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   Gracilaria vermiculophylla (aquatic plant)
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    Taxonomic name: Gracilaria vermiculophylla (Ohmi) Papenfuss
    Synonyms: Gracilaria asiatica Zhang & Xia, Gracilariopsis vermiculophylla Ohmi
    Common names:
    Organism type: aquatic plant
    Gracilaria vermiculophylla (Ohmi) Papenfuss is a red alga and was originally described in Japan in 1956 as Gracilariopsis vermiculophylla. It is thought to be native and widespread throughout the Northwest Pacific Ocean. G. vermiculophylla is primarily used as a precursor for agar, which is widely used in the pharmaceutical and food industries. It has been introduced to the East Pacific, the West Atlantic and the East Atlantic, where it rapidly colonises new environments. It is highly tolerant of stresses and can grow in an extremely wide variety of conditions; factors which contribute to its invasiveness. It invades estuarine areas where it outcompetes native algae species and modifies environments.
    Gracilaria vermiculophylla is a red macroalga that is cartilaginous, cylindrical and up to 50 cm long. It is coarsely branched, often profusely so. G. vermiculophylla can be found as loose-lying thalli or attached to small stones or shells. Red algae are often found in the vegetative state, and characterisation of reproductive structures is often necessary for correct identification of Gracilaria species (AlgaeBase 2010; Liao & Hommersand 2003; Nyberg et al. 2009; Rueness 2005).
    Similar Species
    Gracilaria gracilis, Gracilariopsis longissima

    Occurs in:
    estuarine habitats, marine habitats
    Habitat description
    Gracilaria vermiculophylla is thought to be a temperate to subtropical alga, and can grow in both temperate and tropical regions. It is well-adapted to low energy, shallow-bottom bays, lagoons, estuaries, harbours and inslets (Yokoya et al. 1999; Thomsen & McGlathery 2007; Nyberg et al. 2009; M. S. Thomsen, pers. comm.). It forms extensive beds in the intertidal zone and upper sublittoral zones, where it attaches to rocks or pebbles, often covered with sand and mud (Bellorin et al. 2004). It often occurs as pure stands to the exclusion of other algae species (Rueness 2005).

    G. vermiculophylla is able to grow in a wide range of temperatures (5-35 °C), light intensities (20–100 μmol photons m-2 s-1) and salinities (5-60 psu). Optimum growing conditions are between 15-25 °C and 10-45 psu (Rainkar et al. 2001; Rueness 2005). It is also tolerant to other stressses including sedimentation, desiccation, grazing and low nutrients (Rueness 2005). Nybert et al. (2009) found in one instance that this alga was able to survive in complete darkness for more than five months in the laboratory.

    General impacts
    Ecosystem impacts: Gracilaria vermiculophylla inhibits the growth and survival of native algae through competition (Council of Europe 2009; Hamman et al. n.d.). It has been demonstrated to have negative effects on native seagrass beds of Zostera marina by decreasing net leaf photosynthesis and survival rates. Negative effects on seagrass are greater at higher temperatures, suggesting that impacts could increase with future ocean warming (Martínez-Lüscher & Holmer, 2010). In some areas such as Hog Island Bay in Virginia G. vermiculophylla dominate algal assemblages, in all seasons and elevation levels (Thomsen et al. 2006b). Accumulation of G. vermiculophylla may also impair environmental conditions for threatened Charophytes and Zostera noltii in Sweden (Gärdenfors 2005 in Nyberg et al., 2009).

    In high abundance G. vermiculophylla may have dramatic effects on ecosystems. The introduction of G. vermiculophylla adds structural complexity to relatively homogenous soft-bottom systems and add new attachment sites for filamentous algae and sessile animals (Thomsen et al. 2006a; Nyberg et al., 2009). Thus G. vermiculophylla can provide shelter and food for other organisms, including microalgae, gastropods, crustaceans, polychaetes, and mny other small invertebrates. In Virginia research has shown that most invertebrate groups were positively affected by the presence of G. vermiculophylla in native algae (Thomsen et al., 2010).

    While G. vermiculophylla may enhance local diversity, the ability to utilize increased habitat complexity will vary between species (Nyberg et al. 2009). Furthermore these changes could lead to effects on higher trophic levels (Aikins & Kukuchi 2002; Freshwater et al. 2006; Gustafsson 2005 in Nyberg et al. 2009; Nyberg et al. 2009; Thomsen et al. 2007c).

    Loose-lying G. vermiculophylla populations have the potential to develop into dense mats, particularly in shallow bays, lagoons, harbours and estuaries. These mats can modify the habitat available for the benthic faunal community and bottom dwelling fish. Algal mats can also form physical barriers for settling larvae, decrease light intensity, increase the likelihood of anoxia and change water movement patterns, which in turn affects sedimentation rate and thus food availability for deposit feeders (Nyberg et al. 2009).

    Additionally, the movement, accumulation and decomposition of G. vermiculophylla is likely to have important implications for nutrient cycling and trophic dynamics in areas it invades (Thomsen et al. 2009).

    Fisheries: G. vermiculophylla is reported to be a problem in fishing industries through fouling of nets (Freshwater et al. 2000).

