A Global Review of the Distribution, Taxonomy, and Impacts of Introduced Seaweeds

We reviewed over 407 global seaweed introduction events and have increased the total number of introduced seaweed species to 277. Using binomial tests we show that several algal families contain more successful invaders than would be expected by chance, highlighting groups that should be targeted for management. Hull-fouling and aquaculture are the most significant sources of seaweed invaders and should be carefully regulated. The ecological effects of introduced seaweeds have been studied in only 6% of the species, but these studies show mostly negative effects or changes to the native biota. Herbivores generally prefer native to introduced seaweeds, and are unlikely to control spread, as they can do in other habitats. Undisturbed marine communities can be at least initially resistant to most introduced seaweeds aside from the siphonous green species; however, disturbances and eutrophication can facilitate invasion. Major research gaps include community-level ecological studies and economic assessments. 327 First published online as a Review in Advance on August 8, 2007 A nn u. R ev . E co l. E vo l. Sy st . 2 00 7. 38 . D ow nl oa de d fr om a rj ou rn al s. an nu al re vi ew s. or g by U ni ve rs ity o f C al if or ni a Sa nt a B ar ab ar a on 1 1/ 27 /0 7. F or p er so na l u se o nl y. ANRV328-ES38-14 ARI 31 July 2007 20:27 Invader: a species that colonizes a region outside its natural biogeographical distribution Invasive: a condition whereby a species becomes excessively abundant usually causing ecological or economic harm Introduced seaweed: a species in the Phyla Charophyta, Chlorophyta, Ochrophyta, or Rhodophyta introduced beyond its native range by human activities, and successfully established “Considering our present knowledge it will be many years before we will be able to predict with any degree of certainty the effects an introduced species may have on an existing ecosystem.” Phycologist L. Druehl in a letter to Science (Druehl 1973) predicting the establishment of Sargassum muticum in the eastern Atlantic after Japanese oysters were introduced from British Columbia to France. INTRODUCTION AND SCOPE OF REVIEW Seaweeds make a substantial contribution to marine primary production and provide habitat for nearshore benthic communities (Mann 1973). Over 200 seaweed species support an international economy in primarily phycocolloid (algins, agars, and carrageenans) and food products valued at over U.S. $6.2 billion (Zemke-White & Ohno 1999). Seaweed production has more than doubled over the past two decades. Through human activities including aquaculture, seaweeds have been introduced to non-native locations around the world. Excellent reviews on seaweed introductions have been recently published (Inderjit et al. 2006, Ribera & Boudouresque 1995, Ribera Siguan 2003, Schaffelke et al. 2006, Trowbridge 2006) as have case histories on specific species (Chapman 1998, Mathieson et al. 2003, Meinesz 1999). Regional reviews and checklists help document the arrival of new invaders into specific locations (Boudouresque & Verlaque 2002a, Castilla et al. 2005, Maggs & Stegenga 1999, Orensanz et al. 2002, Ribera Siguan 2002). The Global Invasive Species Database (http://www.issg.org/database) of the International Union for the Conservation of Nature (IUCN) provides extensive data (native/introduced ranges, references) on introduced seaweeds. Our objective was to update and integrate the known information on global seaweed introductions and their ecological effects. Specifically we quantitatively assessed (a) the taxonomic affinities of introduced seaweeds, (b) their morphological characteristics (functional groups), (c) the native and introduced ranges of seaweed invaders, (d ) the vectors of introduction, and (e) the ecological effects of introduced seaweeds on native biota and vice versa. Details of the physiology, molecular evidence of biogeographic affinities, economic impacts, and management of introduced seaweeds were beyond the scope of this review. CLASSIFICATION AND ANALYSIS We define an introduced seaweed (or invader) as a species belonging to the Phyla Charophyta, Chlorophyta, Ochrophyta (formerly Phaeophyta) or Rhodophyta that has been introduced beyond its native range through human activities and has become successfully established in the new locale. Information on each unique introduction was compiled from published scientific literature, books, and Algaebase (Guiry & Guiry 2007) and is shown in Supplemental Table 1 (follow the Supplemental Material link from the Annual Reviews home page at http://www.annualreviews.org/). Taxonomic information included basic classification using the nomenclature accepted by Algaebase (Guiry & Guiry 2007) on February 2, 2007. Functional group categories 328 Williams · Smith A nn u. R ev . E co l. E vo l. Sy st . 2 00 7. 38 . D ow nl oa de d fr om a rj ou rn al s. an nu al re vi ew s. or g by U ni ve rs ity o f C al if or ni a Sa nt a B ar ab ar a on 1 1/ 27 /0 7. F or p er so na l u se o nl y. ANRV328-ES38-14 ARI 31 July 2007 20:27 Crustose: an alga exhibiting a crust—like morphology that tightly adheres to the substratum and can be fleshy or calcified Corticated: algal morphology consisting of multiple cell layers, most regularly an outer pigmented cortical layer and an inner unpigmented medualary layer Macrophyte: a macroscopic alga (seaweed) were assigned to each species after Steneck & Dethier (1994) and included filamentous, crustose, corticated foliose, corticated macrophyte, leathery macrophyte, articulated calcareous, and sipohonous (a unique category for the Bryopsidales, see Vroom & Smith 2001). Vector of Introduction The vector for each unique introduction was recorded as reported in the literature using the following designations (Ruiz et al. 2000): unreported (no clear indication of