Abstract
We examined the multiple effects of a typhoon strike and agricultural wastewater effluent on benthic faunal communities at the mangrove estuary in Nagura Lagoon, Ishigaki Island, Okinawa, Japan. Environmental parameters and benthic macrofaunal community structures were compared at wastewater-impacted and intact reference sites (which were nested in canopy-covered forests and fringing mudflats), before and after the typhoon strike. Most physical and chemical factors were not affected by wastewater loading, typhoon strikes, or habitat differences; however, organic parameters (food resource environment) were changed; wastewater input raised amounts of microphytobenthos and mangrove litter, while a typhoon strike significantly increased phytoplankton biomass. Wastewater effluent also increased the numerical abundance and species richness of benthic macrofauna; however, a typhoon strike did not induce such changes. Species compositions were clearly divided into pre-and post-typhoon periods at the reference site, but were classified into the same cluster at the wastewater site, regardless of the typhoon. The typhoon-induced compositional shift is caused by the removal of vulnerable arboreal species and facultative opportunistic species recruitment. However, wastewater that causes organic-rich conditions would lock such community dynamics by enhancing the predominance of species that prefer and tolerate eutrophic conditions. Overall, the impact of anthropogenic wastewater could outweigh those of natural typhoon disturbances on benthic faunal communities in mangrove estuaries.
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References
Armitage, A. R., C. A. Weaver, J. S. Kominoski & S. C. Pennings, 2020. Resistance to hurricane effects varies among wetland vegetation types in the marsh-mangrove ecotone. Estuaries and Coasts 43(5): 960–970.
Bender, E. A., T. J. Case & M. E. Gilpin, 1984. Perturbation experiments in community ecology: theory and practice. Ecology 65(1): 1–13.
Bosire, J. O., J. G. Kairo, J. Kazungu, N. Koedam & F. Dahdouh-Guebas, 2005. Predation on propagules regulates regeneration in a high-density reforested mangrove plantation. Marine Ecology Progress Series 299: 149–155.
Bouchez, A., N. Pascault, C. Chardon, M. Bouvy, P. Cecchi, L. Lambs, M. Herteman, F. Fromard, P. Got & C. Leboulanger, 2013. Mangrove microbial diversity and the impact of trophic contamination. Marine Pollution Bulletin 66(1–2): 39–46.
Bouillon, S., N. Koedam, A. V. Raman & F. Dehairs, 2002. Primary producers sustaining macro-invertebrate communities in intertidal mangrove forests. Oecologia 130(3): 441–448.
Buma, B., 2015. Disturbance interactions: characterization, prediction, and the potential for cascading effects. Ecosphere 6(4): 70.
Cahoon, L., 1999. The role of benthic microalgae in neritic ecosystems. Oceanography and Marine Biology: An Annual Review 37: 47–86.
Cloern, J., 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210: 223–253.
Commito, J. A., S. F. Thrush, R. D. Pridmore, J. E. Hewitt & V. J. Cummings, 1995. Dispersal dynamics in a wind-driven benthic system. Limnology and Oceanography 40(8): 1513–1518.
Connell, J. H., 1987. Change and persistence in some marine communities. In J., G. A., C. M. J. & E. P. J. (eds) Colonization, succession, and stability: the 26th Symposium of the British Ecological Society held jointly with the Linnean Society of London. Blackwell, Oxford, England, 339–352.
Corredor, J. E. & J. M. Morell, 1994. Nitrate depuration of secondary sewage effluents in mangrove sediments. Estuaries 17(1): 295–300.
Costa, L. L., I. R. Zalmon, L. Fanini & O. Defeo, 2020. Macroinvertebrates as indicators of human disturbances on sandy beaches: a global review. Ecological Indicators 118: 106764.
Costanza, R., R. dArge, R. deGroot, S. Farber, M. Grasso, B. Hannon, K. Limburg, S. Naeem, R. V. ONeill, J. Paruelo, R. G. Raskin, P. Sutton & M. vandenBelt, 1997. The value of the world's ecosystem services and natural capital. Nature 387(6630):253-260.
Cote, I. M., E. S. Darling & C. J. Brown, 2016. Interactions among ecosystem stressors and their importance in conservation. Proceedings of Royal Society B 283: 20152592.
Creese, R. G. & W. J. Ballantine, 1983. An assessment of breeding in the intertidal limpet, Cellana radians (Gmelin). Journal of Experimental Marine Biology and Ecology 67(1): 43–59.
Das, S. & A. S. Crepin, 2013. Mangroves can provide protection against wind damage during storms. Estuarine, Coastal and Shelf Science 134: 98–107.
