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

ARTICLE in POLAR BIOLOGY · SEPTEMBER 2015 Impact Factor: 1.59 · DOI: 10.1007/s00300-015-1773-1

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Yusbelly Diaz Ileana Ortega Simon Bolívar University Simon Bolívar University

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Available from: Yusbelly Diaz Retrieved on: 20 October 2015 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

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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

1 1,2 1 1,3 Alberto Martı´n • Patricia Miloslavich • Yusbelly Dı´az • Ileana Ortega • 1 4,5 6,7 1 Eduardo Klein • Jesu´s Troncoso • Cristian Aldea • Ana K. Carbonini

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

1 Departamento de Estudios Ambientales, Universidad Simo´n Keywords Diversity Á Macrobenthos Á Macroalgae Á Bolı´var, Valle de Sartenejas, Caracas, Estado Miranda 89000, Biomass Á Amphipods Á Gastropods Venezuela 2 Australian Institute of Marine Science, Townsville, QLD, Australia Introduction 3 Programa de Po´s-graduac¸a˜o em Oceanografia Biolo´gica, ´ Universidade Federal do Rio Grande (FURG), Av Italia, Antarctic benthos has been one of the main targets in km 8, Campus Carreiros, Rio Grande, RS 96201-90, Brazil 4 Antarctic research (Arntz et al. 1994). In the last decades, ECIMAT - Toralla Marine Sciences Station, University of studies of Antarctic benthos have increased particularly Vigo, 36331 Vigo, Spain since the establishment of permanent research stations in 5 ´ ´ Departamento de Ecologıa y Biologıa , Facultad de coastal zones and the introduction of scuba diving tech- Ciencias del Mar, Universidad de Vigo, Campus Lagoas Marcosende, 36310 Vigo, Spain niques (Jazdzewski et al. 2001; Huang et al. 2007). The Antarctic benthic fauna in general is known to be endemic 6 Laboratorio de Ecologı´a 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-Anta´rtica, 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 123 Author's personal copy

