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Did Species and Functional Diversities of Sandy Intertidal Marine Nematodes Reveal Similar Response to Environmental Changes?

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Abstract

Free living marine nematodes were sampled from two sandy beaches in Dalian City, in December of 2015, and April, July, and October of 2016. The spatial and seasonal variations of marine nematode species diversity (based on species abundance dataset) and functional diversity (based on functional traits dataset: feeding types and life history strategies) were investigated to understand the environmental drivers and how they respond to specific environmental variations. Sediment granularity was revealed to be the main environmental factor causing spatial differences in nematode diversity indices between the two beaches. Species diversity indices, namely species number, Margalef index, Shannon-Wiener diversity index (H′), were higher in fine-grained sediments, while the functional diversity indices, including functional evenness, functional dispersion, and Rao’s quadratic entropy index (RaoQ), were higher in coarse-grained sediments. Nematode species diversity indices also fluctuated with seasonal variations of temperature, dissolved oxygen, pH, salinity, and sediment chlorophyll-a within the study beaches. However, functional diversity indices did not show significant seasonal variations and exhibited weak correlation with the studied environmental variables. Overall, the functional diversity indices were negatively correlated with the species diversity indices, suggesting an inconsistent response to environmental changes. A decrease in nematode species diversity in coarse sands, accompanied by an increase in functional diversity, can be regarded as an early warning signal of environment disturbance. If more biological traits are involved in calculating functional diversity indices, it will be helpful for the future study of the internal connections of species diversity and functional diversity.

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References

  • Anderson, M. J., Gorley, R. N., and Clarke, K. R., 2008. PERMANOVA+for PRIMER: Guide to Software and Statistical Methods. Plymouth, UK, 214pp.

  • Appeltans, W., Ahyong, S. T., Anderson, G., Angel, M. V., Artois, T., Bailly, N., et al., 2012. The magnitude of global marine species diversity. Current Biology, 22: 2189–2202, DOI: https://doi.org/10.1016/j.cub.2012.09.036.

    Article  Google Scholar 

  • Armonies, W., and Reise, K., 2000. Faunal diversity across a sandy-shore. Marine Ecology Progress Series, 196: 49–57, DOI: https://doi.org/10.3354/meps196049.

    Article  Google Scholar 

  • Baia, E., Rollnic, M., and Venekey, V., 2021. Seasonality of pluviosity and saline intrusion drive meiofauna and nematodes on an Amazon freshwater-oligohaline beach. Journal of Sea Research, 170: 102022, DOI: https://doi.org/10.1016/j.seares.2021.102022.

    Article  Google Scholar 

  • Baldrighi, E., and Manini, E., 2015. Deep-sea meiofauna and macrofauna diversity and functional diversity: Are they related? Marine Biodiversity, 45(3): 469–488, DOI: https://doi.org/10.1007/s12526-015-0333-9.

    Article  Google Scholar 

  • Bezerra, T. N., Eisendle, U., Hodda, M., Holovachov, O., Leduc, D., Mokievsky, V., et al., 2021. Nemys: World Database of Nematodes. Accessed at http://nemys.ugent.be on 2021-09-27, DOI: https://doi.org/10.14284/366.

  • Bianchelli, S., Buschi, E., Danovaro, R., and Pusceddu, A., 2018. Nematode biodiversity and benthic trophic state are simple tools for the assessment of the environmental quality in coastal marine ecosystems. Ecological Indicators, 95(1): 270–287, DOI: https://doi.org/10.1016/j.ecolind.2018.07.032.

    Article  Google Scholar 

  • Bongers, T., Alkemade, R., and Yeates, G. W., 1991. Interpretation of disturbance induced maturity decrease in marine nematode assemblages by means of the maturity index. Marine Ecology Progress Series, 76: 135–142, DOI: https://doi.org/10.3354/meps076135.

    Article  Google Scholar 

  • Bongers, T., and Bongers, M., 1998. Functional diversity of nematodes. Applied Soil Ecology, 10: 239–251.

    Article  Google Scholar 

  • Bongers, T., de Goede, R. G. M., Korthals, G. W., and Yeates, G. W., 1995. Proposed changes of c-p classification for nematodes. Russian Journal of Nematology, 3: 61–62.