Duque, G., D. E. Gamboa-García, A. Molina & P. Cogua, 2020. Effect of water quality variation on fish assemblages in an anthropogenically impacted tropical estuary, Colombian Pacific. Environmental Science and Pollution Research 27(20): 25740–25753.
Feller, I. C., E. M. Dangremond, D. J. Devlin, C. E. Lovelock, C. E. Proffitt & W. Rodriguez, 2015. Nutrient enrichment intensifies hurricane impact in scrub mangrove ecosystems in the Indian River Lagoon, Florida, USA. Ecology 96(11): 2960–2972.
Ferreira, J. G., J. H. Andersen, A. Borja, S. B. Bricker, J. Camp, M. Cardoso da Silva, E. Garcés, A.-S. Heiskanen, C. Humborg, L. Ignatiades, C. Lancelot, A. Menesguen, P. Tett, N. Hoepffner & U. Claussen, 2011. Overview of eutrophication indicators to assess environmental status within the European Marine Strategy Framework Directive. Estuarine, Coastal and Shelf Science 93(2): 117–131.
Griffen, B. D., B. A. Belgrad, Z. J. Cannizzo, E. R. Knotts & E. R. Hancock, 2016. Rethinking our approach to multiple stressor studies in marine environments. Marine Ecology Progress Series 543: 273–281.
Halpern, B. S., S. Walbridge, K. A. Selkoe, C. V. Kappel, F. Micheli, C. D’Agrosa, J. F. Bruno, K. S. Casey, C. Ebert, H. E. Fox, R. Fujita, D. Heinemann, H. S. Lenihan, E. M. P. Madin, M. T. Perry, E. R. Selig, M. Spalding, R. Steneck & R. Watson, 2008. A global map of human impact on marine ecosystems. Science 319(5865): 948–952
Hedouin, L., O. Pringault, P. Bustamante, R. Fichez & M. Warnau, 2011. Validation of two tropical marine bivalves as bioindicators of mining contamination in the New Caledonia lagoon: field transplantation experiments. Water Research 45(2): 483–496.
Heip, C., D. Basford, J. A. Craeymeersch, J. M. Dewarumez, J. Dorjes, P. Dewilde, G. Duineveld, A. Eleftheriou, P. M. J. Herman, U. Niermann, P. Kingston, A. Kunitzer, E. Rachor, H. Rumohr, K. Soetaert & T. Soltwedel, 1992. Trends in biomass, density and diversity of North Sea macrofauna. ICES Journal of Marine Science 49(1): 13–22.
Hobbs, R. J. & L. F. Huenneke, 1992. Disturbance, diversity, and invasion—implications for conservations. Conservation Biology 6(3): 324–337.
Hogarth, P. J., 2007. The Biology of Mangroves and Seagrasses, 2nd ed. Oxford University Press, New York:
Holm-Hansen, O., C. J. Lorenzen, R. W. Holmes & J. D. H. Strickland, 1985. Fluorometric determination of chlorophyll. Journal Du Conseil / Conseil Permanent International Pour L’exploration De La Mer 30(1): 3–15.
Japan Metrological Agency, 2018. Report for typhoon no. 8 in 2018. https://www.jma-net.go.jp/okinawa/data/kencho/T2018/T1808.pdf/
Kenny, A. J. & I. Sotheran, 2013. Characterising the physical properties of seabed habitat. In Eleftheriou, A. (ed), Methods for the Study of Marine Benthos 4th ed. Wiley-Blackwell, West Sussex: 47–95.
Komiyama, A., J. E. Ong & S. Poungparn, 2008. Allometry, biomass, and productivity of mangrove forests: a review. Aquatic Botany 89(2): 128–137.
Kon, K., H. Kurokura & K. Hayashizaki, 2007. Role of microhabitats in food webs of benthic communities in a mangrove forest. Marine Ecology Progress Series 340: 55–62.
Krauss, K. W., T. W. Doyle, T. J. Doyle, C. M. Swarzenski, A. S. From, R. H. Day & W. H. Conner, 2009. Water level observations in mangrove swamps during two hurricanes in Florida. Wetlands 29(1): 142–149.
Lebata, J. H. L. & J. H. Primavera, 2001. Gill structure, anatomy and habitat of Anodontia edentula: evidence of endosymbiosis. Journal of Shellfish Research 20(3): 1273–1278.
Lee, S. Y., 1998. Ecological role of grapsid crabs in mangrove ecosystems: a review. Marine and Freshwater Research 49(4): 335–343.
