Citation: | Jing-yi Cong, Hai-yan Long, Yong Zhang, Nan Wang, 2022. Ecological environment response of benthic foraminifera to heavy metals and human engineering: A case study from Jiaozhou Bay, China, China Geology, 5, 12-25. doi: 10.31035/cg2021040 |
The estuary and coastal zone are the key areas for socio-economic development, and they are also the important channels for pollutants transported to the sea. The construction of the Jiaozhou Bay Bridge changed the hydrodynamic condition of the bay, which made the self-purification capacity of the bay weakened and the pollution in the estuary and adjacent coastal zone become more serious. In this study, 55 surface sediment samples were collected from the three seriously polluted estuaries and the adjacent coastal zone of Jiaozhou Bay to comprehensively study how the benthic foraminifera response to heavy metal pollution and human engineering, and to assess the ecological risks of the bay. A total of 80 species, belonging to 42 genera, were identified in this study. The results showed that Cu, Pb, Cr, Hg, Zn, and As had low to median ecological risks in the study area which would definitely affect the ecological system. The construction of the Jiaozhou Bay Bridge has resulted in pollutants accumulated at the river mouth of Loushan River, which has adverse effects on the survival and growth of benthic foraminifera. The lowest population density and diversity as well as the highest FAI (Foraminiferal Abnormality Index) and FMI (Foraminiferal Monitoring Index) occurred at Loushan River Estuary which indicated that the ecological environment of the northeastern part of Jiaozhou Bay (Loushan River Estuary) had been seriously damaged. Licun River and Haipo River estuaries and the adjacent coastal zone were slightly polluted and had low ecological risk. As a consequence, it suggested that the supervision of industrial and domestic waste discharge and the protection of the ecological environment in northeast Jiaozhou Bay should be paid more attention.
Alve E, Nagy J. 1990. Main features of foraminiferal distribution reflecting estuarine hydrography in Oslo Fjord. Marine Micropaleontology, 16(3‒4), 181–206. doi: 10.1016/0377-8398(90)90003-5. |
Alve E. 1995. Benthic foraminiferal responses to estuarine pollution. Journal of Foraminiferal Research, 25(3), 190–203. doi: 10.2113/gsjfr.25.3.190. |
Alve E, Olsgard F. 1999. Benthic foraminiferal colonization in experiments with copper-contaminated sediments. Journal of Foraminiferal Research, 29(3), 186–195. doi: 10.1016/S0031-0182(99)00022-X. |
Armynot du Châtelet E, Debenay JP, Soulard R. 2004. Foraminiferal proxies for pollution monitoring in moderately polluted harbors. Environmental Pollution, 127(1), 27–40. doi: 10.1016/S0269-7491(03)00256-2. |
Albani A, Barbero RS, Donnici S. 2007. Foraminifera as ecological indicators in the lagoon of Venice, Italy. Ecological Indicators, 7(2), 239–253. doi: 10.1016/j.ecolind.2006.01.003. |
Andreas AL, Bowser SS. 2021. Effects of lead and cadmium exposure on oxygen respiration rates of individual Antarctic foraminifera during agglutinated shell formation. Journal of Experimental Marine Biology and Ecology, 537, 151514. doi: 10.1016/j.jembe.2021.151514. |
Bradshaw JS. 1957. Laboratory studies on the rate of growth of the foraminifer, “streblus beccarii (linné) var. tepida (cushman)”. Journal of Paleontology, 31(6), 1138–1147. |
Boltovskoy E, Scott DB, Medioli FS. 1991. Morphological variations of benthic foraminiferal tests in response to changes in ecological parameters: A review. Journal of Paleontology, 65(2), 175–185. doi: 10.1017/S0022336000020394. |