    Google Scholar 

  • Bremner, J., Rogers, S. I., and Frid, C. L. J., 2003. Assessing functional diversity in marine benthic ecosystems: A comparison of approaches. Marine Ecology Progress Series, 254: 11–25, DOI: https://doi.org/10.3354/meps254011.

    Article  Google Scholar 

  • Cai, L. Z., Fu, S. J., Zhou, X. P., Tseng, L. C., and Hwang, J. S., 2020. Benthic meiofauna with emphasis on nematode assemblage response to environmental variation in the intertidal zone of the Danshuei River estuary, northwest Taiwan. Ecological Research, 35(5): 857–870, DOI: https://doi.org/10.1111/1440-1703.12159.

    Article  Google Scholar 

  • Clarke, K. R., and Gorley, R. N., 2015. PRIMER v7: User Manual/Tutorial (Plymouth Routines in Multivariate Ecological Research). PRIMER-E, Plymouth, 296pp.

    Google Scholar 

  • Danovaro, R., 2010. Methods for the Study of Deep-Sea Sediments Their Functioning and Biodiversity. CRC Press, Boca Raton, FL, 458pp.

    Google Scholar 

  • Fenchel, T. M., 1978. The ecology of micro- and meiobenthos. Annual Review of Ecology and Systematics, 9: 99–121.

    Article  Google Scholar 

  • Friberg, N., Bonada, N., Bradley, D. C., Dunbar, M. J., Edwards, F. K., Grey, J., et al., 2011. Biomonitoring of human impacts in freshwater ecosystems: The good, the bad and the ugly. Advances in Ecological Research, 44: 1–68, DOI: https://doi.org/10.1016/B978-0-12-374794-5.00001-8.

    Article  Google Scholar 

  • Gagic, V., Bartomeus, I., Jonsson, T., Taylor, A., Winqvist, C., Fischer, C., et al., 2015. Functional identity and diversity of animals predict ecosystem functioning better than species-based indices. Proceedings of the Royal Society of London B Biological Sciences, 282: 1–8.

    Google Scholar 

  • Gheskiere, T., Vincx, M., Urban-Malinga, B., Rossano, C., Scapini, F., and Degraer, S., 2005. Nematodes from wave-dominated sandy beaches: Diversity, zonation patterns and testing of the isocommunities concept. Estuarine, Coastal and Shelf Science, 62: 365–375.

    Article  Google Scholar 

  • Giere, O., 2009. Meiobenthology: The Microscopic Motile Fauna of Aquatic Sediments. Springer-Verlag, Berlin, 538pp.

    Google Scholar 

  • Grzelak, K., Gluchowska, M., Gregorczyk, K., Winogradow, A., and Weslawski, J. M., 2016. Nematode biomass and morphometric attributes as biological indicators of local environmental conditions in arctic fjords. Ecological Indicators, 69: 368–380.

    Article  Google Scholar 

  • Harris, R. P., 1972. The distribution and ecology of the interstitial meiofauna of a sandy beach at Whitsand Bay, East Cornwall. Journal of the Marine Biological Association of the United Kingdom, 52(1): 1–18.

    Article  Google Scholar 

  • Heip, C., Vinx, M., and Vranken, G., 1985. The ecology of marine nematodes. Oceanography and Marine Biology, 23: 399–489.

    Google Scholar 

  • Hooper, D. U., Chapin, F. S., Ewel, J. J., Hector, A., Inchausti, P., Lavorel, S., et al., 2005. Effects of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecological Monographs, 75: 3–35, DOI: https://doi.org/10.1890/04-0922.

    Article  Google Scholar 

  • Hua, E., Li, J., Dong, J., Xu, F. F., and Zhang, Z. N., 2012. Responses of sandy beach nematodes to oxygen deficiency: Microcosm experiments. Acta Ecologica Sinica, 32(13): 3975–3986 (in Chinese with English abstract).

    Article  Google Scholar 

  • Hua, E., Mu, F. H., Zhang, Z. N., Yang, S. C., Zhang, T., and Li, J., 2016a. Nematode community structure and diversity pattern in sandy beaches of Qingdao, China. Journal of Ocean University of China, 15: 33–40.

