SpringerLink
Log in

Factors Affecting the Distribution Patterns of Benthic Invertebrates at a Major Shorebird Staging Site in the Yellow Sea, China

  • Original Research
  • Published:
Wetlands Aims and scope Submit manuscript

Abstract

The tidal flats of the Yellow Sea support benthic communities that are vitally important to migratory birds, but baseline information on benthic community structure and variability is largely lacking. We investigated spatial and temporal patterns of macrobenthic invertebrates in areas used by large numbers of shorebirds and how these patterns related to environmental factors at Yalu Jiang coastal wetland in the north Yellow Sea during boreal spring (March–May) from 2010 to 2012. At least 61 species were documented during the study. Monthly benthos sampling from 54 stations indicated that polychaetes and bivalves dominated the benthic communities, with capitellid or maldanid polychaetes dominating upper tidal flats and the bivalve Potamocorbula laevis dominating intermediate and lower tidal flats. The middle and eastern sites approximately 10 km apart showed substantial differences in benthic species abundance and distribution, with bivalves dominating in the middle but not the eastern site. The spatial distribution of benthos was correlated with both exposure time during the tidal cycle and sediment particle size. Benthic communities showed both annual and within season variation. Two of the frequent prey for migratory birds, namely ghost shrimps Nihonotrypaea japonica and young Potamocorbula laevis, were relatively common in 2010 and 2011, respectively, but not in 2012.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Barter M (2002) Shorebirds of the Yellow Sea: importance, threats and conservation status - Wetlands International Global Series 9. International Wader Studies 12, Canberra, Australia

  • Bennett EL, Reynolds CJ (1993) The value of a mangrove area in Sarawak. Biodiversity and Conservation 2:359–375. doi:10.1007/bf00114040

    Article  Google Scholar 

  • Beukema JJ (1979) Biomass and species richness of the macrobenthic animals living on a tidal flat area in the Dutch Wadden Sea—effects of a severe winter. Netherlands Journal of Sea Research 13:203–223. doi:10.1016/0077-7579(79)90003-6

    Article  Google Scholar 

  • Beukema JJ (1982) Annual variation in reproductive success and biomass of the major macrozoobenthic species living in a tidal flat area of the Wadden Sea. Netherlands Journal of Sea Research 16:37–45. doi:10.1016/0077-7579(82)90015-1

    Article  Google Scholar 

  • Bijleveld AI, van Gils JA, van der Meer J, Dekinga A, Kraan C, van der Veer HW, Piersma T (2012) Designing a benthic monitoring programme with multiple conflicting objectives. Methods in Ecology and Evolution 3:526–536. doi:10.1111/j.2041-210X.2012.00192.x

    Article  Google Scholar 

  • BirdLife International (2005) Important Bird Areas and potential Ramsar Sites in Asia. BirdLife International, Cambridge

    Google Scholar 

  • BirdLife International (2009) Directory of Important Bird Areas in China (mainland): key sites for conservation. BirdLife International, Cambridge, English language edition

    Google Scholar 

  • Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New York

    Book  Google Scholar 

  • Borja A, Franco J, Perez V (2000) A marine Biotic Index to establish the ecological quality of soft-bottom benthos within European estuarine and coastal environments. Marine Pollution Bulletin 40:1100–1114. doi:10.1016/s0025-326x(00)00061-8

    Article  CAS  Google Scholar 

  • Chang Y, Chen J (2008) The status of mariculture in northern China. In: Lovatelli A, Phillips MJ, Arthur JR, Yamamoto K (eds) FAO/NACA Regional workshop on the future of mariculture: a regional approach for responsible development in the Asia-Pacific region. FAO, Guangzhou, pp 271–284

    Google Scholar 

  • Chen ZB, Guo L, ** BS, Wu JH, Zheng GH (2009) Effect of the exotic plant Spartina alterniflora on macrobenthos communities in salt marshes of the Yangtze River Estuary, China. Estuarine Coastal and Shelf Science 82:265–272. doi:10.1016/j.ecss.2009.01.014

