Distribution pattern of the green alga Codium fragile ( Suringar ) Hariot , 1889 in its native range , Korea

The examination of native habitats of newly introduced species is one of the factors that can provide information for predicting and preventing invasion success. In this study, we investigated the distribution patterns of a green macroalga, Codium fragile, in its native range in Korea. There were two distinct patterns for Codium spp. within their native habitat. In undisturbed communities, Codium species were members of the understory assemblage below the dominant canopy species. In disturbed habitats where native algae have been harvested for food, the activity created major gaps in the community structure where opportunistic algae expanded their abundance within the community. Codium fragile not only becomes a dominant canopy species in disturbed habitats, but it also colonizes new habitats such as fouling communities. Thus, the distribution patterns of Codium fragile in its native range suggests that it has the capability of taking advantage of disturbed habitats, which may help to explain why it has been such a successful invader in other regions of the world. One interesting finding was the lack of specialized sacoglossan herbivores associated with the Korean populations studied while such herbivores do feed on introduced populations in other regions, and may limit their distribution at some locations.


Introduction
Factors influencing the successful establishment of invasive species are complex and poorly known (Carlton 1979).However, increasing numbers of studies are being conducted that identify and elucidate the factors causing the spread of invaders by emphasizing propagule pressure, suitability of habitat, and previous success in other invasions (Williamson 1996).Other factors have also been suggested as predictors of invasion success; these include (1) the intrinsic rate of natural increase, (2) reproductive and genetic characteristics, (3) abundance and range in native habitat, (4) taxonomic isolation, (5) climatic matching, and (6) vacant niche and ancestral habitat (Williamson 1996).Examination of native habitats may generate interesting information for the prediction of invasion success, yet few such studies have been conducted in marine invasive species (Lohrer et al. 2000a, b).
Subspecies tomentosoides of the green macroalga, Codium fragile (Suringar) Hariot, 1889, has been of interest over the years because its subspecies have successful invasion of many temperate habitats in both the Northern and Southern Hemispheres (Silva 1955, 1957, 1979, Fralick and Mathieson 1972, Carlton and Scanlon 1985, Trowbridge 1995, 1998, Trowbridge and Todd 1999a, b, Chapman 1999, Scheibling and Anthony 2001, Harris and Mathieson 2000, Hubbard and Garbary 2002).The center of Codium fragile distribution is assumed to be in East Asia, where the species is highly variable (Silva 1955, Goff et al. 1992, Provan et al. 2005).From western scientists' perspectives, Codium fragile has six subspecies, with three of them being considered weeds in several parts of the world (Silva 1955, 1957, Goff et al. 1992, Trowbridge 1998, 1999).However, in Japan and Korea, C. fragile has been considered a single species with no subspecies (Kang 1966, Lee and Kang 1986, Oh et al. 1987, Segawa 1996).Compared to other subspecies, the subspecies tomentosoides has received more attention because of its rapid spread in the NE and NW Atlantic, Australian and New Zealand ecosystems (Carlton and Scanlon 1985, Trowbridge 1995, 1998, 1999, Chapman 1999).In the Gulf of Maine, C. fragile ssp.tomentosoides has recently become a dominant member of benthic communities (Harris and Mathieson 2000, Harris and Tyrrell 2001, Levin et al. 2002), and is continuing to spread (Mathieson et al. 2003).This invasive alga was first observed at the Isles of Shoals, off the New Hampshire coast, in 1982 (Carlton and Scanlon 1985), and now has been successfully established in areas that were previously dominated by native kelps and overgrazed by sea urchins (Prince 1988, Prince and LeBlanc 1992, Harris and Mathieson 2000, Harris and Tyrrell 2001, Levin et al. 2002).Vacant niches due to overfishing of native sea urchins and community disturbance may facilitate the spreading of this green alga in the Gulf of Maine (Harris andTyrrell 2001, Levin et al. 2002).The spread of C. fragile ssp.tomentosoides has resulted in major changes in community composition and function in the invaded areas (Harris and Mathieson 2000, Harris and Tyrrell 2001, Chavanich and Harris 2004).
To predict and prevent the establishment and spread of invasive species, knowledge of the ecology of a species in its native range can be very important.The purpose of this study was to examine the distribution patterns of Codium fragile within the community structure of two different native habitats in Korea.One habitat was located within a marine protected area, while the second location was exposed to intensive harvesting of native algal species.In addition, Codium species were surveyed for epibionts and potential herbivores.