Leopardas, V., K. Honda, G. A. Go, K. Bolisay, A. D. Pantallano, W. Uy, M. Fortes & M. Nakaoka, 2016. Variation in macrofaunal communities of sea grass beds along a pollution gradient in Bolinao, northwestern Philippines. Marine Pollution Bulletin 105(1): 310–318.
Liu, H. Q., K. Q. Zhang, Y. P. Li & L. Xie, 2013. Numerical study of the sensitivity of mangroves in reducing storm surge and flooding to hurricane characteristics in southern Florida. Continental Shelf Research 64: 51–65.
Lotze, H. K., H. S. Lenihan, B. J. Bourque, R. H. Bradbury, R. G. Cooke, M. C. Kay, S. M. Kidwell, M. X. Kirby, C. H. Peterson & J. B. C. Jackson, 2006. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312(5781): 1806–1809.
Matthews, T. G. & P. G. Fairweather, 2003. Growth rates of the infaunal bivalve Soletellina alba (Lamarck, 1818) (Bivalvia: Psammobiidae) in an intermittent estuary of southern Australia. Estuarine. Coastal and Shelf Science 58(4): 873–885.
Mazda, Y., M. Magi, Y. Ikeda, T. Kurokawa & T. Asano, 2006. Wave reduction in a mangrove forest dominated by Sonneratia sp. Wetlands. Forest Ecology and Management 14(4): 365–378.
Monk, W. A., Z. G. Compson, C. B. Choung, K. L. Korbel, N. K. Rideout & D. J. Baird, 2019. Urbanisation of floodplain ecosystems: Weight-of-evidence and network meta-analysis elucidate multiple stressor pathways. Science of The Total Environment 684: 741–752.
Mukherjee, S., A. Chaudhuri, S. Sen & S. Homechaudhuri, 2012. Effect of Cyclone Aila on estuarine fish assemblages in the Matla River of the Indian Sundarbans. Journal of Tropical Ecology 28: 405–415.
Myers, R. A. & B. Worm, 2003. Rapid worldwide depletion of predatory fish communities. Nature 423(6937): 280–283.
Nagelkerken, I., S. J. M. Blaber, S. Bouillon, P. Green, M. Haywood, L. G. Kirton, J.-O. Meynecke, J. Pawlik, H. M. Penrose, A. Sasekumar & P. J. Somerfield, 2008. The habitat function of mangroves for terrestrial and marine fauna: a review. Aquatic Botany 89(2): 155–185.
Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, E. Szoecs, & H. Wagner (2020) vegan: Community Ecology Package. R package version 2.5.7. https://CRAN.R-project.org/package=vegan.
Onitsuka, T., T. Kawamura, T. Horii, N. Takiguchi, H. Takami & Y. Watanabe, 2007. Synchronized spawning of abalone Haliotis diversicolor triggered by typhoon events in Sagami Bay, Japan. Marine Ecology Progress Series 351: 129–138.
Ostrowski, A., R. M. Connolly & M. Sievers, 2021. Evaluating multiple stressor research in coastal wetlands: a systematic review. Marine Environmental Research 164: 105239.
Patrick, C. J., L. Yeager, A. R. Armitage, F. Carvallo, V. M. Congdon, K. H. Dunton, M. Fisher, A. K. Hardison, J. D. Hogan, J. Hosen, X. Hu, B. K. Reese, S. Kinard, J. S. Kominoski, X. Lin, Z. Liu, P. A. Montagna, S. C. Pennings, L. Walker, C. A. Weaver & M. Wetz, 2020. A system level analysis of coastal ecosystem responses to hurricane impacts. Estuaries and Coasts 43(5): 943–959.
Pausas, J. G. & J. E. Keeley, 2009. A burning story: the role of fire in the history of life. Bioscience 59(7): 593–601.
Pausas, J. G., J. E. Keeley & M. Verdu, 2006. Inferring differential evolutionary processes of plant persistence traits in Northern Hemisphere Mediterranean fire-prone ecosystems. Journal of Ecology 94(1): 31–39.
Pearson, T. & R. Rosenberg, 1977. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanography and Marine Biology: An Annual Review 16: 229–311.
Queiroz, H. M., T. O. Ferreira, C. A. K. Taniguchi, D. Barcellos, J. C. do Nascimento, G. N. Nóbrega, X. L. Otero & A. G. Artur, 2020. Nitrogen mineralization and eutrophication risks in mangroves receiving shrimp farming effluents. Environmental Science and Pollution Research 27(28): 34941–34950.
Ren, S., A. Ali, H. Liu, Z. Yuan, Q. Yang, G. Shen, S. Zhou & X. Wang, 2021. Response of community diversity and productivity to canopy gap disturbance in subtropical forests. Forest Ecology and Management 502: 119740.
