Caulerpa Taxifolia in Seagrass Meadows: Killer Or Opportunistic Weed?
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Biol Invasions DOI 10.1007/s10530-012-0347-1 ORIGINAL PAPER Caulerpa taxifolia in seagrass meadows: killer or opportunistic weed? Tim M. Glasby Received: 28 May 2012 / Accepted: 17 October 2012 Ó Springer Science+Business Media Dordrecht 2012 Abstract Seagrass habitats are being lost throughout been affected by the introduction of C. taxifolia in the the world and the invasive alga C. taxifolia has often embayments studied. A review of literature on effects been implicated in seagrass declines. Although C. taxi- of species of Caulerpa on seagrasses provided limited folia can impact a variety of species, evidence for its experimental evidence for negative impacts of this effects on seagrasses is largely correlative. This study genus on seagrass abundance. combined observational studies and manipulative experiments done over many years to test hypotheses Keywords Invasive species Á Caulerpa taxifolia Á about effects of C. taxifolia on two Australian Marine algae Á Seagrass Á Experimental Á Review seagrasses, namely Posidonia australis and Zostera capricorni. Results indicated that C. taxifolia is not having adverse impacts on the coverage of these seagrasses in the sites studied. Rather, C. taxifolia Introduction appears to be an opportunist, persisting longer and its coverage being greater in previously non-vegetated There are numerous examples of negative correlations sediments than amongst seagrasses. C. taxifolia between abundances of introduced and native species co-existed with P. australis and did not cause reduc- (Parker et al. 1999; Ruiz et al. 1999; Bruno et al. 2005; tions in the cover of the seagrass. Outcomes of Simberloff 2009), but there are fewer instances for experimental manipulations of C. taxifolia amongst which there is experimental evidence that an intro- Z. capriconi were less clear due to losses of Z. capri- duced species has caused the decline of a native (i.e. coni in all plots, regardless of the presence of been the driver of change; MacDougall and Turking- C. taxifolia. It was possible that C. taxifolia may have ton 2005). Removal experiments can be useful for enhanced the decline in canopy cover of Z. capricorni, testing whether an introduced species is driving but the presence of alga did not alter the final fate of ecological change (removal would result in the Z. capricorni. There was also no evidence that long- recovery of the native assemblage, e.g. Bulleri et al. term areal coverage of P. australis or Z. capriconi has 2010), although results could be confused if impacts are long-term (e.g. recovery is slow, Glasby and Underwood 1996), or if there have been historical or T. M. Glasby (&) multiple interacting drivers of change (Didham et al. New South Wales Department of Primary Industries, 2005). Moreover, due to varying degrees of hysteresis, Port Stephens Fisheries Institute, Locked Bag 1, Nelson Bay, NSW 2315, Australia recovery after the removal of an invader might elicit e-mail: [email protected] community responses that are quite different from 123 T. M. Glasby those associated with the initial invasion (Dı´az et al. Various authors have asserted that C. taxifolia can 2003). A more direct test of impacts of invasion, cause the regression of seagrasses (e.g. Boudouresque therefore, is to use experimental additions of an et al. 1995; Glardon et al. 2008; Francour et al. 2009; introduced species, noting that this can potentially Lapointe and Bedford 2010; Peirano et al. 2011), but raise ethical concerns and impacts might still take a most evidence for this comes from correlative studies. long time to manifest. Observations of Posidonia oceanica beds in the Marine macroalgae account for some 20 % of the Mediterranean Sea soon after they were invaded by known introductions of marine species globally C. taxifolia indicated that the seagrass showed signs of (Schaffelke et al. 2006). The ecological effects of etiolation, chlorosis and had reduced numbers of leaves introduced marine macroalgae have been reviewed compared to an uninvaded site (Meinesz et al. 1993;de comprehensively over the last few years (e.g. Schaff- Ville`le and Verlaque 1995). After C. taxifolia invaded elke et al. 2006; Williams and Smith 2007; Thomsen sites in southern California, Williams and Grosholz et al. 2009) and the consensus is that there is a dearth of 2002) documented considerably reduced biomass experimental data and hence limited understanding of of the seagrass Ruppia maritima in patches where their impacts. The few high profile invasive macroal- C. taxifolia was abundant. Manipulative experiments gae that have been studied experimentally can have in Italy demonstrated that the shoot density of negative effects on native biota, but impacts are not the seagrass Cymodocea nodosa was decreased by always detected (Williams and Smith 2007; Thomsen C. taxifolia over a period of 4 months (Ceccherelli and et al. 2009). In comparison to other marine habitats, Cinelli 1997), but a subsequent 13 month study the effects of introduced species in seagrass has indicated no significant effects (Ceccherelli and Sechi received relatively little attention (Williams 2007). 