g DW), while for M. subquadrata densities were similar at
both sites (Table 4).
A clear correlation was found between macroalgal bio-
mass and the number of associated macroinvertebrates
measured as total abundance (Adenocystis r = 0.704,
p \ 0.0001; Iridaea r = 0.502, p = 0.003 on log scale;
Figs. 2 and 3). Mean abundance of macroinvertebrates per

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Table 4 Average densities (ind/g DW) and standard deviation (SD) of mollusks associated with the macroalgae Adenocystis utricularis and
Iridaea cordata at the three localities in King George Island
Adenocystis utricularis Iridaea cordata
Ardley Bay Mareograph Beach Tank’s Bay Mareograph Beach Tank’s Bay
Average Standard Average Standard Average Standard Average Standard Average Standard
density deviation density deviation density deviation density deviation density deviation

Eatoniella caliginosa (G) – – 0.01 0.04 – – – – – –

Laevilacunaria antarctica (G) 0.35 0.44 1.05 1.47 1.70 1.41 1.68 2.76 1.53 1.02
Laevilitorina antarctica (G) 56.11 37.57 68.42 38.75 34.78 35.90 0.65 0.99 10.56 8.28
Laevilitorina caliginosa (G) 2.34 1.35 6.93 5.67 15.31 10.26 2.13 3.05 1.43 1.45
Laevilitorina cf wandelensis – – – – – – 0.02 0.12 – –
(G)
Laevilitorina umbilicata (G) 0.25 0.31 1.23 1.26 0.54 0.88 0.16 0.69 0.07 0.14
Nacella polaris concinna (G) 0.04 0.09 – – – – – 0.01 0.03 0.07
Nacella polaris polaris (G) 0.05 0.17 – – – – 0.01 0.03 – –
Onoba steineni (G) 0.80 1.27 – – 0.01 0.06 – – – –
Lissarca miliaris (B) – – 0.10 0.19 0.08 0.21 1.15 2.17 1.47 3.46
Mysella narchii (B) 0.44 0.72 0.04 0.12 0.01 0.06 – – – –
Mysella subquadrata (B) 63.47 48.43 3.30 4.75 1.42 2.43 1.37 3.85 1.87 3.02
Philobrya cf. wandelensis (B) – – – – 0.01 0.06 – – – –
Larvae indet. (B) – – 1.04 1.78 0.08 0.26 0.11 0.36 0.39 1.09

gram of the algae A. utricularis in Ardley Bay was sig-
nificantly higher than those obtained for the other two
locations (Mareograph Beach and Tank’s Bay, ANOVA
followed by Tukey’s honestly significant difference (HSD),
p \ 0.0001) (Fig. 2b). At Ardley Bay, more organisms per
algae weight of A. utricularis were found; however, less
weight of these algae was found at this locality in com-
parison with Mareograph Beach (Fig. 4). Tank’s Bay had
the lowest algal biomass of all sites. For I. cordata, no
differences in the mean density of macrobenthos per algae
DW were found between both localities (ANOVA,
p = 0.2010, Fig. 3b).
Total abundance of the different taxonomic groups
associated with the two macroalgal species was signifi-
cantly different between sites (PERMANOVA, p \ 0.001).
The assemblage associated with A. utricularis in Ardley
Bay is clearly different from the assemblages of Mare-
ograph Beach and Tank’s Bay, while the separation
between these two localities is less evident and shows some
overlapping (Fig. 5). For I. cordata, assemblages from
Tank’s Bay and Mareograph Beach show some separation,
but there is an evident overlap in their ordination (Fig. 6).
Biodiversity
To evaluate the relative contribution of each taxon to the
dissimilarity of each station, we conducted a partition
analysis of the similarity or SIMPER using the abundance
of higher taxonomic groups. In A. utricularis gastropods
and bivalves were responsible for 70–75 % of the dissim-
ilarity between localities followed by amphipods (Fig. 7).
In I. cordata gastropods and amphipods were responsible
for 71 % of the dissimilarity (Fig. 8).
Amphipods
Significant differences on amphipod species assemblages
were observed between the macroalgae (PERMANOVA,
p \ 0.001), and for each of these, species assemblages
were different between sites (nMDS using B–C index over
data log ? 1 transformed) (Figs. 9 and 10). Comparing the
assemblage associated with A. utricularis, the most dis-
similar beaches were Ardley Bay and Mareograph Beach
being O. ultima mostly responsible for these differences.
For I. cordata, dissimilarities between sites were due to G.
antarctica (Table 5).
Mollusks
Significant differences on mollusk species assemblages
were observed between macroalgae (PERMANOVA,
p \ 0.001), and species assemblages for each of these were
also different between sites (nMDS using B–C index over
data log ? 1 transformed) (Figs. 11 and 12). Comparing
the assemblage associated with A. utricularis, the most
dissimilar beaches were Ardley Bay and Tank’s Bay being
L. antarctica and M. subquadrata the species responsible
for most of these differences. For I. cordata, dissimilarities

