Impacts of Spartina alterniflora invasion on coastal wetland ecosystem: Advances and prospects

doi:10.13287/j.1001-9332.202006.032

Abstract

Abstract: Coastal wetland, affected by the interaction of land and marine ecosystems, is a typical fragile and sensitive zone. Spartina alterniflora is the most successful invasive species in global coastal zone, with important impact on coastal wetland ecosystems. We systematically summarized available literature, and reviewed the effects of S. alterniflora invasion on biogeochemical cycling (soil carbon, nitrogen, phosphorus cycling, and soil heavy metal migration) and biological community (microorganisms, plants, and animals) in coastal wetlands. Then, three perspectives were proposed for the future research: 1) strengthening the mechanism of the impact of S. alterniflora invasion on ecosystem health of coastal wetlands; 2) focusing on the coupling mechanism of the interaction between S. alterniflora community and coastal wetland environment in the context of global change; 3) carrying out long-term positioning monitoring to clarify the responses of coastal wetlands at different stages of S. alterniflora invasion. This review could provide guidance for the ecological utilization and management of S. alterniflora.

XIE Xue-feng, SUN Xiao-min, WU Tao, JIANG Guo-jun, PU Li-jie, XIANG Qi. Impacts of Spartina alterniflora invasion on coastal wetland ecosystem: Advances and prospects[J]. Chinese Journal of Applied Ecology, 2020, 31(6): 2119-2128.

References 75

[1]	Sun BD, Cui LJ, Li W, et al. A meta-analysis of coastal wetland ecosystem services in Liaoning Province, China. Estuarine, Coastal and Shelf Science, 2018, 200: 349-358
[2]	谢宝华, 韩广轩. 外来入侵种互花米草防治研究进展. 应用生态学报, 2018, 29(10): 3464-3476 [Xie B-H, Han G-X. Control of invasive Spartina alterniflora: A review. Chinese Journal of Applied Ecology, 2018, 29(10): 3464-3476]
[3]	Zuo P, Zhao S, Liu CA, et al. Distribution of Spartina spp. along China’s coast. Ecological Engineering, 2012, 40: 160-166
[4]	Mao D, Liu MY, Wang ZM, et al. Rapid invasion of Spartina alterniflora in the coastal zone of mainland China: Spatiotemporal patterns and human prevention. Sensors, 2019, 19(10): 2308
[5]	Daehler C, Strong D. Status, prediction and prevention of introduced cordgrass Spartina spp. invasions in Pacific estuaries, USA. Biological Conservation, 1996, 78: 51-58
[6]	Xiao Y, Tang JB, Qing H, et al. Trade-offs among growth, clonal propagation and sexual reproduction of Spartina alterniflora responding to clonal integration and inundation. Hydrobiologia, 2011, 658: 353-363
[7]	Tang L, Gao Y, Wang CH, et al. A plant invader declines through its modification to habitats: A case study of a 16-year chronosequence of Spartina alterniflora invasion in a salt marsh. Ecological Engineering, 2012, 49: 181-185
[8]	Wu YT, Wang CH, Zhang XD, et al. Effects of saltmarsh invasion by Spartina alterniflora on arthropod community structure and diets. Biological Invasions, 2009, 11: 635-649
[9]	Zhang P, Nie M, Li B, et al. The transfer and allocation of newly fixed C by invasive Spartina alterniflora and native Phragmites australis to soil microbiota. Soil Biology and Biochemistry, 2017, 113: 231-239
