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Ocean Sci. J. (2013) 48(4):319-328http://dx.doi.org/10.1007/s12601-013-0030-1

Available online at http://link.springer.com

Comparative Study on the Fauna Composition of Intertidal Invertebrates between Natural and Artificial Substrata in the Northeastern Coast of Jeju Island

Jae-Hoon Cha1*, Kwang-Bae Kim1, Ji-Na Song1, In-Soo Kim2, Jeong-Bin Seo2, and Chul-Hwi Kwoun1

1Land ocean environment Co Ltd., Suwon 443-702, Korea2Rural Research Institute, Korea Rural Community Corporation, Ansan 426-908, Korea

Received 17 June 2013; Revised 28 November 2013; Accepted 17 December 2013© KSO, KIOST and Springer 2013

Abstract − This study was carried out to learn about differencesin the sessile macrobenthic fauna communities between theartificial and natural habitats. There were some differences in termsof species composition and dominant species and communitystructure between two habitat types. The dominant species includePollicipes mitella and Granuilittorina exigua in natural rockyintertidal zones; Monodonta labio confusa, Ligia exotica, Tetraclitajaponica in the artificial rocky intertidal zones. Among all thespecies, L. exotica and T. japonica occurred only in the artificialrocky intertidal zone. The results of cluster analysis and nMDSanalysis showed a distinct difference in community structurebetween artificial and natural rocky intertidal zones. The faunain the natural rocky intertidal zones were similar to each otherand the fauna in the artificial rocky intertidal zones were divideddepending on the slope of the substratum. In the case of asloping tetrapod, M. labio confusa and P. mitella were dominant,but at the vertical artificial seawall, Cellana nigrolineata, L.exotica T. japonica were dominant. The analysis of the speciespresented in natural and artificial rocky intertidal areas showed theexclusive presence of 10 species on natural rocks and 12 specieson artificial rocks. The species in the natural rocky intertidal areaincluded mobile gastropods and cnidarians (i.e. rock anemones),and the species in the artificial rocky intertidal area mostly includednon-mobile attached animals. The artificial novel structure seemsto contribute to increasing the heterogeneity of habitats for marineinvertebrate species and an increase the species diversity inrocky coastal areas.

Key words −Rocky shore, fauna composition, intertidal inver-tebrates, artificial substratum, Jeju Island

1. Introduction

Benthic organisms in the rocky intertidal are influencedby the environment (Harley and Helmuth 2003; Kronberg1988; Ricciardi and Bourget 1999). Especially the formationof a benthic ecosystem is likely to be influenced by thetemperature, the nature of substratum and hydrodynamicforces (Meajer et al. 2011; McCoy and Bell 1991; Menge et al.1985). However, the development of small and large harborsaccommodating a wide range of ships in recent years hasled to an increase of artificial rocky intertidal zones, whichis a trend not only in Korea but also in many other countries.As a result, the consequential changes in the ecosystem areattracting the interests of rocky intertidal ecologists (Walker1988; Bulleri et al. 2005; Knott et al. 2004; Thompson et al.2002; Bacchiocchi and Airoldi 2003; Moschella et al. 2005).

In general the diversity of species in artificial rockyintertidal areas is not as important as that of natural rockyintertidal areas that provide habitats with a wide range ofconditions due to small cracks, small and large tide pools,and dryness and moisture according to the solar position(Chapman and Bulleri 2003). In Australia and Italy, artificialbreakwaters have less rare species compared to the naturalrocky intertidal areas (Bulleri and Chapman 2004; Bulleri2005a, b). In the case of Victoria Port in Hong Kong, bothnatural rocks and artificial breakwaters show similar speciesassemblage, but there are differences in the coverage rateof some species. Some species appear on artificial rocksexclusively and some species appear only on natural rocks.However natural rocks have a gentle slope while artificial*Corresponding author. E-mail: [email protected]

Article

320 Cha, J.-H. et al.

rocks have a vertical slope, which results in completelydifferent groups of living organisms. Greater horizontalspatial variation in faunal assemblages on natural rocky shoresmay be associated with greater habitat diversity (e.g. rockpools, crevices and roughness on surface) than on smoothvertical seawall (Nelson et al. 2009).