Polar Biol density and biomass are very scarce (Gambi et al. 1994). Bellingshausen Sea area (Aldea et al. 2008). Cryptic spe- With expanded sampling efforts, some studies have shown cies are also an important feature of Antarctic intertidal a great diversity of certain marine groups surrounding the communities and may be very diverse and abundant Antarctic continent, increasing the number of endemic (Shabica 1972; Stockton 1973; Barnes et al. 1996; Waller species. Antarctic endemism may be associated with its et al. 2006; Waller 2008; Bick and Arlt 2013). For these, isolation and climate change over an evolutionary time the ice foot is probably the most important source of dis- scale. Despite this relative isolation, recent evidence sug- turbance limiting colonization. gests some degree of connectivity between the Antarctic Knowledge of the benthic community associated with and South American faunas (Fortes and Absalao 2011). macroalgae is limited to a few geographic areas. In the The prevalence of ice cover, the abrasive action of ice , Amsler et al. (2015) studied the floes or ice foot, and the reduction in incoming solar abundance and diversity of gastropods associated with radiation during the polar winter has led to the assumption subtidal macroalgae reporting abundances of up to 38 that the Antarctic intertidal fauna is scarce or even absent. individuals per 100 g fresh weight of alga regardless of Seasonal changes of salinity caused by the summer ice melt algal species or site. In the , there and runoff with terrestrial sediments as well as high UV are some studies on the and the local and irradiation in the austral summer are thought to be addi- regional distribution of macroalgae (Weykam et al. 1996; tional reasons for the poorly populated intertidal habitats in Farı´as et al. 2002), but knowledge of the fauna associated Polar regions (Bick and Arlt 2013). Disturbance has long with these macroalgae is limited to some localities in King been recognized as an integral part of ecosystems as its George Island, like Admiralty Bay, Potter Cove and Ade- frequency and magnitude are critical in shaping community laide Island (Jazdzewski et al. 1986, 1991, 1992, 2001; structure and its biodiversity. In rocky shores, there are Broitman et al. 2001; Quartino et al. 2008a). In the subti- many physical and biological factors operating at different dal, zonation patterns of the benthic communities from scales to determine community structure. For example, at a some Antarctic and Subantarctic areas are well known local scale, desiccation limits the distribution of many (Aldea et al. 2008; Saiz et al. 2013), and some quantitative organisms in the high intertidal zone, while competition data from subtidal habitats and shallow sublittoral mac- and predation have shown to be important in the lower robenthos are available at a local scale (Bone 1972; Bre- subtidal zones. At a regional scale, the community struc- gazzi 1972a, b; Richardson and Whitaker 1979; Jazdzewski ture is highly influenced by salinity and wave exposure, et al. 2001; Huang et al. 2007). while at a larger scale, temperature and biogeographical Seaweeds are an important source of energy for herbi- factors play key roles (Ingo´lfsson 2005; Pabis and Sicinski vores, as well as an important source of organic matter for 2010). In the Antarctic, the benthic community structure detritivores and suspension feeders in shallow areas of the has been proposed to be shaped by ice disturbance along Antarctic littoral (Quartino et al. 2008a, b; Oliveira et al. with biological interactions such as herbivory, competition, 2009). In Admiralty Bay seaweed beds cover about 30 % predation and food availability (Jazdzewski et al. 2001; of the bottom surface, thereby constituting an estimated Momo et al. 2008). The absence of ice in large areas of the 74,000 tons of fresh biomass (Zielinski 1990; Nedzarek coast during austral summer allows the development of a and Rakusa-Suszczewski 2004). The morphological com- diverse intertidal community of algae and invertebrates plexity of macroalgae is one of the parameters that shape which is very dynamic in terms of succession even in the the epifaunal community. However, the relationship most stable substrates due to frequent disturbances (Barnes between the morphological complexity of the macroalgae et al. 1996; Pugh and Davenport 1997; Sicinski et al. 2011). with abundance, richness and structure of the associated Due to the high impact of ice in the Antarctic coastal faunal assemblage is not simple nor follows a general zone, it has been proposed that species diversity in the pattern as it may also be influenced by other species- littoral zone is low in shallow areas and increases with specific attributes of the seaweed (Veiga et al. 2014). In depth (Echeverria and Paiva 2006). In the intertidal zone, addition, habitat availability and complexity also play an the ice foot can have a thickness of some meters and persist important role in shaping the diversity and abundance for much of the year (Barnes and Conlan 2007). In areas patterns of epifaunal communities (Cacabelos et al. 2010; where ice impact is lower, macroalgal growth can be Torres et al. 2015). observed. These macroalgae host a community of gas- The macroalgal species Iridaea cordata and Adenocystis tropods, bivalves and crustaceans among other inverte- utricularis have been associated with subtidal and shallow brates (Jazdzewski et al. 2001). Further in depth, rocky shores (0–5 m) and intertidal pools with tempera- biodiversity patterns may become more complex, even if tures over 1 °C, low-to-medium salinities and high solar not necessarily related to depth as reported for bivalve and radiation conditions (Quartino et al. 2008a, b). Iridaea gastropod species for the South Shetland Islands to cordata is frequently found on the drift. Small specimens 123 Author's personal copy