[10]	Qi XZ, Liu HY, Lin ZS, et al. Impacts of age and expansion direction of invasive Spartina alterniflora on soil organic carbon dynamics in coastal salt marshes along eastern China. Estuaries and Coasts, 2019, 42: 1858-1867
[11]	Yang W, An SQ, Zhao H, et al. Impacts of Spartina alterniflora invasion on soil organic carbon and nitrogen pools sizes, stability, and turnover in a coastal salt marsh of eastern China. Ecological Engineering, 2016, 86: 174-182
[12]	Liao CZ, Peng RH, Luo YQ, et al. Altered ecosystem carbon and nitrogen cycles by plant invasion: A meta-analysis. New Phytologist, 2008, 177: 706-714
[13]	Zhang Y, Ding W, Luo J, et al. Changes in soil organic carbon dynamics in an eastern Chinese coastal wetland following invasion by a C4 plant Spartina alterniflora. Soil Biology and Biochemistry, 2010, 42: 1712-1720
[14]	Zhang GL, Bai JH, Jia J, et al. Soil organic carbon contents and stocks in coastal salt marshes with Spartina alterniflora following an invasion chronosequence in the Yellow River Delta, China. Chinese Geographical Science, 2018, 28(3): 14-25
[15]	Huang LD, Zhang YH, Shi YM, et al. Comparison of phosphorus fractions and phosphatase activities in coastal wetland soils along vegetation zones of Yancheng National Nature Reserve, China. Estuarine, Coastal and Shelf Science, 2015, 157: 93-98
[16]	Yang W, An SQ, Zhao H, et al. Labile and recalcitrant soil carbon and nitrogen pools in tidal salt marshes of the Eastern Chinese Coast as affected by short-term C4 plant Spartina alterniflora invasion. CLEAN-Soil, Air, Water, 2015, 43: 872-880
[17]	Liao C, Luo Y, Jiang L, et al. Invasion of Spartina alterniflora enhanced ecosystem carbon and nitrogen stocks in the Yangtze Estuary, China. Ecosystems, 2007, 10: 1351-1361
[18]	Wang W, Sardans J, Wang C, et al. The response of stocks of C, N and P to plant invasion in the coastal wetlands of China. Global Change Biology, 2019, 25: 733-743
[19]	Zhang LC, Luo YQ, Fang CM, et al. Litter pool sizes, decomposition, and nitrogen dynamics in Spartina alterniflora-invaded and native coastal marshlands of the Yangtze Estuary. Oecologia, 2008, 156: 589-600
[20]	于彩芬,陈鹏飞,刘长安,等. 互花米草湿地碳储量及碳汇研究进展. 海洋开发与管理, 2014, 31(8): 85-89 [Yu C-F, Chen P-F, Liu C-A, et al. Research progress on carbon storage and carbon sequestration in Spartina alterniflora wetland. Ocean Development and Management, 2014, 31(8): 85-89]
[21]	Feng JX, Zhou J, Wang LM, et al. Effects of short-term invasion of Spartina alterniflora and the subsequent restoration of native mangroves on the soil organic carbon, nitrogen and phosphorus stock. Chemosphere, 2017, 184: 774-783
[22]	Song HL, Liu XT. Anthropogenic effects on fluxes of ecosystem respiration and methane in the Yellow River Estuary, China. Wetlands, 2016, 36: 113-123
[23]	Yuan JJ, Ding WX, Liu DY. Exotic Spartina alterniflora invasion alters ecosystem-atmosphere exchange of CH4 and N2O and carbon sequestration in a coastal salt marsh in China. Global Change Biology, 2015, 21: 1567-1580
[24]	Sheng Q, Zhao B, Huang M, et al. Greenhouse gas emissions following an invasive plant eradication program. Ecological Engineering, 2014, 73: 229-237
[25]	Feng GG, Fei LP, Jun SZ, et al. Exotic Spartina alterniflora invasion increases CH4 while reduces CO2 emissions from mangrove wetland soils in southeastern China. Scientific Reports, 2018, 8(1): 9243