The coastal areas of Jeju Island are made of basalt, a kindof volcanic rock, and the surface is rough, and there aremany holes and crevices on the rocks which are differentfrom other rocky shores of the Korean Peninsula (Lee 1990).Furthermore there is a significant difference in substratetypes from the breakwaters and tetrapod made of concrete,a kind of artificial rocky shore, which seems to lead tohave the presence of a quite different biological assemblage.In Jeju Island, many synecological studies of the rockyintertidal invertebrates have been conducted (Lee et al.1989; Lee and Kim 1993; Lee and Hyun 1992, 2002), andthe ecological studies of some taxonomic groups have alsobeen conducted (Lee 1990; Noseworthy and Choi 2010).However studies on impact of artificial substrats in rockyintertidal benthos in Jeju Island have seldom been conductedequally in other coastal areas of Korea. In particular, therocky shores in the coast of Jeju Island are completelydifferent from artificial hard structures. Thus the purpose of

this study is to evaluate the ecological changes due to thecoastal development of artificial hard structures and to comeup with appropriate measures in advance by observing thefaunal assemblages between different substrate types.

2. Materials and Methods

Sampling sites and timeField observations were conducted in summer and winter.

The first survey was conducted on Sep 9th in 2012 and thesecond research was conducted on Jan 8th, 2013. The samplingsites were selected at three places located in the northeastern partof Jeju Island: three natural rocky coastal areas of Gujaweup,Jeju Island (Kimryeongri, Woljungri, Handongri); andthree artificial rocky coasts with concrete structures such astetrapod and water breakers built before the year of 2000(Fig. 1). The stations were marked as a (natural substrata) andb (artificial substrata). About a 4 km distance between studysites was maintained. In the case of artificial rocky structures,ST 1 is a small port with structures for small ship to set sail,and the sides of them were investigated. ST 2 was surveyedfocusing on the tetrapods of ports and ST3 was surveyedfocusing on the vertical seawall (Fig. 2). At both ST 1 andST 3, natural rocky intertidal zone and artificial rocky

Fig. 1. Map showing the sampling stations at the northeastern coastal area in Jeju Island

Fauna composition of intertidal invertebrates between natural and artificial Substrata 321

intertidal zone are adjacent to each other, and they are 300 mapart from ST 2 (Fig. 1).

Sampling methodsA quantitative sampling method was conducted for the

species showing its even distribution at the lower intertidalzones by using a 50 cm × 50 cm quadrat; and for rare species, a20-30 minute qualitative samplings as well as photographswith a waterproof digital camera (Olympus TG-1, Olympus,Japan) were performed. As Jeju Island has significant tidaldifference, research was conducted during low tide. The surveydistance of stations was about 10-30 m and photographywas mainly conducted on foot, using a non-destructive method.Some samples were collected for scrutiny. The samplescollected were fixed with a 5% neutral buffered formalin andthen were moved to the labs and finally fixed with 80% ethylalcohol, and then were identified to species level. This samplingdesign allowed us to study variations in intertidal faunalassemblages between habitats, among sites. However thecomparison between transects within each habitat wasdifficult due to different surface areas between the naturaland artificial substratum at the survey stations. In particular, thestratification of the artificial intertidal zone was too narrow andvariable to compare with the natural substratum.

Data analysisSpecies composition analysis focused on the material

property of rocks rather than season and thus an analysiswas conducted separately on the natural substratum and theartificial substratum. Population density was analyzed bycalculating mean values. Poriferia was excluded from thecalculation of population density and dominant speciescalculation because it lives in colonies.