Riva, F., J. Pinzon, J. H. Acorn & S. E. Nielsen, 2020. Composite effects of cutlines and wildfire result in fire refuges for plants and butterflies in boreal treed peatlands. Ecosystems 23(3): 485–497.
Salmo, S. G., I. R. Tibbetts & N. C. Duke, 2019. Recolonization of mollusc assemblages in mangrove plantations damaged by Typhoon Chan-hom in the Philippines. Estuarine, Coastal and Shelf Science 228(15): 106365
Sheaves, M. & B. Molony, 2000. Short-circuit in the mangrove food chain. Marine Ecology Progress Series 199: 97–109.
Smith, T. J., K. G. Boto, S. D. Frusher & R. L. Giddins, 1991. Keystone species and mangrove forest dynamics: the influence of burrowing by crabs on soil nutrient status and forest productivity. Estuarine, Coastal and Shelf Science 33(5): 419–432.
Smith, T. J., M. B. Robblee, H. R. Wanless & T. W. Doyle, 1994. Mangroves, hurricanes, and lightning strikes. Bioscience 44(4): 256–262.
Swiadek, J. W., 1997. The impacts of Hurricane Andrew on mangrove coasts in southern Florida: a review. Journal of Coastal Research 13(1): 242–245.
Taylor, J. D. & E. A. Glover, 2010. Chemosymbiotic bivalves. In Kiel, S. (ed), The Vent and Seep Biota: Aspects from Microbes to Ecosystems Springer, Dordrecht: 107–135.
Van den Brink, P., C. Choung, W. Landis, M. Mayer-Pinto, V. Pettigrove, P. Scanes, R. Smith & J. Stauber, 2016. New approaches to the ecological risk assessment of multiple stressors. Marine and Freshwater Research 67: 429–439.
Verhoeven, J. T. A., B. Arheimer, C. Yin & M. M. Hefting, 2006. Regional and global concerns over wetlands and water quality. Trends in Ecology & Evolution 21(2): 96–103.
Wada, K., A. Komiyama & K. Ogino, 1987. Underground vertical distribution of macrofauna and root in a mangrove forest of Southern Thailand. Publications of the Seto Marine Biological Laboratory 32: 329–333.
Withers, P. J. A., C. Neal, H. P. Jarvie & D. G. Doody, 2014. Agriculture and eutrophication: where do we go from here? Sustainability 6(9): 5853–5875.
Wong, Y. S., C. Y. Lan, G. Z. Chen, S. H. Li, X. R. Chen, Z. P. Liu & N. F. Y. Tam, 1995. Effect of wastewater discharge on nutrient contamination of mangrove soils and pants. Hydrobiologia 295(1–3): 243–254.
Wong, Y. S., N. F. Y. Tam, G. Z. Chen & H. Ma, 1997. Response of Aegiceras corniculatum to synthetic sewage under simulated tidal conditions. Hydrobiologia 352: 89–96.
World Meteorological Organization (2015) Typhoon committee operational manual 2015. 2015 edn. World Meteorological Organization, Geneva, 169.
Zar, J. H., 2010. Biostatistical analysis, 5th ed. Prentice Hall, New Jersey
Zhang, K. Q., H. Q. Liu, Y. P. Li, H. Z. Xu, J. Shen, J. Rhome & T. J. Smith, 2012. The role of mangroves in attenuating storm surges. Estuarine, Coastal and Shelf Science 102: 11–23.
Zheng, G. M. & D. Tang, 2007. Offshore and nearshore chlorophyll increases induced by typhoon winds and subsequent terrestrial rainwater runoff. Marine Ecology Progress Series 333: 61–74.
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The authors are grateful to the staff of the Yaeyama Field Station, Fisheries Technology Institute for assistance in fieldwork.
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The present work was supported in part by Grants-in-Aid for Scientific Research (B) from the Ministry of Education, Science, Sports, and Culture of Japan (17H03628).
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KK contributed to conceptualization, formal analysis, investigation, and writing—original draft. AG contributed to formal analysis and investigation. IT contributed to resources, investigation, writing- reviewing, and editing. HY contributed to writing- reviewing and editing and funding acquisition.
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Kon, K., Goto, A., Tanita, I. et al. Multiple effects of a typhoon strike and wastewater effluent on benthic macrofaunal communities in a mangrove estuary. Hydrobiologia 849, 2569–2579 (2022). https://doi.org/10.1007/s10750-022-04877-x
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DOI: https://doi.org/10.1007/s10750-022-04877-x