Multivariate analyses of Antarctic and sub-Antarctic seaweed distribution patterns: An evaluation of the role of the Antarctic Circumpolar Current

SEARES-01442; No of Pages 10 Journal of Sea Research xxx (2016) xxx–xxx

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Multivariate analyses of Antarctic and sub-Antarctic seaweed distribution patterns: An evaluation of the role of the Antarctic Circumpolar Current Paola Franzan Sanches a,⁎, Franciane Pellizzari b, Paulo Antunes Horta c a b c

Universidade de São Paulo, Laboratório de Manejo, Ecologia e Conservação Marinha, Instituto Oceanográfico, Praça do Oceanográfico, 191, CEP. 05508-120 São Paulo-SP, Brazil Universidade Estadual do Paraná, Campus Paranaguá, Laboratório de Ficologia e Qualidade de água do Mar, Rua Comendador Correia Júnior, 117, CEP. 83203-280 Paranaguá-PR, Brazil Programa de Pós Graduação em Ecologia, Centro de Ciências Biológias Universidade Federal de Santa Catarina, CEP. 88040-970 Florianópolis-SC, Brazil

a r t i c l e

i n f o

Article history: Received 20 October 2014 Received in revised form 15 February 2016 Accepted 17 February 2016 Available online xxxx Keywords: Antarctica Circulation patterns Marine phytogeography Macroalgae

a b s t r a c t Biogeographic barriers and ecological corridors are fundamental in defining macroecological and evolutionary processes. Ocean circulation, considering present and past patterns of continental drift, can isolate or connect many groups of marine organisms, including seaweeds. These benthic organisms present spores and propagules as planktonic stages that drift with currents and or tides, and have been a sensible indicator of changes to biogeographical distribution patterns. Phycological studies have been exhaustive in the sub-Antarctic and Antarctic seaweed communities. However, the role of the Antarctic Circumpolar Current (ACC) in shaping marine phytogeographic diversity has been poorly investigated. The ACC connects the major world oceans and redistributes oceanic properties, such as heat, salt, and nutrients, consisting of three major circumpolar fronts (in order of north to southward): the Sub-Antarctic Front (SAF), the Antarctic Polar Front (PF), and the Southern Antarctic Circumpolar Front (SACF). This paper's aim is to understand the role of the ACC fronts as a constraint on seaweed distribution patterns in different taxonomic levels, in relation to the southern Sub-Tropical areas, as well as to compare sections connected with South America (1: north), influenced by the Ross Sea Gyre (2: Western Antarctica Peninsula) and by the Weddell Sea Gyre (3: Eastern Antarctica Peninsula). nMDS showed differences in the distributional patterns of species and genera in relation to the zones and sections. The predicted latitudinal gradient of species richness was observed, and by comparing biogeographic zones, two main clusters were observed: Sub-tropical and Sub-Antarctica; and Polar Front (Antarctic Peninsula) and SACF (areas surrounding continental Antarctica), suggesting, for this sort of macroscale analysis, that ACC still has a role of “watershed barrier”. However, a lower dissimilarity (higher similarity) was observed between the 2nd (Eastern Antarctica Peninsula – EAP – or under influence of the Weddell Sea Gyre, and some sub-Antarctic islands as South Orcadas, South Georgia and Crozet Archipelago) and the 1st sectors (Chilean and Argentinean Patagonia and surrounding islands, Falklands, South Shetlands and including Antarctic Peninsula). When considering recently reported changes in diversity patterns of these locations, this result could demonstrate the existence of a clear species distributional flux, despite evidence of the ACC being a limit to dispersal. Therefore, this contribution has used previously published data to provide a tool for monitoring future biogeographical changes to the flora and fauna of this region of the Antarctic and sub-Antarctic areas due to changes in biogeographical distribution, resulting either from natural dispersion due to global meteoceanographic changes, and or biological invasions related to anthropogenic activities. We could be witness to a period of changes in Antarctic diversity, suggesting that Antarctica may not be as isolated as was once thought. © 2016 Elsevier B.V. All rights reserved.

1. Introduction For many decades, species distribution patterns have been guiding scientists toward an understanding of the planet's history, climate and ⁎ Corresponding author. E-mail addresses: [email protected], [email protected] (P.F. Sanches), [email protected], [email protected] (F. Pellizzari), [email protected] (P.A. Horta).

geological changes. In marine environments, the role of currents is still being discussed (Myers, 1997) as biogeographical barriers in terms of limiting dispersal, acting as physical barriers, or serving as ecological filters based on specific oceanographic properties of the temperature, salinity, density, pH, or sea surface height. Conversely, they can also function as ecological corridors, providing a connection between many geographic areas and distinct ecosystems (Treml et al., 2008) by transporting larvae, spores, and propagules of different groups of organisms (Barber et al., 2000), including seaweeds.

http://dx.doi.org/10.1016/j.seares.2016.02.002 1385-1101/© 2016 Elsevier B.V. All rights reserved.

Please cite this article as: Sanches, P.F., et al., Multivariate analyses of Antarctic and sub-Antarctic seaweed distribution patterns: An evaluation of the role of the Antarctic Cir..., J. Sea Res. (2016), http://dx.doi.org/10.1016/j.seares.2016.02.002

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P.F. Sanches et al. / Journal of Sea Research xxx (2016) xxx–xxx