2002). When seagrass beds are invaded, it is often by There is evidence that abundances of seagrasses at macroalgae and in situations where the seagrass beds some sites in the Mediterranean declined prior to the have already been disturbed (Williams 2007). Species introduction of C. taxifolia (Chisholm et al. 1997) and of the genus Caulerpa are the best known macroalgal that seagrass coverage has not in fact declined since invaders of seagrass beds and one of the better studied the introduction of the alga (Jaubert et al. 1999; species is Caulerpa taxifolia. Ceccherelli and Sechi 2002). Given the limited Much has been written about C. taxifolia since its experimental evidence for impacts of C. taxifolia on rise to prominence in the mid 1980s. C. taxifolia is a seagrasses (see Table 1), it is quite possible that the highly invasive green alga, capable of spreading alga may, at least in some cases, be responding rapidly over large areas and creating dense mats opportunistically to reductions of seagrass that are (Meinesz et al. 2001; Wright and Davis 2006). caused by some other disturbance. What seems clear is C. taxifolia can invade sheltered or exposed marine that it is inappropriate to generalise about any impacts habitats (Meinesz et al. 1993), including seagrass beds of C. taxifolia on seagrasses. (Ceccherelli and Cinelli 1998), non-vegetated soft Caulerpa taxifolia was first discovered in the sediments (Jaubert et al. 1999) and rocky reefs temperate waters of New South Wales (NSW), Aus- (Bellan-Santini et al. 1996; Ceccherelli et al. 2002). tralia, in 2000 and is currently present in 13 estuaries or Beds of C. taxifolia can affect the feeding behaviour coastal lakes. It appears that the strain of C. taxifolia in and distribution of benthic fishes (Levi and Francour NSW is different from that in the Mediterranean 2004; Longepierre et al. 2005) and support assem- (Meusnier et al. 2004), although genetic data suggest blages of fish (York et al. 2006) and invertebrates there have been several introductions of C. taxifolia (McKinnon et al. 2009; Gribben et al. 2009a) that into NSW (Schaffelke et al. 2002). C. taxifolia was differ from those in adjacent native habitats. The declared noxious in NSW after its appearance in recruitment of clams can be enhanced in beds of isolated patches some 750 km south of native sub- C. taxifolia relative to non-vegetated habitats, but the tropical populations in Queensland, and its subsequent growth, survivorship and reproductive capacity of rapid spread (Glasby and Creese 2007). Observations those clams can be reduced by the alga (Gribben and in NSW indicated that, as in the Mediterranean Wright 2006; Wright et al. 2007; Gribben et al. 2009b; (Ceccherelli and Cinelli 1999), there were negative Byers et al. 2010). associations between abundances of seagrasses 123 Caulerpa taxifolia in seagrass meadows Table 1 Putative effects of Caulerpa spp. on seagrasses based on mensurative studies Seagrass Putative Evidence Apparent response of seagrass Reference species effect Posidonia -ve C Shorter, narrower leaves at one site with C. taxifolia cf another without. de Ville`le and oceanica Necrosis of leave base where C. taxifolia smothering seagrass Verlaque (1995) -ve C P. oceanica leaves produced more phenolic compounds (presumed to be a Cuny et al. stress response) at one site with C. taxifolia cf another without (1995) -ve C Longevity of P. oceanica leaves reduced where C. taxifolia was dense. At Dumay et al. some times of sampling, shorter leaves at one site with C. taxifolia cf (2002) another without. Leaf productivity greater (thought to be a stress response) in presence of C. taxifolia n C Areal coverage of seagrass unchanged 8 years after invasion of Jaubert et al. C. taxifolia (2003) n C Number of leaves similar in areas with or without C. taxifolia Dumay et al. (2002) n C No indication that rhizome growth or shoot density where C. taxifolia Peirano et al. present were worse than uninvaded sites (2005) -ve C Tendency for reduced meristematic activity in P. oceanica when mixed Garcias-Bonet with C. taxifolia or C. prolifera et al. (2008) -ve C Leaves of P. oceanica smaller (and leaf turnover enhanced) when in the Pergent et al. presence of C. taxifolia (2008) -ve C More plagiotropic shoots (thought to be a stress response) at one seagrass Molenaar et al. site with C. taxifolia cf another without (2009) -ve C Negative associations between P. oceanica shoot density and biomass of Holmer et al. three species of Caulerpa (C. prolifera, C. racemosa, C. taxifolia) (2009) Posidonia n E Cover of seagrass not affected by C. taxifolia Current study australis Cymodocea -ve E Reduced seagrass shoot density in presence of C. taxifolia (over 4 months) Ceccherelli and nodosa Cinelli (1997) -ve E Reduced seagrass shoot density in presence of C.