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2015 Rothman-Et-Al-Ecklonia-Jpy.Pdf J. Phycol. 51, 236–246 (2015) © 2014 Phycological Society of America DOI: 10.1111/jpy.12264 A MOLECULAR INVESTIGATION OF THE GENUS ECKLONIA (PHAEOPHYCEAE, LAMINARIALES) WITH SPECIAL FOCUS ON THE SOUTHERN HEMISPHERE1 Mark D. Rothman2 Department of Agriculture, Forestry and Fisheries, Private Bag X2, Rogge Bay 8012, South Africa Biological Sciences Department and Marine Research Institute, University of Cape Town, Cape Town 7701, South Africa Lydiane Mattio Biological Sciences Department and Marine Research Institute, University of Cape Town, Cape Town 7701, South Africa Thomas Wernberg UWA Oceans Institute and School of Plant Biology, The University of Western Australia, Crawley, Western Australia 6009, Australia Robert J. Anderson Department of Agriculture, Forestry and Fisheries, Private Bag X2, Rogge Bay 8012, South Africa Biological Sciences Department and Marine Research Institute, University of Cape Town, Cape Town 7701, South Africa Shinya Uwai Faculty of Science, Niigata University, Ikarashi-2, Nishi-Ku, Niigata 950-2181, Japan Margaret B. Mohring UWA Oceans Institute and School of Plant Biology, The University of Western Australia, Crawley, Western Australia 6009, Australia and John J. Bolton Biological Sciences Department and Marine Research Institute, University of Cape Town, Cape Town 7701, South Africa Brown algae of the order Laminariales, commonly and E. maxima as two distinct species in South referred to as kelps, are the largest and most Africa, E. radiata as a single species throughout the productive primary producers in the coastal inshore Southern Hemisphere (in South Africa, Australia, environment. The genus Ecklonia (Lessoniaceae, and New Zealand) and East Asiatic species as a Phaeophyceae) consists of seven species with four distinct lineage from the Southern Hemisphere species in the Northern Hemisphere and three in the clade. Results further pointed out a close sister Southern Hemisphere. It was recently transferred to relationship between Eckloniopsis radicosa and two the family Lessoniaceae based on phylogenetic Eisenia species (including the type species: Eisenia analyses of nuclear and chloroplastic markers, arborea) to the genus Ecklonia suggesting that the though the type of the genus was not included and genera Eckloniopsis and Eisenia are superfluous. its relationship with allied genera Eckloniopsis and Key index words: Ecklonia Eisenia atp8; ; ITS; kelp forests; remained unresolved. The present study is Lessoniaceae; phylogeny; rbcL; trnWI the first to produce a phylogeny focussed on the genus Ecklonia. It included sequences from nuclear, Abbreviations: atp8, adenosine tri-phosphate dehy- mitochondrial, and chloroplastic DNA, for most of drogenase subunit 8; GTR, general-time-reversible; the distribution range of the three current Southern ITS, internal transcribed spacer; RuBisCO, ribulose- Hemisphere species (Ecklonia radiata, Ecklonia 1,5-bisphosphate carboxylase/oxygenase; maxima, and a sample of a putative Ecklonia brevipes trnWI (section between trnW and trnI genes), t-RNAs specimen), sequences for East Asiatic species (Ecklonia cava, Ecklonia kurome, and Ecklonia stolonifera), as well as the closely related genera Eckloniopsis and Eisenia. Results confirmed E. radiata Ecklonia Hornemann is a genus of brown seaweed in the family Lessoniaceae (previously Alariaceae) of 1Received 4 July 2014. Accepted 15 October 2014. the Laminariales (Lane et al. 2006). Ecklonia is dis- 2Author for correspondence: e-mail [email protected]. tributed in both Hemispheres (Steneck et al. 2002, Editorial Responsibility: C. Lane (Associate Editor) Steneck and Johnson 2013, Guiry and Guiry 2014), 236 MOLECULAR INVESTIGATION OF ECKLONIA 237 but largely limited to East Asia in the Northern the tips of blades), and the very long, hollow stipe Hemisphere, with only small populations recorded of E. maxima. Ecklonia radiata is particularly polymor- in cooler deep water habitats in Oman and off the phic (Fig. 1, j–m; Wernberg et al. 2003). In Austra- north-west coast of Africa (Sheppard et al. 1992, lia, Wernberg and Vanderklift (2010) described Guiry and Guiry 2014). In the Southern Hemi- variations in rugosity, spinosity, stipe length, frond sphere, it is found in South Africa, Australia, and thickness, and frond densities which they linked to New Zealand (Luning€ 1990, Stegenga et al. 1997, wave exposure. In New Zealand, Wing et al. (2007) Bolton 2010, Guiry and Guiry 2014). According to also measured morphological variations of E. radiata Guiry and Guiry (2014), of a total 23 species and (frond length, width, thickness and number, as well infraspecific names available for the genus, only 10 as stipe length and diameter) and found some of Ecklonia species (and three forms) are currently