Bergin F, Kucuksezgin F, Uluturhan E, Barut IF, Meric E, Avsar N, Nazik A. 2006. The response of benthic foraminifera and ostracoda to heavy metal pollution in gulf of izmir (eastern aegean sea). Estuarine Coastal & Shelf Science, 66(3), 368–386. doi: 10.1016/j.ecss.2005.09.013. |
Brasier MD. 1973. Foraminifera. Nature, 246(5434), 541–541. doi: 10.1002/9781118685440.ch15. |
Brouillette PE, Kabengi N, Goldstein ST. 2019. Effects of heavy-metal contaminants (Cd, Pb, Zn) on benthic foraminiferal assemblages grown from propagules, Sapelo Island, Georgia (USA). Marine Micropaleontology, 147, 1–11. doi: 10.1016/j.marmicro.2019.01.004. |
Bergamin L, Taddei Ruggiero E, Pierfranceschi G, Andres B, Constantino R, Crovato C, D’Ambrosi A, Marassich A, Romano E. 2020. Benthic foraminifera and brachiopods from a marine cave in Spain: Environmental significance. Mediterranean Marine Science, 21(3), 506–518. doi: 10.12681/mms.23482. |
Benito X. 2020. Benthic Foraminifera and Diatoms as Ecological Indicators. In: Cristóbal G, Blanco S, Bueno G (eds), Modern Trends in Diatom Identification. Developments in Applied Phycology, vol 10. Springer, Cham. doi: 10.1007/978-3-030-39212-3_15. |
Coccioni R. 2000. Benthic Foraminifera as Bioindicators of Heavy Metal Pollution – A Case Study from the Goro Lagoon (Italy). In: Martin RE (ed.), Environmental Micropaleontology: The Application of Microfossils to Environmental Geology. New York, Kluwer Academic/Plenum Publishers, 71‒103. |
Coccioni R, Frontalini F, Marsili A, Mana D. 2009. Benthic foraminifera and trace element distribution: A case-study from the heavily polluted lagoon of Venice (Italy). Marine Pollution Bulletin, 59(8‒12), 257–267. doi: 10.1016/j.marpolbul.2009.08.009. |
Chen YY, Song DH, Bao XW, Yan YH. 2019. Impact of the cross-bay bridge on water exchange in Jiaozhou Bay, Qingdao, China. Oceanologia et Limnologia Sinic, 50(4), 707–718 (in Chinese with English abstract). doi: 10.11693/hyhz20180900211. |
Debenay JP, Bénéteau E, Zhang J, Stouff V, Geslin E, Redois F, Fernandez-Gonzalez M. 1998. Ammonia beccarii and Ammonia tepida (Foraminifera): Morphofunctional arguments for their distinction. Marine Micropaleontology, 34(3), 235–244. doi: 10.1016/S0377-8398(98)00010-3. |
Debenay JP, Fernandez JM. 2009. Benthic foraminifera records of complex anthropogenic environmental changes combined with geochemical data in a tropical bay of New Caledonia (SW Pacific). Marine Pollution Bulletin, 59(8‒12), 311–322. doi: 10.1016/j.marpolbul.2009.09.014. |
Dong H. 2012. Study on the Exchange Flux of Nutrients at the Sediment-Water Interface in Estuary Area-Take Licun River as an Example. Qingdao, Ocean University of China, Master thesis, 39‒39 (in Chinese with English abstract). |
El-Kahawy R, El-Shafeiy M, Helal S, Aboul-Ela N, El-Wahab MA. 2018. Morphological deformities of benthic foraminifera in response to nearshore pollution of the Red Sea, Egypt. Environmental Monitoring and Assessment, 190(5), 312. doi: 10.1007/s10661-018-6695-2. |
El Kateb A, Beccari V, Stainbank S, Spezzaferri S, Coletti G. 2020. Living (stained) foraminifera in the Lesser Syrtis (Tunisia): Influence of pollution and substratum. PeerJ, 8(10), . doi: 10.7717/peerj.8839. |
Ferraro L, Sprovieri M, Alberico I, Lirer F, Prevedello L, Marsella E. 2006. Benthic foraminifera and heavy metals distribution: A case study from the Naples Harbour (Tyrrhenian sea, southern Italy). Environmental Pollution, 142(2), 274–287. doi: 10.1016/j.envpol.2005.10.026. |
