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Biogeography of intertidal and subtidal native and invasive barnacles in Korea in relation to oceanographic current ecoregions and global climatic changes

Published online by Cambridge University Press:  05 November 2020

Hyun Kyong Kim ,
Benny K. K. Chan Open the ORCID record for Benny K. K. Chan [Opens in a new window] ,
Sang-kyu Lee  and
Won Kim Open the ORCID record for Won Kim [Opens in a new window]
Hyun Kyong Kim
Affiliation:
School of Biological Sciences, Seoul National University, Seoul08826, Republic of Korea
Benny K. K. Chan*
Affiliation:
Biodiversity Research Center, Academia Sinica, Taipei115, Taiwan
Sang-kyu Lee
Affiliation:
Marine Research Center, National Park Research Institute, Korea National Park, Yeosu59723, Republic of Korea
Won Kim*
Affiliation:
School of Biological Sciences, Seoul National University, Seoul08826, Republic of Korea
*
Author for correspondence: Benny K. K. Chan, E-mail: [email protected]; Won Kim, E-mail: [email protected]
Author for correspondence: Benny K. K. Chan, E-mail: [email protected]; Won Kim, E-mail: [email protected]
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Abstract

The coastline of the Korean Peninsula is influenced by three major oceanographic ecoregions, including the estuarine Yellow Sea ecoregion on the west coast, the warmer and saline East China Sea ecoregion on the south coast, and the cold East Sea ecoregion on the east coast. The influence of these marine ecoregions on the distribution of intertidal barnacles has not been extensively studied. The present study examines the biogeography of thoracican barnacles from intertidal and shallow subtidal zones, along the coasts of Korea. Twenty-one species in seven families were identified, including three species of coral-associated barnacles. Species composition varied significantly in the three marine ecoregions. Multivariate analysis showed barnacle assemblages were significant among the three ecoregions, although there are large overlaps of clusters between the Yellow Sea and East China Sea ecoregions. The estuarine species, Fistulobalanus albicostatus, occurred mainly in the Yellow Sea ecoregion; warm-water species, Tetraclita japonica, and sponge inhabiting barnacles Euacasta dofleini were observed in the East China Sea ecoregion; and cold-water species, Balanus rostratus and Perforatus perforatus, were found in the East Sea ecoregion. Four invasive barnacle species were recorded and the European barnacle Perforatus perforatus expanded its range northward from its recorded distribution nine years earlier. The cold-water species, Chthamalus dalli and Semibalanus cariosus, previously recorded in the East Sea ecoregion, were absent in the present survey. A trend of increasing seawater temperatures in Korean waters may have a significant impact on the distribution of cold-water species and enhance the northward invasion of P. perforatus.

Keywords

Biodiversitybiogeographyinvasive speciesKoreathoracican barnacle
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 100 , Issue 7 , November 2020 , pp. 1079 - 1091
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

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References

Belkin, IM (2009) Rapid warming of large marine ecosystems. Progress in Oceanography 81, 207–213.CrossRefGoogle Scholar
Cha, HR, Buddemeier, RW, Fautin, DG and Sandhei, P (2004) Distribution of sea anemones (Cnidaria, Actiniaria) in Korea analyzed by environmental clustering. Hydrobiologia 530, 497–502.Google Scholar