Study area
Sampling within the native range of Codium fragile was conducted at three locations in the southern part of Korea.Two locations, Munsom and Supsom Islets were located adjacent to Cheju Island, whereas the third site was in Tongyong (Figure 1, Annex 1).The difference among the three study sites is that Munsom and Supsom are within marine reserves, while Tongyong is opened to harvesting and several algal species particular kelps and invertebrate species have been overexploited (personal observations).All locations are moderately exposed to wave action from storms.

Field surveys
To document the distribution patterns of the native habitat of Codium fragile, three types of data were collected via field surveys using SCUBA.Direct counts of canopy species were made using a quadrat (0.5 m x 0.5 m).Photographic sampling was also done using a Sea & Sea MX 10 underwater camera and YS-40A electronic flash to document the understory composition.Algal samples were also collected for species identification and to survey for epibiont densities and composition on Codium spp.All field work was performed during June to August, 2000 when water temperatures averaged 20-25 degrees C.
At each site, the surveys were made at three different depths (-4, -9, -18 m below the mean seawater level), except at Tongyong where the bottom becomes silt and mud below 9 m and Codium was absent in that zone.Therefore, only -3, -6 and -9 m depths were surveyed at Tongyong.At each depth, 10 replicate quadrats were placed randomly and densities of canopy species were recorded.To determine percent cover of understory species, 15 photographs were taken randomly at each depth.Each photo quadrat was approximately 0.25 x 0.25 m 2 in area.Percent coverage of algae was quantified by projecting the images onto a grid and counting the presence of algae under 100 dots.To document fauna associated with members of the genus Codium, five plants of each species of Codium were collected randomly at different depths in each location.The whole plants and trapped benthic organisms were covered with plastic bags and removed from the substratum.The bags were tied shut and returned to the Korea Ocean Research and Development Institute (KORDI) for later counting and species identification.In the laboratory, macrofauna were removed from the algae, fixed in 75% ethanol and identified to species.The Codium plants were then blotted, dried, and weighed for calculating densities of epibionts per gram of algal dry weight

Statistical analysis
Paired t-tests were used to examine differences between average densities of associated macrofauna on each Codium species.Tests were done using Systat 7.0 (Systat 1997).

Codium distribution
Codium fragile occurred at all three locations.At Munsom and Supsom, where there is a high diversity of algae, C. fragile was present only as an understory species (Figures 2-4, Annex 2).The canopy species were Sargassum filicinum, S. serratifolium and Ecklonia cava and there was a pattern of increasing percent of Ecklonia cava with depth (Figure 3, Annex 2).At four meters, Sargassum spp.comprised over 50% of the population, but they had dropped to less than 20% of the canopy composition by nine meters, with Ecklonia cava representing the remaining 80% (Figure 3).Three other Codium species, in addition to C. fragile, were present at Munsom and Supsom as understory species (Annex 2).Those species were Codium minus, C. adhaerens and C. cylindricum.The most common understory species were arborescent red algal turf species and crustose coralline algae, which occupied more than 80% coverage at four and nine meters while unconsolidated sediments became the dominant substrate type at 18 m (Figure 4).There was also a pattern between increased depth and the percent cover of green algal species at Munsom and Supsom (Figure 4).At Tongyong, Codium fragile inhabited both the subtidal sites, and was also found growing as a fouling organism on floating docks and pilings (Annex 2).Overall, the diversity of algal species was very low (Annex 2).All common algal species occurred at all depths (Annex 2).Codium fragile was the dominant canopy species at all depths and it increased its density and percent cover with depth (Figure 3).More than 80% of the understory algae were composed of the green alga Ulva pertusa and less than 20% were red algae, of which Polysiphonia spp.were most common (Figure 4).Codium cylindricum was also found in this area but at low densities and it occurred as a member of the understory (Annex 2).

