Short Communication

 

Southern Ocean areas of endemism: a reanalysis using benthic hydroids (Cnidaria, Hydrozoa)

Áreas de endemismo del Océano Austral: un re-análisis basado en datos adicionales de hidroides bentónicos

 

Thaís P. Miranda¹, Álvaro L. Peña Cantero² & Antonio C. Marques¹

¹ Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo Rua do Matão Trav. 14, 101, 05508-090, São Paulo, Brazil
² Instituto Cavanilles de Biodiversidad y Biología Evolutiva, Departamento de Zoología Universidad de Valencia, Apdo. Correos 22085, 46071 Valencia, Spain
Corresponding author: Thaís P. Miranda (thaispmir@ib.usp.br)

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ABSTRACT. The biogeographic history of the Southern Ocean (SO) fauna is complex and poorly studied, especially the areas of endemism. We reanalyzed the data of Marques & Peña Cantero (2010), along with other geographical records of endemic benthic hydroids below 45°S. A Parsimony Analysis of Endemicity (PAE) based on 5° latitude by 5° longitude matrix with 61 species resulted in eight areas of endemism. We discuss these results in the context of different hypotheses of the evolution of the SO fauna and previously proposed biogeography patterns.

Keywords: Antarctica, barriers, biogeography, endemism, Hydrozoa, PAE, Southern Ocean.

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RESUMEN. La historia biogeográfica de la fauna del océano Antártico (OA) es compleja y está poco estudiada, principalmente en relación a las áreas de endemismo. Se ha reanalizado los datos de Marques & Peña Cantero (2010) junto con otros registros geográficos de hidrozoos bentónicos endémicos de la zona abajo de los 45°S. Una Análisis de Parsimonia de Endemismos (PAE) a partir de una matriz de 5° latitud por 5° longitud con 61 especies, obtuvo ocho áreas de endemismo. Se discute los resultados tomando en cuenta diferentes hipótesis sobre la evolución de la fauna del OA y los patrones biogeográficos de la literatura.

Palabras clave: Antárctica, barreras, biogeografía, endemismo, Hydrozoa, PAE, Oceano Austral.

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Marine polar regions are often considered to have low biodiversity, a pattern generally thought to be associated with extreme abiotic factors (Clarke & Crame, 1992). However, several studies on biodiversity, biogeography and paleontology of polar regions (e.g., Beu et al., 1997; Clarke & Johnston, 2003; Adey et al., 2008) revealed greater than expected biodiversity, particularly for the Southern Ocean (SO; viz., Clarke & Johnston, 2003).

The SO is a unique oceanographic system in which the Antarctic Circumpolar Current (ACC) dominates (Barker & Thomas, 2004) and moves around the southern seas with no continental barriers. The ACC originated with the opening of the Drake Passage (ca. 30 Ma), thereby causing biogeographically and thermal isolation of the SO (Lawver & Gahagan, 2003). This, in turn, contributed to the isolation and development of endemic marine fauna (Clarke & Crame, 1989; Beu et al., 1997; Barker & Thomas, 2004; Clarke et al., 2004).

On the other hand, there are historical similarities of the Antarctic fauna to those from northern regions (Cañete et al., 1999; Yasuhara et al., 2007; Kaiser et al., 2011), mainly in the Antarctic Peninsula and the subantarctic region of South America (Clarke & Johnston, 2003; Clarke et al., 2005). The connection between both continents is through the Scotia Arc, and since it will have influenced dispersal of their marine fauna, we may question exactly how isolated was the SO (Clarke et al., 2005).

Thus, several hypotheses have been proposed to explain the origin of the SO fauna: (H1) evolution in situ, (H2) derivation from adjacent deep-water basins, (H3) dispersal from South America through the Scotia Arc, and (H4) dispersal from Antarctica through the Scotia Arc (cf., Knox & Lowry, 1977). These not-mutually-independent hypotheses are partially supported by fauna and geography and have been contrasted with abiotic factors of the SO (viz., Beu et al., 1997; Cañete et al., 1999; Yasuhara et al., 2007; Kaiser et al., 2011).

Theoretical and practical frameworks concerning areas of endemism (cf. Harold & Mooi, 1994; Morrone, 1994; Szumik et al., 2002) are complicated in marine biogeography. The tridimensional nature of the marine realm, the dynamics of currents and oceanic fronts, the difficulties to establish thresholds in ecophysiological continuums and the amazingly diverse strategies of dispersal, all make for a unique definition of areas, or "volumes," of endemism (see Miranda & Marques, 2011). Clearly, this will also be an issue in the SO, and in which few studies examine the origin and evolution of all marine organisms, not just endemics (e.g., Clayton, 1994; Brandt, 1999; Clarke et al., 2004).

