Abstract
Seagrasses play an important role in coastal marine ecosystems, but they have been increasingly threatened by human activities. In recent years, seagrass communities have rapidly degenerated in the coastal marine ecosystems of China. To identify the reasons for the decline in seagrasses, the phytotoxic effects of trace metals (Cu, Cd and Zn) on the seagrass Thalassia hemprichii were investigated, and the environmental contents of the metals were analyzed where the seagrass grows. The results showed that leaf necrosis in T. hemprichii exposed to 0.01–0.1 mg L−1 of Cu2+ for 5 days was more serious than that in plants exposed to the same concentrations of Cd2+ and Zn2+. The chlorophyll content in T. hemprichii declined in a concentration-dependent manner after 5 days of exposure to Cu2+, Cd2+ and Zn2+. The evident reduction in ΔF/Fm’ in T. hemprichii leaves was observed at day 1 of exposure to 0.01–1.0 mg L−1 of Cu2+ and at day 3 of exposure to 0.1–1.0 mg L−1 of Cd2+. The antioxidant enzyme activities (SOD, POD and CAT) in T. hemprichii leaves exposed to the three metal ions also showed significant changes. In seawater from Xincun Bay (Hainan, China), where T. hemprichii grows, Cu had reached a concentration (i.e., 0.01 mg L−1) that could significantly reduce chlorophyll content and ΔF/Fm’ in T. hemprichii leaves. Our results indicate that Cu influences the deterioration of seagrasses in Xincun Bay.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alina M, Azrina A, Mohd Yunus AS, Mohd Zakiuddin S, Mohd Izuan Effendi H, Muhammad Rizal R (2012) Heavy metals (mercury, arsenic, cadmium, plumbum) in selected marine fish and shellfish along the Straits of Malacca. Int Food Res J 19:135–140
Ambo-Rappe R (2014) Developing a methodology of bioindication of human-induced effects using seagrass morphological variation in Spermonde Archipelago, South Sulawesi, Indonesia. Mar Poll Bull 86:298–303
Barwick M, Maher W (2003) Biotransference and biomagnification of selenium copper, cadmium, zinc, arsenic and lead in a temperate seagrass ecosystem from Lake Macquarie Estuary, NSW, Australia. Mar Environ Res 56:471–502
Bazzano A, Rivaro P, Soggia F, Ardini F, Grotti M (2014) Anthropogenic and natural sources of particulate trace elements in the coastal marine environment of Kongsfjorden, Svalbard. Mar Chem 163:28–35
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
Bestwick CS, Brown IR, Mansfield JW (1998) Localized changes in peroxidase activity accompany hydrogen peroxide generation during the development of a nonhost hypersensitive reaction in lettuce. Plant Physiol 118:1067–1078
Bonanno G, Orlando-Bonaca M (2018) Trace elements in Mediterranean seagrasses and macroalgae. A review. Sci Total Environ 618:1152–1159
Bonanno G, Orlando-Bonaca M (2017) Trace elements in Mediterranean seagrasses: accumulation, tolerance and biomonitoring. A review. Mar Poll Bull 125:8–18
Chanu HK, Gupta A (2014) Necrosis as an adaptive response to copper toxicity in Ipomoea aquatica Forsk. and its possible application in phytoremediation. Acta Physiol Plant 36:3275–3281
Chen S-Q, Wang D-R, Wu Z-J, Zhang G-X, Li Y-C, Tu Z-G, Yao H-J, Cai Z-F (2015) Discussion of the change trend of the seagrass beds in the east coast of Hainan island in nearly a decade. Mar Environ Sci 34:48–53. (In Chinese with English abstract)
Chen S, Wu Z, Chen X, Li Y, Cai Z, Zhang G, Yao H, Huang J (2015) Investigation and analysis of the distribution status of seagrass resources in the southern part of Hainan island. Acta Oceanol Sin 37:106–113. (In Chinese with English abstract)