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Fig. 2 Total abundance of macrobenthos per algal biomass of
Adenocystis utricularis in the three sampling localities. a Organism
density by 100 cm2 of alga, b organism density per dry weight alga.
Fig. 3 Total abundance of macrobenthos per algal biomass for
samples of Iridaea cordata in the two sampling localities. a Organism
density by algae dry weight, b organism density per sampling station.
between sites were due mainly to high abundances of L.
antarctica (Table 6).
Discussion
Benthic marine macroalgae are a conspicuous and diverse
group of primary producers virtually present along all
coasts worldwide where hard substrate is available (Torres
et al. 2015). Macroalgal diversity is low in the Antarctic in
The center bar of the box plot represents the median, the box
extremes the first and third quartiles and the whiskers the 0.05 and
0.95 percentile
The center bar of the box plot represents the median, the box
extremes the first and third quartiles and the whiskers the 0.05 and
0.95 percentile
comparison with tropical and temperate zones; however,
they are highly endemic due to the isolation of the Southern
Ocean (Wiencke et al.2007). Both species found in this
study, typically associated with rocky shores in shallow
waters, have a circumpolar distribution and may also
extend to sub-Antarctic Islands and Tierra del Fuego in the
southern tip of South America. Adenocystis utricularis may
even occur in Australia and New Zealand (Wiencke et al.
2007; Quartino et al. 2008a). In the Antarctic, seasonal
changes in macronutrient concentration occur, but these are
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Fig. 4 Dry biomass of Adenocystis utricularis in the three sampling
locations. The center bar of the box plot represents the median, the
box extremes the first and third quartiles and the whiskers the 0.05
and 0.95 percentile
Fig. 5 Non-metric multidimensional scale ordination (nMDS) of the
macroinvertebrates associated with Adenocystis utricularis in the
sampled localities, stress = 0.139
not a limiting factor for macroalgal growth since their
levels are high throughout the year (Wiencke et al. 2007).
The higher average density of A. utricularis observed at
Ardley Bay in comparison with the other two localities
could be due to an extra nutrient load from the Belling-
shausen Station, which is located in front of the sampled
site. Adenocystis utricularis has been reported to have an
opportunistic life strategy in terms of growth and responds
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Fig. 6 Non-metric multidimensional scale ordination (nMDS) of
macroinvertebrates associated with Iridaea cordata in the sampled
localities, stress = 0.127
to seasonal environmental changes (Wiencke et al. 2007).
As observed in some Antarctic species, competition may
determine zonation. In this way, the extensive growth of A.
utricularis at this site could be preventing the growth of I.
cordata (not observed in the area) as the large canopy of
the first may limit the expansion of the second, a light
responder species (Wiencke et al. 2007). Information is
very scarce regarding macroalgal cover and biomass for the
Antarctic. In the subtidal zone of Antarctic Peninsula,
down to 20 m in depth, most of the macroalgal cover is
represented by common brown algae of the genera Des-
marestia and Himantothallus. The red alga, I. cordata is
reported as a conspicuous species between 2 and 5 m depth
(Amsler et al. 1995; Huang et al. 2007).
Macroalgae provide habitat that supports diverse epi-
phytic algae, as well as a variety of sessile and mobile
animals (Torres et al. 2015). Biological and physical fac-
tors regulate the distribution and abundance of grazers
associated with marine plants. While the vast majority of
studies have been conducted in temperate and tropical
marine systems, it is likely that grazers associate in a
similar way with marine plants in polar marine environ-
ments and that these interactions are essential to under-
standing the dynamics of these communities (Huang et al.
2007). The significant differences in mollusk and amphi-
pod densities found between the two macroalgal species
could be due to differences in their architecture or mor-
phological complexity, palatability and defense mecha-
nisms. A positive relationship has been observed between
macroalgal morphological complexity (e.g., degree of
branching, algal width and the log of the stem) and the
abundance and diversity of their associated epifauna. In
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Polar Biol

