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The First Detection of the Invasive Macroalga Codium Fragile Subsp

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The First Detection of the Invasive Macroalga Codium Fragile Subsp BioInvasions Records (2015) Volume 4, Issue 2: 75–80 Open Access doi: http://dx.doi.org/10.3391/bir.2015.4.2.01 © 2015 The Author(s). Journal compilation © 2015 REABIC Research Article The first detection of the invasive macroalga Codium fragile subsp. fragile (Suringar) Hariot in Western Australia Justin I. McDonald1*, John M. Huisman2,3, Felicity N. Hart2, Rainbo R.M. Dixon2 and John A. Lewis4 1Western Australian Fisheries Department, Biosecurity Research and Monitoring Section, Fisheries and Marine Research Laboratories, PO Box 20, North Beach, WA 6920, Australia 2School of Veterinary and Life Sciences, Murdoch University, Murdoch, WA 6150, Australia 3W.A. Herbarium, Science Division, Department of Parks and Wildlife, Locked Bag 104, Bentley Delivery Centre, WA 6983, Australia 4ES Link Services Pty Ltd, PO Box 10, Castlemaine Vic., 3450, Australia *Corresponding author E-mail: [email protected] Received: 12 June 2014 / Accepted: 15 January 2015 / Published online: 21 February 2015 Handling editor: Darren Yeo Abstract Codium fragile subsp. fragile (Suringar) Hariot is a large, dichotomously branched green alga that has invaded many temperate locations around the globe. Despite its wide distribution and pest status, there are few accounts of Codium fragile subsp. fragile that provide morphological descriptions, including illustrations, for comparison. In 2008, a seaweed sample suspected to be Codium fragile subsp. fragile was collected from Albany, Western Australia. As this taxon superficially resembles other local erect and dichotomously branching Codium species, a detailed morphological and molecular analysis of the suspect alga was conducted. Investigations confirmed the identity of this alga as the invasive subspecies Codium fragile subsp. fragile. This represents the first record of this species in Western Australia. Key words: Albany, algae, bioinvasion, Codiaceae, pest, Ulvophyceae Introduction (1999) predicted that C. fragile subsp. fragile would spread to wave-protected bays, lagoons, Codium fragile subsp. fragile (Suringar) Hariot, and estuaries in New South Wales, Victoria, 1889 [formerly C. fragile subsp. tomentosoides Tasmania, South Australia, and Western Australia. (van Goor) Silva, 1955; see Maggs and Kelly In 2008, a seaweed sample collected by the 2007] is a large, dichotomously branched green Western Australian Department of Fisheries alga that has spread dramatically during the last (DoF) from the Port of Albany was suspected to century (Trowbridge 1998). Regarded as native be the invasive alga Codium fragile subsp. to the coastal waters of Japan and Korea (Provan fragile based on gross morphology. More detailed et al. 2005; Scheibling and Gagnon 2006; Lyons microscopical analysis confirmed the tentative and Scheibling 2009), this alga has spread to identification as Codium fragile subsp. fragile. temperate seas virtually worldwide. In Australia, This species and subspecies had not been C. fragile subsp. fragile has invaded most temperate recorded from Western Australia previously, coasts; it was first reported from Victoria at despite several extensive marine pest surveys Corner Inlet in 1995 and has spread through (CRIMP 1997). Codium fragile subsp. fragile Victoria, South Australia and Tasmania (Figure was identified by Hayes et al. (2005) as one of 1). In eastern Australia C. fragile subsp. fragile the ten most damaging potential domestic target infests numerous coastal regions, to such an species based on overall impact potential extent that attempting eradication was considered (economic and environmental). The species was futile (Campbell 1999). Based on the alga’s collected as one of the key target marine pest temperature and salinity tolerances, Trowbridge species identified at the time by the Australian 75 J.I. McDonald et al. Figure 1. Map of reported Codium fragile subsp. fragile distributions in Australia. Codium fragile subsp. fragile was first reported from Victoria at Corner Inlet in 1995 (A) and spread to Port Phillip Bay (1997) (B), Western Port (1998) (C) and then D’Entrecasteaux Channel in Tasmania (1999) (D). It subsequently spread to Adelaide, South Australia (E) then Albany Port, Western Australia (2008) (F). National System for the Prevention and Manage- woodchips (45% in 2011) (Albany Port Authority ment of Marine Pest Incursions. The tendency of 2013). The port currently has four operational this species to overgrow and smother oyster beds berths (combined total length of 825 m), a tug has earned it the nickname 'oyster thief’ (Naylor boat marina, and seven anchorage positions. et al. 2001). Codium fragile subsp. fragile will The Albany area underwent comprehensive