Macrofauna associated with Codium species
Macrofauna were found on almost all Codium species, except for C. cylindricum at Supsom (Figure 5).Six species of arthropods and five species of molluscs were found associated with Codium species (Annex 3).There were differences in species richness on different Codium species (Figure 5).C. fragile at Tongyong had the highest number of associated fauna (6 species), followed by C. fragile at Munsom (3 species) and C. adhaerens at Supsom (3 species).No fauna was found associated with C. cylindricum.Also, no members of the Sacoglossa (Opisthobranchia, Gastropoda), which are specialist herbivores on siphonaceous green algae, were collected during this study.The dominant macrofauna were gastropods and amphipods (Figure 6).The density of gastropods and amphipods differed significantly in each Codium species (Figure 6).At Supsom and Munsom, the density of amphipods on each Codium species was higher than that of gastropods, except on C. adhaerens at Supsom, while at Tongyong, the density of gastropods was higher (Figure 6).Although the composition of associated macrofauna varied among sites, amphipods were typically the most common animals associated with Codium species.The most abundant amphipod species at Munsom and Supsom was Ampithoe valida shimizuensis (60% of total number of amphipods), whereas at Tongyong, the higher number of A. valida shimizuensis and Caprella penatis were found (50% and 36.36% of total number of amphipods, respectively) (Annex 3).A herbivorous gastropod, Tristichotrochus unicus, also occurred at high density on Codium fragile at Tongyong (58.3% of total number gastropods) (Figure 6, Annex 3).Other species, including crabs, shrimps and bivalves were present in very low numbers.