Fig. 7 Relative contribution in abundance (ind/sample) of macroinvertebrate taxa associated with Adenocystis utricularis in the three sampled
localities. a Ardley Bay, b Mareograph Beach, c Tank’s Bay

Fig. 8 Relative contribution in abundance (ind/sample) of macroinvertebrate taxa associated with Iridaea cordata in the two sampled localities.
a Mareograph Beach, b Tank’s Bay

this regard, it has been suggested that high morphological
complexity increases epifaunal abundance and diversity by
reducing predation and physical disturbance (Huang et al.
2006; Jacobucci et al. 2008) while increasing food avail-
ability and the number of different niches (Chemello and
Milazzo, 2002; Torres et al. 2015). Quartino et al. (2008b)
proposed that the abundant benthic herbivore fauna
observed at Potter Cove, King George Island, probably
depends on seaweeds as their main source of particulate
and dissolved organic carbon. Regarding palatability,
Wessels et al. (2006) studied herbivore–macroalgae inter-
actions in Kongsfjorden (Arctic waters) and found that only

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Fig. 9 Non-metric multidimensional scale ordination (nMDS) of Fig. 11 Non-metric multidimensional scale ordination (nMDS) of
amphipods associated with Adenocystis utricularis in the three mollusk assemblage associated with Adenocystis utricularis in the
sampled sites, Stress = 0.091 sampled sites, stress = 0.096

Fig. 10 Non-metric multidimensional scale ordination (nMDS) of Fig. 12 Non-metric multidimensional scale ordination (nMDS) of
amphipods associated with Iridaea cordata in both sampling sites, mollusk assemblage associated with Iridaea cordata in the sampled
stress = 0.083 sites, stress = 0.152

Table 5 Contribution to the site diversity of the main amphipod species of each alga for the sampled sites
Algae Locality Dissimilarity (%) Species Contribution percentage

Adenocystis utricularis Ardley Bay-Mareograph Beach 80.37 Orchomenella (Orchomenella) ultima 49.98
Paramoera edouardi 34.70
Gondogeneia Antarctica 14.02
Ardley Bay-Tank’s Bay 78.03 Orchomenella (Orchomenella) ultima 49.57
Paramoera edouardi 35.55
Mareograph Beach-Tank’s Bay 71.83 Paramoera edouardi 73.31
Orchomenella (Orchomenella) ultima 13.24
Iridaea cordata Mareograph Beach-Tank’s Bay 53.14 Gondogeneia Antarctica 85.22
Ischyrocerus camptonyx 5.39