To determine dominance ranking, Le Bris index (Le Bris1988) was used because it considers not only abundance butdistribution of population. The dominant species in numberin various stations rather than one station were chosen asdominant species. In this study, the species with the indicatorabove 10,000 were chosen as dominant species.

Fij = (Pij/Pj) × 100 Pij: the frequency of the occurrence of (i)species in the (j)th colonyPj: the number of total stations in the (j)th stationDij = [{(Nik/Nk) × 100}/Pj]Nik: Number of (i) species in the (k)th station of (j) colonyNk: Total number of species in (k)th stationD'ij = Fij × Dij × 100The population density data of the survey conducted in

two seasons was averaged before analysis. As for regionalanalysis, the averages by station were analyzed. As for theanalytical method, the species abundance was transformedto square roots, and the matrix of similarity was calculated usingthe Bray-Curtis similarity index (Clark and Ainsworth 1993).

From the similarity index, the dendrogram of clusteranalysis and Non-metric multidimensional scaling (nMDS)analysis were plotted.

PRIMER 6.0 software package (developed in PlymouthMarine Laboratory) was used for statistical analysis (Clarkeand Gorley 2006).

3. Results and Discussions

Comparison of fauna group composition between twohabitat types

A total of 43 species appeared in the natural and artificialsubstrata, at 3 stations in two seasons. 30 species and 32species appeared in the natural and the artificial substratumrespectively (Fig. 3). The ratio of species composition wassimilar to each other. In particular, the composition ratio ofMollusks and Arthropods were similar to each other. The sumof these two fauna was dominant in the natural substrata(80%) and the artificial substrata (85%). The only difference

Fig. 2. The typical nature of each substratum at 3 sampling stations


was that firstly, 3 cnidarian species appeared in the naturalstratum, secondly, 2 sponge species appeared in the naturalstratum and 4 sponge species appeared in the artificialstratum. In the case of cnidaria, actinian anemones appearedmainly on the moist rocks. As it lives in tide pools, it is notlikely to live on artificial structures (Chapman 2003).

Regarding population abundance, the population densityof the natural substratum was higher than that of the artificialsubstratum. With regard to fauna, mollusks showed thehighest population density in both strata, followed by arthropods,indicating a high proportion of these two faunas in populationdensity such as species number (Fig. 3).

Comparison of dominant species from two habitat typesThe results of the comparison regarding dominant species

between the natural substrata and the artificial substrata are

presented in Table 1.Pollicipes mitella, Granulilittorina exigua, and Hydroides

ezoensis were dominant in the natural substratum; Monodontalabio confusa, Ligia exotica and Tetraclita japonica weredominant in the artificial substratum (Table 1). Commonstalk banacle, P. mitella and an granulated periwinkle, G. exiguawere easily found in the natural substratum. P. mitella wasfound between the crevices of basalt and G. exigua wasfound the most between holes of basalt (Fig. 4). In addition,Heminerita japonica and Japanese common chiton, Acanthopleurajaponica, were also often found in the natural substratum.

The lipped periwinkle, M. labio confusa and the bumpylimpet, L. dorsuosa were often found in the artificial substratum.However M. labio confusa appeared in the similar populationdensity proportions as in the natural substratum, suggestingM. labio confusa is able to inhabit in both substrata. However,

Fig. 3. The faunal composition of marine invertebrates on two different substrata of rocky shores in Jeju Is. (a): total species at naturalhabitats, (b): total species at artificial habitats. (c): density at natural habitat, (d): density at artificial habitats


M. labio confusa have not been reported as a dominant speciesin the ecological studies on the intertidal zone of Jeju Island(Lee and Kim 1993; Lee and Hyun 1992, 2002; Lee et al.2001).

The wharf roach, L. exotica selected as the second dominantspecies, was limited to specific stations with high speciesabundance. The black banacle, T. japonica was found inartificial rocks. But the species most widely distributed inthe artificial rocks was the bumpy limpet, L. dorsuosa thatlives on the vertical sea wall (Fig. 5).