    Article  Google Scholar 

  • Choi C-Y, Battley PF, Potter MA, Rogers KG, Ma ZJ (2014a) The importance of Yalu Jiang coastal wetland in the north Yellow Sea to Bar-tailed Godwits Limosa lapponica and Great Knots Calidris tenuirostris during northward migration. Bird Conservation International In press

  • Choi CY, Gan XJ, Hua N, Wang Y, Ma ZJ (2014b) The babitat use and home range analysis of Dunlin (Calidris alpina) in Chongming Dongtan, China and their conservation implications. Wetlands 34:255–266. doi:10.1007/s13157-013-0450-9

    Article  Google Scholar 

  • Choi CY, Gan XJ, Ma Q, Zhang KJ, Chen JK, Ma ZJ (2009) Body condition and fuel deposition patterns of calidrid sandpipers during migratory stopover. Ardea 97:61–70

    Article  Google Scholar 

  • Choi J-W, Koh C-H (1994) Macrobenthos community in Keum-Mankyung-Dong** estuaries and its adjacent coastal region, Korea. Journal of the Korean Society of Oceanography 29:304–318

    Google Scholar 

  • Choi KH, Lee SM, Lim SM, Walton M, Park GS (2010) Benthic habitat quality change as measured by macroinfauna community in a tidal flat on the west coast of Korea. Journal of Oceanography 66:307–317

    Article  Google Scholar 

  • Cloern JE (1982) Does the benthos control phytoplankton biomass in south San Francisco Bay. Marine Ecology Progress Series 9:191–202. doi:10.3354/meps009191

    Article  Google Scholar 

  • Colwell MA, Landrum SL (1993) Nonrandom shorebird distribution and fine-scale variation in prey abundance. Condor 95:94–103. doi:10.2307/1369390

    Article  Google Scholar 

  • Compton TJ, Holthuijsen S, Koolhaas A, Dekinga A, ten Horn J, Smith J, Galama Y, Brugge M, van der Wal D, van der Meer J, van der Veer HW, Piersma T (2013) Distinctly variable mudscapes: distribution gradients of intertidal macrofauna across the Dutch Wadden Sea. Journal of Sea Research 82:103–116. doi:10.1016/j.seares.2013.02.002

    Article  Google Scholar 

  • Dauer DM (1993) Biological criteria, environmental-health and estuarine macrobenthic community structure. Marine Pollution Bulletin 26:249–257. doi:10.1016/0025-326x(93)90063-p

    Article  Google Scholar 

  • Davies JL (1980) Geographical variation in coastal development, 2nd edn. Longman, London

    Google Scholar 

  • De Caceres M, Jansen F (2013) Indicspecies: Studying the statistical relationship between species and groups of sites. http://cran.r-project.org/web/packages/indicspecies/index.html (Version 1.6.7) Accessed 16 Jun 2013

  • De Caceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574

    Article  PubMed  Google Scholar 

  • ESRI (2010) ArcGIS 10.0. Environmental Systems Research Institute, Redlands

    Google Scholar 

  • Esselink P, Zwarts L (1989) Seasonal trend in burrow depth and tidal variation in feeding-activity of Nereis diversicolor. Marine Ecology Progress Series 56:243–254. doi:10.3354/meps056243

    Article  Google Scholar 

  • Godet L, Toupoint N, Fournier J, Le Mao P, Retiere C, Olivier F (2009) Clam farmers and Oystercatchers: effects of the degradation of Lanice conchilega beds by shellfish farming on the spatial distribution of shorebirds. Marine Pollution Bulletin 58:589–595. doi:10.1016/j.marpolbul.2008.11.001