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Table 6 Contribution to the site diversity of the main mollusk species of each alga for the sampled sites
Algae Locality
Adenocystis utricularis Ardley Bay-Mareograph Beach
Ardley Bay-Tank’s Bay
Mareograph Beach-Tank’s Bay
Iridaea cordata Mareograph Beach-Tank’s
two species (the sea urchin Strongylocentrotus droe-
bachensis and the amphipod Gammarellus homari) out of
19 invertebrate species associated with macroalgae did
actually feed on it, indicating that herbivory plays a minor
role in this area. Laboratory experiments carried out by the
same authors demonstrated that both the sea urchin and the
amphipod had specific preferences when offered different
types of algae and that tissue-specific and physical plant
properties also affected the feeding response of the
amphipod. As for defense mechanisms, inducible defense,
or the production of metabolites by the algae in response to
herbivory, has been reported mostly for brown macroalgae
(the case of A. utricularis), while few examples exist for
red macroalgae (the case of I. cordata) (Rothäusler et al.
2005). Macaya et al. (2005) found in brown algae of
Southern Chile that inducible defense expressed as a
reduction in palatability may occur in 12 days with the
presence of amphipod grazers. In addition to herbivory and
these other biological regulators, the Antarctic benthos is
also subjected to other devastating ice-related impacts such
as high wind and wave action, hypoxia, freshwater flood-
ing, localized pollution, and ultraviolet (UV) radiation,
among others (Barnes and Conlan 2007). These effects
may be mitigated when the macroalgae are found in high
densities.
Jazdzewski et al. (1991, 1995, 2001) reported that
macrobenthos associated with shallow waters at Admiralty
Bay, King George Island, is composed mainly by amphi-
pods followed by gastropods and bivalves, varying their
densities throughout the year, regardless of macroalgal
presence. Similar in timing to our study, these authors
report that in the Austral summer (January to February),
amphipods were the most abundant group, followed by
gastropods. Jazdzewski et al. (2001) discussed that in the
west Antarctic, sea-ice appears less severe, allowing the
seasonal growth of macroalgae in sheltered places of the
Dissimilarity (%) Species Contribution percentage
56.88 Laevilitorina antarctica 46.53
Mysella subquadrata 42.69
Laevilitorina caliginosa 6.10
70.59 Mysella subquadrata 52.56
Laevilitorina antarctica 35.98
Laevilitorina caliginosa 8.63
59.94 Laevilitorina antarctica 79.32
Laevilitorina caliginosa 10.77
78.01 Laevilitorina antarctica 55.36
Laevilacunaria antarctica 16.24
Mysella subquadrata 12.36
Laevilitorina caliginosa 11.92
sublittoral/littoral fringe. In this mostly immersed zone, it
is common to observe the patellid gastropod N. concinna,
the amphipods P. edouardi and G. antarctica, gastropods
of the genera Laevilitorina and Laevilacunaria, and the
bivalve M. subquadrata. Sicinski et al. (2011) reported that
amphipod species G. antarctica and P. edouardi, and the
limpet N. concinna are the most important components of
the invertebrate assemblage on rocky (boulders, cobbles
and pebbles) substrates in the littoral zone. Some amphipod
species may migrate between areas with and without veg-
etation. For example, G. antarctica which was found to be
responsible for the dissimilarities between sites for I. cor-
data is a species with high mobility and can swim actively
between pools (usually with more vegetation) and shallow
zones (Thurston 1974). Gastropods like Laevilacunaria and
Laevilitorina are known to consume epiphytic diatoms and
macroalgae and can also migrate to shallower zones where
macroalgae are less frequent (Jazdzewski et al. 2001).
Previous amphipod biodiversity studies in the areas of
Maxwell Bay and the Western Atlantic Peninsula have
reported at least 55 species for this group (Rauschert 1989,
1990, 1991, 1994, 1997; Ren and Huang 1991; Rauschert
and Andres 1993, 1994; Huang et al. 2007; Kim et al.
2014). The structure of these species-specific macroalgal-
associated amphipod communities can vary across spatial
scales of 3 km (Huang et al. 2007). In our study we found
10 species, one of them (Ampithoe kergueleni originally
described for the Iles Kerguelen, southern Indian Ocean by
De Broyer et al. 2007) consisting of a new report for the
Antarctic Peninsula. Few species exhibit a circum-sub-
Antarctic pattern, with records on the southern shelf of
South America and around the sub-Antarctic islands of the
southern Indian Ocean as well as around Macquarie Island
and/or the New Zealand sub-Antarctic islands. Most of
these species show low dispersal capacity (De Broyer and