Biogeographic studies of macroalgae started with Lamouroux in 1826, who correlated diversity and latitudinal changes in species composition (Garbary, 1987). Descriptive taxonomy and species lists comparing similarities among areas were the basis of primary techniques and assessments (Camus, 2001). Theoretical experimentation introduced tests of limiting factors for distribution, including physiological tolerance (Garbary, 1987; Zacher et al., 2007; Wiencke and Dieck, 1990). Biomolecular approaches allowed the establishment of phylogenetic relationships, which improved our understanding of algal evolutionary relationships (Macaya and Zuccarello, 2010; Teske et al., 2011). Due to historical and practical limitations (i.e., problems related to sampling effort and lack of feasible alternatives in methodology), the diversity of Antarctic seaweeds has been underestimated (Clayton, 1994; Oliveira et al., 2009). Most seaweeds of this particular region have no specific keys, and as a result, some taxa have been misidentified. Even so, as well as physiology and chemistry (Wiencke, 1988; Gómez, 2001; Amsler et al., 2005a, 2005b), diversity studies are broad (Lamb and Zimmerman, 1977; Neushul, 1964; Zielinski, 1981; Ramirez and Villouta, 1984; Cormaci et al., 1992; Papenfuss, 1964; Pedrini, 1992; Westermeier et al., 1992; Chung et al., 2000; Wiencke and Clayton, 2002; Quartino et al., 2005; Oliveira et al., 2009; Pellizzari et al., in press). By now, Antarctica has about 130 species of macroalgae (Wincke and Clayton, 2002), including 75 species of Rhodophyta, 25 Phaeophyceae and 15 Chlorophyta (Skottsberg, 1960), with ca. 30% of these taxa being endemic. The endemism is highest among Phaeophyceae, (Ascoseirales) and some genera such as Gainia, Antarcticothamnion, Notophycus, Himantothallus, Cystophaera, Phaeurus, Lambia and Lola (Rakusa-Suszczewski and Zieliński, 1993; Clayton, 1994; Wiencke and Clayton, 2002). However, biogeographic approaches related to seaweed distributional patterns observed in high latitudes in the Southern Hemisphere are scarce (Hommersand et al., 2009). Thus, previous studies attempting to address the biogeography of this group have been conducted in different regions, at various scales, and have used different sources of data (van den Hoek, 1975, 1984; Santelices, 1980; Bolton and Stegenga, 1987, 1990; Stegenga et al., 1997; Bolton et al., 2004; Kerswell, 2006). As traditionally discussed since Knox (1960), oceanic circulation patterns, in most cases, represent one of main drivers of biogeographical boundaries. Although much is known about the role of marine currents distributing seaweeds and generating biogeographic patterns in middle southern latitudes (Bolton, 1994), few studies have been conducted in the Antarctic and sub-Antarctic regions. The Polar Front (called the Antarctic Convergence in the older literature) is the strongest of a series of eastward-flowing jets of the Antarctic Circumpolar Current (ACC). The ACC consists of three major circumpolar fronts, which are, from north to south, the sub-Antarctic Front (SAF), the Antarctic Polar Front (PF), and the Southern Antarctic Circumpolar Current Front (SACCF). The fronts separate distinct surface water masses and are associated with strong currents and strong lateral gradients in temperature, salinity, and biological productivity (Moore and Abbott, 2000, 2002). The PF is also a strong barrier to free north– south exchange of water, and thus represents a potential distinctive biogeographical discontinuity. Associated with this is a high degree of species-level endemism in the Antarctic marine invertebrate and fish faunas and seaweeds, which is indicative of a long period of evolution in relative isolation. The only exceptions to this are the faunas of the midwater and the deep-sea, in which the Polar Front appears to not have been a barrier. However, the traditional view of Antarctica and the surrounding Southern Ocean as an isolated system is now being challenged by the recent discovery of adult North Atlantic spider crabs and larvae of subpolar marine invertebrates at the Antarctic Peninsula (Clarke et al., 2005). These observations question whether the welldescribed biogeographical similarities between the benthic fauna of the Antarctic Peninsula and the Magellan region of South America result

from history (i.e., the two regions were once contiguous), or from a previously unrecognized low level of faunal exchange. Clarke et al. (2005), suggest that such exchange might be influenced by regional climate change, and also could be exacerbated by changes in human impact. Regarding seaweeds, Pellizzari et al. (in press) also suggest that the higher number of taxa recorded in the South Shetland Islands compared to previous studies in Antarctica could not be only associated with past sampling failure, but also with possible changes in connectivity patterns of the Southern Ocean and Antarctica, natural or otherwise. The complex system of fronts of the northern boundaries of the Southern Ocean is defined by the interaction of the ACC with northern oceanic systems (Atlantic, Indian and Pacific oceans). The onset of the ACC is related to the break-up of Gondwana and, in particular, to the separation of Australia from Antarctica, and of South America from the Antarctic Peninsula. The precise dates for these events are still debated, but are generally considered to be ca. 25 million years before present. This event was crucial in determining the thermal properties, sea surface height and consequently the biogeographical isolation of the Southern Ocean. Until the past decade, no evidence was found for the north–south exchange of macroalgae species in this area. However, distributional influences of the ACC were demonstrated for marine invertebrates and crustaceans (Clarke et al., 2005). Pierrat et al. (2013) also showed that this barrier was insufficient in preventing the dispersal of bivalves. On the other hand, Barnes et al. (2006) showed that the PF virtually guarantees endemism with no establishment of exotic species in these high latitudes. Ivar do Sul et al. (2011) reported that fishing operations in the Southern Ocean were identified as the major source of marine debris. Depending on the type of debris, plastics from lower latitudes may easily cross the PF, providing a possible link for plastic marine debris or alien species between Antarctica and South America (the closest intercontinental connection). Following Barnes et al. (2006) ice shelf and icebergs forced the evolution of a distinct biota adapted to conditions imposed by the ACC, or by isolation. These two papers show that connectivity exists, but also the barrier does. Thus, morphological, reproductive, and physiological characteristics, which determine species tolerances to environmental conditions, were susceptible to evolutionary pressure and were, ultimately, reflected in the phylogenetic relationships among them (Verbrugen et al., 2009). In mobile marine taxa (spores, or propagules, in the case of seaweeds), at all stages of their life cycle, there is evidence of mechanisms that drive diversification serving more as filters to evolution than barriers (Boehm et al., 2013). Thus, relationships among ocean circulation, marine barriers, dispersal potential, and tolerances to environmental conditions combined with selective pressures are possibly leading to species diversification patterns (Floeter et al., 2008). In this context, Verbrugen et al. (2009) questioned whether “species distribution is restricted to an ocean by local environmental limits, or by a species intrinsic distribution limit.” It is well known that latitudinal gradients determine richness in both marine and terrestrial environments. However, according to Kerswell (2006), seaweeds do not always respond to this pattern. Moreover, polar organisms are more tolerant to adverse and extreme environmental conditions than tropical organisms (Peck, 2005). It is worthy to note that some studies using molecular markers (Hommersand et al., 2009; Medeiros, 2013) are revealing that cryptic taxa previously listed in both Maritime Antarctica and South America, attributed to the genera Plocamium, Ulothrix and even Iridaea, are in fact cryptic species representing distinct taxonomic entities (Pellizzari et al., in press). Therefore, this contribution aims to discuss if the ACC would constitute a true barrier to present-day seaweed dispersion, and whether there might be differences in species compositions among the three major ACC circumpolar fronts (SAF, PF and SACCF). Finally, we aim to verify the putative influence of ACC fronts on the species, genera, family and order composition of the Rhodophyta, Phaeophyceae and Chlorophyta, based on previous checklists of benthic Antarctic and

Please cite this article as: Sanches, P.F., et al., Multivariate analyses of Antarctic and sub-Antarctic seaweed distribution patterns: An evaluation of the role of the Antarctic Cir..., J. Sea Res. (2016), http://dx.doi.org/10.1016/j.seares.2016.02.002