Chan, BKK and Lee, PF (2012) Biogeography of intertidal barnacles in different marine ecosystems of Taiwan – potential indicators of climate change? In Lawrence, S (ed.), Global Advances in Biogeography. Rijeka, Croatia: In Tech, pp. 119–136.Google Scholar
Chan, BKK, Tsang, LM and Chu, KH (2007) Cryptic diversity of Tetraclita squamosa complex (Crustacea, Cirripedia) in Asia: description of a new species from Singapore. Zoological Studies 46, 46–56.Google Scholar
Chan, BKK, Akihisa, M and Lee, PF (2008 a) Latitudinal gradient in the distribution of the intertidal acorn barnacles of the Tetraclita species complex (Crustacea: Cirripedia) in NW Pacific and SE Asian waters. Marine Ecology Progress Series 362, 201–210.CrossRefGoogle Scholar
Chan, BKK, Garm, A and Høeg, JT (2008 b) Setal morphology and cirral setation of thoracican barnacle cirri: adaptations and implications for thoracican evolution. Journal of Zoology 275, 294–306.CrossRefGoogle Scholar
Chan, BKK, Hsu, CH and Southward, AJ (2008c) Morphological variation and biogeography of an insular intertidal barnacle Hexechamaesipho pilsbryi (Crustacea: Cirripedia) in the western Pacific. Bulletin of Marine Science 83, 315–328.Google Scholar
Chan, BKK, Kolbasov, G, Hirose, M, Mezaki, T and Suwae, R (2014) Biodiversity and biogeography of the coral boring barnacles of the genus Berndtia (Cirripedia: Acrothoracica) in the West Pacific, with description of three new species. Journal of Natural History 48, 1503–1541.CrossRefGoogle Scholar
Chan, BKK, Xu, G, Kim, HK, Park, JH and Kim, W (2018) Living with marginal coral communities: diversity and host-specificity in coral-associated barnacles in the northern coral distribution limit of the East China Sea. PLoS ONE 13, e0196309.CrossRefGoogle ScholarPubMed
Chang, YW, Chan, JSM, Hayashi, R, Shuto, T, Tsang, LM, Chu, KH and Chan, BKK (2017) Genetic differentiation of the soft shore barnacle Fistulobalanus albicostatus (Cirripedia: Thoracica: Balanomorpha) in the West Pacific. Marine Ecology 38, e12422.CrossRefGoogle Scholar
Cheang, CC, Tsang, LM, Ng, WC, William, GA, Chu, KH and Chan, BKK (2012) Phylogeography of the cold-water barnacle Chthamalus challengeri in the north-western Pacific: effect of past population expansion and contemporary gene flow. Journal of Biogeography 39, 1819–51835.CrossRefGoogle Scholar
Choi, KH, Choi, HW, Kim, IH and Hong, JS (2013) Predicting the invasion pathway of Balanus perforatus in Korean seawaters. Ocean and Polar Research 35, 63–68.Google Scholar
Clarke, KR (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117–143.CrossRefGoogle Scholar
Clarke, KR and Gorley, RN (2006) PRIMER: Getting Started with v6. Plymouth: PRIMER-E Ltd.Google Scholar
Dawson, SJ, Makretsov, N, Blows, FM, Driver, KE, Provenzano, E, Le Quesne, J, Baglietto, L, Giles, GG, Mclean, CA, Callagy, G, Green, AR, Ellis, I, Gelmon, K, Turashvili, G, Leung, S, Aparicio, S, Huntsman, D and Caldas, C (2010) BCL2 in breast cancer: a favourable prognostic marker across molecular subtypes and independent of adjuvant therapy received. British Journal of Cancer 103, 668–675.CrossRefGoogle ScholarPubMed
Dong, YW, Wang, HS, Han, GD, Ke, CH, Zhan, X, Nakano, T and Williams, GA (2012) The impact of Yangtze River discharge, ocean currents and historical events on the biogeographic pattern of Cellana toreuma along the China coast. PLoS ONE 7, e36178.CrossRefGoogle ScholarPubMed
Fenberg, PB and Rivadeneira, MM (2019) On the importance of habitat continuity for delimiting biogeographic regions and shaping richness gradients. Ecology Letters 2, 664–673.CrossRefGoogle Scholar