Polar Biol are also common in rocky pools, cracks and crevices in the between sites was compared through an ANOVA, and total lower inter-tidal zone. The thallus is often clathrate, abundance of the different taxonomic groups between sites greenish to red, with a blade that may reach up to 35 cm in was compared through a PERMANOVA. To visualize these length. The holdfast is a flat disk with a flat stipe of 1–4 cm data, an nMDS was performed using the Bray Curtis index, in length (Boraso 2013). Adenocystis utricularis is a very on log ?1 transformed data (Clarke and Gorley 2006). The common species throughout Admiralty Bay and is found relative contribution of each taxon to the dissimilarity either growing epiphytically on larger algae, especially between sites was assessed with SIMPER analysis, included Desmarestia spp., or in pools, crevices and clefts protected in PRIMER 6.0 (Clarke and Gorley 2006). Biodiversity of from ice scouring at the intertidal zone. Its morphology and each locality was assessed by studying the relative contri- size may vary a great deal with depth and water movement bution of each species (taxa) of amphipods and mollusks on (Oliveira et al. 2009). The tallus is hollow, shaped like a each type of algae. A PERMANOVA using all the species bladder and with a solid crust filled with liquid. The stipe is abundances was carried out to test if there were differences short and the holdfast is small (Boraso 2013). between localities and the sampling method used for each In this work we evaluate the cover and biomass of the macroalga. 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 Results abundance. Substrate cover by A. utricularis varied from 71 to 81 % in Mareograph Beach, from 14 and 100 % at Tank’s Bay, and Materials and methods from 32 and 96 % at Ardley Bay. This macroalga was dominant in the supralittoral, and in some quadrats, its Samples of I. cordata and A. utricularis were obtained at cover reached 100 %. The average cover of I. cordata was three sites between February 7 and 9, 2009 at: (1) Ardley between 4 and 53 % at Mareograph Beach and between 0 Bay (3R) in front of the Bellingshausen Station (-62.1984, and 20 % at Tank’s Bay. Iridaea cordata was not found at -58.9542 l), (2) the beach near the oil deposits of the Ardley Bay. Fresh biomass of I. cordata varied between Bellingshausen Station (Tank’s Bay) (2R) (-62.1972, 0.8 and 61.4 g/individual, while the fresh biomass of A. -58.9368) and (3) Mareograph Beach (1 M) near the utricularis varied between 4.7 and 93.0 g/100 cm2. Uruguayan General Artigas Antarctic Base (62.1883, -58.9048) (Fig. 1). Macroalgal cover at each site was Abundance of associated invertebrates quantified with 50 9 50 cm randomly placed quadrats (n = 20) subdivided into 100 squares. To obtain the Abundance of macroinvertebrates associated with these associated benthic fauna, the macroalgae were collected macroalgae was very high. A total of 35,308 individuals manually in each site during low tide from randomly with an average of 111.6 ± 75.1 ind/g DW were obtained placed quadrats of 10 9 10 cm in which only one indi- in association with A. utricularis samples from the three vidual alga was present. Given the morphological differ- sites: 80.64 ± 47.18 ind/g DW in Tank’s Bay, 92.8 ± ences between both algal species, I. cordata was collected 50.8 ind/g DW in Mareograph Beach and 161.5 ± by detaching the complete algae from the substrate, while 93.6 ind/g DW in Ardley Bay. Macrobenthic abundance A. utricularis was collected by scraping the quadrat sur- associated with I. cordata was lower with a total count of face. A total of 22 samples were collected for each species. 7908 individuals (26.91 ± 21.25 ind/g DW) from the two Each macroalgal sample was placed in a plastic bag and sites in which this macroalga was found: 31.00 ± fixed in 10 % formaldehyde diluted in seawater. In the 14.48 ind/g DW in Tank’s Bay and 22.65 ± 24.23 ind/ laboratory, each sample was gently stirred to detach the g DW in Mareograph Beach (Table 1). Due to limitations associated fauna. Once detached, the algae were removed in taxonomic expertise, only bivalves, gastropods and from the bag and their fresh and dry weight measured amphipods were identified to species level (and a few only (0.1 g precision scale). were then sieved through a to ). The rest of the specimens were not identified and 500-lm Tyler sieve. The macrobenthos was separated into are deposited at the Museo de Ciencias Naturales Univer- taxonomic groups, and the amphipods, bivalves and gas- sidad Simo´n Bolı´var, available for examination and inter- tropods were identified to species level. For storage, all institutional loan. The taxonomic groups represented in the animals were preserved in ethanol 70 %. samples were amphipods, polychaetes, gastropods, Macrobenthic density was standardized to individuals per bivalves, platyhelminthes, copepods, isopods, oligochaetes, gram of algal dry weight (ind/g DW). Mean total abundance nematodes, ostracods, sipunculids, acari and tanaids. The 123 Author's personal copy