P.F. Sanches et al. / Journal of Sea Research xxx (2016) xxx–xxx

sub-Antarctic phycoflora, while also contributing knowledge to marine conservation programs in the area facing a meteoceanographic changes scenario. 2. Material and methods 2.1. Oceanographic aspect of Southern Hemisphere The connection among the Pacific, Atlantic and Indian Oceans guarantees the continuous potential exchange of water masses, heat, fresh water, carbon, and biodiversity. This connection is formed by the Sub-Tropical Front and the three major circumpolar fronts that compose the ACC: Sub-Antarctic Front (SAF), Polar Front (PF) and, and the Southern Antarctic Circumpolar Front (SACCF) (Dong et al., 2006). The Ross and Weddell Gyres are the main circulation meander south the influence of the SACCF. The ACC was formed in the Cenozoic period from the disjunction of the Antarctic Peninsula from South America, followed by the opening of the Drake Passage and the deep corridor between Eastern Antarctica, Australia and Tasmania (Kennett, 1977). Surface waters of the Sub-Tropical Front change from warm and saline (12 °C, 35.0 psu, respectively), which are characteristics of low latitudes, to cold and fresh (10 °C, 34.6 psu), which are characteristics of polar latitudes. Accordingly, the Sub-Antarctic Front is characterized by cold waters (ca. 4 °C) and lower salinity, due to fresh surface waters. The Polar Front, on the other hand, starts when cold surface water turns northward and sinks down to the less dense portions. At 200 m in depth, the temperature is less than 2 °C. At latitudes of the Antarctic Convergence, water temperature reaches 1.8 °C. The Weddell and Ross Gyres are controlled by cyclonic forces from pressure differentials found in deeper waters (Klinck and Nowland, 2001). Thus, these divisions are established by a thermohaline gradient. Following Dong et al. (2006) the spatial and temporal resolutions of the altimetric sea surface height (SSH) measurements have also been used since Gille (1994, 1999); however, data are still coarse compared to sea surface temperature (SST). Circumpolar fronts present clockwise movement, encircling the Antarctic mainland (Nowlin and Klinck, 1986). The circulation and the

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extension of the ACC changes seasonally and is influenced by convection. Dong et al. (2006) also suggested that the zonal wind stress accelerates the zonal transport of the PF, and that the meridional shifts of the Antarctic PF path correspond to the meridional shifts of the wind field. 2.1.1. Macroalgae checklists analysis Among zones, we chose 58 localities, directly or indirectly influenced by the ACC fronts. Zones were divided into Sub-Tropical (Sub-Trop: 40°–45°S), Sub-Antarctic (Sub-Ant: 46°S–55°), Polar Front (PF: 56°S–63°S) and Southern Antarctic Circumpolar Current Front (Ant Div: 64°S–77°S). Localities were also classified into 3 sections: 1st — connection between South America and Antarctic Peninsula; 2nd — Eastern Antarctica Peninsula or under influence of the Weddell Sea Gyre; and 3rd — connection between Southern Australia and New Zealand, and Western Antarctica Peninsula or areas under influence of the Ross Sea Gyre (Fig. 1 and Table 1). The dataset was established from species lists obtained in specialized literature and virtual databases from distinct areas including diversity, biogeography and descriptive ecology; the terms included in the virtual research were: “list of species* macroalgae* seaweeds* distribution*”. To generate the presence and absence matrix the following literature was used: Neushul (1964), Papenfuss (1964), Lamb and Zimmerman (1977), Zielinski (1981), Etcheverry (1983), Womersley (1984, 1994, 1996, 1998), Pedrini (1992), Weykam et al. (1996), Quartino et al. (1997), Stegenga et al. (1997), Wiencke (1988), Chung et al. (2000), Korb and Gerard (2000), Gómez (2001), Westermeier et al. (1992), Wiencke and Clayton (2002), Zaixo (2004), Boraso et al. (2004), Amsler et al. (2005a, 2005b), Peters et al. (2005), Quartino et al. (2005), Navarrete et al. (2008), Hommersand et al. (2009), Oliveira et al. (2009), Boraso and Zaixso (2011). The nomenclatural update followed Guiry and Guiry (2015). 2.2. Statistical analysis Multivariate analyses were performed aiming to compare zones and sectors with respect to species, genera, families and orders, utilizing the

Fig. 1. Schematic of the analyzed localities detailed in the Table 1 (South America, Southern African Mainland, Australia, Tasmania, New Zealand, Antarctica and the Sub-Antarctica Islands considered) and the relative position of the Antarctic Circumpolar Current (Black Line, Gray Line and Dashed Line).

Please cite this article as: Sanches, P.F., et al., Multivariate analyses of Antarctic and sub-Antarctic seaweed distribution patterns: An evaluation of the role of the Antarctic Cir..., J. Sea Res. (2016), http://dx.doi.org/10.1016/j.seares.2016.02.002

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P.F. Sanches et al. / Journal of Sea Research xxx (2016) xxx–xxx

Table 1 Localities, geographical coordinates, indication of zones: Sub-Tropical (Sub-Trop), Subantarctic (Sub-Ant), Polar Front (PF) and Southern Antarctic Circumpolar Front (SACF), and sections (1, 2 and 3), with the respective numbers indicated on Fig. 1. N°

Localities

Abbreviation

Coordinates

Zone

Section

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58

Elephant Island King George Island Nelson Island Robert Island Greenwich Island Livingston Island Snow Island Deception Island Half Moon Island Graham Land End of Peninsula Trinidad Island Astrolabio Island Bransfield Island Moss Island DeLaca Island Anvers Island Joubin Island Palmer Archipelago Wilhelm Archipelago Melchior Islands Argentine Islands Marguerite Adelaide Island Henkes Island Joinville James Ross Island Cockburn Island Antarctic Peninsula Enderby Land Mac Robertson Land Ingrid Coast Queen Mary Land Wilkes Land Cape Denison Adelie Coast George V Coast Victoria's Land McMurdo Sound Ross Island Ross Sea Balany Tasmany New Zealand Chatham Antipodes Island Auckland Island Campbell Island Macquarie Island South Orkneys Islands Falklands Islands South Georgia Islands Heard Island Kerguelen Island Crozet Archipelago Prince Eduard e Marion Island Patagonia South Chile

Elep King Nels Robert Green Liv Snow Decep Sh Grah End Trini Astro Bran Moss DeLa Anvers Jou Pl Wi Mel Arg Ma Ade Is He Join Jm Cock Pe Ender Mc In Queen Wl Denis Adelie Geor Vi MMur Ross Ro Ba Ta NZ Ch At Au Ca Mq Or Fa SG Hd Ke Cr PrE Pa CS