Frontalini F, Coccioni R. 2008. Benthic foraminifera for heavy metal pollution monitoring: A case study from the central Adriatic Sea coast of Italy. Estuarine Coastal & Shelf Science, 76(2), 404–417. doi: 10.1016/j.ecss.2007.07.024. |
Frontalini F, Buosi C, Da Pelo S, Coccioni R, Cherchi A, Bucci C. 2009. Benthic foraminifera as bio-indicators of trace element pollution in the heavily contaminated Santa Gilla Lagoon (Cagliari, Italy). Marine Pollution Bulletin, 58(6), 858–877. doi: 10.1016/j.marpolbul.2009.01.015. |
Frontalini F, Coccioni R. 2011. Benthic foraminifera as bioindicators of pollution: A review of Italian research over the last three decades. Revue De Micropaléontologie, 54(2), 115–127. doi: 10.1016/j.revmic.2011.03.001. |
Frontalini F, Curzi D, Giordano FM, Bernhard J, Falcieri E, Coccioni R. 2015. Effects of lead pollution on Ammonia parkinsoniana (foraminifera): Ultrastructural and microanalytical approaches. European Journal of Histochemistry, 59(1), 2460. doi: 10.4081/ejh.2015.2460. |
Frontalini F, Greco M, Di LB, Lejzerowicz F, Reo E, Caruso A, Cosentino C, Maccotta A, Scopelliti G, Pia Nardelli M, Losada MT, Armynot du CE, Coccioni R, Pawlowski J. 2017. Assessing the effect of mercury pollution on cultured benthic foraminifera community using morphological and eDNA metabarcoding approaches. Marine Pollution Bulletin, 129(2), 512–524. doi: 10.1016/j.marpolbul.2017.10.022. |
Fernandez NF, Gundersen GW, Rahman A, Grimes M L, Rikova K, Hornbeck P, Ma’ayan A. 2017. Clustergrammer, a web-based heatmap visualization and analysis tool for high-dimensional biological data. Scientific data, 4, 170151. doi: 10.1038/sdata.2017.151. |
Geslin E, Debenay JP, Duleba W, Bonetti C. 2002. Morphological abnormalities of foraminiferal tests in Brazilian environments: Comparison between polluted and non-polluted areas. Marine Micropaleontology, 45(2), 151–168. doi: 10.1016/S0377-8398(01)00042-1. |
Guo JH, Yin YF, Chen FR, Li JX, Xiao L, Wang XR. 2012. The distribution characteristics of heavy metals in sediments of Jiaozhou Ba and its potential ecological risk evaluation. Environmental Pollution & Contro, 34(3), 13–21 (in Chinese with English abstract). doi: 10.3969/j.issn.1001-3865.2012.03.004. |
Gong XB, Han P, Zhang LJ, Xue M, Yang XF, Wang WS. 2015. Distribution and controlling factors of sea surface partial pressure of CO2 in Jiaozhou Bay during April. Journal of Ocean University of China (Natural Science Edition), 45(4), 95–102 (in Chinese with English abstract). doi: 10.16441/j.cnki.hdxb.20130429. |
Gildeeva O, Akita LG, Biehler J, Frenzel P, Alivernini M. 2021. Recent brackish water Foraminifera and Ostracoda from two estuaries in Ghana, and their potential as (palaeo) environmental indicators. Estuarine, Coastal and Shelf Science, 256, 107270. doi: 10.1016/j.ecss.2021.107270. |
Jain S. 2017. Benthic Foraminifera. In: Fundamentals of Invertebrate Palaeontology. New Delhi, Springer, Springer Geology. doi: 10.1007/978-81-322-3658-0. |
Kitazato H. 1988. Locomotion of some benthic foraminifera in and on sediments. Journal of Foraminiferal Research, 18(4), 344–349. doi: 10.2113/gsjfr.18.4.344. |
Kaithwar A, Singh DP, Saraswat R. 2020. A highly diverse living benthic foraminiferal assemblage in the oxygen deficient zone of the southeastern Arabian Sea. Biodiversity and Conservation, 29(14), 3925–3958. doi: 10.1007/s10531-020-02056-9. |
Le Cadre V, Debenay JP, Lesourd M. 2003. Low pH effects on Ammonia beccarii test deformation: Implication for studying test deformation as a pollution indicator. Journal of Foraminiferal Research, 33(1), 1–9. doi: 10.2113/0330001. |
