Abstract
Microplastics (MPs) are ubiquitous in marine sedimentary environments. Their occurrence in horseshoe crabs and interactions with the sedimentary environment has not been determined. In this study, MPs, mostly microfibers, were found in all extracted gastrointestinal tract (GIT) samples of the juvenile Tachypleus tridentatus from the northern Beibu Gulf, China. The MP concentrations (4–53 items ind−1) were higher than those in most marine benthic invertebrates (< 15 items ind−1) reported in Chinese waters, despite their generally low level in habitat sediments (9-1818 items kg−1). The correlation between the juveniles and sediments was not evident, but the abundance in juvenile horseshoe crab GITs decreased with ages. The findings were relevant to the life-history characteristics of the species, typically with limited dispersal capability and their spending nine years or longer time living in mangrove wetlands during low tides, with apparent ontogenetic changes in their diets. These baseline data enable a better understanding of MP availability in benthic macroinvertebrates, and the ecological risks present in the ecosystems.
Similar content being viewed by others
References
Amin, R. M., Sohaimi, E. S., Anuar, S. T., and Bachok, Z., 2020. Microplastic ingestion by zooplankton in Terengganu coastal waters, southern South China Sea. Marine Pollution Bulletin, 150: 110616.
Andrady, A. L., 2011. Microplastics in the marine environment. Marine Pollution Bulletin, 62: 1596–1605.
Arthur, C., Baker, J., and Bamford, H., 2009. Proceedings of the International Research Workshop on the Occurrence, Effects, and Fate of Microplastic Marine Debris. NOAA Technical Memorandum NOS-OR&R-30, 528pp.
Botton, M. L., 2009. The ecological importance of horseshoe crabs in estuarine and coastal communities: A review and speculative summary. In: Biology and Conservation of Horseshoe Crabs. Tanacredi, J. T., et al., eds., Springer, Massachusetts, Boston, 45–63.
Bour, A., Avio, C. G., Gorbi, S., Regoli, F., and Hylland, K., 2018a. Presence of microplastics in benthic and epibenthic organisms: Influence of habitat, feeding mode and trophic level. Environmental Pollution, 243: 1217–1225.
Bour, A., Haarr, A., Keiter, S., and Hylland, K., 2018b. Environmentally relevant microplastic exposure affects sediment-dwelling bivalves. Environmental Pollution, 236: 652–660.
Brockmann, H. J., and Smith, M. D., 2009. Reproductive competition and sexual selection in horseshoe crabs. In: Biology and Conservation of Horseshoe Crabs. Tanacredi, J. T., et al., eds., Springer, Massachusetts, Boston, 199–221.
Bürkle GmbH, 2021. Chemical resistance of plastics. https://www.buerkle.de/en/chemical-resistance. Accessed on 13 August 2021.
Carbery, M., O’Connor, W., and Palanisami, T., 2018. Trophic transfer of microplastics and mixed contaminants in the marine food web and implications for human health. Environmental International, 115: 400–409.
Chae, Y., and An, Y. J., 2020. Effects of food presence on microplastic ingestion and egestion in Mytilus galloprovincialis. Chemosphere, 240: 124855.
Fu, Y., Huang, S., Wu, Z., Wang, C. C., Su, M., Wang, X., et al., 2019. Socio-demographic drivers and public perceptions of consumption and conservation of Asian horseshoe crabs in northern Beibu Gulf, China. Aquatic Conservation: Marine and Freshwater Ecosystems, 29: 1268–1277.
Gaines, E. F., Carmichael, R. H., Grady, S. P., and Valiela, I., 2002. Stable isotopic evidence for changing nutritional sources of juvenile horseshoe crabs. Biological Bulletin, 203: 228–230.
Garcés-Ordóñez, O., Mejía-Esquivia, K. A., Sierra-Labastidas, T., Patiño, A., Blandón, L. M., and Díaz, L. F. E., 2020. Prevalence of microplastic contamination in the digestive tract of fishes from mangrove ecosystem in Cispata, Colombian Caribbean. Marine Pollution Bulletin, 154: 111085.
Haegerbaeumer, A., Mueller, M. T., Fueser, H., and Traunspurger, W., 2019. Impacts of micro-and nano-sized plastic particles on benthic invertebrates: A literature review and gap analysis. Frontiers in Environmental Science, 7: 17.
Hämer, J., Gutow, L., Köhler, A., and Saborowski, R., 2014. Fate of microplastics in the marine isopod Idotea emarginata. Environmental Science and Technology, 48: 13451–13458.