    Article  CAS  PubMed  Google Scholar 

  • Hashizume K, Tatarazako N, Kobata K, Nakamura Y, Morita M (2012) Life history characteristics of the Surf Clam Mactra veneriformis (Bivalvia: Veneroida: Mactridae) on a sandy tidal flat in Tokyo Bay, Japan. Pacific Science 66:335–346. doi:10.2984/66.3.7

    Article  Google Scholar 

  • Honkoop PJC, Pearson GB, Lavaleye MSS, Piersma T (2006) Spatial variation of the intertidal sediments and macrozoo-benthic assemblages along Eighty-mile Beach, North-western Australia. Journal of Sea Research 55:278–291. doi:10.1016/j.seares.2005.11.001

    Article  Google Scholar 

  • Hua N, Piersma T, Ma Z (2013) Three-phase fuel deposition in a long-distance migrant, the Red Knot (Calidris canutus piersmai), before the flight to high arctic breeding grounds. PLoS ONE 8:e62551. doi:10.1371/journal.pone.0062551

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • IUCN (2012) IUCN red list of threatened species. Version 2012.2

  • Kimmel DG, Newell RIE (2007) The influence of climate variation on eastern oyster (Crassostrea virginica) juvenile abundance in Chesapeake Bay. Limnology and Oceanography 52:959–965

    Article  Google Scholar 

  • Koh CH, Shin HC (1988) Environmental characteristics and distribution of macrobenthos in a mudflat of the west coast of Korea (Yellow Sea). Netherlands Journal of Sea Research 22:279–290

    Article  Google Scholar 

  • Legendre P, Borcard D, De Caceres M (2012) STI: space-time ANOVA models without replications. https://sites.google.com/site/miqueldecaceres/software/STI_1.0.2.zip?attredirects=0 (Version 1.0.2). Accessed 16 Jun 2013

  • Legendre P, De Caceres M, Borcard D (2010) Community surveys through space and time: testing the space-time interaction in the absence of replication. Ecology 91:262–272. doi:10.1890/09-0199.1

    Article  PubMed  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology 2nd English edition. Elsevier Science BV, Amsterdam

    Google Scholar 

  • Levin LA, Boesch DF, Covich A, Dahm C, Erseus C, Ewel KC, Kneib RT, Moldenke A, Palmer MA, Snelgrove P, Strayer D, Weslawski JM (2001) The function of marine critical transition zones and the importance of sediment biodiversity. Ecosystems 4:430–451. doi:10.1007/s10021-001-0021-4

    Article  CAS  Google Scholar 

  • Li DL, Chen SH, Lloyd H, Zhu SY, Shan K, Zhang ZW (2013) The importance of artificial habitats to migratory waterbirds within a natural/artificial wetland mosaic, Yellow River Delta, China. Bird Conservation International 23:184–198. doi:10.1017/s0959270913000099

    Article  CAS  Google Scholar 

  • Liu J, She J (2003) Reproductive behaviour of Potamocorbula laevis (Hinds). Fisheries Science 22:12–13

    Google Scholar 

  • Liu WX, Hu J, Chen JL, Fan YS, **ng B, Tao S (2008) Distribution of persistent toxic substances in benthic bivalves from the inshore areas of the Yellow Sea. Environmental Toxicology and Chemistry 27:57–66. doi:10.1897/07-115.1

    Article  PubMed  Google Scholar 

  • Luo XX, Zhang SS, Yang JQ, Pan JF, Tian L, Zhang LJ (2013) Macrobenthic community in the **aoqing River Estuary in Laizhou Bay, China. Journal of Ocean University of China 12:366–372. doi:10.1007/s11802-013-1955-9

    Article  CAS  Google Scholar 

  • Ma ZJ, Li B, Li WJ, Han NY, Chen JK, Watkinson A (2009) Conflicts between biodiversity conservation and development in a biosphere reserve. Journal of Applied Ecology 46:527–535