Ciscato M, Vangronsveld J, Valcke R (1999) Effects of heavy metals on the fast chlorophyll fluorescence induction kinetics of photosystem II: a comparative study. Z Naturforsch C 54:735–739
Clijsters H, Van AF (1985) Inhibition of photosynthesis by heavy metals. Photosynth Res 7:31–40
De MS, Fowler SW, Wyse E, Azemard S (2004) Distribution of heavy metals in marine bivalves, fish and coastal sediments in the Gulf and Gulf of Oman. Mar Poll Bull 49:410–424
Duarte CM (1999) Seagrass ecology at the turn of the millennium: challenges for the new century. Aquat Bot 65:7–20
Duffy JE (2006) Biodiversity and the functioning of seagrass ecosystems. Mar Ecol Prog 311:233–250
Green EP, Short FT (2004) World atlas of seagrasses. Bot Mar 47:259–260
Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266
Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637
Jain CK (2004) Metal fractionation study on bed sediments of River Yamuna, India. Water Res 38:569
Jiang YF, Ling J, Wang YS, Chen B, Zhang YY, Dong JD (2015) Cultivation-dependent analysis of the microbial diversity associated with the seagrass meadows in Xincun Bay, South China Sea. Ecotoxicology 24:1540–1547
Lewis MA, Dantin DD, Chancy CA, Abel KC, Lewis CG (2007) Florida seagrass habitat evaluation: a comparative survey for chemical quality. Environ Poll 146:206–218
Lewis MA, Devereux R (2009) Nonnutrient anthropogenic chemicals in seagrass ecosystems: fate and effects. Environ Toxicol Chem 28:644–661
Liu S, Jiang Z, Zhang J, Wu Y, Lian Z, Huang X (2016) Effect of nutrient enrichment on the source and composition of sediment organic carbon in tropical seagrass beds in the South China Sea. Mar Poll Bull 110:274–280
Macinnis-NG CMO, Ralph PJ (2002) Towards a more ecologically relevant assessment of the impact of heavy metals on the photosynthesis of the seagrass, Zostera capricorni. Mar Poll Bull 45:100–106
Macinnis-Ng CMO, Ralph PJ (2004) Variations in sensitivity to copper and zinc among three isolated populations of the seagrass, Zostera Capricorn. J Exp Mar Biol Ecol 302:63–83
McElroy JS, Kopsell DA (2009) Physiological role of carotenoids and other antioxidants in plants and application to turfgrass stress management. NZ J Crop Hort Sci 37:327–333
Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S, Short FT, Waycott M, Williams SL (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996
Ouzounidou G (1994) Copper-induced changes on growth, metal content and photosynthetic function of Alyssum montanum L. plants. Environ Exp Bot 34:165–172
Ouzounidou G (1995) Cu-ions mediated changes in growth, chlorophyll and other ion contents in a Cu-tolerant Koeleria splendens. Biol Plant 37:71–78
Pagès JF, Pérez M, Romero J (2010) Sensitivity of the seagrass Cymodocea nodosa to hypersaline conditions: A microcosm approach. J Exp Mar Bio Ecol 386:34–38
Prange JA, Dennison WC (2000) Physiological responses of five seagrass species to trace metals. Mar Poll Bull 41:327–336
Rainbow PS (2007) Trace metal bioaccumulation: models, metabolic availability and toxicity. Environ Inter 33:576–582
Roach AC, Maher W, Krikowa F (2008) Assessment of metals in fish from Lake Macquarie, New South Wales, Australia. Arch Environ Contam Toxicol 54:292–308
Sánchez-Quiles D, Marbà N, Tovar-Sánchez A (2017) Trace metal accumulation in marine macrophytes: Hotspots of coastal contamination worldwide. Sci Total Environ 576:520–527
Sandoval-Gil JM, Marín-Guirao L, Ruiz JM (2012) The effect of salinity increase on the photosynthesis, growth and survival of the Mediterranean seagrass Cymodocea nodosa. Estuar Coast Shelf Sci 115:260–271
Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365