Harris, P. T., 2020. The fate of microplastic in marine sedimentary environments: A review and synthesis. Marine Pollution Bulletin, 158: 111398.
Hipfner, J. M., Galbraith, M., Tucker, S., Studholme, K. R., Domalik, A. D., Pearson, S. F., et al., 2018. Two forage fishes as potential conduits for the vertical transfer of microfibres in northeastern Pacific Ocean food webs. Environmental Pollution, 239: 215–222.
Hu, M., Kwan, B. K. Y., Wang, Y., Cheung, S. G., and Shin, P. K. S., 2015. Population structure and growth of juvenile horseshoe crabs Tachypleus tridentatus and Carcinoscorpius rotundicauda (Xiphosura) in southern China. In: Changing Global Perspectives on Horseshoe Crab Biology, Conservation and Management. Carmichael, R. H., et al., eds., Springer, Zug, Cham, 167–180.
Hu, M., Wang, Y., Chen, Y., Cheung, S. G., Shin, P. K. S., and Li, Q., 2009. Summer distribution and abundance of juvenile Chinese horseshoe crabs Tachypleus tridentatus along an intertidal zone in southern China. Aquatic Biology, 7: 107–112.
Jabeen, K., Su, L., Li, J., Yang, D., Tong, C., Mu, J., et al., 2017. Microplastics and mesoplastics in fish from coastal and fresh waters of China. Environmental Pollution, 221: 141–149.
John, B. A., Nelson, B. R., Sheikh, H. I., Cheung, S. G., Wardiatno, Y., Dash, B. P., et al., 2018. A review on fisheries and conservation status of Asian horseshoe crabs. Biodiversity and Conservation, 27: 3573–3598.
Koongolla, J. B., Lin, L., Pan, Y. F., Yang, C. P., Sun, D. R., Liu, S., et al., 2020. Occurrence of microplastics in gastrointestinal tracts and gills of fish from Beibu Gulf, South China Sea. Environmental Pollution, 258: 113734.
Kwan, B. K. Y., Hsieh, H. L., Cheung, S. G., and Shin, P. K. S., 2016. Present population and habitat status of potentially threatened Asian horseshoe crabs Tachypleus tridentatus and Carcinoscorpius rotundicauda in Hong Kong: A proposal for marine protected areas. Biodiversity and Conservation, 25: 673–692.
Kwan, K. Y., Bopp, J., Huang, S., Chen, Q., Wang, C. C., Wang, X., et al., 2021. Ontogenetic resource use and trophic dynamics of endangered juvenile Tachypleus tridentatus among diversified nursery habitats in the northern Beibu Gulf, China. Integrative Zoology, 16 (6): 908–928, https://doi.org/10.1111/1749-4877.12495.
Laurie, K., Chen, C. P., Cheung, S. G., Do, V., Hsieh, H. L., John, A., et al., 2019. Tachypleus tridentatus (Errata Version Published in 2019). e.T21309A149768986. IUCN, Gland, Switzerland, 60pp.
Li, J., Lusher, A. L., Rotchell, J. M., Deudero, S., Turra, A., Bråte, I. L. N., et al., 2019. Using mussel as a global bioindicator of coastal microplastic pollution. Environmental Pollution, 244: 522–533.
Li, J., Yang, D., Li, L., Jabeen, K., and Shi, H., 2015. Microplastics in commercial bivalves from China. Environmental Pollution, 207: 190–195.
Li, J., Zhang, H., Zhang, K., Yang, R., Li, R., and Li, Y., 2018. Characterization, source, and retention of microplastic in sandy beaches and mangrove wetlands of the Qinzhou Bay, China. Marine Pollution Bulletin, 136: 401–406.
Li, J. N., Qu, X. Y., Su, L., Zhang, W. W., Yang, D. Q., Kolandhasamy, P., et al., 2016. Microplastics in mussels along the coastal waters of China. Environmental Pollution, 214: 177–184.
Li, R., Yu, L., Chai, M., Wu, H., and Zhu, X., 2020a. The distribution, characteristics and ecological risks of microplastics in the mangroves of Southern China. Science of the Total Environment, 708: 135025.
Li, R., Zhang, S., Zhang, L., Yu, K., Wang, S., and Wang, Y., 2020b. Field study of the microplastic pollution in sea snails (Ellobium chinense) from mangrove forest and their relationships with microplastics in water/sediment located on the north of Beibu Gulf. Environmental Pollution, 263: 114368.