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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 species associated with I. cordata was Gondogeneia amphipods (44.29 %) and the gastropods (34.82 %), while antarctica (94.30 %). Within the mollusks the most for A. utricularis the most abundant group was the gas- abundant species were the gastropod Laevilitorina tropods (58.46 %). Macrobenthic density in A. utricularis antarctica (63.29 % in A. utricularis and 46.92 % in I. was much higher than in I. cordata for all sampled beaches. cordata) and the bivalve Mysella subquadrata (25.38 % in For A. utricularis, the highest average density was found in A. utricularis and 12.68 % in I. cordata). Ardley Bay, which was almost twofold in comparison with The highest average densities of the amphipods P. the other sites, while for I. cordata the average value was edouardi and O. ultima on A. utricularis were observed in relatively similar between sites (Table 2). Ardley Bay (10.45 ± 38.75 and 19.10 ± 24.29 ind/g DW, The three most abundant groups in all samples were respectively), being these values more than tenfold in Amphipoda (11 species), (8 species) and comparison with Mareograph beach. The lowest density Bivalvia (5 species). Within the amphipods, the most values for P. edouardi were observed at Mareograph beach abundant species associated with A. utricularis were Or- (1.27 ± 2.69 ind/g DW), while the lowest values for O. chomenella (Orchomenella) ultima (47.24 %) and ultima were observed at Tank’s Bay (0.06 ± 0.16 ind/ Paramoera edouardi (41.15 %), while the most abundant 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). g DW), while for M. subquadrata densities were similar at For the mollusks, on the macroalgae A. utricularis, average both sites (Table 4). densities of L. antarctica were higher in Mareograph Beach A clear correlation was found between macroalgal bio- (68.42 ± 38.75 ind/g DW), while for M. subquadrata the mass and the number of associated macroinvertebrates highest value was found in Ardley Bay (63.46 ± measured as total abundance (Adenocystis r = 0.704, 48.42 ind/g DW). On I. cordata, average densities of L. p \ 0.0001; Iridaea r = 0.502, p = 0.003 on log scale; antarctica were higher in Tank’s Bay (10.56 ± 8.28 ind/ 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 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- and bivalves were responsible for 70–75 % of the dissim- nificantly higher than those obtained for the other two ilarity between localities followed by amphipods (Fig. 7). locations (Mareograph Beach and Tank’s Bay, ANOVA In I. cordata gastropods and amphipods were responsible followed by Tukey’s honestly significant difference (HSD), for 71 % of the dissimilarity (Fig. 8). p \ 0.0001) (Fig. 2b). At Ardley Bay, more organisms per algae weight of A. utricularis were found; however, less Amphipods weight of these algae was found at this locality in com- parison with Mareograph Beach (Fig. 4). Tank’s Bay had Significant differences on amphipod species assemblages the lowest algal biomass of all sites. For I. cordata,no were observed between the macroalgae (PERMANOVA, differences in the mean density of macrobenthos per algae p \ 0.001), and for each of these, species assemblages DW were found between both localities (ANOVA, were different between sites (nMDS using B–C index over p = 0.2010, Fig. 3b). data log ? 1 transformed) (Figs. 9 and 10). Comparing the Total abundance of the different taxonomic groups assemblage associated with A. utricularis, the most dis- associated with the two macroalgal species was signifi- similar beaches were Ardley Bay and Mareograph Beach cantly different between sites (PERMANOVA, p \ 0.001). being O. ultima mostly responsible for these differences. The assemblage associated with A. utricularis in Ardley For I. cordata, dissimilarities between sites were due to G. Bay is clearly different from the assemblages of Mare- antarctica (Table 5). ograph Beach and Tank’s Bay, while the separation between these two localities is less evident and shows some Mollusks overlapping (Fig. 5). For I. cordata, assemblages from Tank’s Bay and Mareograph Beach show some separation, Significant differences on mollusk species assemblages but there is an evident overlap in their ordination (Fig. 6). were observed between macroalgae (PERMANOVA, p \ 0.001), and species assemblages for each of these were Biodiversity also different between sites (nMDS using B–C index over data log ? 1 transformed) (Figs. 11 and 12). Comparing To evaluate the relative contribution of each taxon to the the assemblage associated with A. utricularis, the most dissimilarity of each station, we conducted a partition dissimilar beaches were Ardley Bay and Tank’s Bay being analysis of the similarity or SIMPER using the abundance L. antarctica and M. subquadrata the species responsible of higher taxonomic groups. In A. utricularis gastropods for most of these differences. For I. cordata, dissimilarities