    Article  Google Scholar 

  • Ma ZJ, Hua N, Peng HB, Choi CY, Battley PF, Zhou QY, Chen Y, Ma Q, Jia N, Xue WJ, Bai QQ, Wu W, Feng XS, Tang CD (2013) Differentiating between stopover and staging sites: functions of the southern and northern Yellow Sea for long-distance migratory shorebirds. Journal of Avian Biology 44:504–512. doi:10.1111/j.1600-048X.2013.00213.x

  • MacKinnon J, Verkuil YI, Murray N (2012) IUCN situation analysis on East and Southeast Asian intertidal habitats, with particular reference to the Yellow Sea (including the Bohai Sea). Occasional Paper of the IUCN Species Survival Commission No. 47. IUCN, Gland, Switzerland and Cambridge, UK

  • McNeely JA, Kapoor-Vijay P, Zhi L, Olsvig-Whittaker L, Sheikh KM, Smith AT (2009) Conservation biology in Asia: the major policy challenges. Conservation Biology 23:805–810. doi:10.1111/j.1523-1739.2009.01284.x

    Article  PubMed  Google Scholar 

  • Melville DS (2010) Pilot survey of intertidal benthos Yalu Jiang Nature Reserve, Liaoning Province April 2008

  • Newell RC (1970) Biology of intertidal animals. Logos Press Limited, London

    Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MH, Wagner H. (2013). Vegan: community ecology package. http://vegan.r-forge.r-project.org/ (Version 2.0-7). Accessed 14 May 2013

  • R Core Team (2013) R: a language and environment for statistical computing: R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org (Version 3.0.1). Accessed 19 Jun 2013

  • Reise K (2002) Sediment mediated species interactions in coastal waters. Journal of Sea Research 48:127–141. doi:10.1016/s1385-1101(02)00150-8

    Article  Google Scholar 

  • Riegen AC, Vaughan GR, Rogers KD (2014) Yalu Jiang Estuary shorebird survey report 1999–2010. Yalu Jiang Estuary Wetland National Nature Reserve, China and Miranda Naturalists’ Trust, New Zealand

  • Rogers D (2005) Distribution of shorebirds along Eighty-Mile Beach. In: Pearson G, Piersma T, Hickey R, Lavaleye M (eds) The long mud: benthos and shorebirds of the foreshore of eighty-mile beach, Western Australia. Texel, Netherlands, pp 163–206

    Google Scholar 

  • Rogers DI, Yang HY, Hassell CJ, Boyle AN, Rogers KG, Chen B, Zhang ZW, Piersma T (2010) Red Knots (Calidris canutus piersmai and C. c. rogersi) depend on a small threatened staging area in Bohai Bay, China. Emu 110:307–315

    Article  Google Scholar 

  • Rogers DI, Hassell CJ, Boyle A, Gosbell K, Minton C, Rogers KG, Clarke RT (2011) Shorebirds of the Kimberley Coast – Populations, key sites, trends and threats. Journal of the Royal Society of Western Australia 94:377–391

    Google Scholar 

  • Ronnback P (1999) The ecological basis for economic value of seafood production supported by mangrove ecosystems. Ecological Economics 29:235–252. doi:10.1016/s0921-8009(99)00016-6

    Article  Google Scholar 

  • Ryu J, Khim JS, Choi JW, Shin HC, An S, Park J, Kang D, Lee CH, Koh CH (2011) Environmentally associated spatial changes of a macrozoobenthic community in the Saemangeum tidal flat, Korea. Journal of Sea Research 65:390–400. doi:10.1016/j.seares.2011.03.003

    Article  Google Scholar 

  • Sato S (2006) Drastic change of bivalves and gastropods caused by the huge reclamation projects in Japan and Korea. Plankton & Benthos Research 1:123–137

    Article  Google Scholar 

  • Sato S, Azuma M (2002) Ecological and paleoecological implications of the rapid increase and decrease of an introduced bivalve Potamocorbula sp after the construction of a reclamation dike in Isahaya Bay, western Kyushu, Japan. Palaeogeography Palaeoclimatology Palaeoecology 185:369–378. doi:10.1016/s0031-0182(02)00423-6