Shioi Y, Tamai H, Sasa T (1978) Effects of copper on photosynthetic electron transport systems in spinach chloroplasts. Plan Cell Physiol 19:203–209
Short FT, Polidoro B, Livingstone SR, Carpenter KE, Bandeira S, Bujang JS, Calumpong HP, Carruthers TJ, Coles RG, Dennison WC (2011) Extinction risk assessment of the world’s seagrass species. Biol Conserv 144:1961–1971
Sinha S, Sinam G, Mishra RK, Mallick S (2010) Metal accumulation, growth, antioxidants and oil yield of Brassica juncea L. exposed to different metals. Ecotoxicol Environ Saf 73:1352–1361
Timmermans KR, Hattum BV, Kraak MHS, Davids C (1989) Trace metals in a littoral foodweb: concentrations in organisms, sediment and water. Sci Total Environ 87:477–494
Tupan CI, Uneputty PA (2017) Concentration of heavy metals lead (Pb) and cadmium (Cd) in water, sediment and seagrass Thalassia hemprichii in Ambon Island waters. AACL Bioflux 10:1610–1617
Unsworth RKF, Cullen LC (2010) Recognising the necessity for Indo-Pacific seagrass conservation. Conserv Lett 3:63–73
Upadhyaya A, Sankhla D, Davis TD, Sankhla N, Smith BN (1985) Effect of paclobutrazol on the activities of some enzymes of activated oxygen metabolism and lipid peroxidation in senescing soybean leaves. J Plant Physiol 121:453–461
Vörösmarty CJ, Mcintyre PB, Gessner MO, Dudgeon D, Prusevich A, Green P, Glidden S, Bunn SE, Sullivan CA, Liermann CR (2010) Global threats to human water security and river biodiversity. Nature 467:555
van der Heide T, Smolders AJP, Rijkens BGA, van Nes EH, van Katwijk MM, Roelofs JGM (2008) Toxicity of reduced nitrogen in eelgrass (Zostera marina) is highly dependent on shoot density and pH. Oecologia 158:411–419
Wang C, Zhang SH, Wang PF, Hou J, Zhang WJ, Li W, Lin ZP (2009) The effect of excess Zn on mineral nutrition and antioxidative response in rapeseed seedlings. Chemosphere 75:1468–1476
Ward TJ (1989) The accumulation and effects of metals in seagrass habitats. In: Larkum AWD, McComb AJ, Shepherd SA (eds) Biology of seagrmses: A treatise on the biology of seagrasses with special reference to the Australian Region. Elsevier, Amsterdam, pp 797–820
Waycott M, Duarte CM, Carruthers TJ, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL, Hughes AR (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci 106:12377–12381
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313
Wilkes R, Bennion M, McQuaid N, Beer C, McCullough-Annett G, Colhoun K, Inger R, Morrison L (2017) Intertidal seagrass in Ireland: pressures, WFD status and an assessment of trace element contamination in intertidal habitats using Zostera noltei. Ecol Indic 82:117–130
Yang D, Yang C (2009) Detection of seagrass distribution changes from 1991 to 2006 in xincun bay, hainan, with satellite remote sensing. Sensors 9:830–844
Yuan CG, Shi JB, He B, Liu JF, Liang LN, Jiang GB (2004) Speciation of heavy metals in marine sediments from the East China Sea by ICP-MS with sequential extraction. Environ Inter 30:769–783
Funding
This work was funded by the National Key R&D Program of China (2017YFC1200105) and the National Natural Science Foundation of China (31570398). The study was also supported by the Guangdong Province Natural Science Foundation (2017A030313167, 2015A030311023).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
These authors contributed equally: Jin Zheng, Xiao-Qian Gu.
Rights and permissions
About this article
Cite this article
Zheng, J., Gu, XQ., Zhang, TJ. et al. Phytotoxic effects of Cu, Cd and Zn on the seagrass Thalassia hemprichii and metal accumulation in plants growing in Xincun Bay, Hainan, China. Ecotoxicology 27, 517–526 (2018). https://doi.org/10.1007/s10646-018-1924-6
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-018-1924-6