Giovanni database, NASA, USA (2011) Ocean Color Radiometry Online Visualization and Analysis. Global Monthly Products. http://gdata1.sci.gsfc.nasa.gov/daac-bin/G3/gui.chi?instance_id=ocean_month;download4 (accessed 13 December 2018).Google Scholar
Guan, BX (1994) Patterns and structures of the currents in Bohai, Huanghai and East China Seas. Oceanology of China Seas 1, 17–26.Google Scholar
Han, IS and Lee, JS (2020) Change in the annual amplitude of sea surface temperature due to climate change in a recent decade around the Korean Peninsula. Journal of the Korean Society of Marine Environment & Safety 26, 233–241.CrossRefGoogle Scholar
Hawkins, SJ, Moore, PT, Burrow, MT, Poloczanska, E, Mieszkowska, N, Herbert, RJH, Jenkins, SR, Thompson, RC, Genner, MJ and Southward, AJ (2008) Complex interactions in a rapidly changing world: responses of rocky shore communities to recent climate change. Climate Research 37, 123–133.CrossRefGoogle Scholar
Hawkins, SJ, Sugden, HE, Mieszkowska, N, Moore, PJ, Poloczanska, E, Leaper, R, Herbert, RJH, Genner, MJ, Moschella, PS, Thompson, RC, Jenkins, SR, Southward, AJ and Burrows, MT (2009) Consequences of climate-driven biodiversity changes for ecosystem functioning of North European rocky shores. Marine Ecology Progress Series 396, 245–259.CrossRefGoogle Scholar
Helmuth, B, Mieszkowska, N, Moore, P and Hawkins, SJ (2006) Living on the edge of two changing worlds: forecasting the responses of rocky intertidal ecosystems to climate change. Annual Review of Ecology, Evolution, and Systematics 37, 373–404.CrossRefGoogle Scholar
Henry, DP and McLaughlin, PA (1975) The barnacles of the Balanus amphitrite complex (Cirripedia, Thoracica). Zoologische verhandelingen 141, 1–254.Google Scholar
Intergovernmental Panel on Climate Change (2019) Special Report on the Ocean and Cryosphere in a Changing Climate. https://www.ipcc.ch/srocc/home/.Google Scholar
Jacobs, GA, Hur, HB and Riedlinger, SK (2000) Yellow and East China Seas response to winds and currents. Journal of Geophysical Research: Oceans 105, 21947–21968.CrossRefGoogle Scholar
Jung, JB, Jung, JW and Kim, W (2018) Subdividing the common intertidal hermit crab Pagurus minutus Hess, 1865 (Decapoda: Anomura: Paguridae) based on molecular, morphological and coloration analyses. Zoological Studies 57, 61.Google ScholarPubMed
Jung, JB, Yoshida, R and Kim, W (2019) Diversity of parasitic peltogastrid barnacles (Crustacea: Cirripedia: Rhizocephala) on hermit crabs in Korea. Zoological Studies 58, 33.Google ScholarPubMed
Kim, HS (1973) Anomura and Brachyura. Illustrated Encyclopedia of Fauna & Flora of Korea 14, 1–694.Google Scholar
Kim, HS (1977) Macrura. Illustrated Encyclopedia of Fauna & Flora of Korea 19, 1–694.Google Scholar
Kim, W (1982) Classification and geographical distribution of Korean crabs (Crustacea, Decapoda, Brachyura) (MS thesis). Seoul National University, Seoul, Korea.Google Scholar
Kim, IH (1998) Cirripedia, symbiotic Copepoda, and Pycnogonida. Illustrated Encyclopedia of Fauna & Flora of Korea 38, 1–1038.Google Scholar
Koh, CH and Khim, JS (2014) The Korean tidal flat of the Yellow Sea: physical setting, ecosystem and management. Ocean and Coastal Management 102, 398–414.CrossRefGoogle Scholar
Korea Hydrographic and Oceanographic Agency (2017) Oceanographic Observation – Water Temperature Observation. http://www.khoa.go.kr (accessed 30 March 2020).Google Scholar
Lie, HJ and Cho, CH (2016) Seasonal circulation patterns of the Yellow and East China seas derived from satellite-tracked drifter trajectories and hydrographic observations. Progress in Oceanography 146, 121–141.CrossRefGoogle Scholar