Some species were selected as the dominant species inboth substrata such like M. labio confusa, however some

species were selected as the dominant species in onesubstratum, indicating the difference in groups between thetwo substrata (Table 1).

Community analysis of the two substrata The results of community analysis for the benthic

invertebrates on the two substrata for two seasons are shownin Fig. 6.

The cluster analysis showed that the sampling sites wereclustered into 3 groups. The first group was composed of 3stations in the natural substratum and the second group,composed of ST1 and ST2 in the artificial substratum, and

Table 1. The list of dominant species in two substrata. (Sub: Nature of substratum, FO: Frequency of Occurrence (in total 6 investigations), Arth.:Arthropoda, Moll.: Mollusca, Anne.: Annelida, D’ij: Le Bris index)

Sub Species name Taxon FO ind./m2 % D'ij

Natural subst - ratum

Pollicipes mitella Arth. 5 99 26.01 255009.1 Granulilittorina exigua Moll. 4 128 33.74 216257.9 Hydroides ezoensis Anne. 2 32 8.44 29581.4 Heminerita japonica Moll. 4 17 4.39 25542.8 Monodonta labio confusa Moll. 3 15 4.04 16531.1 Acanthopleura japonica Moll. 4 7 1.76 11334.8

Artificialsubst- ratum

Monodonta labio confusa Moll. 5 15 6.08 108138.0 Ligia exotica Arth. 2 19 7.67 36535.9 Tetraclita japonica Arth. 2 35 14.02 31082.3 Cellana nigrolineata Moll. 3 14 5.56 29586.2 Lottia dorsuosa Moll. 4 13 5.29 28520.3 Pollicipes mitella Arth. 2 9 3.44 25420.3 Acanthopleura japonica Moll. 3 13 5.29 21089.8 Siphonaria japonica Moll. 4 10 3.97 20962.4 Cellana toreuma Moll. 3 5 1.85 17664.7 Hydroides ezoensis Anne. 1 21 8.20 13668.4 Septifer virgatus Moll. 1 41 16.40 13146.7 Nerita albicilla Moll. 2 6 2.38 12708.8

Fig. 4. The dominant species in natural intertidal substrata in Jeju Island. Right: Pollicipes mitella, Left: Granuilittorina exigua


final group was composed of ST3 in artificial substratum.The first group in the natural substratum looks like it isgrouped together because the sites were under similar

environmental conditions and substrates. In the case of thegroups on artificial substratum, there were differences ininstallation time and in the angle of attachment surface. Todetermine the characteristics of these groups, the dominantspecies of each group are shown in Table 2.

Group C1 is a faunal group from the natural substrata,identical to the dominant species in the natural substratapresented in Table 2. However group C2 and C3, on theartificial substratum, show differences. In group C2, M. labioconfusa, P. mitella, and common limpet, Cellana toreumawere dominant; in Group C3, wharf roach, L. exotica, andblack limpet limpet, T. japonica, were dominant, whichindicates the community composition may vary dependingon the slope of the substratum in the case of the artificialhabitats (Whorff et al. 1995; Gabrielle et al. 1999).

In group C2, a mobile gastropod M. labio confusa wasdominant and presented in C1 as a dominant species. Thecommon stalked barnacle, P. mitella was the most dominantin the natural substratum, yet does not appear in group C3,showing a difference between groups C2 and C3. The blackbarnacle T. japonica and the bumpy limpet, L. dorsuosa ingroup C3, were not presented in C2. They are likely todemand large attachment areas except for the mobile L.exotica that appeared only in the summer. Group C2 consistsof the species which 1) have less mobility and 2) live on agentle slope 3) do not prefer to come in contact with directwaves compared to group C3 (Table 2).