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Fig. 2 Total abundance of macrobenthos per algal biomass of The center bar of the box plot represents the median, the box Adenocystis utricularis in the three sampling localities. a Organism extremes the first and third quartiles and the whiskers the 0.05 and density by 100 cm2 of alga, b organism density per dry weight alga. 0.95 percentile

Fig. 3 Total abundance of macrobenthos per algal biomass for The center bar of the box plot represents the median, the box samples of Iridaea cordata in the two sampling localities. a Organism extremes the first and third quartiles and the whiskers the 0.05 and density by algae dry weight, b organism density per sampling station. 0.95 percentile between sites were due mainly to high abundances of L. comparison with tropical and temperate zones; however, antarctica (Table 6). 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 Discussion waters, have a circumpolar distribution and may also extend to sub-Antarctic Islands and Tierra del Fuego in the Benthic marine macroalgae are a conspicuous and diverse southern tip of South America. Adenocystis utricularis may group of primary producers virtually present along all even occur in Australia and New Zealand (Wiencke et al. coasts worldwide where hard substrate is available (Torres 2007; Quartino et al. 2008a). In the Antarctic, seasonal et al. 2015). Macroalgal diversity is low in the Antarctic in changes in macronutrient concentration occur, but these are

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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

Fig. 4 Dry biomass of Adenocystis utricularis in the three sampling locations. The center bar of the box plot represents the median, the to seasonal environmental changes (Wiencke et al. 2007). box extremes the first and third quartiles and the whiskers the 0.05 As observed in some Antarctic species, competition may and 0.95 percentile 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 Fig. 5 Non-metric multidimensional scale ordination (nMDS) of the marine systems, it is likely that grazers associate in a macroinvertebrates associated with Adenocystis utricularis in the similar way with marine plants in polar marine environ- sampled localities, stress = 0.139 ments and that these interactions are essential to under- standing the dynamics of these communities (Huang et al. not a limiting factor for macroalgal growth since their 2007). The significant differences in mollusk and amphi- levels are high throughout the year (Wiencke et al. 2007). pod densities found between the two macroalgal species The higher average density of A. utricularis observed at could be due to differences in their architecture or mor- Ardley Bay in comparison with the other two localities phological complexity, palatability and defense mecha- could be due to an extra nutrient load from the Belling- nisms. A positive relationship has been observed between shausen Station, which is located in front of the sampled macroalgal morphological complexity (e.g., degree of site. Adenocystis utricularis has been reported to have an branching, algal width and the log of the stem) and the opportunistic life strategy in terms of growth and responds abundance and diversity of their associated epifauna. In