61° 8′ 0″ S, 55° 7′ 0″ W 62° 2′ 0″ S, 58° 21′ 0″ W 62° 18′ S, 59°03′ W 62° 24′ S, 59°30′ W 62° 31′ 0″ S, 59° 47′ 0″ W 62° 36′ 0″ S, 60° 30′ 0″ W 62° 47′ S, 61°23′ W 62° 58′ 37″ S, 60° 39′ 0″ W 62° 16 41′ S, 60° 05′ 20″ W 68° 25′ 03″ S, 68° 24′ 39″ W 63° 15′ 32″ S, 56° 55′ 32″ W 63° 48′ 56.5″ S, 60° 44′ 0.8″ W 63° 17′ S, 58° 40′ W 63° 11′ 0″ S, 56° 36′ 0″ W 64° 9′ 0″ S, 61° 2′ 60″ W 64° 47′ 0″ S, 64° 7′ 0″ W 64.77′ S, 64.05° W 64° 47′ 0″ S, 64° 27′ 0″ W 64° 46′ 27″ S, 64° 3′ 11″ W 65° 8′ 0″ S, 64° 20′ 0″ W 64° 19′ 0″ S, 62° 57′ 0″ W 65° 15′ 0″ S, 64° 16′ 0″ W 68° 30′ 0″ S, 68° 30′ 0″ W 67° 15′ 0″ S, 68° 30′ 0″ W 67° 54′ 14″ S, 69° 32′ 59″ W 63° 15′ 0″ S, 55° 45′ 0″ W 64° 10′ 0″ S, 57° 45′ 0″ W 64° 12′ 0″ S, 56° 51′ 0″ W 64° 14′ 02″ S, 61° 13′ 38″ W 67° 30′ 0″ S, 53° 0′ 0″ E 69° 20″ S, 75° 41′ E 69° 30′ 0″ S, 77° 0′ 0″ E 66° 45′ 0″ S, 96° 0′ 0″ E 69° 0′ 0″ S, 120° 0′ 0″ E 67° 0′ 0″ S, 142° 40′ 0″ E 66° 12′ S 136° 11′ E–66° 48′ S 142° 02′ E 68° 30′ S, 148° 0′ E 71° 15′ 0″ S, 163° 0′ 0″ E 77° 30′ 0″ S, 165° 0′ 0″ E 77° 30′ 0″ S, 168° 0′ 0″ E 75° 03′ 22″ S, 172° 42′ 09″ W 66° 55′ 0″ S, 163° 45′ 0″ E 42° 0′ 0″ S, 147° 0′ 0″ E 42° 0′ 0″ S, 174° 0′ 0″ E 43° 53′ 54″ S, 176° 31′ 44″ W 49.67° S, 178.77° E 50° 42′ 0″ S, 166° 5′ 0″ E 52° 36′ 06″ S, 169° 03141″ E 54° 37′ 0.12″ S, 158° 51′ 0″ E 60° 44′ 31″ S, 45° 24′ 14″ W 52° 05′ 05″ S, 60° 01′ 01″ W 54° 20′ 47″ S, 37° 10′ 02″ W 53° 13′ 20″ S, 73° 28′ 26″ E 49° 41′ 15″ S, 69° 16′ 18″ E 46° 31′ 19″ S, 51° 40′ 34″ E 46° 45′ 30″ S, 37° 53′ 02″ W 55° 07′ 52″ S, 66° 05′ 59″ W 41° 28′ 18″ S, 72° 56′ 12″ W

PF PF PF PF PF PF PF PF PF SACF PF PF PF PF SACF SACF SACF SACF SACF SACF SACF SACF SACF SACF SACF PF SACF SACF PF SACF SACF SACF SACF SACF SACF SACF SACF SACF SACF SACF SACF SACF Sub-Trop Sub-Trop Sub-Trop Sub-Ant Sub-Ant Sub-Ant Sub-Ant PF Sub-Ant Sub-Ant Sub-Ant Sub-Ant Sub-Ant Sub-Ant Sub-Ant Sub-Trop

1 1 1 1 1 1 1 1 1 1 2 2 1 1 1 1 1 1 1 1 1 1 1 1 1 2 2 2 1 2 2 2 2 1 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 2 1 2 2 2 2 2 1 1

software PRIMER 6.1.15 and PERMANOVA 1.0.5 (PRIMER-E Ltd., Plymouth Marine Laboratory, Plymouth, United Kingdom). A similarity matrix was generated using all sites considering each specific zone as factors (Clarke and Warwick, 1994). Nonmetric Multidimensional Scaling (nMDS) graphics were created to depict relationships among the studied areas considering the Bray Curtis dissimilarity matrix using transformed data of presence and absence. The percent contribution by individual species to differences in assemblages among each biogeographic zone was determined using Similarity Percentages (SIMPER) (CLARKE, 1993). In order to verify the effect of zone factor, ANOSIN and PERMANOVA were performed, fixing the zones and nesting them into sections, considering species as variable in the latter

case, once a higher variability was observed in this taxonomical level. Monte Carlo test was additionally performed in the PERMANOVA model, in order to quantify the heuristic probability of the clustered model. 3. Results A total of 860 species were included in the matrix representing 377 genera, 105 families and 45 orders. The number of individuals in each taxonomic level was inversely proportional to latitude, with SubTropical (Sub-Trop) presenting the highest number of species (666) and Southern Antarctic Circumpolar Front (SACF) the smallest (129).

Please cite this article as: Sanches, P.F., et al., Multivariate analyses of Antarctic and sub-Antarctic seaweed distribution patterns: An evaluation of the role of the Antarctic Cir..., J. Sea Res. (2016), http://dx.doi.org/10.1016/j.seares.2016.02.002

