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Origin of Fucus Serratus (Heterokontophyta; Fucaceae) Populations in Iceland and the Faroes: a Microsatellite-Based Assessment

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Origin of Fucus Serratus (Heterokontophyta; Fucaceae) Populations in Iceland and the Faroes: a Microsatellite-Based Assessment Eur. J. Phycol. (2006), 41(2): 235–246 Origin of Fucus serratus (Heterokontophyta; Fucaceae) populations in Iceland and the Faroes: a microsatellite-based assessment J. A. COYER1, G. HOARAU1, M. SKAGE2, W. T. STAM1 AND J. L. OLSEN1 1Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands 2Department of Biology, University of Bergen, 5007 Bergen, Norway (Received 13 October 2005; accepted 22 February 2006) The common intertidal seaweed Fucus serratus was almost certainly introduced to Iceland and the Faroes by humans from Europe, as previous genetic studies have confirmed that life-history constraints preclude long-distance dispersal. Introduction must have occurred sometime in the 1,000 years between arrival of the first Icelandic settlers c. 900 AD and when the species was first noted in a phycological survey in 1900. We genotyped 19 populations from throughout northern Europe, Iceland, and the Faroes with seven microsatellite loci in order to identify the source or sources of the Icelandic/Faroese populations. Assignment tests indicated that the Sma˚skjaer area of the Oslofjorden in Norway was the source for the Icelandic populations and the Hafnarfjo¨ rôur area of Iceland was the likely source for the single Faroese population. The time of introduction to Iceland was probably during the 19th century, whereas introduction to the Faroes occurred during the late 20th century. Additionally, molecular data verified hybridization between the introduced F. serratus and the native F. evanescens. Key words: Fucus serratus, hybridization, Iceland, species introductions, seaweeds, the Faroes Introduction biological surveys in the mid-1800s was largely Recent introductions of marine species due to the a result of post-glaciation colonization, and that it shipping and fisheries activities of human societies was only after the surveys that novel species were continue to be a widely discussed topic. With the noted and attributed to human-induced introduc- heightened awareness of the extent and effect of tions. In reality, however, extensive maritime contemporary introductions, it is easy to forget activities existed along the northeastern Atlantic that marine species have been transported from coast for many centuries before the first biological one area to another, on or in the hulls of wooden surveys, and marine species undoubtedly were ships and their rock or sand ballast, for centuries routinely transported via the wooden hulls, rock or millennia before the first biological surveys ballast, or packing materials. began in the mid-1800s (Carlton, 1999; 2003). Maritime activities between northern Europe Indeed, the long history of species introductions and the central North Atlantic islands (Iceland, facilitated by human maritime activities almost the Faroes, Greenland) effectively began with the certainly has clouded present worldwide views of Norse Vikings in the late 800s. Travel among the coastal marine ecology, biodiversity, and biogeo- islands, and between the islands and Norway, graphy (Carlton, 2000, 2003; Jackson, 2001; continued through the 1300s, preceding the Steneck & Carlton, 2001). sequential activities of English, German, and The North Atlantic Ocean is one area in which Danish traders from the 1400s to the 1700s the coastal marine communities are often a blurred (Karlsson, 2000; Byock, 2001; Jones, 2001). mixture of species that have colonized naturally Additionally, as the need for fish in Catholic and those that have been introduced by humans. Europe developed in the mid-1300s, innumerable As Carlton (2003) has noted, it is often assumed fishing vessels began to journey between coastal that the species composition of marine commu- European countries and the fishing grounds off the nities in the North Atlantic before the advent of central islands (particularly Iceland), as well as to the eastern North American coast (particularly Correspondence to: J. A. Coyer. e-mail: [email protected] Newfoundland; Lindroth, 1957; Buckland, 1988; ISSN 0967-0262 print/ISSN 1469-4433 online/06/020235–246 ß 2006 British Phycological Society DOI: 10.1080/09670260600652820 J. A. Coyer et al. 236 Karlsson, 2000). Consequently, numerous avenues and Shetlands (Lu¨ ning, 1990; Hardy & Guiry, and mechanisms existed for human-induced intro- 2003). It was accidentally introduced to the north- ductions of marine species throughout the North western Atlantic (Nova Scotia) in the late 1880s Atlantic well before the ‘‘benchmark’’ biological (Hay & MacKay, 1887; Robinson, 1903; Edelstein surveys of the mid-1800s. et al., 1971–73). The species also is a dominant Marine macroalgae are easily transported from member of the intertidal community along c. one area to another by shipping or fisheries. 