First report of the Japanese red alga Antithamnion nipponicum ( Ceramiales , Rhodophyta ) in Norway , an invasive species new to northern Europe

The red alga Antithamnion nipponicum was discovered on the west coast of Norway, south of Bergen in 2007. From its native range in Japan and Korea the alga was first introduced to the Mediterranean Sea in 1988. Except for a possible report from the Azores (as A. pectinatum) there are no published records from European Atlantic coasts. The introduction to Norway most likely occurred via fouling on ship hulls, or by ballast water. Vegetative and tetrasporangium-bearing plants were found, and the specimens conform to the detailed description recently published by Cho et al. (2005), based on material from Pacific and Atlantic coasts of North America where the alga is also a recent introduction.

In a recent paper Cho et al. (2005) give detailed analyses of Antithamnion nipponicum Yamada et Inagaki and some related taxa based on morphological and molecular data.A. nipponicum was first described from Japan and is also known from Korea.Verlaque and Riouall (1989) reported this alga for the first time in Europe from the Thau Lagoon in (France, a hot spot of marine species introductions in Europe (Verlaque 2001).Later finds of a similar alga from the Azores (Athanasiadis and Tittley 1994) were classified as Antithamnion pectinatum (Montagne) Brauner, a species described from New Zealand, with A. nipponicum reduced to synonymy (with a question mark).Subsequent reports of the alga from Venice Lagoon, Italy were referred to as A. pectinatum (Curiel et al. 1996(Curiel et al. , 1998)), but as shown by Cho et al. (2005), after examination of type material, A. pectinatum should be considered as a separate, valid southern hemisphere species, distinct from A. nipponicum.This suggests that reports of A. pectinatum from Europe could represent A. nipponicum, and that the alga is a recent introduction from Japan that has spread to the Mediterranean Sea and the Azores.The distribution also includes the Pacific coast of California and recently also the American east coast (Cho et al. 2005).This distribution conforms to the well-known trend of invasive marine organisms that have colonized the Atlantic Ocean and the Mediterranean Sea from Pacific NE Asia.According to Antonio Secilla (pers.comm.), the alga in question was recently discovered near the harbor of Bilbao, on the Atlantic coast of northern Spain.
We here report on the discovery of A. nipponicum from the Norwegian west coast, a find that greatly extends the geographical range in Europe.The alga may have spread unnoticed along the Atlantic coasts of Europe, or it may have been introduced via shipping from more remote populations.
The Norwegian specimens of A. nipponicum were discovered during a Nordic field course in phycology held in September 2007 at Espeland Marine Biological Station south of Bergen, Norway.Samples came from an exposed locality (Store Kalsøy 60°06'N, 05°03'E) where A. nipponicum grew as an epiphyte on Corallina officinalis and Laminaria sp. at lower intertidal and upper subtidal levels.Re-examination of a previous collection of an antithamnioid alga from the same site (from a rock pool at Store Kalsøy, 17 April 2007) confirmed that these specimens belonged to the same species.Only vegetative plants were recorded in April, whereas both vegetative and tetrasporangiumbearing plants were found in September.Unialgal cultures were established from apical cuttings and are kept at the University of Oslo.Tetrasporangia were produced after ca. 3 weeks in culture.The thallus consisted of prostrate and erect, bright red axes, 10 -15 mm high (Figure 1 A).The prostrate axes were attached to the substratum by 2-5 celled uniseriate rhizoids ending in a disc.Rhizoids (15-17 µm in diameter) are formed from the basal cells of pinnae (terminology according to Wollaston and Womersley 1998) both in creeping and erect axes (Figure 1 F).By this means, thallus fragments may easily reattach and thereby facilitate vegetative reproduction and the spread of the alga, as seen in culture.
Axes bear pairs of opposite pinnae composed of 10-13 cylindrical cells (rachis cells).These are 3-4 x longer than broad, and distinctly differ in this from the smaller and isodiametric basal cells (coxal cells) that are from 12 to 25 µm in their greatest dimension.Pinnules are produced in opposite pairs on the first 3-5 cells and with 2-3 more branches on the next cells on the abaxial side (Figure 1 C).The terminal cells of pinnules are pointed, 5-7 x 12-14 µm.Secondary lateral branches are formed from basal cells of pinnae at irregular intervals on upright axes (Figure 1F).Tetrasporangia were recorded in September.They arise singly on the lower pinnule cells and measure 50 x 65 µm when mature and are cruciately divided (Figure 1 E).Sexual reproductive structures have so far not been seen in Norwegian populations.Gland cells are common and ovate, ca.20 µm long and 10-12.5 µm broad.They are formed on shorter or longer pinnules, always covering the adaxial face of two cells (Figure 1 D).In this respect the alga somewhat resembles Antithamnion cruciatum (C.Agardh) Nägeli, but in the latter species gland cells are formed on reduced branchlets 3-4 cells in length and usually covering three cells.Another feature that is reminiscent of A. cruciatum is the densely tufted apices formed by closely packed pairs of opposite pinnae.Antithamnion densum (Suhr) Howe is a species that is considered introduced to European coasts from southern Atlantic (type locality Peru) and so far recorded as far north as the Brittany coast of France and off the west coast of Ireland (Maggs and Hommersand 1993).It resembles A. nipponicum in having gland cells covering part of two adjacent cells, but differs in branching pattern with pinnulae born adaxially in unilateral series.Despite its small size, A. nipponicum is well characterized morphologically and is not easily confused with any other antithamnioid algae known from Scandinavian waters.Antithamnionella ternifolia (Hooker et Harvey) Lyle and A. spirographidis Sciffner are both introduced into the NE Atlantic from other parts of the world and are known to have spread in European waters (Maggs and Stegenga 1999), but have so far not been recorded in Norway.Both species have gland cells which, in contrast to A. nipponicum, cover only one cell.A. ternifolia has small isodiametric basal cells of pinnae like A. nipponicum, whereas in A. spirographidis the basal cell is cylindrical and equal in length to next cell.
The disccovery of A. nipponicum on the Norwegian west coast is not unexpected in view of the "globalisation" in marine ecosystems (Streftaris et al. 2005) and the increasing number of crude oil carriers arriving at harbors on the Norwegian west coast.Most of the introduced macroalgae have probably spread from primary or secondary introduction sites in other parts of Europe.Examples of recently introduced red algae in the Norwegian flora include Heterosiphonia japonica (Bjaerke andRueness 2004, Husa andSjøtun 2006), Neosiphonia harveyi and Aglaothamnion halliae (Bjaerke 2004).Biological features of species that may favor the success of introduced red algae include effective clonal reproduction by fragmentation and the presence of anti-grazing secondary metabolites.The gland cells of Antithamnion and many other red algae contain halogenated compounds that may act as grazing deterrents.
The disccovery of A. nipponicum on the Norwegian west coast is not unexpected in view of the "globalisation" in marine ecosystems (Streftaris et al. 2005) and the increasing number of crude oil carriers arriving at harbors on the Norwegian west coast.Most of the introduced macroalgae have probably spread from primary or secondary introduction sites in other parts of Europe.Examples of recently introduced red algae in the Norwegian flora include Heterosiphonia japonica (Bjaerke andRueness 2004, Husa andSjøtun 2006), Neosiphonia harveyi and Aglaothamnion halliae (Bjaerke 2004).Biological features of species that may favor the success of introduced red algae include effective clonal reproduction by fragmentation and the presence of anti-grazing secondary metabolites.The gland cells of Antithamnion and many other red algae contain halogenated compounds that may act as grazing deterrents.