[26]	Gao GF, Li FP, Zhong JX, et al. Spartina alterniflora invasion alters soil bacterial communities and enhances soil N2O emissions by stimulating soil denitrification in mangrove wetland. Science of the Total Environment, 2019, 653: 231-240
[27]	Chen, Chen G, Ye Y. Coastal vegetation invasion increases greenhouse gas emission from wetland soils but also increases soil carbon accumulation. Science of the Total Environment, 2015, 526: 19-28
[28]	Yang W, Zhao H, Leng X, et al. Soil organic carbon and nitrogen dynamics following Spartina alterniflora invasion in a coastal wetland of eastern China. Catena, 2017, 156: 281-289
[29]	Jin BS, Lai DYF, Gao DZ, et al. Changes in soil organic carbon dynamics in a native C4 plant-dominated tidal marsh following Spartina alterniflora invasion. Pedosphere, 2017, 27: 856-867
[30]	李家兵, 张秋婷, 张丽烟, 等. 闽江河口春季互花米草入侵过程对短叶茳芏沼泽土壤碳氮分布特征的影响. 生态学报, 2016, 36(12): 3628-3638 [Li J-B, Zhang Q-T, Zhang L-Y, et al. Effect of Spartina alterniflora invasion sequence on soil carbon and nitrogen distribution in a Cyperus malaccensis marsh of the Min River estuary in spring. Acta Ecologica Sinica, 2016, 36(12): 3628-3638]
[31]	张祥霖, 石盛莉, 潘根兴, 等. 互花米草入侵下福建漳江口红树林湿地土壤生态化学变化. 地球科学进展, 2008, 23(9): 974-981 [Zhang X-L, Shi S-L, Pan G-X, et al. Changes in eco-chemical properties of a mangrove wetland under Spartina invasion from Zhangjiangkou, Fujian, China. Advances in Earth Science, 2008, 23(9): 974-981]
[32]	侯贯云, 翟水晶, 高会, 等. 盐度对互花米草枯落物分解释放硅、碳、氮元素的影响. 生态学报, 2017, 37(1): 184-191 [Hou G-Y, Zhai S-J, Gao H, et al. Effect of salinity on silicon, carbon, and nitrogen during decomposition of Spartina alterniflora litter. Acta Ecolo-gica Sinica, 2017, 37(1): 184-191]
[33]	苗萍, 谢文霞, 于德爽, 等. 胶州湾互花米草湿地氮、磷元素的垂直分布及季节变化. 应用生态学报, 2017, 28(5): 1533-1540 [Miao P, Xie W-X, Yu D-S, et al. Vertical distribution and seasonal variation of nitrogen, phosphorus elements in Spartina alterniflora wetland of Jiaozhou Bay, Shandong, China. Chinese Journal of Applied Ecology, 2017, 28(5): 1533-1540]
[34]	Crowther TW, Boddy L, Hefin JT. Functional and ecological consequences of saprotrophic fungus-grazer intera-ctions. The ISME Journal, 2012, 6: 1992-2001
[35]	Schmidt R, Mitchell J, Scow K. Cover cropping and no-till increase diversity and symbiotroph: Saprotroph ratios of soil fungal communities. Soil Biology and Biochemistry, 2019, 129: 99-109
[36]	金宝石, 闫鸿远, 王维奇, 等. 互花米草入侵下湿地土壤碳氮磷变化及化学计量学特征. 应用生态学报, 2017, 28(5): 1541-1549 [Jin B-S, Yan H-Y, Wang W-Q, et al. Changes of soil carbon, nitrogen and phosphorus and stoichiometry characteristics in marsh invaded by Spartina alterniflora. Chinese Journal of Applied Ecology, 2017, 28(5): 1541-1549]
[37]	Li J, Lai Y, Xie R, et al. Sediment phosphorus speciation and retention process affected by invasion time of Spartina alterniflora in a subtropical coastal wetland of China. Environmental Science and Pollution Research, 2018, 25: 35365-35375
[38]	Wang WQ, Wang C, Sardang J, et al. Plant invasive success associated with higher N-use efficiency and stoichiometric shifts in the soil-plant system in the Minjiang River tidal estuarine wetlands of China. Wetlands Ecology and Management, 2015, 23: 865-880