    Article  Google Scholar 

  • Hua, E., Sun, Y. T., Zhang, Z. N., He, L., Cui, C. Y., and Mu, F. H., 2019. Effects of reduced seawater pH on nematode community composition and diversity in sandy sediments. Marine Environmental Research, 150: 104773, DOI: https://doi.org/10.1016/j.marenvres.2019.104773.

    Article  Google Scholar 

  • Hua, E., Zhang, Z. N., Zhou, H., Mu, F. H., Li, J., Zhang, T., et al., 2016b. Meiofauna distribution in intertidal sandy beaches along China shoreline (18°–40°N). Journal of Ocean University of China, 15(1): 19–27.

    Article  Google Scholar 

  • Hua, E., Zhu, Y. M., Huang, D. M., and Liu, X. S., 2021. Are free-living nematodes effective environmental quality indicators? Insights from Bohai Bay, China. Ecological Indicators, 127: 107756, DOI: https://doi.org/10.1016/j.ecolind.2021.107756.

    Article  Google Scholar 

  • Ingels, J., dos Santos, G., Hicks, N., Vazquez, Y. V., Neres, P. F., Pontes, L. P., et al., 2018. Short-term CO2 exposure and temperature rise effects on metazoan meiofauna and free-living nematodes in sandy and muddy sediments: Results from aflume experiment. Journal of Experimental Marine Biology and Ecology, 502: 211–226.

    Article  Google Scholar 

  • Jin, Z. X., 2021. Analysis of Dalian City climate change in recent 50 years. Territory and Natural Resources Study, 4: 16–21 (in Chinese with English abstract).

    Google Scholar 

  • Kasia, S., Paula, C., Soraia, V., and Helena, A., 2021. What makes a better indicator? Taxonomic vs functional response of nematodes to estuarine gradient. Ecological Indicators, 121: 107113, DOI: https://doi.org/10.1016/j.ecolind.2020.107113.

    Article  Google Scholar 

  • Leduc, D., Rowden, A. A., Pilditch, C. A., Maas, E. W., and Probert, P. K., 2013. Is there a link between deep-sea biodiversity and ecosystem function? Marine Ecology, 34(3): 334–344, DOI: https://doi.org/10.1111/maec.12019.

    Article  Google Scholar 

  • Liao, J. X., Wei, C. L., and Yasuhara, M., 2020. Species and functional diversity of deep-sea nematodes in a high energy submarine canyon. Frontiers in Marine Science, 7: 591, DOI: https://doi.org/10.3389/fmars.2020.00591.

    Article  Google Scholar 

  • Linden, P. V. D., Patrício, J., Marchini, A., Cid, N., Neto, J. M., and Marques, J. C., 2012. A biological trait approach to assess the functional composition of subtidal benthic communities in an estuarine ecosystem. Ecological Indicators, 20: 121–133.

    Article  Google Scholar 

  • Liu, C. L., Zhu, Z. G., He, X. L., Zhang, B., and Ning, X., 2007. Rapid determination of organic carbon in marine sediment samples by potassium dichromate oxidation ferrous sulphate titrimetry. Rock and Mineral Analysis, 26(3): 205–208 (in Chinese with English abstract).

    Google Scholar 

  • Liu, H., Wu, Y. P., Gao, S. D., and Zhang, Z. N., 1998. The variations of chlorophyll-a and phaeophytin in the sediment of Jimo shrimp pond before the outbreak of shrimp disease. Transactions of Oceanology and Limnology, 1: 65–69.

    Google Scholar 

  • Liu, X. S., Liu, Q. H., Zhang, Y., Hua, E., and Zhang, Z. N., 2018. Effects of Yellow Sea Cold Water Mass on marine nematodes based on biological trait analysis. Marine Environmental Research, 141: 167–185, DOI: https://doi.org/10.1016/j.marenvres.2018.08.013.

    Article  Google Scholar 

  • Lorenzen, C. J., and Jeffrey, S. W., 1980. Determination of chlorophyll in seawater. UNESCO Technical Papers in Marine Science, 35(1): 1–12.

    Google Scholar 

  • Lv, Y., Zhang, W. D., Gao, Y., Ning, S. X., and Yang, B., 2011. Preliminary study on responses of marine nematode community to crude oil contamination in intertidal zone of Bathing Beach, Dalian. Marine Pollution Bulletin, 62(12): 2700–2706, DOI: https://doi.org/10.1016/j.marpolbul.2011.09.018.