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The highest average of similarity occurred within the Polar Front (PF) zone for species (26.93%) and genus (31.97%). However, regarding family and order similarities, the highest values were obtained within Sub-Trop (42.85% and 59.22%, respectively). The smallest similarity occurred within Southern Antarctic Circumpolar Front (SACF) for all levels: 11.59% for species, 14.04% for genera, 22.69% for families, and 34.01% for orders (Table 2), suggesting a specialized and endemic phycoflora in the surrounding areas of continental Antarctica. The number of exclusive species and other taxonomic levels was heterogeneous in the four analyzed zones. However, SACF has only one more exclusive species and genus than PF, meaning, in terms of percentage of exclusivity, 3.10% of the species in SACF are exclusive to this zone. Neither SACF, PF or Sub-Ant has any exclusive families, sharing, respectively, one, three and 12 families with the Sub-Trop zone, which comprised 36 families. Regarding orders, only Sub-Ant and Sub-Trop have exclusivity. SACF and PF share two orders with Sub-Ant and SubTrop. Sub-Trop presented the highest percentage of exclusivity for all taxonomic levels (44.60% of exclusive species, 55. 38% of exclusive genera, 36.37% of exclusive families and 12.50% exclusive orders) (Table 2), and consequently higher richness. This may be associated with this zone being composed of four distinct and geographically distant areas (Tasmania, New Zealand, Chatham Island and South Chile), which represents environmental heterogeneity, allowing orders to differ. Co-occurrence was always higher between the Sub-Trop and SubAnt zones, representing more than 12% of each taxonomic level for both zones. The dissimilarity among zones showed a similar pattern among species and genera. Higher latitudes presented the lowest dissimilarity among adjacent zones, suggesting that lower dissimilarities were influenced by the ACC surrounding zones: PF and SACF (82.75% for species and 78.73% for genera). Although this relationship is stochastic for species, according to ANOSIM (Table 3) or PERMANOVA (significance N0.05) (Table 4), 16 species co-occurred in both zones, which represents 11.04% and 12.41% of their phycoflora, and 14 genera co-occurred, which represents 13.87% and 14.74%. Comparison of the Sub-Ant and PF presented the second lowest dissimilarity (87.19% for species and 79.13% for genera) among the assemblages, where two species co-occurred. The same was not observed for genera. The third lowest dissimilarity (higher similarity) was verified between Sub-Trop and Sub-Ant zones (89.97% for species and 79.78% for genus), where 110 species and 73 genus co-occurred (Table 3). As expected, the highest dissimilarity occurs between the most distant zones, i.e., Sub-Trop and SACF (shores around Continental Antarctica) (97.64% for species and 93.63% for genus), showing co-occurrence of Table 2 Total number, number of exclusivity and percentage of exclusivity of species, genera, families and orders, and the average similarity by zone: Southern Antarctic Circumpolar Front (SACF), Polar Front (PF), Sub-Antarctic (Sub-Ant) and Sub-Tropical (Sub-Trop). Taxonomic level

Zones

Total number

Number of exclusivity

Percentage % of exclusivity

Average similarity (%)

Species

SACF PF Sub-Ant Sub-Trop SACF PF Sub-Ant Sub-Trop SACF PF Sub-Ant Sub-Trop SACF PF Sub-Ant Sub-Trop

129 145 339 666 95 101 189 307 48 55 61 99 29 29 39 40

4 3 58 297 2 1 26 170 0 0 0 36 0 0 2 5

3.10 2.07 17.11 44.60 2.11 0.99 13.76 55.38 0 0 0 36.37 0 0 5.13 12.50

11.59 26.93 17.77 13.81 14.04 31.97 26.34 27.49 22.69 37.33 40.28 42.85 34.01 50.26 49.18 59.22

Genera

Families

Orders

5

Table 3 Dissimilarity (Dissim) and significance level (Sig level) of the ANOSIM test and number of co-occurrence for each taxonomic level (species, genera, families and orders) for the given relationships of the zones: Sub-Tropical (Sub-Trop), Sub-Antarctic (Sub-Ant), Polar Front (PF) and Southern Antarctic Circumpolar Front (SACF). Taxonomic level

Relationships

Dissim

Sig level

Co-occurrence

Species

Sub-Trop × Sub-Ant Sub-Trop × PF Sub-Trop × SACF Sub-Ant × PF Sub-Ant × SACF PF × SACF Sub-Trop × Sub-Ant Sub-Trop × PF Sub-Trop × SACF Sub-Ant × PF Sub-Ant × SACF PF × SACF Sub-Trop × Sub-Ant Sub-Trop × PF Sub-Trop × SACF Sub-Ant × PF Sub-Ant × SACF PF × SACF Sub-Trop × Sub-Ant Sub-Trop × PF Sub-Trop × SACF Sub-Ant × PF Sub-Ant × SACF PF × SACF

89.97 94.91 97.64 87.19 92.38 82.75 79.78 87.97 93.63 79.13 87.31 78.73 65.69 70.12 80.42 64.17 73.48 69.98 51.16 59.69 71.32 53.45 63.43 59.94

0.033 0.001 0.051 0.001 0.058 0.983 0.137 0.001 0.084 0.001 0.257 0.996 0.151 0.127 0.252 0.146 0.739 0.992 0.361 0.079 0.146 0.072 0.52 0.841

110 2 9 2 4 16 73 1 3 0 1 14 12 3 1 1 1 2 7 2 2 2 2 1

Genera

Families

Orders

only nine species and three genera (Table 3) for these zones (ANOSIM p = 0.051 and PERMANOVA p = 0.002, Table 4). Analyzing the relationships among families and orders, patterns of dissimilarity change. The lowest dissimilarity was not observed for families between SACF and Sub-Trop (69.98%), but rather, between Sub-Ant and PF (64.17%), as shown in Table 3, showing that phycoflora between Sub-Antarctic islands and islands of the surrounding Peninsula are similar. Regarding orders, the lowest dissimilarity was between Sub-Trop and Sub-Ant (51.16%), where 7 orders co-occurred. The species and genera in a non-metric multidimensional ordination (nMDS) formed two distinct groups: one group clustered by PF (surrounding islands of the Peninsula) and SACF (areas along Antarctic Continental shores), and another group formed by the Sub-Ant and SubTrop areas. This indicates a difference between these two phycoflora compositions for these zones, within and outside of the ACC. However, this is not shown for families and orders (Fig. 2), suggesting that, in addition, the lower taxonomic level (species) is more sensible to use with this approach. Regarding the analysis by sections, there was a similar pattern for all taxonomic levels, which shows a higher dissimilarity within the 3rd core (Southern Australia and New Zealand, Western Antarctica Peninsula or under influence of the Ross Sea Gyre), and the lowest similarity for the 2nd core (Eastern Antarctic Peninsula or under influence or the Weddell Sea). The 3rd core had the highest number of species at 658, with 69.90% (460) of them exclusive to this core; however, it Table 4 PERMANOVA test (P(perm)), t value (t), number of permutations (perms) and Monte Carlo value (P(MC)) performed for species and the given relationships of the zones: Sub-Tropical (Sub-Trop), Sub-Antarctic (Sub-Ant), Polar Front (PF) and Southern Antarctic Circumpolar Front (SACF). Taxonomic level

Relationships

t

P(perm)

perms

P(MC)

Species

Sub-Trop × Sub-Ant Sub-Trop × PF Sub-Trop × SACF Sub-Ant × PF Sub-Ant × SACF PF × SACF