    Article  Google Scholar 

  • Semeniuk V (2005) Tidal flats. In: Schwartz M (ed) Encyclopedia of coastal science. Springer, Dordrecht, pp 965–975

    Google Scholar 

  • Tutiempo Network (2013) Climate DANDONG from 1956 to 2013

  • UNDP/GEF (2007a) The Yellow Sea: analysis of environmental status and trends, volume 1, part I: National reports - China. UNDP/GEF Yellow Sea Project, Ansan, Republic of Korea, p 316

  • UNDP/GEF (2007b) The Yellow Sea: analysis of environmental status and trends, volume 3: Regional synthesis reports. UNDP/GEF Yellow Sea Project, Ansan, Republic of Korea, p. 408

  • van de Kam J, Battley PF, McCaffery BJ, Rogers DI, Hong JS, Moores N, Ki JY, Lewis J, Piersma T (2008) Invisible connections. Why migrating shorebirds need the Yellow Sea. Wetlands International, Wageningen

    Google Scholar 

  • van Gils JA, Piersma T, Dekinga A, Spaans B, Kraan C (2006) Shellfish dredging pushes a flexible avian top predator out of a marine protected area. PLoS Biology 4:e376. doi:10.1371/journal.pbio.0040376

    Article  PubMed Central  PubMed  Google Scholar 

  • VanDusen BM, Fegley SR, Peterson CH (2012) Prey distribution, physical habitat features, and guild traits interact to produce contrasting shorebird assemblages among foraging patches. PLoS ONE 7:e52694. doi:10.1371/journal.pone.0052694

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vaughn CC, Hakenkamp CC (2001) The functional role of burrowing bivalves in freshwater ecosystems. Freshwater Biology 46:1431–1446. doi:10.1046/j.1365-2427.2001.00771.x

    Article  Google Scholar 

  • Wade S, Hickey R (2008) Map** migratory wading bird feeding habitats using satellite imagery and field data, Eighty-Mile Beach, Western Australia. Journal of Coastal Research 24:759–770. doi:10.2112/05-0453.1

    Article  Google Scholar 

  • Wang Y, Ren ME, Zhu DU (1986) Sediment supply to the continental-shelf by the major rivers of China. Journal of the Geological Society 143:935–944. doi:10.1144/gsjgs.143.6.0935

    Article  CAS  Google Scholar 

  • Wang Z, Duan D, Zhang J, Chen S, Du X, Liu Y, Sui K, Zhao L (2010) A study on macrobenthic biomass of the Yellow River Estuary intertidal in 2008. Journal of Guangdong Ocean University 30:29–35

    Google Scholar 

  • Weber LM, Haig SM (1997) Shorebird—Prey interactions in South Carolina coastal soft sediments. Canadian Journal of Zoology 75:245–252. doi:10.1139/z97-031

    Article  Google Scholar 

  • Wei L, Guan F (1985) The growth of Aloidis laevis. Chinese Journal of Zoology 20:3–7

    Google Scholar 

  • Wentworth CK (1922) A scale of grade and class terms for clastic sediments. Journal of Geology 30:377–392

    Article  Google Scholar 

  • Wilson HB, Kendall BE, Fuller RA, Milton DA, Possingham HP (2011) Analyzing variability and the rate of decline of migratory shorebirds in Moreton Bay, Australia. Conservation Biology 25:758–766. doi:10.1111/j.1523-1739.2011.01670.x

    Article  PubMed  Google Scholar 

  • Yan MF (ed) (2008) Scientific survey of Dandong Yalujiang Wetland National Nature Reserve. Liaoning University Press, Shenyang

