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Impact of the Invasive Seaweed Sargassum Muticum (Phaeophyta) on an Intertidal Macroalgal Assemblage1

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Impact of the Invasive Seaweed Sargassum Muticum (Phaeophyta) on an Intertidal Macroalgal Assemblage1 J. Phycol. 41, 923–930 (2005) r 2005 Phycological Society of America DOI: 10.1111/j.1529-8817.2005.00120.x IMPACT OF THE INVASIVE SEAWEED SARGASSUM MUTICUM (PHAEOPHYTA) ON AN INTERTIDAL MACROALGAL ASSEMBLAGE1 I´n˜igo Sa´nchez2 and Consolacio´n Ferna´ndez A´rea de Ecologı´a, Departamento de Biologı´a de Organismos y Sistemas, Universidad de Oviedo, 33071-Oviedo, Spain The impact of the invasive seaweed Sargassum quences on native communities have been poorly stud- muticum (Yendo) Fensholt on a low intertidal macro- ied (Viejo 1997, Stæhr et al. 2000, Wilson 2001, algal assemblage was assessed at a semiexposed Britton-Simmons 2004) in spite of the potential im- rocky shore in northern Spain between 2002 and pact that it may cause due its recognized competitive 2004. Sargassum muticum plants were removed from abilities (Fletcher and Fletcher 1975, Norton 1977). the mature macroalgal assemblage and from those On the northern coast of Spain, as in other Euro- occurring along the successional process of the as- pean countries, the species has now become estab- semblage. Biomass, richness, diversity, and percent- lished, mainly in sheltered shores in low intertidal and age cover of macroalgae in experimental plots were shallow subtidal habitats (Ferna´ndez et al. 1990, An- compared with unmanipulated controls. The effect drew and Viejo 1998). Intertidal rock pools on more of S. muticum removal on the macroalgal assem- exposed localities can also be colonized (Viejo 1997, blage more than 2 years after the beginning of the Andrew and Viejo 1998). Sargassum muticum predom- experiment was negligible. Moreover, no differenc- inantly colonizes highly disturbed habitats (Deysher es between treatments were detected in the general and Norton 1982, De Wreede 1983, Critchley et al. patterns of succession. Only significant differences 1987, Andrew and Viejo 1998), but there is evidence in S. muticum abundance were detected between that it is also able to invade saturated macroalgal as- treatments at the end of the experiment. We sug- semblages (De Wreede 1983, Viejo 1997, Stæhr et al. gest that the low abundance of S. muticum at this 2000). The invasion by S. muticum at a saturated low intertidal level and its pseudoperennial life cycle intertidal assemblage on the central coast of Asturias may limit competition with native macroalgae. (northern Spain) occurred simultaneously with a con- However, long-term removal experiments may be tinuous decrease in the abundance of the native red a more indicator of the impact of S. muticum at the seaweed Gelidium spinosum (S. G. Gmelin) P. C. Silva, upper limit of its vertical distribution. which almost three decades ago formed dense stands Key index words: competition; intertidal; invasion; at this intertidal level, with a small number of accom- ´ macroalgal assemblages; northern Spain; removal panying species at low abundance (Anadonand ´ ´ experiment; Sargassum muticum; succession Fernandez 1986, Sanchez et al. 2005). The aims of this work were to study the effects of Abbreviations: ANOSIM, analysis of similarity; S. muticum on a native intertidal macroalgal assemblage ANOVA, analysis of variance; H0, species diversity; by experimental manipulation of the presence of nMDS, nonmetric multidimensional scaling; S, S. muticum and to test how the presence of an invader species richness established in a saturated community can affect the successional process after a strong disturbance. We predicted that in those plots where S. muticum Biological invasions in coastal marine habitats have plants were removed, the structure of native algal been recognized as one of the main causes of decline of assemblages would recover to the preinvasion state. biodiversity and changes in native populations, com- We asked whether S. muticum alters the general model munity dynamics, and major ecosystem processes of succession described for this intertidal level (Grosholz 2002). The Japanese seaweed Sargassum (Ferna´ndez et al. 1981). muticum (Yendo) Fensholt was accidentally introduced into European waters in the early 1970s. Since its first MATERIALS AND METHODS record in the English Channel (Farnham et al. 1973), Study site. The study was carried out from January 2002 to the species rapidly spread north- and southward across March 2004 at Aramar (431 360 N, 51 460 W), a semiexposed the Atlantic coast of western Europe (Critchley et al. locality in northern Spain. The study area was situated on a 1983, Rueness 1989, Ferna´ndez 1999, Karlsson and gently sloping rocky platform moderately exposed to wave Loo 1999). Although its occurrence and expansion action. The upper intertidal is dominated by invertebrates have been well documented, the ecological conse- and the mid and low intertidal is dominated by macroalgae (Ferna´ndez and Niell 1982). Experiments