Liao, Y., Hsieh, H. L., Xu, S., Zhong, Q., Lei, J., Liang, M., et al., 2019. Wisdom of Crowds reveals decline of Asian horseshoe crabs in Beibu Gulf, China. Oryx, 53: 222–229.
Liao, Y. Y., and Li, X. M., 2001. Present situation of horseshoe crab resources in the sea area of China and tactics of preservation. Resource Science, 23: 53–57 (in Chinese with English abstract).
Lo, H. S., Wong, C. Y., Tam, N. F. Y., and Cheung, S. G., 2019. Spatial distribution and source identification of hydrophobic organic compounds (HOCs) on sedimentary microplastic in Hong Kong. Chemosphere, 219: 418–426.
Lo, H. S., Xu, X., Wong, C. Y., and Cheung, S. G., 2018. Comparisons of microplastic pollution between mudflats and sandy beaches in Hong Kong. Environmental Pollution, 236: 208–217.
Nor, N. H. M., and Obbard, J. P., 2014. Microplastics in Singapore’s coastal mangrove ecosystems. Marine Pollution Bulletin, 79: 278–283.
Ory, N. C., Gallardo, C., Lenz, M., and Thiel, M., 2018. Capture, swallowing, and egestion of microplastics by a planktivorous juvenile fish. Environmental Pollution, 240: 566–573.
Qiu, Q., Peng, J., Yu, X., Chen, F., Wang, J., and Dong, F., 2015. Occurrence of microplastics in the coastal marine environment: First observation on sediment of China. Marine Pollution Bulletin, 98: 274–280.
Rochman, C. M., Tahir, A., Williams, S. L., Baxa, D. V., Lam, R., Miller, J. T., et al., 2015. Anthropogenic debris in seafood: Plastic debris and fibers from textiles in fish and bivalves sold for human consumption. Scientific Reports, 5: 14340.
Scherer, C., Brennholt, N., Reifferscheid, G., and Wagner, M., 2017. Feeding type and development drive the ingestion of microplastics by freshwater invertebrates. Scientific Reports, 7: 17006.
Setälä, O., Norkko, J., and Lehtiniemi, M., 2015. Feeding type affects microplastic ingestion in a coastal invertebrate community. Marine Pollution Bulletin, 102: 95–101.
Sfriso, A. A., Tomio, Y., Rosso, B., Gambaro, A., Sfriso, A., Corami, F., et al., 2020. Microplastic accumulation in benthic invertebrates in Terra Nova Bay (Ross Sea, Antarctica). Environmental International, 137: 105587.
Shen, X., Qi, H., Liu, X., Ren, X., and Li, J., 2013. Two-way non-parametric ANOVA in SPSS. Chinese Journal of Health Statistics, 30: 913–914 (in Chinese with English abstract).
Sun, X., Wang, T., Chen, B., Booth, A. M., Liu, S., Wang, R., et al., 2021. Factors influencing the occurrence and distribution of microplastics in coastal sediments: From source to sink. Journal of Hazardous Materials, 410: 124982.
Wang, C. C., Kwan, K. Y., Shin, P. K. S., Cheung, S. G., Itaya, S., Iwasaki, Y., et al., 2020. Future of Asian horseshoe crab conservation under explicit baseline gaps: A global perspective. Global Ecology and Conservation, 24: e01373.
Weng, Z. H., Xie, Y. J., Xiao, Z. Q., Huang, L. M., Li, J., Wang, S. H., et al., 2012. Survey on resource distribution of Chinese horseshoe crab (Tachypleus tridentatus) in Fujian and other coast water of China. Chinese Journal of Zoology, 47: 40–48 (in Chinese with English abstract).
Willemsen, P. W. J. M., Horstman, E. M., Borsje, B. W., Friess, D. A., and Dohmen-Janssen, C. M., 2016. Sensitivity of the sediment trapping capacity of an estuarine mangrove forest. Geomorphology, 273: 189–201.
Woodall, L. C., Sanchez-Vidal, A., Canals, M., Paterson, G. L. J., Coppock, R., Sleight, V., et al., 2014. The deep sea is a major sink for microplastic debris. Royal Society Open Science, 1: 140317.
Woods, M. N., Stack, M. E., Fields, D. M., Shaw, S. D., and Matrai, P. A., 2018. Microplastic fiber uptake, ingestion, and egestion rates in the blue mussel (Mytilus edulis). Marine Pollution Bulletin, 137: 638–645.
Wright, S. L., Thompson, R. C., and Galloway, T. S., 2013. The physical impacts of microplastics on marine organisms: A review. Environmental Pollution, 178: 483–492.