100 km of southwestern Iceland and offshore Historically, the most common method probably Heimaey, as well as in a single fjord in the was via rock ballast. For example, the type of Faroes (Trongisva´ gsfjørôur on the southernmost Viking ship (kno¨rr) widely used for transit between island of Suôuroy; Bruntse et al., 1999; Iceland and Norway required 16 tons of ballast Gunnarsson & Jo´ nsson, 2002). Collection records stones or weighted cargo (Buckland & Sadler, indicate that it was present off Iceland and the 1990) and algal species could have survived for Faroes before 1900, although the record from the several days in the damp holds while attached to Faroes is highly doubtful (Jo´ nsson, 1903; Bruntse the ballast, assuming that the ballast was collected et al., 1999). from intertidal or shallow subtidal habitats. Given its life history characteristics, it is almost Seaweeds have also been used as fodder for sheep certain that F. serratus was introduced to Iceland and cattle in the Icelandic settlements (Amorosi and the Faroes by humans. It is dioecious, et al., 1998 and references therein) and it is perennial (3–4 years), and reproduces sexually reasonable to expect that seaweeds were used to (annually) with no vegetative reproduction, either sustain livestock during the several-day transit via holdfast sprouting or vegetative propagules from Scandinavia to Iceland/the Faroes in the (Malm et al., 2001). Dispersal of eggs is restricted open-decked knerrir. Contemporary methods of to within 1–2 m of the parent (Arrontes, 1993), introduction include the use of seaweed as packing although distances >6 m are possible, as have been material for invertebrate fisheries, microscopic life reported for F. vesiculosus and the related genus, stages accompanying oysters as they are shipped Ascophyllum (Serra˜o et al., 1997; Dudgeon et al., worldwide, and entanglement of reproductive 2001; Engel et al., 2005). The genetic consequences fragments in fishing gear (reviewed in Siguan, of low dispersal were demonstrated in a recent 2003; Miller et al., 2004 and references therein). population genetic study showing that the panmic- Well-studied examples of recent (<50 years ago) tic unit for F. serratus was between 0.5 and 2 km macroalgal introductions include the large brown (Coyer et al., 2003). Dispersal is further limited algae Undaria pinnatifida and Sargassum muticum because: (i) the egg-produced pheromones effec- and the green algae Codium fragile subsp. tomen- tively attract sperm only within distances of tosoides and Caulerpa taxifolia (reviewed in Walker micrometers to millimeters (Serra˜o et al., 1996); & Kendrick, 1998; Siguan, 2003; see also, Jousson (ii) nearly 100% fertilization success of gametes et al., 1998; Trowbridge & Todd, 1999a, b; is possible only when release occurs during Meusnier et al., 2002; Thornber et al., 2004; calm water conditions (Pearson & Brawley, 1996; Provan et al., 2005; Voisin et al., 2005). Two Serra˜o et al., 1996; Pearson et al., 1998); and (iii) examples of older introductions (>100 years ago) fertilization success decreases rapidly with increas- are Fucus evanescens and F. serratus, both of which ing water motion (Pennington, 1985; Denny & are major components of rocky intertidal com- Shibata, 1989; Levitan et al., 1992), which munities on North Atlantic shores. The former is obviously separates the gametes and negates the a circumpolar species, occurring in the North influence of pheromones. Because thalli lack Pacific, as well as off northeastern North flotation vesicles, they sink when detached, so America, Greenland, Spitzbergen, Iceland, and that open ocean rafting between either Iceland or northwestern Norway (Powell, 1957; Lu¨ ning, the Faroes from Northern Europe is unlikely 1990). It was accidentally introduced into the because of: (i) the distance (300 km from the Oslofjorden (southeastern Norway) in the mid- British Isles to the Faroes; 400 km from the 1890s and expanded to southern Sweden by 1966 Faroes to Iceland; 900 km from Iceland to and the western Baltic by 1992 (Schueller & Peters, Norway); (ii) depths (>500 m); and (iii) the 1994; Wikstro¨ m et al., 2002). Furthermore, prevailing west-to-east flowing Gulf Stream. F. evanescens has hybridized extensively with Additionally, F. serratus has never been recorded the native F. serratus in the Blushøj region on from Greenland (Jo´ nsson, 1912; Lund, 1959; Denmark’s Kattegat coast (Coyer et al., 2002a). Pedersen, 1976), a straight-line distance of 600 km The closely related F. serratus is a northeastern from its present distribution in southwestern Atlantic species, ranging from the northern Iberian Iceland. Peninsula to the White Sea and into the Kattegat/ A recent microsatellite-based
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