    G. vermiculophylla is widely collected for the production of the biopolymer agar, which is used extensively in the pharmaceutical and food industries (Mollet et al. 1998; Sousa et al. 2010).
    Over 179 species are included in the genera Gracilaria and Gracilariopsis. The delineation of species in these genera has been notoriously difficult due to morphological similarities between species (Goff et al. 1994; Rueness 2005). Taxonomic problems have been particularly pronounced for Gracilaria vermiculophylla (Bellorin et al. 2004).

    In a recent review Terada and Yamamota (2002 in Rueness 2005) reduced G. asiatica Zhang & Xia into synonymy with G. vermiculophylla.

    The morphological similarities between G. vermiculophylla and other related algal species mean that the invasion of this alga is often cryptic, requiring DNA analysis for reliable identification (Thomsen et al. 2006a; Thomsen et al. 2006b). To avoid future taxonomic confusion Thomsen et al. (2006b) recommend researchers create silica-gel, air-dried, and/or herbarium presses as voucher specimens so that the correct identification can be confirmed using morphological and molecular analysis.

    Geographical range
    Native range: Northwest Pacific ocean including Japan and east Asia (Rueness 2005).
    Introduced range: North American eastern and western coasts, Europe, northeastern Atlantic coast extending from Morocco to southwest Sweden, eastern Pacific (Weinberger et al. 2008; Bellorin et al. 2004).
    Introduction pathways to new locations
    Aquaculture: G. vermiculophylla is a highly efficient recruiter around oyster reefs as they attach to shells via small holdfasts, causing them to be moved with translocation of oysters (Thomsen & McGlathery 2006; Thomsen et al. 2006b; Thomsen et al. 2007c). Indeed in Europe many G. vermiculophylla populations are in the vicinity of oyster farms (Rueness 2005).
    Floating vegetation/debris:
    Natural dispersal: Natural spread of G. vermiculophylla is by spores and fragments as small as 1 mm (Nyberg 2007 in Nyberg et al. 2009)
    Other: Migrating seabirds (Nyberg et al. 2009).
    Seafreight (container/bulk): Spread is likely to occur on vectors such as fishing and leisure boats (Nyberg 2007 in Nyberg et al. 2009).
    Ship ballast water:
    Ship/boat hull fouling:
    Translocation of machinery/equipment: Fishing gear (Nyberg et al. 2009).

    Local dispersal methods
    Aquaculture (local): G. vermiculophylla is a highly efficient recruiter around oyster reefs as they attach to shells via small holdfasts, causing them to be moved with translocation of oysters (Thomsen & McGlathery 2006; Thomsen et al. 2006b; Thomsen et al. 2007c). Indeed in Europe many G. vermiculophylla populations are in the vicinity of oyster farms (Rueness 2005).
    Boat: Secondary dispersal between regions and estuaries is probably facilitated by entanglement to boat screws, fishing gear, trawling nets and various ‘extensions’ of smaller boats (Thomsen et al. 2007c).
    On animals: Migrating seabirds (Nyberg et al. 2009).
    Other (local): Ship/boat hull fouling (Nyberg et al. 2009).
    Translocation of machinery/equipment (local): Fishing gear (Nyberg et al. 2009).
    Water currents: Drifting fragments are dispersed by currents (Weinberger et al. 2008).
    Management information
    Accurate identification of Gracilaria vermiculophylla has been problematic in the past, leading to much confusion with similar species. DNA analysis, including rapid DNA barcoding, is now used for accurate identification (Bellorin et al. 2004; Saunders 2009).

    Prevention: Movement of oysters is a major vector for the introduction of G. vermiculophylla to new locations worldwide. Thus making sure oysters are not transplanted may reduce the incidences of new infestations (M.S. Thomsen, pers. comm. 2011).

    Physical control: Mechanical removal (harvesting) of G. vermiculophylla for use in the production of agar and other applications is a potential control method (Sousa et al. 2010; Villanueva et al. 2010).

    Gracilaria vermiculophylla belongs to the phylum Rhodophyta (red algae). Red algae are primitive photosynthetic eukaryotes (Xie et al. 2010).
    Gracilaria vermiculophylla reproduces by spores, which are non-motile, therefore restricting this alga to passive dispersal mechanisms. Male and female gametophytes and tetrasporophytes have a similar morphology (Freshwater et al. 2006; Nyberg et al. 2009; Woelkerling 1990, in Freshwater et al. 2006).
    Lifecycle stages
    Gracilaria vermiculophylla is a perennial species with alternating generations (isomorphic life cycle). Dioecious haploid gametophytes produce either male or female gametes. These fuse to create a diploid zygote which grows into a diploid tetrasporophyte, (Nyberg et al. 2009; Rueness 2005; Thornber 2006). There is also a parasitic heteromorphic carposporophyte generation (Xie et al. 2010).
    Reviewed by: M. S. Thomsen, Marine Department, National Environmental Research Institute, University of Aarhus.
    Compiled by: National Biological Information Infrastructure (NBII) & IUCN/SSC Invasive Species Specialist Group (ISSG)
    Last Modified: Saturday, 9 April 2011

ISSG Landcare Research NBII IUCN University of Auckland