    Article  Google Scholar 

  • Materatski, P., Ribeiro, R., Moreira-Santos, M., Sousa, J. P., and Adão, H., 2018. Nematode biomass and morphometric attributes as descriptors during a major Zostera noltii collapse. Marine Biology, 165(2): 1–17, DOI: https://doi.org/10.1007/s00227-018-3283-5.

    Article  Google Scholar 

  • McLachlan, A., and Brown, A. C., 2006. The Ecology of Sandy Shores. Academic Press, Burlington, 392pp, DOI: https://doi.org/10.1016/B978-0-12-372569-1.X5000-9.

    Google Scholar 

  • Mouillot, D., Graham, N. A. J., Villéger, S., Mason, N. W. H., and Bellwood, D. R., 2013. A functional approach reveals community responsesto disturbances. Trendsin Ecology and Evolution, 28: 167–177.

    Article  Google Scholar 

  • Mulder, C., Boit, A., Mori, S., Vonk, J. A., Dyer, S. D., Faggiano, L., et al., 2012. Distributional (in)congruence of biodiversityecosystem functioning. Advances in Ecological Research, 48: 1–88.

    Google Scholar 

  • National Marine Data and Information Service, 2015. Tide Tables. Maritime Press, Beijing, 536pp (in Chinese with English abstract).

    Google Scholar 

  • Nicholas, W. L., 2001. Seasonal variations in nematode assemblages on an Australian temperate ocean beach; the effect of heavy seas and unusually high tides. Hydrobiologia, 464(1/3): 17–26.

    Article  Google Scholar 

  • Petchey, O. L., and Gaston, K. J., 2002. Functional diversity (FD), species richness and community composition. Ecology Letters, 5(3): 402–411, DOI: https://doi.org/10.1046/j.1461-0248.2002.00339.x.

    Article  Google Scholar 

  • Petchey, O. L., and Gaston, K. J., 2006. Functional diversity: Back to basics and looking forward. Ecology Letters, 9(6): 741–758, DOI: https://doi.org/10.1111/j.1461-0248.2006.00924.x.

    Article  Google Scholar 

  • Platt, H. M., and Warwick, R. M., 1983. Free-Living Marine Nematodes. Part I British Enoplids. Cambridge University Press, Cambridge, 307pp.

    Google Scholar 

  • Platt, H. M., and Warwick, R. M., 1988. Free-Living Marine Nematodes. Part II British Chromadorids. Cambridge University Press, Cambridge, 502pp.

    Google Scholar 

  • Rao, C. R., 1982. Diversity and dissimilarity coefficients: A unified approach. Theoretical Population Biology, 21(1): 24–43.

    Article  Google Scholar 

  • Riera, R., Núez, J., Brito, M. D. C., and Tuya, F., 2011. Seasonal variability of a subtropical intertidal meiofaunal assemblage: Contrasting effects at the species and assemblage-level. Vie et Milieu -Life and Environment, 61(3): 129–137.

    Google Scholar 

  • Santos, T. M. T., Petracco, M., and Venekey, V., 2021. Recreational activities trigger changes in meiofauna and free-living nematodes on Amazonian macrotidal sandy beaches. Marine Environmental Research, 167: 105289.

    Article  Google Scholar 

  • Schlacher, T. A., Schoeman, D. S., Dugan, J., Lastra, M., Jones, A., Scapini, F., et al., 2008. Sandy beach ecosystems: Key features, sampling issues, management challenges and climate change impacts. Marine Ecology, 29: 70–90, DOI: https://doi.org/10.1111/j.1439-0485.2007.00204.x.

    Article  Google Scholar 

  • Schratzberger, M., Warr, K., and Rogers, S. I., 2007. Functional diversity of nematode communities in the southwestern North Sea. Marine Environmental Research, 63(4): 368–389.

    Article  Google Scholar 

  • Semprucci, F., Balsamo, M., and Frontalini, F., 2014. The nematode assemblage of a coastal lagoon (Lake Varano, southern Italy): Ecology and biodiversity patterns. Scientia Marina, 78: 579–588.