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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 proposed that the abundant benthic herbivore fauna complexity increases epifaunal abundance and diversity by observed at Potter Cove, King George Island, probably reducing predation and physical disturbance (Huang et al. depends on seaweeds as their main source of particulate 2006; Jacobucci et al. 2008) while increasing food avail- and dissolved organic carbon. Regarding palatability, ability and the number of different niches (Chemello and Wessels et al. (2006) studied herbivore–macroalgae inter- Milazzo, 2002; Torres et al. 2015). Quartino et al. (2008b) 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 Dissimilarity (%) Species Contribution percentage

Adenocystis utricularis Ardley Bay-Mareograph Beach 56.88 Laevilitorina antarctica 46.53 Mysella subquadrata 42.69 Laevilitorina caliginosa 6.10 Ardley Bay-Tank’s Bay 70.59 Mysella subquadrata 52.56 Laevilitorina antarctica 35.98 Laevilitorina caliginosa 8.63 Mareograph Beach-Tank’s Bay 59.94 Laevilitorina antarctica 79.32 Laevilitorina caliginosa 10.77 Iridaea cordata Mareograph Beach-Tank’s 78.01 Laevilitorina antarctica 55.36 Laevilacunaria antarctica 16.24 Mysella subquadrata 12.36 Laevilitorina caliginosa 11.92 two species (the sea urchin Strongylocentrotus droe- sublittoral/littoral fringe. In this mostly immersed zone, it bachensis and the amphipod Gammarellus homari) out of is common to observe the patellid gastropod N. concinna, 19 invertebrate species associated with macroalgae did the amphipods P. edouardi and G. antarctica, gastropods actually feed on it, indicating that herbivory plays a minor of the genera Laevilitorina and Laevilacunaria, and the role in this area. Laboratory experiments carried out by the bivalve M. subquadrata. Sicinski et al. (2011) reported that same authors demonstrated that both the sea urchin and the amphipod species G. antarctica and P. edouardi, and the amphipod had specific preferences when offered different limpet N. concinna are the most important components of types of algae and that tissue-specific and physical plant the invertebrate assemblage on rocky (boulders, cobbles properties also affected the feeding response of the and pebbles) substrates in the littoral zone. Some amphipod amphipod. As for defense mechanisms, inducible defense, species may migrate between areas with and without veg- or the production of metabolites by the algae in response to etation. For example, G. antarctica which was found to be herbivory, has been reported mostly for brown macroalgae responsible for the dissimilarities between sites for I. cor- (the case of A. utricularis), while few examples exist for data is a species with high mobility and can swim actively red macroalgae (the case of I. cordata) (Rotha¨usler et al. between pools (usually with more vegetation) and shallow 2005). Macaya et al. (2005) found in brown algae of zones (Thurston 1974). Gastropods like Laevilacunaria and Southern Chile that inducible defense expressed as a Laevilitorina are known to consume epiphytic diatoms and reduction in palatability may occur in 12 days with the macroalgae and can also migrate to shallower zones where presence of amphipod grazers. In addition to herbivory and macroalgae are less frequent (Jazdzewski et al. 2001). these other biological regulators, the Antarctic benthos is Previous amphipod biodiversity studies in the areas of also subjected to other devastating ice-related impacts such Maxwell Bay and the Western Atlantic Peninsula have as high wind and wave action, hypoxia, freshwater flood- reported at least 55 species for this group (Rauschert 1989, ing, localized pollution, and ultraviolet (UV) radiation, 1990, 1991, 1994, 1997; Ren and Huang 1991; Rauschert among others (Barnes and Conlan 2007). These effects and Andres 1993, 1994; Huang et al. 2007; Kim et al. may be mitigated when the macroalgae are found in high 2014). The structure of these species-specific macroalgal- densities. associated amphipod communities can vary across spatial Jazdzewski et al. (1991, 1995, 2001) reported that scales of 3 km (Huang et al. 2007). In our study we found macrobenthos associated with shallow waters at Admiralty 10 species, one of them (Ampithoe kergueleni originally Bay, King George Island, is composed mainly by amphi- described for the Iles Kerguelen, southern Indian Ocean by pods followed by gastropods and bivalves, varying their De Broyer et al. 2007) consisting of a new report for the densities throughout the year, regardless of macroalgal Antarctic Peninsula. Few species exhibit a circum-sub- presence. Similar in timing to our study, these authors Antarctic pattern, with records on the southern shelf of report that in the Austral summer (January to February), South America and around the sub-Antarctic islands of the amphipods were the most abundant group, followed by southern Indian Ocean as well as around Macquarie Island gastropods. Jazdzewski et al. (2001) discussed that in the and/or the New Zealand sub-Antarctic islands. Most of west Antarctic, sea-ice appears less severe, allowing the these species show low dispersal capacity (De Broyer and seasonal growth of macroalgae in sheltered places of the Jazdzewska 2014), and genetic studies suggest that