Lim, NL, Lee, HM, Jeung, HD, Noseworthy, RG, Jung, S and Choi, KS (2019) Early larval development and annual gametogenesis of the brooding oyster Ostrea circumpicta (Pilsbry, 1904) in the shallow subtidal benthic ecosystem in Jeju Island, off the south coast of Korea. Zoological Studies 58, 29.Google ScholarPubMed
Liu, Y, Xue, J, Lin, J and Wu, H (2015) Invasion and morphological variation of the non-indigenous barnacle Chthamalus challengeri (Hoek, 1883) in Yangshan Port and its surrounding areas. Journal of Ocean University of China 14, 575–583.CrossRefGoogle Scholar
Ma, KY, Chow, LH, Wong, KJ, Chen, HN, Ip, BH, Schubart, CD, Tsang, LM, Chan, BKK and Chu, KH (2019) Speciation pattern of the horned ghost crab Ocypode ceratophthalmus (Pallas, 1772): an evaluation of the drivers of Indo-Pacific marine biodiversity using a widely distributed species. Journal of Biogeography 46, 830.CrossRefGoogle Scholar
Mieszkowska, N and Sugden, HE (2016) Climate-driven range shifts within benthic habitats across a marine biogeographic transition zone. Advances in Ecological Research 55, 325–369.CrossRefGoogle Scholar
Mieszkowska, N, Hawkins, SJ, Burrows, MT and Kendall, MA (2007) Long-term changes in the geographic distribution and population structures of Osilinus lineatus (Gastropoda: Trochidae) in Britain and Ireland. Journal of the Marine Biological Association of the United Kingdom 87, 537–545.CrossRefGoogle Scholar
Mieszkowska, N, Burrows, MT, Pannacciulli, FG and Hawkins, SJ (2014) Multidecadal signals within co-occurring intertidal barnacles Semibalanus balanoides and Chthamalus spp. linked to the Atlantic Multidecadal Oscillation. Journal of Marine Systems 133, 70–76.CrossRefGoogle Scholar
Ni, G, Li, QI, Kong, L and Yu, H (2014) Comparative phylogeography in marginal seas of the northwestern Pacific. Molecular Ecology 23, 534–548.CrossRefGoogle ScholarPubMed
Nitani, H (1972) Beginning of the Kuroshio. Kuroshio, Physical Aspect of the Japan Current. Tokyo: University of Tokyo Press.Google Scholar
Park, C, Kim, ST, Hong, JS and Choi, KH (2017) A rapid assessment survey of invasive species of macrobenthic invertebrates in Korean waters. Ocean Science Journal 52, 387–395.CrossRefGoogle Scholar
Parmesan, C (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics 37, 637–669.CrossRefGoogle Scholar
Rebstock, GA and Kang, YS (2003) A comparison of three marine ecosystems surrounding the Korean peninsula: responses to climate change. Progress in Oceanography 59, 357–379.CrossRefGoogle Scholar
Rivadeneira, MM and Fernández, M (2005) Shifts in southern endpoints of distribution in rocky intertidal species along the south-eastern Pacific coast. Journal of Biogeography 32, 203–209.CrossRefGoogle Scholar
Roberts, CM, McClean, CJ, Veron, JEN, Hawkins, JP, Allen, GR, McAllister, DE, Mittermeier, CG, Schueler, FW, Spalding, M, Wells, F, Vynne, C and Werner, TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295, 1280–1284.CrossRefGoogle ScholarPubMed
Sanda, S, Hamasaki, K, Dan, S and Kitada, S (2019) Expansion of the northern geographical distribution of land hermit crab populations: colonization and overwintering success of Coenobita purpureus on the coast of the Boso Peninsula, Japan. Zoological Studies 58, 25.Google ScholarPubMed
Sanford, E, Sones, JL, García-Reyes, M, Goddard, JH and Largier, JL (2019) Widespread shifts in the coastal biota of northern California during the 2014–2016 marine heatwaves. Scientific Reports 9, 1–14.CrossRefGoogle ScholarPubMed
SMAP sea surface salinity, NASA, USA (2011) Global salinity measurements continue the time series. https://salinity.oceansciences.org/smap-salinity.htm#mollweide (Accessed 13 December 2018).Google Scholar