these to depend on light levels related to wave accepted taxonomically. However, on the basis of exposure. Morphological variations in South African morphology, Bolton and Anderson (1994) consid- populations of E. radiata have also been observed ered Ecklonia fastigiata (Endlicher & Diesing) Papen- (Fig. 1, b–e), including a range of frond morpho- fuss, and Ecklonia richardiana J. Agardh to be logies (spiny to smooth), frond colors (striped to synonymous with Ecklonia radiata (C. Agardh) plain), and marginal serration (Fig. 1, f–g). Differ- J. Agardh. They further included Ecklonia biruncinata ences such as these have contributed to taxonomic (Bory de Saint-Vincent) Papenfuss in E. radiata, fol- confusion in the past, and the description of a lowing the treatments of Womersley (1967) and No- number of different species and subspecies, now vaczek (1980), thus leading to a final count of seven considered synonymous (see Bolton and Anderson current species. Four of those species occur exclu- 1994). sively in the Northern Hemisphere: Ecklonia muratii Bolton and Anderson (1994) noted that E. radi- Feldmann in Mauritania (Northeastern Atlantic), ata, E. cava, E. kurome, and E. muratii are difficult Ecklonia cava Kjellman, Ecklonia stolonifera Okamura, to tell apart based on morphological descriptions. and Ecklonia kurome Okamura in Japan and Korea, They also noted that E. muratii, as described by with E. kurome also occurring in China (Bolton Feldmann (1973), was similar to plants from Oman 2010, Guiry and Guiry 2014). Two species occur under the name E. radiata and reassigned it to an exclusively in the Southern Hemisphere: Ecklonia “E. radiata complex” including the four species maxima (Osbeck) Papenfuss (Fig. 1a) and Ecklonia mentioned above. Moreover, the main morphologi- brevipes J. Agardh. E. brevipes was described from cal character used to separate E. maxima from E. northern New Zealand (Lindauer et al. 1961, Adams radiata is the morphology of the stipe, which in 1994), but was also tentatively recorded from Hame- the former is long (sometimes up to 10 m) and lin Bay, Western Australia (Huisman 2000), while hollow, and in the latter is shorter and solid. How- E. maxima forms large kelp forests along the west ever, because intermediate morphologies have been coast of southern Africa (Stegenga et al. 1997, Guiry observed, the distinction between these species also and Guiry 2014). The latter has also been reported is not clear in some populations (M. Rothman, from several islands in the south Atlantic, Indian personal observation). and Pacific Oceans: St. Helena, Tristan da Cunha, Consequently, the taxonomic confusion surround- Falkland Island, St. Paul Island, and Auckland ing the genus Ecklonia has been evident for a long Island (Guiry and Guiry 2014). However, except for time (Bolton and Anderson 1994). While a few St. Paul Island, which has a number of other sea- sequences have been published, no study has yet weed species in common with South Africa, Papen- assessed Ecklonia species molecularly or examined fuss (1942) considered these reports doubtful, and their phylogenetic relationships. Using small sub- they have not subsequently been substantiated. unit rDNA sequences, Boo et al. (1999) confirmed Ecklonia radiata (Fig. 1b) is the most widely dis- the placement of E. cava in the order Laminariales. tributed species, occurring in the Southern Hemi- Subsequently, Boo and Yoon (2000), using internal sphere in South Africa, Australia and New Zealand, transcribed spacer (ITS) and rbcL sequence data but also reported from Madagascar, and in the sets, constructed a scheme of the Laminariales Northern Hemisphere from Oman and the central- which grouped Ecklonia, Eckloniopsis (Kjellman) eastern Atlantic Ocean (Mauritania, Senegal, the Okamura, and Eisenia Areschoug in a clade that was Canary and Cape Verde Islands; Stegenga et al. later upheld by Lane et al. (2006). Based on phylo- 1997, John et al. 2004, Wing et al. 2007). genetic analyses of the large subunit rDNA, ITS, the The characters separating species of Ecklonia are ribulose-1,5-bisphosphate carboxylase/oxygenase almost entirely based on external morphology, par- (RuBisCO) operon, and the NADH dehydrogenase ticularly stipe and holdfast characteristics. As Bolton subunit 6 (nad6) regions, Lane et al. (2006) further and Anderson (1994) pointed out, the morphologi- proposed the transfer of Ecklonia, Eckloniopsis, and cal distinction between some species remains Eisenia from the family Alariaceae to the Lessonia- unclear, aside from the very different modes of ceae. The authors stressed the need to include a growth of E. stolonifera (spreading stolon-like hold- sequence of E. maxima, the type species of the genus fast) and E. brevipes (forming new holdfasts from Ecklonia, to
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