Discussion
This study focused on the distribution patterns of Codium fragile in its native habitat in Korea.From field surveys, two distinct communities were observed at the sites selected.Munsom and Supsom, located in a marine protected area had a high diversity of algal species and the dominant canopy species were the brown algae Sargassum spp.and Ecklonia cava (Figure 3, Annex 2).All four Codium species were present as understory species and coexisted with other algal species in the same communities.At Tongyong, the algal diversity was low and the green algae C. fragile and Ulva pertusa were the dominant canopy and understory species respectively (Figure 3, Annex 2).Over the past several years, some algal canopy species particular kelps and macroinvertebrates have been overharvested for food in Tongyong, which has led to communities dominated by a canopy of the green alga C. fragile instead of the historical dominance by the brown algae Sargassum spp.
(personal observations).This study documents two distinct patterns for Codium fragile within its native habitat.In undisturbed communities (Munsom and Supsom), Codium plays a subordinate role as member of the understory assemblage below the dominant canopy species.In disturbed habitats, where several native algal species such as Sargassum spp.and Ecklonia have been harvested for food, the activity creates large areas of unoccupied habitat where opportunistic algae such as C. fragile can become a dominant species.Williamson (1996) suggested that the removal of native species from habitats creates a vacuum that facilitates the successful colonization by introduced species, especially those species that have the ability to take advantage of such openings.It is interesting that only Codium fragile of the four endemic species of Codium demonstrated the ability to greatly expand its niche, when overharvesting of dominant algal species created the vacuum in the sites studied.C. fragile not only increased its density and role in the benthic communities, but it also colonized novel substrates like floating docks and pilings.Similarly, overharvesting of urchins in the Gulf of Maine appears to have favored the colonization and expansion to dominance of Codium fragile ssp.tomentosoides in the Gulf of Maine (Harris and Mathieson 2000, Harris and Tyrrell 2001, Levin et al. 2002) and elsewhere in the North Atlantic region (Chapman 1999).Codium fragile in Tongyong (Figure 3) and in parts of the Gulf of Maine (Harris and Tyrrell 2001) showed a similar pattern of becoming the dominant canopy species, which provides an alternate community state to the historical climax community in each location.Consequently, changes in community structure and composition, such as in the Gulf of Maine, have affected other native species by shifting habitat selection and feeding behaviors (Chavanich 2001, Chavanich and Harris 2004, Harris and Jones 2005).
A second possible related factor besides the overharvesting of dominant seaweeds at Tongyong may be the resulting of low algal diversity.The open space and reduced competetion from competitive dominants are likely to function synergistically to favor a species like Codium fragile with flexible growth potential and habitat requirements.In high diversity habitats with low disturbance, such as Munsom and Supsom, C. fragile is restricted to the role of understory species, similar to the three other Codium species.At Tongyong, Codium fragile responds to the intense disturbance by expanding its size to become the dominant canopy species (Figure 3), and its habitat selection to colonize new habitats.It has been suggested that communities with high species richness tend to have resistance against the invasion of nonindigenous species (Trowbridge 1995, Williamson 1996, Stohlgren et al. 1999, Levine 2000).On the other hand, communities with low species richness are invaded more frequently (Trowbridge 1995, Williamson 1996, Stohlgren et al. 1999, Levine 2000).In the Northwest Atlantic, C. fragile ssp.tomentosoides has invaded several areas that had low species diversity.On New Zealand rocky shores, bare rocks, and less complex communities are occupied by high densities of C. fragile (Trowbridge 1995).However, more evidence and field studies are needed to determine the role of species richness in community resistance against invasion.
The animals associated with Codium species consisted mainly of arthropods and molluscs (Annex 3).Most associated fauna were small herbivorous species such as the amphipod Ampithoe valida shimizuensis and the gastropod Tristichotrochus unicus.There were differences in the numbers of fauna found on Codium species among the three locations.Codium fragile at Tongyong had the highest species richness (6 species), but had a lower average density of associated fauna compared to Munsom and Supsom (gastropods=2.07 individuals gram dw -1 , amphipods=0.19individuals gram dw -1 ).The differences between species abundance and number of species found on Codium may be attributed to the differences in the diversity of algal species and environmental conditions among locations.It is interesting to note that the density of associated fauna is relatively low in Codium's native range (<5 individuals per gram algal dry weight) compared with the invasive area in the Gulf of Maine, where the density of associated fauna can be as high as 25 individuals per gram of algal dry weight (Chavanich 2001).
One group of snails, Sacoglossa, typically found associated with siphonaceous green algae were conspicuous in their absence.The Sacoglossa contain several species that are known to feed on Codium fragile in other regions of the world (Trowbridge 1992, 1993, Harris and Mathieson 2000, Trowbridge and Todd 2001, Trowbridge 2002, van Bragt 2004), and to influence its distribution (Trowbridge 2002, Harris andJones 2005).The small herbivores found on Codium species in this study (Annex 3) and in the Gulf of Maine (Chavanich 2001, Chavanich andHarris 2004) feed on diatoms and filamentous algae associated with Codium species, but do not feed directly on Codium.There are certainly sacoglossans found in Asia, but the lack of specialist herbivores at the locations studied may be one of the reasons for Codium fragile's success in the highly disturbed Tongyong location.
In summary, knowledge of the distribution patterns and ecological roles of Codium species in their native habitats provide insights into their potential roles and impacts as introduced species.It is of particular interest that one Codium species, C. fragile, that demonstrated an opportunistic response in the highly disturbed Tongyong location, is the species which has proven to be a successful invasive species in a number of regions around the world.In its native range, disturbance, low diversity and lack of specialist herbivores, combined with a highly flexible life history as C. fragile commonly reproducing parthenogenesis, appears to have allowed it to become pre-adapted to successfully colonize new habitats and to even become a dominant species when conditions permit.More detailed studies of the ecology of Codium fragile within its native range should provide a better understanding of how it has been able to evolve the attributes that promote its success as an invasive species.

Figure 1 .
Figure 1.Map of Southern Korea, showing study sites

Figure 5 .
Figure 5. Number of species of associated fauna on different Codium species at three locations

Figure 6 .
Figure 6.Average density of gastropods and amphipods plus 1 SE on different Codium species at 3 locations.Asterisk represents significant difference between the average density of gastropods and amphipods