The hydroids - benthic hydrozoans of the orders Anthoathecata and Leptothecata (cf. Marques & Collins, 2004; Collins et al., 2006) - provide an example with many endemics in the SO (Peña Cantero, 2012). For example, a Parsimony Analysis of Endemicity (PAE) for the endemic SO genus Oswaldella (a single study using strict endemicity analysis) suggested four areas of endemism: (1) Magellanic Zone, (2) Antarctic Peninsula Zone, (3) Western High Antarctica Zone and (4) Eastern High Antarctica Zone (Marques & Peña Cantero, 2010). In another PAE for the SO, we used additional geographic data of endemic benthic hydroids to test previous hypotheses and to better understand the biogeography of the SO. We used a matrix of 5° latitude by 5° longitude and geographic records of 61 species of the genera Antarctoscyphus, Mixoscyphus, Oswaldella and Staurotheca (Table 1). PAE was carried out following Marques & Peña Cantero (2010), but using semistrict consensus trees. Eight areas of endemism were found for the SO, concentrated in the Magellan region, the Antarctic Peninsula, the subantarctic islands, the Ross Sea, the Weddell Sea and Wilkes Land (Figs. 1, 2). Areas I, II and V (Figs. 1, 2) are similar to the previously mentioned Magellanic and Antarctic Peninsula zones (Marques & Peña Cantero, 2010). These areas began with the ACC as a system of deep eastward currents connecting the Magellan region and Scotia Arc to the Weddell Sea, Queen Maud Land and Wilkes Land (Beu et al., 1997; Lawver & Gahagan, 2003; Marques & Peña Cantero, 2010). These currents caused dispersal towards Queen Maud Land (Marques & Peña Cantero, 2010), thereby supporting the third hypothesis of a South American origin for the SO fauna (Knox & Lowry, 1977).

 

Table 1. List of the 61 species of benthic hydroids used in PAE and quadrants in which they are present.

 

Figure 1. Semistrict consensus of the PAE in the 5° x 5° matrix grid. Codes I to VIII indicate the resultant areas of endemism. Colors are as in Figure 2.

 

Figure 2. Areas of endemism from PAE for the 5° x 5° matrix grid. Colors indicate monophyletic groups delimited in the semistrict consensus from Figure 1 and are the same for the clades in Figure 1.

 

Areas of endemism I, III, V and VI (Figs. 1, 2) coincide with the Scotia Arc of Marques & Peña Cantero (2010), and may be a transitional region for dispersal events of species distributed both in the Antarctic Peninsula and in the Magellan region (Peña Cantero et al., 1997; Peña Cantero & Vervoort, 2003, 2004 - except the monotypic genus Mixoscyphus, which is exclusively in Antarctica (cf. Peña Cantero & Vervoort, 2005). These areas support the previously mentioned third and fourth hypotheses (Knox & Lowry, 1977). Nonetheless, this does not refute the hypothesis that vicariance influenced the isolation of the Magellanic (e.g., area V, Figs. 1, 2) from the Antarctic Peninsula (areas I and II, Figs. 1, 2). Thus, evolution in situ (hypothesis H1) may have also occurred with a fauna derived from the adjacent deep-water basin (hypothesis H2; cf. Knox & Lowry, 1977). Other areas of endemism (I, IV, VI to VIII; Figs. 1, 2) coincide with the Western High Antarctica Zone and Eastern High Antarctica Zone (Marques & Peña Cantero, 2010), and may be due to variations in depth, present oceanic currents and paleocurrents of the SO (Marques & Peña Cantero, 2010).

These results are coherent in part with ecological areas based on earlier informal biogeographic analyses (Hedgpeth, 1969; Briggs, 1974; Spalding et al., 2007). But, these results agree completely with previously hypothesized areas of endemism (Marques & Peña Cantero, 2010, cf. their Fig. 2), but now with more detail and defined subregions of those areas. These subregions suggest specific microhabitats for the benthic hydroid fauna of the SO that may be derived from dispersal or vicariant events.

If dispersal, then this suggests the formation of microhabitats, as a consequence of different strategies of larvae transportation, such as rafting of incrusting biota (e.g., on algae, wood) and oceanographic mechanisms (e.g., vortices and oceanic fronts). Both of these mechanisms are important for transportation of subantarctic/Antarctic plankton and benthos (including larvae of benthic or epipelagic organisms) along the southern polar region. If vicariance, historical and ecological barriers may have involved continental drift and climatic changes over time. Nevertheless, vicariance does not imply the absence of dispersal in the formation of the SO benthic hydroid fauna.

Considering the evolutionary history of the SO, an important question to be answered is how important were the intensity and periodicity of changes in sea level and ice (both in extent and quantity) in causing the depth and occupation of habitats along the Antarctic continental shelf (Clarke & Crame, 1989; Clarke et al., 2004). These phenomena influence marine areas of endemism because they contribute to the formation of new habitats and the availability of ecological niches, which in turn may alter the geographic distribution of the species. The SO biota has a complex evolutionary history associated with dispersal, vicariance and subsequent processes of oceanic restructuring. The use of different data sets and multiple evolutionary hypotheses will increase the explanatory power for understanding the peculiar processes leading to endemism and biogeographic patterns in the SO realm.

ACKNOWLEDGEMENTS

This study was supported by CAPES (Proc. 9194/118; PROCAD and PROTAX), CNPq (Proc. 557333/2005-9; 490348/2006-8; 304720/2009-7, 562143/2010-6, 563106/2010-7, 564945/2010-2; 477156/2011-8), and FAPESP (Proc. 2004/09961-4; 2010/06927-0; 2010/52324-6; 2011/50242-5). This study is a contribution of NP-BioMar, USP. This study was also developed thanks to a research project (Ref. CTM2009-11128ANT) funded by the Ministerio de Ciencia e Innovación of Spain and the Fondo Europeo de Desarrollo Regional (FEDER). James J. Roper revised the English in its entirety.

 

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Received: 28 February 2013; Accepted: 10 September 2013