    Article  Google Scholar 

  • Sheaves, M., 2006. Scale-dependent variation in composition of fish fauna among sandy tropical estuarine embayments. Marine Ecology Progress Series, 310: 173–184, DOI: https://doi.org/10.3354/meps310173.

    Article  Google Scholar 

  • Song, H. L., Mu, F. H., Sun, Y., and Hua, E., 2021. Comparison of community structure and diversity of free-living marine nematodes in the sandy intertidal zone of Dalian in winter. Haiyang Xuebao, 43(8): 139–151, DOI: https://doi.org/10.12284/hyxb2021060 (in Chinese with English abstract).

    Google Scholar 

  • Song, J. M., and Duan, L. Q., 2019. The Bohai Sea. In: World Seas: An Environmental Evaluation. Volume II: The Indian Ocean to the Pacific. Sheppard, C., ed., Academic Press, United Kingdom, 377–394, DOI: https://doi.org/10.1016/B978-0-08-100853-9.00024-5.

    Google Scholar 

  • Su, J. L., and Yuan, Y. L., 2005. Hydrology in China Offshore. Ocean Press, Beijing, 367pp (in Chinese with English abstract).

    Google Scholar 

  • Sun, X. Y., Zhou, H., Hua, E., Xu, S. H., Cong, B. Q., and Zhang, Z. N., 2014. Meiofauna and its sedimentary environment as an integrated indication of anthropogenic disturbance to sandy beach ecosystems. Marine Pollution Bulletin, 88: 260–267, DOI: https://doi.org/10.1016/j.marpolbul.2014.08.033.

    Article  Google Scholar 

  • Vanaverbeke, J., Merckx, B., Degraer, S., and Vincx, M., 2011. Sediment-related distribution patterns of nematodes and macrofauna: Two sides of the benthic coin? Marine Environmental Research, 71: 31–40.

    Article  Google Scholar 

  • Villéger, S., Mason, N. W. H., and Mouillot, D., 2008. New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology, 89: 2290–2301, DOI: https://doi.org/10.1890/07-1206.1.

    Article  Google Scholar 

  • Warwick, R. M., Platt, H. M., and Somerfield, P. J., 1998. Free-Living Marine Nematodes. Part III British Monhysterids. The Linnean Society of London and the Estuarine and Coastal Sciences Association, London, 296pp.

    Google Scholar 

  • Wieser, W., 1953. Die Beziehung zwischen Mundhohlengestalt, Ernahrungsweise und Vorkommen bei freilebenden marinen Nematoden. Eine skologisen-morphologische studie. Arkiv für Zoologie, 4: 439–484.

    Google Scholar 

  • Wright, L., and Short, A., 1983. Morphodynamics of beaches and surf zones in Australia. In: Handbook of Coastal Processes and Erosion. Komar, P. D., ed., CRC Press, Boca Raton, 35–64.

    Google Scholar 

  • Xu, F. X., 2002. Lectures on ocean wave forecast part 5: Geographical distribution and seasonal variation of ocean waves. Marine Forecasts, 19(2): 74–79 (in Chinese with English abstract).

    Google Scholar 

  • Xu, M., Liu, Q. H., Zhang, Z. N., and Liu, X. S., 2016. Response of free-living marine nematodes to the southern Yellow Sea Cold Water Mass. Marine Pollution Bulletin, 105(1): 58–64.

    Article  Google Scholar 

  • Zhong, X., Qiu, B. C., and Liu, X. S., 2020. Functional diversity patterns of macrofauna in the adjacent waters of the Yangtze River Estuary. Marine Pollution Bulletin, 154: 111032, DOI: https://doi.org/10.1016/j.marpolbul.2020.111032.

    Article  Google Scholar 

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (Nos. 41976100, 41576153). We would like to thank all the members of the Laboratory of Biological Oceanography and Benthic Ecology in Ocean University of China for their assistance and support in the field sampling and laboratory processing activities.

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  1. College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China

    Huili Song, Fanghong Mu, Yan Sun & Er Hua

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Song, H., Mu, F., Sun, Y. et al. Did Species and Functional Diversities of Sandy Intertidal Marine Nematodes Reveal Similar Response to Environmental Changes?. J. Ocean Univ. China 22, 527–540 (2023). https://doi.org/10.1007/s11802-023-5256-7

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