mechanism), aquarium introductions (release of aquarium organisms into the wild), aquaculture (the intentional introduction of algae for cultivation), shellfish farming (the introduction of algae growing on or associated with cultured shellfish), ballast (propagules transported within ballast water or attached to ballast rocks), hull fouling (species attached to oceanic vessels), fishing gear, research, and “lessespian” immigrants (species that migrated through the Suez Canal since 1869). Native and Introduced Ranges The native distributional range for each introduced seaweed was recorded as reported in Algaebase (Guiry & Guiry 2007). To assess global patterns, broad geographic regions were defined as follows: NE, NW, SE, SW, and central Atlantic and Pacific oceans; Caribbean; Australia and New Zealand; Mediterranean; Indian; Antarctic; Arctic; and the Black and Caspian Seas. Each introduction to a new region was entered as a separate entry in Supplemental Table 1 [e.g., Caulerpa taxifolia has been introduced to three regions: the Mediterranean, California (NE Pacific), and Australia]. However, species that have secondarily spread to states or countries within a region were only recorded once. Analyses and Data Summary We used the total number of unique seaweed introductions (where species may be counted more than once) for most of our analyses. However, for all questions related to the taxonomic affiliation of invaders, the total number of species was used. Because taxonomy has been shown to be a useful predictor for identifying potential invaders (flowering plants, Daehler 1998; and birds, Lockwood 1999), we tested whether certain algal families contained more introduced species than would be expected by chance. We used the binomial distribution to generate an expected number of invaders per family for all groups containing invaders. The number of species (n) in each family was taken from Algaebase (Guiry & Guiry 2007). The expected proportion ( p) of invaders was calculated by summing the total number of invaders and dividing by the total number of known marine algal species. The probability of obtaining a value equal to the observed (X) or more extreme than the observed (both higher and lower) was calculated using a two-tailed binomial test (Zar 1999) using www.annualreviews.org • Introduced Seaweeds 329 A nn u. R ev . E co l. E vo l. Sy st . 2 00 7. 38 . D ow nl oa de d fr om a rj ou rn al s. an nu al re vi ew s. or g by U ni ve rs ity o f C al if or ni a Sa nt a B ar ab ar a on 1 1/ 27 /0 7. F or p er so na l u se o nl y. ANRV328-ES38-14 ARI 31 July 2007 20:27 the following equation: R = (n!/X !(n − X )!)pxq n-x where n is family size, X is the number of observed invaders per group, p is the proportion of species expected to be invasive and q = 1 − p. Within each family the cumulative two-tailed R value was then considered significant if it was <0.05 and marginally significant if it was <0.1 (arbitrary adjustments for multiple tests were not performed). Another database for ecological effects was compiled using data from studies published in primarily international scientific journals, excluding proceedings and reports owing to their uncertain peer review. We separated studies into observational (lacking statistical analysis, limited comparisons, models, calculations), mensurative, or experimental categories. Mensurative and experimental studies included a replicated statistical design; experimental studies involved manipulations of native organisms and/or the introduced seaweed. Response variables were sorted into abundance, diversity, community structure (relative abundances), community function (primary productivity, nitrogen fixation), individual performance (survival, growth, reproduction, size), and feeding response (preference of introduced seaweed relative to native as food source or foraging habitat). We accepted the peer-reviewed statistical results if the effect could be categorized as changed (community structure), negative (lower compared to preintroduction or to native biota), no effect, or enhanced (higher relative to preintroduction or native biota) at alpha = 0.05. “Case” refers to a singleresponse variable in a single study. RESULTS We estimate that the global number of introduced seaweed species is 277, increasing the previous estimates from recent reviews by at least 27 species (Ribera Siguan 2003, Schaffelke et al. 2006, Trowbridge 2006), with a total of 408 unique introductions (some species have been introduced to multiple regions) (see Supplemental Table 1). The taxonomic distribution of introduced seaweeds includes 165 Rhodophytes (red algae), 66 Ochrophytes (brown algae), 45 Chlorophytes (green algae) and 1 Charophyte. Some groups, specifically larger families, have many more invaders than others (Figure 1a–1c), and in fact family size was positively correlated with invader number (Figure 1d ). These results suggest that there may simply be proportional −−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→ Figure 1 The total number of species and the number of introduced species in a given family for (a) Chlorophytes, (b) Ochrophytes and (c) Rhodophytes. Bold + or – symbols designate families with significantly more ( p < 0.05) or fewer introduced species than would be expected by chance, respectively, based on Binomial probability, whereas nonbold symbols show marginal significance at p < 0.1, respectively. (d ) Pearson correlation between family size and invader number. (∗These estimates are likely high as the number that was used to calculate the expected number of invaders included some freshwater species.) 330 Williams · Smith A nn u. R ev . E co l. E vo l. Sy st . 2 00 7. 38 . D ow nl oa de d fr om a rj ou rn al s. an nu al re vi ew s. or g by U ni ve rs ity o f C al if or ni a Sa nt a B ar ab ar a on 1 1/ 27 /0 7. F or p er so na l u se o nl y. ANRV328-ES38-14 ARI 31 July 2007 20:27