Le Cadre V, Debenay JP. 2006. Morphological and cytological responses of Ammonia (foraminifera) to copper contamination: Implication for the use of foraminifera as bioindicators of pollution. Environmental Pollution, 143(2), 304–17. doi: 10.1016/j.envpol.2005.11.033. |
Lawrence AL, Mason RP. 2001. Factors controlling the bioaccumulation of mercury and methylmercury by the estuarine amphipod leptocheirus plumulosus. Environmental Pollution, 111(2), 217–231. doi: 10.1016/S0269-7491(00)00072-5. |
Li Y, Yu ZM, Song XX. 2006. Application of principal component analysis(PCA) for the estimation of source of heavy metal contamination in marine sediments. Environmental Science, 27(1), 137–141 (in Chinese with English abstract). doi: 10.1016/S1872-2040(06)60041-8. |
Li P, Li G, Qiao L, Chen X, Shi J, Gao F, Wang N, Yue S. 2014. Modeling the tidal dynamic changes induced by the bridge in Jiaozhou Bay, Qingdao, China. Continental Shelf Research, 84(4), 43–53. doi: 10.1016/j.csr.2014.05.006. |
Li T, Xiang R, Li T. 2014. Influence of trace metals in recent benthic foraminifera distribution in the Pearl River estuary. Marine Micropaleontology, 108(4), 13–27. doi: 10.1016/j.marmicro.2014.02.003. |
Li T, Li X, Zhong H, Yang C, Sun G, Luo W. 2015. Distribution of trace metals and the benthic foraminiferal assemblage as a characterization of the environment in the north Minjiang River Estuary (Fujian, China). Marine Pollution Bulletin, 90(1–2), 227–241. doi: 10.1016/j.marpolbul.2014.10.047. |
Li TT, Luo W, Lv YL, Song S, Wang P, Xu L, Shang JM, Gao JJ. 2016. On distribution and pollution of heavy metals in water environment of Jiaozhou Bay in Yellow Sea. Journal of Southwest China Normal University (Natural Science Edition), 41(6), 60–66 (in Chinese with English abstract). doi: 10.13718/j.cnki.xsxb.2016.06.011. |
Linshy VN, Saraswat R, Kurtarkar S, Nigam R. 2013. Experiment to decipher the effect of heavy metal cadmium on coastal benthic foraminifer Pararotalia nipponica (Asano). Journal of the Palaeontological Society of India, 58(2), 205–211. |
Long ER, MacDonald DD, Smith SL, Calder FD. 1995. Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environmental Management, 19, 81–97. doi: 10.1007/BF02472006. |
Lo Giudice Cappelli E, Clarke J, Smeaton C, Davidson K, Austin WEN. 2019. Organic-carbon-rich sediments: Benthic foraminifera as bio-indicators of depositional environments. Biogeosciences, 16, 4183–4199. doi: 10.5194/bg-16-4183-2019. |
Liu R, Huang Y. 2019. Characteristics and evaluation of heavy metal pollution in soil and near-surface atmospheric dust of typical mining cities in Southwest China—A case study from Panzhihua city. Acta Geologica Sinica (English Edition), 93(supp. 2), 439. |
Martins V, Silva EFD, Sequeira C, Rocha F, Duarte AC. 2010. Evaluation of the ecological effects of heavy metals on the assemblages of benthic foraminifera of the canals of Aveiro (Portugal). Estuarine Coastal & Shelf Science, 87(2), 293–304. doi: 10.1016/j.ecss.2010.01.011. |
Mendes I, Dias JA, Schönfeld J, Ferreira O, Rosa F, José Lobo F. 2013. Living, dead and fossil benthic foraminifera on a river dominated shelf (northern gulf of cadiz) and their use for paleoenvironmental reconstruction. Continental Shelf Research, 68, 91–111. doi: 10.1016/j.csr.2013.08.013. |
Murray JW. 1963. Ecological experiments on foraminiferida. Journal of the Marine Biological Association of the UK, 43(3), 621–642. doi: 10.1017/S0025315400025571. |
Murray JW. 1991. Ecology and Paleoecology of Benthic Foraminifera. Longman, Harlow, Essex, England, Longman Scientific and Technical. New York, Wiley, 397. doi: 10.4324/9781315846101. |