10.037 12.295 12.712 15.956 15.942 11.235

0.502 0.04 0.002 0.001 0.001 0.117

998 999 997 998 997 996

0.426 0.119 0.042 0.001 0.002 0.183

Please cite this article as: Sanches, P.F., et al., Multivariate analyses of Antarctic and sub-Antarctic seaweed distribution patterns: An evaluation of the role of the Antarctic Cir..., J. Sea Res. (2016), http://dx.doi.org/10.1016/j.seares.2016.02.002

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P.F. Sanches et al. / Journal of Sea Research xxx (2016) xxx–xxx

Fig. 2. Non-metric multidimensional ordination (nMDS) of composition similarities in species (A), genera (B), families (C) and orders (D) between localities in Sub-Tropical (Sub-Trop ■), Sub-Antarctic (Sub-Ant ◆), Polar Front (PF ↑) and Southern Antarctic Circumpolar Front (Div Ant ↓) zones.

also had the smallest average similarity (7.37%). The 1st section, closest to South America and including the Antarctic Peninsula, showed the second highest number of species (388), 165 of which were exclusive (42.53%), and the highest average similarity (19.82%), while the 2nd section (Eastern Antarctica or under influence of the Weddell Sea Gyre) had the smallest number of species (156), only four exclusive (2.57%) and a mean average of 11.28%. This 2nd section presented only one exclusive genus, one exclusive family and no exclusive orders, while the 3rd presented 164 exclusive genera, 31 exclusive families and five exclusive orders, and the 1st section presented 41 exclusive genera, two exclusive families and two exclusive orders (Table 5). Regarding seaweed species, the dissimilarity values between the sections were higher between the 2nd and 3rd core (91.63%), with only nine co-occurrences. The lowest dissimilarity occurred comparing the 1st and 2nd core (86.20%) (Table 5), with 34 co-occurrences, but this is very significant, considering the total number of species on the

2nd section. Comparing the 1st and 3rd core, the dissimilarity of 89.95% is justified by the co-occurrence of 81 species (Table 6). The highest dissimilarity among families occurred between the 1st and 3rd sections (74.47%), but was not significant, considering the number of species of co-occurrence was higher. Comparing the 2nd and 3rd sections, dissimilarity was 71.94%, with only three co-occurrences. Finally, although not significant, the pattern for orders was similar compared to species and genus, with the highest dissimilarity between the 2nd and 3rd sections (66.07%), justified by an absence of cooccurrences. The dissimilarity between the 1st and 2nd sections was 59.11%, sharing two orders. Finally, comparing the 1st and 3rd sections, nine orders co-occurred, with 61.22% of dissimilarity (Table 6). This corroborates the differences between these two sections. The nMDS did not show any group for this factor, when neither PERMANOVA nor ANOSIM showed significance for species in the relationships of sections, (Table 7).

Table 5 Total number, number of exclusivity and percentage of exclusivity of species, genera, families and orders, and the average similarity by: 1 (South America and Antarctica Peninsula core), 2 (Western Antarctica or under influence of the Ross Sea Gyre) and 3 (Eastern Antarctica or under influence of the Weddell Sea Gyre).

Table 6 Dissimilarity (Dissim) and significance level (Sign level) of the ANOSIM test and number of co-occurrence for each taxonomic level (species, genera, families and orders) for the given relationships of the 1st core (South America and Antarctica Peninsula core), 2nd core (Eastern Antarctica or under influence of the Weddell Sea Gyre) and 3rd core (AU, NZ, Western Antarctica or under influence of the Ross Sea Gyre) analyzed sections.

Taxonomic level

Section

Species

1 2 3 1 2 3 1 2 3 1 2 3

Genera

Families

Orders

Total number

Number of exclusivity

Percentage % of exclusivity

Average similarity

388 156 658 206 109 324 70 62 100 40 29 43

165 4 460 41 1 164 2 1 31 2 0 5

42.53 2.57 69.90 19.90 0.92 50.62 2.86 1.61 31.00 5.00 0 11.63

19.82 11.28 7.37 23.90 17.12 11.52 29.69 35.02 21.77 44.37 38.80 33.81

Taxonomic level

Relationships

Dissim

Sign level

Co-occurrence

Species

1×2 1×3 2×3 1×2 1×3 2×3 1×2 1×3 2×3 1×2 1×3 2×3

86.20 89.95 91.63 81.30 84.82 86.29 68.14 74.47 71.94 59.77 61.22 66.07

0.004 0.031 0.065 0.005 0.059 0.121 0.144 0.715 0.302 0.087 0.123 0.111

34 81 9 11 64 7 2 10 3 2 9 0

Genera

Families

Orders

Please cite this article as: Sanches, P.F., et al., Multivariate analyses of Antarctic and sub-Antarctic seaweed distribution patterns: An evaluation of the role of the Antarctic Cir..., J. Sea Res. (2016), http://dx.doi.org/10.1016/j.seares.2016.02.002

P.F. Sanches et al. / Journal of Sea Research xxx (2016) xxx–xxx Table 7 PERMANOVA test (P(perm)), t value (t), number of permutations (perms) and Monte Carlo value (P(MC)) between sections for the taxonomic level of species for the given relationships of the 1st (South America and Antarctica Peninsula core), 2nd (Eastern Antarctica or under influence of the Weddell Sea Gyre) and 3rd (AU, NZ, Western Antarctica or under influence of the Ross Sea Gyre) analyzed sections. Taxonomic level

Relationships

t

P(perm)

Perms

P(MC)