were performed in the low intertidal (0.4–0.8 m above the lowest astronomical 1Received 24 November 2004. Accepted 16 May 2005. tide) where primary space is dominated by S. muticum, Bifur- 2Author for correspondence: e-mail [email protected]. caria bifurcata R. Ross, and G. spinosum.Atthestartofthe 923 924 ´IN˜ IGO SA´NCHEZ AND CONSOLACIO´ N FERNA´NDEZ experiments (January 2002), algal density of S. muticum were used in the mature assemblage experiment (January (45 cm) in the study area was 24.64 Æ 10.92 plants Á m À 2 2002 to March 2004) and a variable number of these meas- (mean Æ SE, n 5 6). The mean length (from holdfast to the ures in the successional experiment, because most of the tip of the longest branch) was 25.01 Æ 3.20 cm (mean Æ SE, species were only present during short periods of time. For n 5 37). Around May and June, S. muticum reaches its these species, repeated-measures ANOVA were performed maximum size and biomass (103 Æ 10.8 cm, mean Æ SE, on the period in which they were dominant (March 2002 to n 5 10; F. Arenas, personal communication). However, the November 2002 for Ulva rigida C. Agardh, September 2002 largest algae (150–200 cm, personal observation) in the study to March 2004 for Stypocaulon scoparium (Linnaeus) Ku¨tzing area are frequently observed at 2–3 m below lowest astro- and Cladostephus spongiosus (Hudson) C. Agardh, and Novem- nomical tide. ber 2002 to March 2004 for Jania rubens (Linnaeus) J. V. Impact of an invader on a native mature assemblage. During Lamouroux). Furthermore, the same analysis was conducted the spring tides of January 2002, 12 permanent 50  50-cm between March 2002 and November 2002 for bare rock data. plots were randomly established along 200 m of coastline. One-way ANOVA was also used to test for differences be- The corners of the quadrats were permanently marked using tween treatments (control and removal) in Sargassum cover at anchor bolts placed in the substratum to allow repeated sam- the end of the successional experiment (March 2004 cover pling. Plots were randomly assigned to control or removal data). Cochran’s test was performed to check for homogene- treatments with six replicates for each. The removal treat- ity of variances (Winer 1971), and where appropriate, arcsine ment entailed removing all S. muticum plants by carefully de- and logarithmic transformations were applied. Student’s t- taching their holdfasts with a scraper, both inside the plot and tests were used to compare the percentage cover of dominant in a 1-m wide buffer zone surrounding the plot. This buffer species at the end of the experiment between control plots zone was established to eliminate large algae in the neigh- from mature and successional experiments. All tests were borhood of the plots. The removal treatment was maintained done with SPSS 11.0 (Chicago, IL, USA) for Windows. over the course of the experiment by periodically removing To describe the assemblage responses to treatments, non- new Sargassum recruits. metric multidimensional scaling (nMDS) ordinations (Field Percentage cover of algae was recorded bimonthly with a et al. 1982) were used. These analyses were based on Bray- 50  50-cm PVC quadrat divided by monofilament nylon fish- Curtis similarity matrices derived from cover data after a ing line into 5  5-cm squares. Two layers of line were used to square root transformation to reduce the influence of domi- avoid parallax errors in sighting (Hawkins and Jones 1992). nant species. The relationship between control and Sargassum Primary and secondary covers (cover of algae directly on the removal plots was compared before manipulation (January substratum and overstorey canopy) were recorded at the 81 2002), in March 2002, and December 2003 as well as at the end intersection points (maximum, 162 points), and the data were of the experiment (March 2004). To avoid seasonal artifacts, transformed as specific cover values. For this reason, estimates January 2002 with December 2003 and March 2002 with of cover may add to values greater than 100%. March 2004 were the pair-wise comparisons interpreted in Species richness (S) and diversity (H0) were estimated for the analyses. each sample. Diversity was calculated using the Shannon- In the first experiment, S. muticum was omitted from the Weaver index (H0): data set to check if the possible differences between treatments were caused not by the presence of this species, but by changes 0 S H ¼ pi  log2 pi in the remaining assemblage. Moreover, the same analysis was also performed omitting the most abundant species (B. bifur- where pi is the proportion of total macroalgal cover of the ith species. cata, G. spinosum, and S. muticum). Because G. spinosum seems to be one of the most affected Two-way crossed analysis of similarity (ANOSIM) (Clarke species since the arrival of S. muticum (Sa´nchez et al. 2005), we 1993) (on square root transformed cover data) was used to test also estimated Gelidium biomass from percentage cover data for differences between time and experimental manipulation, and mean length (Dudgeon et al.
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