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In both studies, the highest proportion of does macroalgal cover along with benthic diversity and amphipod species was associated with brown algae. The abundance vary throughout the year? What is the life cycle most abundant species were O. ultima and P. edouardi in of the most abundant benthic species? Answering some of association with A. utricularis, being O. ultima the main these questions will certainly fill the many gaps we have in responsible for the differences between the three sampling our knowledge of Antarctic intertidal benthic ecology. sites. Jazdzewski et al. (2001) were the first to report O. ultima in very shallow areas (5–10 cm deep) as it had been Acknowledgments This research was supported by the Venezuelan previously found between 3 and 10 m in depth. This Scientific Antarctic Program, through the 2009 exploration campaign carried out by the Ministerio del Poder Popular para Ciencia, Tec- amphipod species is recognized as a typical epibenthic nologı´a e Innovacio´n (MCTI) and the Armada Nacional Bolivariana, dweller in this fringe of the sublittoral rocky shore, capable with the collaboration of the Instituto Anta´rtico Uruguayo. Special of burrowing in suitable sediments. The feeding habits are thanks to Manuel Caballer and Nelsy Rivero, who helped in the unknown but some Orchomenella species have been rec- fieldwork. We also wish to thank Sandra Lo´pez, Humberto Camisotti and Emiliana Mendoza, students at Universidad Simo´n Bolı´var in ognized as scavengers and detritivores. The species P. Caracas, Venezuela for their laboratory assistance and Emanuel edouardi has being categorized as an omnivore/herbivore Valero for his assistance with the figures. We extend our gratitude to but specific feeding habits are unknown (Jazdzewski et al. the four anonymous reviewers who provided invaluable comments 2001). Associated with the alga I. cordata, the most and literature to significantly improve the manuscript. 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 References small crustaceans like copepods and other amphipods. Gondogeneia antarctica is also the predominant herbivore Aldea C, Olabarria C, Troncoso JS (2008) Bathymetric zonation and of epontic microalgae which colonize the icefoot in some diversity gradient of gastropods and bivalves in West Antarctica from the South Shetland Islands to the Bellingshausen Sea. Antarctic islands (Jazdzewski et al. 2001). Deep-Sea Res I 55:350–368 Within the mollusks, the most abundant species were L. Amsler CD, Rowley RJ, Laur DR, Quetin LB, Ross RM (1995) antarctica and M. subquadrata. The first was previously Vertical distribution of Antarctic peninsular macroalgae: cover, reported as a common and abundant shallow-water species biomass and species composition. Phycologia 34:424–430 Amsler MO, Huang YM, Engl W, McClintock JB, Amsler CD (2015) in Admiralty Bay (Arnaud et al. 1986) and in Robert Island Abundance and diversity of gastropods associated with dominant (South Shetland Islands) (Castilla and Rozbaczylo 1985), subtidal macroalgae from the western Antarctic Peninsula. Polar as well as an important component of the shallow sublit- Biol. doi:10.1007/s00300-015-1681-4 toral of Terra Nova Bay (Ross Sea) (Gambi et al. 1994). 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