Southward, AJ (1962) On the behavior of barnacles. IV. The influence of temperature on cirral activity and survival of some warm water species. Journal of the Marine Biological Association of the United Kingdom 42, 163–177.CrossRefGoogle Scholar
Southward, AJ (1991) Forty years of changes in species composition and population density of barnacles on a rocky shore near Plymouth. Journal of the Marine Biological Association of the United Kingdom 71, 495–513.Google Scholar
Southward, AJ, Hawkins, SJ and Burrows, MT (1995) Seventy years’ observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature. Journal of Thermal Biology 20, 127–155.CrossRefGoogle Scholar
Spalding, MD, Fox, HE, Allen, GR, Davidson, N, Ferdaña, ZA, Finlayson, M, Halpern, BS, Jorge, MA, Lombana, AI, Lourie, SA, Martin, KD, McManus, E, Molnar, J, Recchia, CA and Robertson, J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57, 573–583.CrossRefGoogle Scholar
Sugihara, K, Yamano, H, Choi, KS and Hyeong, K (2014) Zooxanthellate scleractinian corals of Jeju Island, Republic of Korea. Ecological Research Monographs 2, 111–130.CrossRefGoogle Scholar
Thompson, RC, Crowe, TP and Hawkins, SJ (2002) Rocky intertidal communities: past environmental changes, present status and predictions for the next 25 years. Environmental Conservation 29, 168–191.CrossRefGoogle Scholar
Tomanek, L and Somero, GN (2002) Interspecific-and acclimation-induced variation in levels of heat-shock proteins 70 (hsp70) and 90 (hsp90) and heat-shock transcription factor-1 (HSF1) in congeneric marine snails (genus Tegula): implications for regulation of hsp gene expression. Journal of Experimental Biology 205, 677–685.Google Scholar
Tsang, LM, Chan, BKK, Wu, TH, Ng, WC, Chatterjee, T, Williams, GA and Chu, KH (2008) Population differentiation of the barnacle Chthamalus malayensis: postglacial colonization and recent connectivity across Pacific and Indian Oceans. Marine Ecology Progress Series 364, 107–118.CrossRefGoogle Scholar
Tsang, LM, Wu, TH, Ng, WC, Williams, GA, Chan, BKK and Chu, KH (2011) Comparative phylogeography of Indo-West Pacific intertidal barnacles. In Held, C, Koenemann, S and Schubart, D (eds), Phylogeography and Population Genetics in Crustacea. Boca Raton, FL: CRC Press, pp. 111–128.Google Scholar
Wang, J, Tsang, LM and Dong, YW (2015) Causations of phylogeographic barrier of some rocky shore species along the Chinese coastline. BMC Evolutionary Biology 15, 114.CrossRefGoogle ScholarPubMed
Wrange, AL, Charrier, G, Thonig, A, Rosenblad, MA, Blomberg, A, Havenhand, JN, Jonsson, PR and André, C (2016) The story of a hitchhiker: population genetic patterns in the invasive barnacle Balanus (Amphibalanus) improvisus Darwin 1854. PLoS ONE 11, e0147082.CrossRefGoogle ScholarPubMed
Wu, TH, Shen, J, Zhu, J, Zhang, J and Li, L (2014) Characteristics of the Changjiang plume and its extension along the Jiangsu Coast. Continental Shelf Research 76, 108–123.CrossRefGoogle Scholar
Wu, TH, Tsang, LM, Chan, BKK and Chu, KH (2015) Cryptic diversity and phylogeography of the island-associated barnacle Chthamalus moro in Asia. Marine Ecology 36, 368–378.CrossRefGoogle Scholar
Yorisue, T, Ellrich, JA and Momota, K (2019) Mechanisms underlying predator-driven biotic resistance against introduced barnacles on the Pacific coast of Hokkaido, Japan. Biological Invasions 21, 2345–2356.CrossRefGoogle Scholar
Yu, SS, Wang, J, Wang, QL, Huang, XW and Dong, YW (2014) DNA barcoding and phylogeographic analysis of Nipponacmea limpets (Gastropoda: Lottiidae) in China. Journal of Molluscan Studies 80, 420–429.Google Scholar