Wu, H., Peng, C., Huang, H., Jefferson, T. A., Huang, S. L., Chen, M., et al., 2020. Dolphin-watching tourism and Indo-Pacific humpback dolphins (Sousa chinensis) in Sanniang Bay, China: Impacts and solutions. European Journal of Wildlife Research, 66: 1–9.
Xie, X., Wu, Z., Wang, C. C., Fu, Y., Wang, X., Xu, P., et al., 2020. Nursery habitat for Asian horseshoe crabs along the northern Beibu Gulf, China: Implications for conservation management under baseline gaps. Aquatic Conservation: Marine and Freshwater Ecosystems, 30: 260–272.
Xu, X., Wong, C. Y., Tam, N. F. Y., Liu, H. M., and Cheung, S. G., 2020a. Barnacles as potential bioindicator of microplastic pollution in Hong Kong. Marine Pollution Bulletin, 154: 111081.
Xu, X., Wong, C. Y., Tam, N. F. Y., Lo, H. S., and Cheung, S. G., 2020b. Microplastics in invertebrates on soft shores in Hong Kong: Influence of habitat, taxa and feeding mode. Science of the Total Environment, 715: 136999.
Yao, P., Zhou, B., Lu, Y., Yin, Y., Zong, Y., Chen, M. T., et al., 2019. A review of microplastics in sediments: Spatial and temporal occurrences, biological effects, and analytic methods. Quaternary International, 519: 274–281.
Zhang, L., Liu, J., Xie, Y., Zhong, S., Yang, B., Lu, D., et al., 2020a. Distribution of microplastics in surface water and sediments of Qin River in Beibu Gulf, China. Science of the Total Environment, 708: 135176.
Zhang, L., Zhang, S., Guo, J., Yu, K., Wang, Y., and Li, R., 2020b. Dynamic distribution of microplastics in mangrove sediments in Beibu Gulf, South China: Implications of tidal current velocity and tidal range. Journal of Hazardous Materials, 399: 122849.
Zhang, S., Sun, Y., Liu, B., and Li, R., 2021a. Full size microplastics in crab and fish collected from the mangrove wetland of Beibu Gulf: Evidences from Raman Tweezers (1–20 µm) and spectroscopy (20–5000 µm). Science of the Total Environment, 759: 143504.
Zhang, T., Sun, Y., Song, K., Du, W., Huang, W., Gu, Z., et al., 2021b. Microplastics in different tissues of wild crabs at three important fishing grounds in China. Chemosphere, 271: 129479.
Zhao, S., Zhu, L., Wang, T., and Li, D., 2014. Suspended microplastics in the surface water of the Yangtze Estuary System, China: First observations on occurrence, distribution. Marine Pollution Bulletin, 86: 562–568.
Zhou, Q., Tu, C., Fu, C., Li, Y., Zhang, H., Xiong, K., et al., 2020. Characteristics and distribution of microplastics in the coastal mangrove sediments of China. Science of the Total Environment, 703: 134807.
Zhu, D., Bi, Q. F., Xiang, Q., Chen, Q. L., Christie, P., Ke, X., et al., 2018. Trophic predator-prey relationships promote transport of microplastics compared with the single Hypoaspis aculeifer and Folsomia candida. Environmental Pollution, 235: 150–154.
Zhu, J., Zhang, Q., Li, Y., Tan, S., Kang, Z., Yu, X., et al., 2019. Microplastic pollution in the Maowei Sea, a typical mariculture bay of China. Science of the Total Environment, 658: 62–68.
Zhu, X., Qiang, L., Shi, H., and Cheng, J., 2020. Bioaccumulation of microplastics and its in vivo interactions with trace metals in edible oysters. Marine Pollution Bulletin, 154: 111079.
Acknowledgements
We thank Dr. Paul Shin and many other researchers who provided feedback and information which considerably enhanced the quality of this manuscript. The assistance from Dr. Chun-Chieh Wang from Guangxi Academy of Sciences for preparing the maps is much appreciated. This research was supported by the National Natural Science Foundation of China (No. 41907320), the Natural Science Foundation of Guangxi Region (No. 2019 JJA150043), the Guangxi BaGui Youth Scholars Programme, and Guangxi Recruitment Program of 100 Global Experts.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Wang, X., Lo, H.S., Fu, Y. et al. High Microplastic Contamination in Juvenile Tri-Spine Horseshoe Crabs: A Baseline Study of Nursery Habitats in Northern Beibu Gulf, China. J. Ocean Univ. China 21, 521–530 (2022). https://doi.org/10.1007/s11802-022-5163-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11802-022-5163-3