often make its home on the shells of oysters, marine-pest surveys in the late 1990’s by the now scallops, and clams. This can cause problems defunct Centre for Research on Introduced Marine because an attached adult plant can hinder the Pests (CRIMP); however C. fragile subsp. fragile movement and feeding of the shellfish was not recorded at that time (CRIMP 1997). In a (Trowbridge 1998). In cases where the attached recent overview, 25 introduced marine species plant is relatively large and wave exposure is were documented from the Albany marine area high, the shellfish can be swept away with the plant. (Huisman et al. 2008). After the initial detection, delimiting surveys The initial Town Jetty sample was identified of the area confirmed the alga’s presence in a by JMH based on morphology. Measurements of relatively small section of the port. Specimens internal structures (utricles, medullary filaments, collected during the later surveys were subjected reproductive structures) were made on portions to DNA sequence analyses to confirm their of the plant 2 cm from the apex, as dictated by identity and to genetically characterize the Albany Trowbridge (1999). In total, fourteen (1 at Town population. This paper documents the initial Jetty, 13 in tug harbour) (Supplementary material discovery and provides a morphological and Table S1) specimens of C. fragile subsp. fragile molecular description of Codium fragile subsp. were collected. Anatomical observations on these fragile in Western Australia to facilitate ready samples were made by FNH and JMH, and DNA identification, and a comparison with Codium analyses by RRMD. All specimens have been spinescens Silva and Womersley, 1956, the only pressed onto herbarium sheets and lodged with local species with spinous utricles and likely to the Western Australian Herbarium (PERTH), with be misidentified as C. fragile subsp. fragile. a small collection retained at Western Australian Department of Fisheries for reference purposes. Methods Molecular analysis The Albany marine area, which includes King George Sound, Princess Royal Harbour, and Eight Australian Codium samples, including five Oyster Harbour, is located on the south coast of from Western Australia, were newly sequenced Western Australia approximately 418 km south- for the molecular analysis, targeting the region east of the state capital, Perth (Figure 1). Albany rps3-rpl16 (UCP6) that was previously used in was one the first sites of European settlement in subspecies delineation in Codium fragile (Brodie Western Australia, being colonised in 1826. The et al. 2007) (Supplementary material Table S1). port predominantly handles bulk products; the Methods for DNA extraction, PCR and sequencing main export trade being grain (43% in 2011) and follow Dixon et al. (2012) with the exception of 76 Codium fragile spreads to Western Australia Figure 2. A-D. Codium fragile subsp. fragile. A, B. Pressed specimens showing habit variation (scale = 1cm). C. Surface view of thallus with hairs and utricular spines visible. D. Utricles showing slight medial ‘waist’; that on the right has a lateral gametangium (scale = 100 µm). E. Codium spinescens, surface view showing utricular spines for comparison. Photographs by J.M. Huisman. a secondary DNA purification step. Primers were slightly shorter, to 1050 µm; slightly narrower to derived from Provan et al. (2008) (primers for rps3- 400 µm in maximum diameter; spines slightly rpl16 (5´–3´) For: CCMGAHCCCATHCGDGTTTC, shorter to 68 µm; and gametangia slightly narrower, Rev: GGBMGHTTWAATGGHGCHGAWAT; annealing 72–92 µm in diameter. The description given by temperature 56°C). González and Santelices (2004) is also similar, The rps3-rpl16 sequences were between 386 with slight differences: utricles slightly shorter and 457 base pairs long. Codium sequences to 1060 µm; slightly narrower to 392 µm in downloaded from GenBank from Provan et al. maximum diameter; spines longer, 78–138 µm in (2008) and Verbruggen et al. (2007) were aligned length; and gametangia slightly more broad, with the new sequences and cut at each terminus, 123–197 µm in diameter. Below we give a detailed resulting in an alignment 370 nucleotides long description to facilitate identification and comparison. (Supplementary data). Morphology Results The Western Australian samples had thalli that Despite its global distribution and receiving were medium to dark green, firm, erect, and much scrutiny due to its pest status, there are repeatedly and regularly dichotomously branched, surprisingly few accounts of Codium fragile subsp. to 30 cm high. Branches were highly tomentose, fragile that provide morphological descriptions, generally terete, 5 mm in diameter basally, including illustrations, for comparison (e.g. Silva attenuating to 2–4 mm in diameter near branch 1957; González and Santelices 2004). The utricles
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