On the other hand, group C3 that lives on the verticalsurface comes in contact with higher waves and thus requiresmore solid attachment than the horizontal one, which meansa gradient was critical to benthos on rocky intertidal areas(Whorff et al. 1995; Gabrielle et al. 1999; Benedetti-Cecchi

Fig. 5. The dominant species in artificial intertidal substrata in Jeju Island. Right: Monodonta labio confusa, Left: Lottia dorsuosa

Fig. 6. Dendrogram of cluster analysis and two-dimensional non-metric multidimentional scaling ordination (nMDS) plot.(a refers to a natural substratum; b refes to an artificialsubstratum)


et al. 2000; Glasby 2000; Knott et al. 2004).As a result of the analysis of species in 3 stations in the

natural and artificial substratum in two seasons, 20 speciesfrom a total of 42 species appeared in both natural andartificial substratum. And 10 species in the natural substratum,and the 12 species in artificial substratum appeared respectively(Table 3).

The species that exclusively appeared in the naturalsubstratum are mainly mobile gastropods, and cnidarianswhich live generally in wet grooves or in tide pools. Howeversome mobile organisms such as gastropod M. labio confusa,N. albicilla and mobile Arthropod L. exotica were foundin the artificial substratum, yet no mobile benthos werediscovered only in the artificial substratum and thus thereare less mobile species in general, which is similar to theAustralian case (Chapman 2003). The mobile species needa protected place to sustain on substrata when the wavescome. So the artificial substrata that have only smoothsurface are preferred by sessile organisms. However, in non-exposed area, some mobile species can be found in the artificialsubstrata.

In fact, the proportion of the mobile Gastropoda andArthropoda on natural substratum in this study was 40%,higher than 19% of the artificial substratum (Fig. 7), whichmeans the irregular shape of the natural substratum is

Table 2. The list of dominant species of 3 communities resulted by cluster analysis Fig. 6 (Co: Community, FO: Frequency of Occurrence,Arth.: Arthropoda, Moll.: Mollusca, Anne.: Annelida)

Co. Species name Taxon FO ind./m2 % D'ij

C1

Pollicipes mitella Arth. 5 99 26.01 255009.1 Granuilittorina exigua Moll. 4 128 33.74 216257.9 Hydroides ezoensis Anne. 2 32 8.44 29581.4 Nerita albicilla Moll. 4 17 4.39 25542.8 Monodonta labio confusa Moll. 3 15 4.04 16531.1 Acanthopleura japonica Moll. 4 7 1.76 11334.8

C2

Monodonta labio confusa Moll. 3 20 8.37 136379.6 Pollicipes mitella Arth. 2 13 5.44 57195.8 Cellana toreuma Moll. 3 7 2.93 39745.6 Hydroides ezoensis Anne. 1 31 12.97 30754.0 Septifer virgatus Moll. 1 62 25.94 29580.2 Nerita albicilla Moll. 2 9 3.77 28594.8 Acanthopleura japonica Moll. 2 15 6.28 24612.3 Nipponacmaea concinna Moll. 2 5 2.09 19841.3 Octomeris sulcata Arth. 1 22 9.21 10496.2

C3

Cellana nigrolineata Moll. 2 36 12.95 153707.9 Ligia exotica Moll. 1 54 19.42 135000.0 Tetraclita japonica Arth. 1 86 30.94 120786.5 Lottia dorsuosa Moll. 2 34 12.23 108651.7

Table 3. The species occurred exclusively on each substratum andthe motility of specie

Substratum Phylum Species name Motility

Rockyshore

Mollusca Chlorostoma lischkei ○

Mollusca Littorina brevicula ○

Mollusca Nipponacmaea concinna radula ×Mollusca Nodilittorina radiata ○

Mollusca Omphalius rusticus ○

Mollusca Pyrene flava ○

Mollusca Japeuthria ferra ○

Cnidaria Haliplanella lucia ×Cnidaria Anthopleura midori ×Cnidaria Anthopleura kurogane ×

Artificialstructure

Mollusca Acanthochitona achates ×Mollusca Acanthochitona defilippi ×Mollusca Lottia kogamogai ×Mollusca Nipponacmaea concinna ×Mollusca Siphonaria japonica ×Mollusca Crassostrea gigas ×Mollusca Saccostrea kegaki ×Mollusca Septifer virgatus ×

Arthropoda Octomeris sulcata ×Arthropoda Tetraclita japonica ×

Porifera Haliclona permollis ×Porifera Hymeniacidon sinapium ×


advantageous to resist waves and to maintain moisturewhereas the artificial substratum does not provide a placefor mobile benthos to inhabit.