Jazdzewska 2014), and genetic studies suggest that
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circumpolar distribution may be best explained by post-
glacial colonization of the sub-Antarctic islands by
macroalgal rafting through the Antarctic Circumpolar
Current (ACC). Nevertheless, a potential source region has
yet to be identified (Nikula et al. 2010).
Regarding amphipod density, Huang et al. (2007) found
up to 20 individuals/g of algal fresh weight which is lower
than the density we found associated with A. utricularis in
Ardley Bay. In both studies, the highest proportion of
amphipod species was associated with brown algae. The
most abundant species were O. ultima and P. edouardi in
association with A. utricularis, being O. ultima the main
responsible for the differences between the three sampling
sites. Jazdzewski et al. (2001) were the first to report O.
ultima in very shallow areas (5–10 cm deep) as it had been
previously found between 3 and 10 m in depth. This
amphipod species is recognized as a typical epibenthic
dweller in this fringe of the sublittoral rocky shore, capable
of burrowing in suitable sediments. The feeding habits are
unknown but some Orchomenella species have been rec-
ognized as scavengers and detritivores. The species P.
edouardi has being categorized as an omnivore/herbivore
but specific feeding habits are unknown (Jazdzewski et al.
2001). Associated with the alga I. cordata, the most
abundant species was the omnivorous G. antarctica, which
feeds primarily on microalgae and secondarily on
macroalgae, but can also feed on detritus and predate on
small crustaceans like copepods and other amphipods.
Gondogeneia antarctica is also the predominant herbivore
of epontic microalgae which colonize the icefoot in some
Antarctic islands (Jazdzewski et al. 2001).
Within the mollusks, the most abundant species were L.
antarctica and M. subquadrata. The first was previously
reported as a common and abundant shallow-water species
in Admiralty Bay (Arnaud et al. 1986) and in Robert Island
(South Shetland Islands) (Castilla and Rozbaczylo 1985),
as well as an important component of the shallow sublit-
toral of Terra Nova Bay (Ross Sea) (Gambi et al. 1994).
Not much is known about the habitat and food preferences
of M. subquadrata. A similar study conducted in the sub-
tidal zone of hard-bottom communities near Palmer Sta-
tion, western Antarctic Peninsula, reported Skenella
umbilicata, Laevilacunaria antarctica and Eatoniella
calignosa as the most abundant gastropod species associ-
ated with macroalgae (Amsler et al. 2015), indicating that
at least the first two are distributed along the whole range
from intertidal to subtidal.
This study provides a first baseline of information of the
diversity and abundance of benthic assemblages associated
with intertidal macroalgae in the southwest of King George
Island and raises several questions for future research. Once
established which benthic species are associated with
macroalgae and how abundant they are, the next questions
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are related to their life cycles and their role on controlling
the assemblage. For example: does herbivory play a major
role on the macroalgal biomass stock? Is any of these her-
bivores exerting a top-down control? Which of the associ-
ated species actually feed on the macroalgae rather than just
benefit from consuming particulate organic matter or from
the shelter that the macroalgae provide? Do these algae
develop inducible defenses against the herbivores? How
does macroalgal cover along with benthic diversity and
abundance vary throughout the year? What is the life cycle
of the most abundant benthic species? Answering some of
these questions will certainly fill the many gaps we have in
our knowledge of Antarctic intertidal benthic ecology.
Acknowledgments This research was supported by the Venezuelan
Scientific Antarctic Program, through the 2009 exploration campaign
carried out by the Ministerio del Poder Popular para Ciencia, Tec-
nologı́a e Innovación (MCTI) and the Armada Nacional Bolivariana,
with the collaboration of the Instituto Antártico Uruguayo. Special
thanks to Manuel Caballer and Nelsy Rivero, who helped in the
fieldwork. We also wish to thank Sandra López, Humberto Camisotti
and Emiliana Mendoza, students at Universidad Simón Bolı́var in
Caracas, Venezuela for their laboratory assistance and Emanuel
Valero for his assistance with the figures. We extend our gratitude to
the four anonymous reviewers who provided invaluable comments
and literature to significantly improve the manuscript.
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