Species

1×2 1×3 2×3

12.249 12.896 10.301

0.027 0.004 0.312

998 996 998

0.074 0.029 0.376

4. Discussion 4.1. Composition of species, genera, families and orders Our macroscale analysis reinforces the notion that the ACC has a role as a “watershed barrier” or biogeographical barrier. Comparing biogeographic zones, there was a clear nMDS segregation of two main clusters: one formed by Sub-Trop and Sub-Ant, and another by PF (Antarctic Peninsula) and SACF (areas surrounding continental Antarctica). The richness in each taxonomic level was, in general, inversely proportional to the latitudinal gradient, i.e., higher at lower latitudes (Sub-Trop zones) and lower at higher latitudes (SACF) as expected and reported in previous studies for different groups of marine organisms (Willig et al., 2003). There is, however, an exception for seaweed that, especially in the southern Indian Ocean on both coasts of Africa and Australia, presented an inverse gradient from low to high latitudes (Kerswell, 2006). Keith et al. (2014) improved the data representation in higher latitudes, but still reinforced the scenario that macroalgal richness decreases toward the tropics, as described by Kerswell (2006). These aforementioned authors have not evaluated with special attention the flora of the Antarctic region, in terms of what can be attributed to the apparent divergence in species composition or absence of taxa compared to higher latitudes. Despite the noted positive correlation of seaweed richness and latitude, when evaluating these previous studies, it is possible to observe a richness loss in areas from intermediary latitudes poleward (i.e. Keith et al., 2014, pp. 520, Fig. 1), corroborating our results. This contradiction reinforces the necessity of improving and standardizing sampling efforts in the Southern oceans in order to shed more light on this discussion, by clarifying the distributional pattern of seaweed in intermediate and higher latitudes in the southern hemisphere. When the three sectors analyses were compared, a lower dissimilarity, or a higher similarity, was observed between phycoflora from the 2nd (Eastern Antarctica Peninsula – EAP – or under influence of the Weddell Sea Gyre, and some sub-Antarctic islands as South Orcadas, South Georgia and Crozet Archipelago) and the 1st sectors (Chilean and Argentinean Patagonia and surrounding islands, Falklands, South Shetlands and including Antarctic Peninsula). This could partially demonstrate the existence of a species distributional flux, considering the direction of the ACC (Eastward), despite the clear role of this current acting as a limit to dispersal. In another instance, a higher dissimilarity was observed (i.e., lower similarity) between the 3rd (Southern Australia and New Zealand, Western Antarctica Peninsula – WAP – or islands under influence of the Ross Sea Gyre) and 2nd sectors. Considering similarity among biogeographical assemblages observed in each zone, the highest index occurred in the Southern PF zone (surroundings of Antarctic Peninsula). This area is influenced by the ACC Eastward circulation pattern (formerly called the West Wind Drift), which facilitates connectivity of populations as observed in Durvillaea antarctica (Bussolini and Waters, 2015). In another instance, the lower similarity in seaweed diversity of the south SACF (surrounding areas of the Antarctic Continent) suggests a highly specialized and adapted phycoflora, followed by a high degree of endemism. However, this area does experience some differences in macroalgae assemblages

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between WAP (Ross Sea side) and EAP (Weddell Sea side). It is noteworthy that this area is influenced by a counter-current Westward (formerly called East Wind Drift), opposite to the ACC direction. In general, the high degree of endemism of the 3rd core is well documented; in the current study, 165 exclusive species were detected and the highest diversity was among sectors, followed by the 1st core. Comparing both, it is valid to also consider that the 3rd core has a larger geographic area, allowing recruitment of the seaweeds in consolidated substrate. Furthermore, it is better studied than the 1st sector. In another instance, the lower diversity and fewer exclusive species of the 2nd sector is already well known, and partially explained by lower availability of hard substrate and the extreme meteoceanographic conditions of the area, where even in summer the surroundings of the Weddell Sea Gyre are covered by ice. We highlight that our data did not consider the temporal scale of the checklists obtained, and that recent and regional-scale studies, such as Pellizzari et al. (in press), could be showing more clearly that, in fact, there is a crescent interconnectivity among these areas, via natural processes or otherwise. The original ages of the analyzed zones differ, resulting in distinct regional and local features, such as differences in substrata, ice free areas, water temperature, nutrient availability, irradiance and rainfall, which are consequences of atmospheric, latitudinal and oceanographic events, in addition to interactions with other organisms, such as competition and predation. According to Smale et al. (2011), patterns of diversity and richness are determined at a local scale; however, these patterns are more influenced by regional context. This was observed in our analysis through the higher dissimilarity of species between zones, especially those farthest apart, such as the Sub-Trop and SACF, represented by the locations around Continental Antarctica (Table 3). nMDS cluster, PERMANOVA and ANOSIM demonstrates these differences between the species and genera compositions for zones within the ACC, but not for families and orders, suggesting a higher sensibility of using species and genera for this approach. After the opening of the Drake Passage, the Antarctic mainland was isolated. However, some authors consider this event as semi-isolation. This isolation forced new interactions among species as evolutionary responses to internal disturbances, which occur on a regional scale (the total Antarctic area, or within each zone or section) and also on a local scale, including portions of the shores, such as EAP and WAP differences, as mentioned above. The better example in this study is the lower dissimilarity, or higher similarity, between phycoflora from the 2nd and the 1st sectors, demonstrating the existence of a species distributional flux, despite the clear role of the ACC acting as a limit to dispersal. For example, in accordance with observations made by Smale et al. (2011) in Australia, the species interactions within kelp forests are dominated by Ecklonia radiata, while in communities below the canopy patterns are determined by competitive exclusion of other species and also in a small-scale diversity. Observing diversity from areas around Tasmania, New Zealand, and Chatham and Antipode Islands, it is evident that these areas have a particular surrounding current system that forms three zones of convergence where cold waters from sub-Antarctic areas encounter those from the Antarctic (i.e., Knox, 1960), defining four biogeographic provinces, and a recognized high degree of endemism in the area. Hommersand and Fredericq (2002) postulated that this phycoflora probably dispersed from Eastern Antarctica by marine currents from higher latitudes throughout the Miocene and Holocene periods. Regarding South America, a local current system also permeates this geographical area in the Atlantic and Pacific Oceans, derived from Cape Horn and the ACC. The deep and stormy zone of the Drake Passage is located between Patagonia and the Antarctic Peninsula. Beyond Cape Horn, the northern part of the Drake Passage, the Falklands Current, in the Atlantic portion, flows from south to north, ensuring direct influence of the sub-Antarctic on Patagonia. Also, the Peru Current flows northward in the Pacific Ocean, along the Chilean coast. This

Please cite this article as: Sanches, P.F., et al., Multivariate analyses of Antarctic and sub-Antarctic seaweed distribution patterns: An evaluation of the role of the Antarctic Cir..., J. Sea Res. (2016), http://dx.doi.org/10.1016/j.seares.2016.02.002