Morvan J, Valérie Le C, Jorissen F, Debenay JP. 2004. Foraminifera as potential bio-indicators of the “Erika” oil spill in the Bay of Bourgneuf: Field and experimental studies. Aquatic Living Resources, 17(3), 317–322. doi: 10.1051/alr:2004034. |
Nigam R, Linshy VN, Kurtarkar SR, Saraswat R. 2009. Effects of sudden stress due to heavy metal mercury on benthic foranimifer Rosalina leei: Laboratory culture experiment. Marine Pollution Bulletin, 59, 362–363. doi: 10.1016/j.marpolbul.2009.08.014. |
Nagendra R, Reddy AN. 2019. Benthic foraminifera response to ecosystem pollution in the Uppanar Estuary, Tamil Nadu Coast, India. Journal of the Geological Society of India, 93(5), 555–566. doi: 10.1007/s12594-019-1217-6. |
Negar F, Mohammad BR, Mohammad ZK. 2020. Spatial analysis of groundwater quality for drinking purpose in Sirjan Plain, Iran by fuzzy logic in GIS. Journal of Groundwater Science and Engineering, 8(1), 67–78. |
Orabi OH, El-Badry AA, Badr-Eldin AM. 2017. Benthic foraminifera for heavy metal pollution monitoring: A case study from Burullus Lagoon of Egypt. Marine Pollution Bulletin, 121(1‒2), 411–17. doi: 10.1016/j.marpolbul.2017.06.015. |
Qiao LL, Liang SK, Song DH. 2019. 2-Jiaozhou Bay. In Wang XH (ed.), Sediment Dynamics of Chinese Muddy Coasts and Estuaries. America, Academic Press, 5‒23. |
Stouff V, Geslin E, Debenay JP, Lesourd M. 1999. Origin of morphological abnormalities in ammonia (foraminifera): Studies in laboratory and natural environments. Journal of Foraminiferal Research, 29(2), 152–170. doi: 10.2113/gsjfr.29.2.152. |
Samir AM, El-Din AB. 2001. Benthic foraminiferal assemblages and morphological abnormalities as pollution proxies in two Egyptian Bays. Marine Micropaleontology, 41(3‒4), 193–227. doi: 10.1016/S0377-8398(00)00061-X. |
Liu S, Gao N, Lee HS, Zhu LM, Li H, Yang J. 2020. Study on soil heavy metal content and ecological risk assessment of Jiaozhou Bay of China. Revista de Chimie, 71(4), 512–522. doi: 10.37358/RC.20.4.8093. |
Wang YP, Gao S, Jia JJ. 2000. Sedimentary distribution and transport patterns in Jiaozhou Bay and adjoining areas. Acta Geographica Sinica, 55(4), 449–458 (in Chinese with English abstract). |
Wang HJ, Ye SY, Du YS, Li SQ, Zhu AM. 2007. The distribution and compare study of surface sediment in eastern Jiaozhou Bay and Qingdao adjacent coastal sea. Transactions of Oceanology and Limnology, 4, 80–86 (in Chinese with English abstract). doi: 10.13984/j.cnki.cn37-1141.2007.04.017. |
Wang PX, Min QB, Bian YH, Cheng XR, Zhu XD. 1986. The foraminifera transport in estuary and its paleoenvironmental significance (Ⅱ). Marine Geology & Quaternary Geology, 3, 55–67. doi: 10.16562/j.cnki.0256-1492.1986.03.00. |
Woodroffe S, Horton BP, Whittaker J. 2005. Intertidal mangrove foraminifera from the central great barrier reef shelf, Australia: Implications for sea-level reconstruction. Journal of Foraminiferal Research, 35(3), 259–270. doi: 10.2113/35.3.259. |
Wu J, Liu CL, Jia LW, Yang TT, Zhang SQ, Yin J. 2013. Foraminiferal and ostracod distribution in surface sediments from Huangmao Bay of Pearl River Estuary and its influencing factors. Journal of Palaeogeography, 15(3), 413–422 (in Chinese with English abstract). |
Xu FJ, Liu ZQ, Cao YC, Qiu L, Feng J, Xu F, Tian X. 2017. Assessment of heavy metal contamination in urban river sediments in the Jiaozhou Bay catchment, Qingdao, China. Catena, 150, 9–16. doi: 10.1016/j.catena.2016.11.004. |
Xiao CL, Chen LF, Li YB. 2017. Distribution characteristics and potential risk assessment of heavy metals in the sediments of Jiaozhou Bay. China Science and Technology Paper, 9, 1079–1086 (in Chinese with English abstract). |