    Google Scholar 

  • Yang H-Y, Chen B, Ma Z-J, Hua N, van Gils JA, Zhang Z-W, Piersma T (2013) Economic design in a long-distance migrating molluscivore: how fast-fuelling red knots in Bohai Bay, China, get away with small gizzards. The Journal of Experimental Biology 216:3627–3636. doi:10.1242/jeb.083576

    Article  PubMed  Google Scholar 

  • Yang HY, Chen B, Barter M, Piersma T, Zhou CF, Li FS, Zhang ZW (2011) Impacts of tidal land reclamation in Bohai Bay, China: ongoing losses of critical Yellow Sea waterbird staging and wintering sites. Bird Conservation International 21:241–259. doi:10.1017/s0959270911000086

    Article  Google Scholar 

  • Yates MG, Goss-Custard JD, McGrorty S, Lakhani KH, Durell SEALVD, Clarke RT, Rispin WE, Moy I, Yates T, Plant RA, Frost AJ (1993) Sediment characteristics, invertebrate densities and shorebird densities on the inner banks of the Wash. Journal of Applied Ecology 30:599–614

    Article  Google Scholar 

  • Ysebaert T, Fettweis M, Meire P, Sas M (2005) Benthic variability in intertidal soft-sediments in the mesohaline part of the Schelde estuary. Hydrobiologia 540:197–216. doi:10.1007/s10750-004-7144-5

    Article  Google Scholar 

  • Yu HM (1994) China coastal ocean uses—conflicts and impacts. Ocean & Coastal Management 25:161–178. doi:10.1016/0964-5691(94)90054-x

    Article  Google Scholar 

  • Zwarts L, Blomert AM, Wanink JH (1992) Annual and seasonal-variation in the food-supply harvestable by knot Calidris canutus staging in the Wadden Sea in late summer. Marine Ecology Progress Series 83:129–139. doi:10.3354/meps083129

    Article  Google Scholar 

Download references

Acknowledgments

CYC was supported by the New Zealand Government under the NZIDRS programme. This study was financially supported by the National Natural Science Foundation of China (31071939). We are indebted to D.-Z. **ng, X.-J. Gan, P. Brakels, Q.-Q. Bai, Y. Chen, H.-B. Peng, N. Jia and D. Melville for field assistance, and M. Irwin for technical advice. We thank the Dandong Yalu Jiang Estuary Wetland National Nature Reserve for facilitating our fieldwork. We are grateful to the Miranda Naturalists’ Trust, especially A. Riegen, for sharing their knowledge and experiences of the study site. We appreciate H.-Y. Yang and I. Henderson for discussion and suggestion on study designs and statistical analysis. We would also like to thank the editors and two anonymous reviewers for their valuable comments on earlier drafts of this manuscript.

Author information

Authors and Affiliations

  1. Ecology Group, Institute of Agriculture and Environment, Massey University, Private Bag 11-222, Palmerston North, 4442, New Zealand

    Chi-Yeung Choi, Phil F. Battley & Murray A. Potter

  2. Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science, Fudan University, Shanghai, 200433, People’s Republic of China

    Zhijun Ma

  3. Shanghai Key Lab for Urban Ecological Processes and Eco-Restoration, College of Resources and Environmental Science, East China Normal University, Shanghai, 200062, People’s Republic of China

    Wenliang Liu

Authors
  1. Chi-Yeung Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Phil F. Battley
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Murray A. Potter
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhijun Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wenliang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chi-Yeung Choi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 123 kb)

ESM 2

(DOC 60 kb)

ESM 3

(DOC 50 kb)

ESM 4

(GIF 249 kb)

High Resolution Image

(TIFF 6382 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Choi, CY., Battley, P.F., Potter, M.A. et al. Factors Affecting the Distribution Patterns of Benthic Invertebrates at a Major Shorebird Staging Site in the Yellow Sea, China. Wetlands 34, 1085–1096 (2014). https://doi.org/10.1007/s13157-014-0568-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13157-014-0568-4

Keywords

Search

Navigation