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nutrient-rich and cold water mass resurges resulting in a highly productive fishing ground. These complex systems of circulation and contrary forces formed in the Southern Ocean and by Antarctic Fronts explain the differences among zones and sectors analyzed. When the Antarctic broke apart from the South American continent ca. 30 million years ago, a proper marine and highly adapted phycoflora developed in these isolated areas surrounded by cold waters and ice (Ramírez, 2010). Hommersand et al. (2009) suggest that distribution patterns of red seaweeds from Antarctica resulted from both events (vicariance and dispersion), suggesting that some species had their origin in the region after the separation and formation of the ACC. However, some species used the currents that flow from the ACC to disperse as observed by Bussolini and Waters (2015). This dispersion is becoming more frequent and clear today, whether or not by natural means, and is probably caused by climate and oceanographic changes. This can also be elucidated by the presence of cosmopolitan Chlorophyte species in the Antarctic Maritime islands (Pellizzari et al., in press). These dispersive events could have occurred in the past via the subAntarctic islands as corridors, or stepping-stones (e.g., MacArthur and Wilson, 1967), acting as a connection between the mainland and Antarctic areas, as suggested by the contribution of higher similarities among South America and the sub-Antarctic islands (sectors 1 and 2). Furthermore, this is supported by the diverse and distinct assemblages in the South Shetlands and in the Antarctic Peninsula (PF in the analysis), and also in EAP and WAP (SACF and 2nd and 3rd sector in the analysis). However, according to Silberfeld et al. (2010), Ascoseira mirabilis, one of the species found in the south PF and SACF (South Shetland Islands and Antarctic Peninsula surroundings, and WAP and EAP, respectively), differentiated between 100 and 120 million years ago, in the Cretaceous age, long before the current could have been considered a biogeographical barrier. In addition, Himantothallus grandifolius, which occurred in SACF and in the Southern PF, differentiated from Desmarestia menziesii about 30 million years ago, a time corresponding to the opening of the Drake Passage. Peters et al. (2009), conversely, showed that Phaeurus antarcticus (presented in SACF and PF) differentiated before H. grandifolius and that these data do not allow corroboration through vicariance. According to van den Hoek and Donze (1967), seaweeds are able to disperse with currents generated by distinct fronts south of the ACC, allowing oceanic islands to be colonized by dispersion over long distances and in short periods of time. Tristan Island, for example, received South African flora about 1 million years ago, albeit against the direction of the local current (van den Hoek and Donze, 1967). Although dispersion in the planktonic phase of animals has been well documented (Brandt et al., 2007; Watson et al., 2011; Teske et al., 2011), no strong evidence can be found for seaweed spores. However, dispersion and introductions can occur by floating species, such as Sargassum spp. from subtropical areas and Durvillaea antarctica from sub-Antarctic areas, where spores and recruits can be carried on the free-floating thallus, or even boats, plastic debris, or, more controversially, ship's ballast water (van den Hoek and Donze, 1967; Macaya et al., 2005). Recently, Pellizzari et al. (in press) reported seven new records of seaweed species for the South Shetlands Islands. This suggests not only that previous sampling failure has occurred in the area, but also possible changes in the connectivity patterns are occurring among sub-Antarctic islands, Patagonia and the areas surrounding the Antarctic Peninsula. These arguments should be investigated in detail and aim to elucidate these new patterns emerging from global meteoceanographic changes or anthropogenic introductions. Among abiotic factors, temperature and ice cover are probably the main limiting factors in this region regarding dispersion and isolation assessments. According to Brown et al. (2004), biological reactions, metabolic rates and other rates of biological activities increase exponentially with higher temperatures, but vary according to phylogeny/

parentage and organismal tolerances. The Antarctic endemic species H. grandifolius, P. antarcticus and A. mirabilis show higher growth rates between 0° and 10 °C. This temperature is lower than that of species from Southern Chile and from northern sub-tropical zones, such as Laminaria (Wiencke and Dieck, 1990). In Antarctica, natural extreme temperature fluctuations began with the opening of the Drake Passage and the circulation of the ACC, which isolated the heat coming from the northern tropics. However, the limiting factors for seaweed establishment are typically climate related (Clarke et al., 2005), and it is likely that future meteoceanographic changes will transform the macroalgae populations in Antarctica. Indeed, there is little evidence from the past two centuries that nonindigenous microbes, fungi, flora and fauna have successfully established in the surroundings of the Antarctic continent (Frenot et al., 2004). Therefore, with the changes in global conditions and the rapid regional warming of the Antarctic Peninsula during the past 50 years (Vaughan et al., 2003), we could be witness to a period of significant changes to the Antarctic fauna and flora, including seaweed diversity (Pellizzari et al., in press). 5. Conclusions This is a contribution that attempts to link influences of the physical oceanography domain with a biological system, in this case, macroalgae. However, this is only the “tip of the iceberg” and more studies are imminently needed. We are aware that the link between seaweed richness patterns and the ACC is based on inferences rather than direct tests. To be more convincing, this approach needs further detailed studies regarding the true influence of drift patterns, current meander and oceanographic modeling on seaweed spore recruitment. As observed by van den Hoek (1984), red seaweeds from South America and Sub-Antarctic Islands showed a similarity of 35%. Indeed, seaweed genera exposed to the polar climate retreated to South America and the Sub-Antarctic Islands, with only extremely tolerant organisms staying in Antarctica, demonstrating that they are well adapted to extreme changes in temperature and irradiance. Considering that the composition of phycoflora found in the PF (Southern Shetland Islands and around Antarctic Peninsula) and along the shores of the continental Antarctica (SACF) is adapted to conditions that are influenced by the ACC fronts, it can be inferred that adaptations were relevant mainly to seaweed populations from the Southern PF. Dominance differences, interactions, and environmental characteristics have made the fauna and flora of the continental Antarctic surroundings (SACF) more specialized, including a higher rate of endemic taxa than other zones (similarity of 11.59%) and showing differences in both sectors of the EAP and WAP (2nd and 3rd, respectively). Therefore, beyond performing thermal isolation, the Southern Ocean could also be a bathymetric and meteorological barrier as a consequence of extreme wind velocities (which have been increasing in the past two decades – Young et al., 2011), deep zones and the highest wave amplitudes in the world. Following our observations, these features may not completely prevent dispersion, but they may influence it, even today, especially with the possible correlation between wind velocities and height wave formation (Young et al., 2011). This contribution reveals relevant particularities of Antarctic seaweed flora, which reinforces the need to take cautions with species introduction through ballast waters, among others vectors. The intrinsic sensibility of the Antarctica and sub-Antarctic areas should be observed especially when considering climate change stressors, mainly ocean warming and nutrient pollution. These environmental changes can induce changes in spore/propagules dispersion and settlement, promoting community structure shifts, and compromising a flora with a high level of particularities and of key importance in coastal polar environments. Conservation initiatives should consider these global sources of stress, and eventually local stressors, as well as tourism cruises and research vessels that should take measures to reduce species introduction

Please cite this article as: Sanches, P.F., et al., Multivariate analyses of Antarctic and sub-Antarctic seaweed distribution patterns: An evaluation of the role of the Antarctic Cir..., J. Sea Res. (2016), http://dx.doi.org/10.1016/j.seares.2016.02.002

P.F. Sanches et al. / Journal of Sea Research xxx (2016) xxx–xxx

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Please cite this article as: Sanches, P.F., et al., Multivariate analyses of Antarctic and sub-Antarctic seaweed distribution patterns: An evaluation of the role of the Antarctic Cir..., J. Sea Res. (2016), http://dx.doi.org/10.1016/j.seares.2016.02.002