Download Distribution pattern of the green alga Codium fragile (Suringar

Aquatic Invasions (2006) Volume 1, Issue 3: 99-108
DOI 10.3391/ai.2006.1.3.1
© 2006 The Author(s)
Journal compilation © 2006 REABIC (http://www.reabic.net)
This is an Open Access article
Research article
Distribution pattern of the green alga Codium fragile (Suringar) Hariot, 1889
in its native range, Korea
Suchana Chavanich1* , Larry G. Harris 2, Jong-Geel Je 3 and Rae-Seon Kang 4
1
Department of Marine Science, Faculty of Science, Chulalongkorn University, Bangkok 10330, Thailand
Department of Zoology, University of New Hampshire, Durham, NH 03824, USA
3
Biological Oceanography Division, Korea Ocean Research and Development Institute, Ansan, Korea
4
Center for Marine Resources, Korea Ocean Research and Development Institute, Ansan, Korea
*Corresponding author
E-mail: [email protected]
2
Received 29 May 2006; accepted in revised form 5 July 2006
Abstract
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.
Key words: Codium fragile, invasive species, invasion success, Korea, macroalga, native range
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,
99
S. Chavanich et al.
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 and Tyrrell 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.
100
Material and Methods
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 m2 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
Distribution pattern of Codium fragile
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).
Figure 1. Map of Southern Korea, showing study sites
Results
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).
Figure 2. Codium fragile in native habitat (photo by R.
Kang)
101
S. Chavanich et al.
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).
Codium fragile was found as deep as 22 m while
C. minus, C. adhaerens and C. cylindricum were
restricted to shallower depths or not deeper than
18 m (Annex 2).
100
Sargassum spp.
Ecklonia cava
Codium fragile
% of Canopy Species
80
60
40
20
0
4
9
18
4
Munsom
9
18
Supsom
3
6
9
Tongyong
Depth (meters)
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.
Figure 3. Relative percentage of canopy species by various
depths at Munsom, Supsom, and Tongyong
% Cover of Understory Species
100
Green Algae
Brown Algae
Red Algae
Sand
Debris
80
60
40
20
0
4
9
Munsom
18
4
9
18
Supsom
3
6
9
Tongyong
Depth (meters)
Figure 4. Relative percent coverage of understory species
by various depths at Munsom, Supsom, and Tongyong
Figure 5. Number of species of associated fauna on different
Codium species at three locations
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
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
102
Distribution pattern of Codium fragile
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.
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
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
103
S. Chavanich et al.
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=0.19 individuals 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
104
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 and Jones 2005). The small herbivores found on Codium species in this study
(Annex 3) and in the Gulf of Maine (Chavanich
2001, Chavanich and Harris 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.
Acknowledgements
We thank Bon-Joo Koo, Byung-Il Kim, HeungSik Park, and Arthur Mathieson for field
assistance and comments on the initial project
and the identification of algae and marine
Distribution pattern of Codium fragile
invertebrates. Jose Escamilla-Casas and Huw
Jones helped on the data analysis. This work was
funded by Korea Summer Fellowship, National
Science Foundation (NSF, USA) and Korean
Science and Engineering Foundation (KOSEF) to
S. Chavanich and J. Je.
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Annex 1
Records of Codium fragile in coastal waters of Korea in 2000*
Location
(name and depth)
Record coordinates
Latitude, N
Record date
Species abundance
Collector
Longitude, E
Munsom (from 4-22 m depths)
33 o 12'
126 o 43'
06.08.2000
<20% of total algae
S. Chavanich
Supsom (from 4-22 m depths)
o
33 16'
126 o 51'
06.08.2000
<20% of total algae
S. Chavanich
o
o
06.08.2000
>80% of total algae
S. Chavanich
Tongyong (from 3-9 m depths)
34 46'
128 24'
*Full reference to the data: Chavanich S, Harris LG, Je JG and Kang RS (2006) Distribution pattern of the green alga Codium
fragile (Suringar) Hariot, 1889 in its native range, Korea. Aquatic Invasions 1(3): 99-108
106
Distribution pattern of Codium fragile
Annex 2
Common algal species found at Munsom, Supsom, and Tongyong in various depths of water
Algal Species
4
Munsom
9
18
4
Supsom
9
18
Tongyong
Fouling
Subtidal
Chlorophyta
+
+
Cladophora sp.
Codium adhaerens (Cabrera) C. Agardh, 1822
Codium cylindricum Holmes, 1896
Codium fragile (Suringar) Hariot, 1889
Codium minus (Schmidt) Silva, 1962
+
+
Ulva lactuca Linnaeus, 1753
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Ulva pertusa Kjellman, 1897
Phaeophyta
Carpomitra cabrerae (Clemente) Kützing, 1843
+
Dictyopteris latiuscula (Okamura) Okamura, 1932
Dictyota dichotoma (Hudson) Lamouroux, 1809
Ecklonia cava Kjellman, 1885
Padina arborescens Holmes, 1896
Sargassum filicinum Harvey, 1860
+
+
+
+
+
+
+
+
+
+
+
Sargassum serratifolium C. Agardh, 1820
Sporochnus scoparius Harvey, 1855
Undaria pinnatifida (Harvey) Suringar, 1873
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Zonaria diesingiana J. Agardh, 1841
Rhodophyta
Amphiroa dilatata Lamouroux, 1816
Carpopeltis angusta (Okamura) Okamura, 1910)
+
+
+
+
+
+
Delisea fimbriata (Lamouroux) Montagne, 1844
Galaxaura falcata Kjellman, 1900
Gelidium amansii (Lamouroux) Lamouroux, 1813
+
Gracilaria textorii (Suringar) De Toni, 1895
Meristotheca papulosa (Montagne) J. Agardh, 1872
Pachymeniopsis lanceolata (Okamura) Yamada ex
Kawabata, 1954
Plocamium telfairiae (W.J. Hooker & Harvey) Harvey ex
Kützing, 1849
+
+
+
+
+
Polysiphonia spp.
Scinaia moniliformis J. Agardh, 1885
+
+
107
S. Chavanich et al.
Annex 3
List of arthropods and molluscs found on Codium adhaerens (1), C. fragile (2), C. minus (3), C. cylindricum (4) at Munsom,
Supsom, and Tongyong
Species
1
Munsom
2
3
1
Supsom
2
3
+
+
4
Tongyong
2
Arthropods
Ampithoe valida shimizuensis Stephensen, 1944
+
Caprella penantis Leach, 1814
Eusiroides monoculoides japonica Hirayama, 1985
Gammaropsis japonica Nagata, 1961
+
+
+
+
+
+
+
Jassa falcata (Montagu, 1808)
+
Pugettia quadridens (de Haan, 1850)
Molluscs
+
Cantharidus callichroa forma bisabalteata (Pilsbry, 1901)
+
+
Eufenella rufocincta (A. Adams, 1861)
Mitrella lischkei Smith, 1879
Mytilus edulis Linnaeus, 1758
Tristichotrochus unicus (Dunker, 1860)
108
+
+
+