Yanko V, Kronfeld J, Flexer A. 1994. Response of benthic foraminifera to various pollution sources: Implications for pollution monitoring. Journal of Foraminiferal Research, 24(1), 1–17. doi: 10.2113/gsjfr.24.1.1. |
Yanko V, Ahmad M, Kaminski MA. 1998. Morphological deformities of benthic foraminiferal tests in response to pollution by heavy metals: Implications for pollution monitoring. Journal of Foraminiferal Research, 28(3), 177–200. |
Yao X, Zhang J, Tian L, Guo J. 2016. The effect of heavy metal contamination on the bacterial community structure at Jiaozhou Bay, China. Brazilian Journal of Microbiology, 48(1), 71–78. doi: 10.1016/j.bjm.2016.09.007. |
Yin P, Lin LJ, Chen B, Xiao GQ, Cao K, Yang JL, Li MN, Duan XY, Qiu JD, Hu YZ, Wang L, Sun XM. 2017. Coastal zone geo-resources and geo-environment in China. Geology in China, 44(5), 842–856 (in Chinese with English abstract). doi: 10.12029/gc20170502. |
Yuan Y, Jalón-Rojas I, Wang XH. 2021. Response of water-exchange capacity to human interventions in Jiaozhou Bay, China. Estuarine, Coastal and Shelf Science, 249, 107088. doi: 10.1016/j.ecss.2020.107088. |
Zhang Y, Chen B, Ning Z, Yang YF, Wang HJ. 2019. Investigation and numerical simulation of summer sedimentation in Jiaozhou Bay, China. China Geology, 2(4), 522–529. doi: 10.31035/cg2018090. |
Zhu XD. 1994. The discovery and environmental indication of abnormal benthic foraminifera in sediments of Lianyungang Port Area. Acta Oceanologica Sinica, 16(4), 91–95. |
(a) Map showing the location of the study area; (b) map showing the water depth of the study area with sampling stations. The locations of the Jiaozhou Bay Bridge and the Cangkou Waterway are also showed on this map.
a‒Pictures of the lower reaches of the Loushan River (cited from
Map showing the distribution of abundance (a), S (b), H (c), FAI (d), FMI (e) of foraminifera.
SEM photomicrographs of benthic foraminifera bearing different morphological abnormalities: 1‒3‒Quinqueloculina bellatula; 4‒6‒Ammonia beccarii; 7‒11‒Elphidium magellanicum; 12‒15‒Buccella frigida; 16‒Elphidium advenum; 17, 18‒Hanzawa sp.; 19‒Ammonia compressiuscula; 20‒Trochammina inflata (all the scale bar=50 μm); 21‒gastropod (as a contrast). 2, 3‒distorted chamber arrangement or change in coiling; 5‒reduced chamber size; 7‒complexity; 1, 4, 6, 10, 12‒15, 19‒aberrant chamber shape and size; 8, 16‒abnormally additional chamber; 9, 17, 18, 20‒distorted chamber arrangement or change in coiling and aberrant chamber shape and size; 11‒spiroconvex.
Map showing the distribution of Cu (a), Pb (b), Zn (c), Cr (d), Cd (e), As (f), Hg (g), pH (h), and TOC (i) of the Jiaozhou Bay, China.
Distribution of suspended sediment concentrations in Jiaozhou Bay during different periods. a–beginning of the flood tide for spring tides; b–maximum flood tide for spring tides; c–high tide for spring tides; d–beginning of the ebb tide for spring tides; e–maximum ebb tide for spring tides; f–low tide for spring tides; g–maximum flood tide for neap tides; h–maximum ebb tide for neap tides (cited from Zhang Y et al., 2019).
Distribution of depth, abundance, and species of Loushan River Estuary, Licun River Estuary, and Haipo River Estuary. The three scatter plots above represent the correlation of depth and abundance of the three estuaries.
Heat map of the relative abundance of each species (rows) in each sample (columns). Dendrogram classification of sampling sites produced by Hierarchical clustering method using Euclidean distance.
Distribution of the relative abundance of the deformities.