However, the artificial substratum provided a place forsome sessile organisms which were not able to inhabit in thenatural substratum. The mixture of natural-artificial substratumseemed to increase the species diversity in the rocky intertidalarea. It is widely known that spatial heterogeneity has agreat effect on the intertidal animal diversity (Archambaultand Bourget 1996; Underwood and Chapman 1996, 1998).

The role of artificial substrata in rocky intertidal areasMost studies of benthic ecosystems in the natural and

artificial substratum were conducted mainly in Australia,Italy, and Hong Kong (Chapman 2003; Bulleri 2005a, b; Nelsonet al. 2009). There were few benthic studies in Koreanwaters, particularly at the natural rocks of Jeju Island where

naval bases and the coasts are being actively developed. Thesubstratum has a lot of holes and is made of irregular basalt,which may lead to a big difference compared to other areas.There were some studies and researches conducted to preparefor the increment of novel artificial structures since the1990s (Underwood and Chapman 1996, 1998; Chapman2003; Nelson et al. 2009). The community structure and thecomposition of fauna studied in Jeju Island showed similarfaunal distribution in both substrata (Fig. 3), however thespecies composition showed a difference (Table 1). From theresult of cluster analysis, the natural substrata showed asimilar cluster over time whereas the artificial substrata showeddiverse clusters depending on the slope of the substratumand installation duration despite having the same materialproperty-concrete.

What roles will the new structures (breakwaters, Tetra podsetc) on the natural substrata play with regard to the benthicecosystem?

From the perspective of the species diversity, someartificial structures will improve the diversity of species tosome extent. According to the study by Tews et al. (2004),the diversity of habitats is closely associated with the diversityof animal species and ‘Keystone structure’ also exists inhabitats, which will have a great influence on the diversityof animal species. In this study, 30 out of a total of 42 animalspecies appeared in the natural substratum, an addition of12 species from artificial substrata. Yet the mobile speciesdecreased and Actinia equina disappeared in the artificialsubstratum. Having considered this point, Chapman (2003)has suggested an artificial structure can make a sharpergradient in breakwaters and make small ‘rock-pools’ insteadof slippery surfaces so that an environment where anemones,sea urchins and octopus are able to live can be created.Recently, she suggested that artificial substratum should beable to create an environment that will improve the speciesdiversity (Browne and Chapman 2011). This idea is similarto the artificial reef in the subtidal zone, yet the artificialreef aims to increase the fishery productivity, whereas theartificial substratum should increase the species diversity orthe target species wanted.

On the other hand, in the artificial structures, foulingorganisms are able to live. Newly made substrata mayunexpectedly lead to the abundance of living organisms.For a good example, artificial structures are able to providethe substratum for jellyfish during the fouling period in theshape of polyps, which may lead to the mass-breeding of

Fig. 7. The ratio of mobile species among the total occurring speciesin each substratum. (A: natural substratum, B: Artificialsubstratum)


jellyfish. Thus there is a need to perform in-depth studies onthe structure and function of artificial structures on coasts.

Acknowledgements

We thank Dr. Choi Jin Woo (KIOST) for valuable commentsabout this study. Special thanks are due to Prof. Choi Kwang-Sik (Jeju Univ.) and others anonymous reviewers for criticizingand upgrading the manuscript. This study was supported bythe Leading industry Development for Jeju Economic Region,and the Ministry of Trade, Industry and Energy Korea aspart of the project “Jeju island offshore wind farm development,measurement and analysis techniques developed for themarine environment”.

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