[39]	李富荣, 段琳琳, 王富华. 盐沼植物互花米草的重金属富集特性研究进展.生态环境学报, 2013, 22(7): 1263-1268 [Li F-R, Duan L-L, Wang F-H. Research progress in heavy metal accumulation of the halophyte Spartina alterniflora. Ecology and Environment, 2013, 22(7): 1263-1268]
[40]	Chai M, Shi F, Li R, et al. Heavy metal contamination and ecological risk in Spartina alterniflora marsh in intertidal sediments of Bohai Bay, China. Marine Pollution Bulletin, 2014, 84: 115-124
[41]	Wang YJ, Zhou LM, Zheng XM, et al. Influence of Spartina alterniflora on the mobility of heavy metals in salt marsh sediments of the Yangtze River Estuary, China. Environmental Science & Pollution Research, 2013, 20: 1675-1685
[42]	陈权, 马克明. 互花米草入侵对红树林湿地沉积物重金属累积的效应与潜在机制. 植物生态学报, 2017, 41(4): 409-417 [Chen Q, Ma K-M. Effects of Spartina alterniflora invasion on enrichment of sedimental heavy metals in a mangrove wetland and the underlying mechanisms. Chinese Journal of Plant Ecology, 2017, 41(4): 409-417]
[43]	Chen L, Gao JH, Zhu QG, et al. Accumulation and output of heavy metals by the invasive plant Spartina alterniflora in a coastal salt marsh. Pedosphere, 2018, 28: 884-894
[44]	Cambrollé J, Mateos-Naranjo E, Redondo-Gómez S, et al. The role of two Spartina species in phytostabilization and bioaccumulation of Co, Cr, and Ni in the Tinto-Odiel estuary (SW Spain). Hydrobiologia, 2011, 671: 95-103
[45]	Yang W, Jeelani H, Zhu ZH, et al. Alterations in soil bacterial community in relation to Spartina alterniflora Loisel. invasion chronosequence in the eastern China. Applied Soil Ecology, 2019, 135: 38-43
[46]	Yang W, Zhang D, Cai XW, et al. Significant alterations in soil fungal communities along a chronosequence of Spartina alterniflora invasion in a Chinese Yellow Sea coastal wetland. Science of the Total Environment, 2019, 693: 133548, https://doi.org/10.1016/j.scitotenv.2019.07.354
[47]	Zhang GL, Bai JH, Zhao QQ, et al. Bacterial succession in salt marsh soils along a short-term invasion chronosequence of Spartina alterniflora in the Yellow River Estuary, China. Microbial Ecology, 2019, 77: https://doi.org/10.1007/s00248-019-01430-7
[48]	郑洁, 刘金福, 吴则焰, 等. 闽江河口红树林土壤微生物群落对互花米草入侵的响应. 生态学报, 2017, 37(21): 7293-7303 [Zheng J, Liu J-F, Wu Z-Y, et al. Soil microbial community of mangrove forests and its responses to the invasion of Spartina alterniflora in the Minjiang River Estuary. Acta Ecologica Sinica, 2017, 37(21): 7293-7303]
[49]	Lin LA, Liu WW, Zhang M, et al. Different height forms of Spartina alterniflora might select their own rhizo-spheric bacterial communities in southern coast of China. Microbial Ecology, 2019, 77: 124-135
[50]	周军, 肖炜, 钦佩. 互花米草入侵对盐沼土壤微生物生物量和功能群的影响. 南京大学学报:自然科学版, 2007, 43(5): 494-500 [Zhou J, Xiao W, Qin P. Effect of an alien species (Spartina alterniflora) on soil microbial biomass and functional groups in salt marshes. Journal of Nanjing University: Natural Science, 2007, 43(5): 494-500]
[51]	Yuan J, Ding W, Liu D, et al. Shifts in methanogen community structure and function across a coastal marsh transect: Effects of exotic Spartina alterniflora invasion. Scientific Reports, 2016, 6(1): 18777, doi: 10.1038/srep18777
[52]	Tang L, Gao Y, Li B, et al. Spartina alterniflora with high tolerance to salt stress changes vegetation pattern by outcompeting native species. Ecosphere, 2014, 5: 1-18
[53]	Ayres DR, Grotkopp E, Zaremba K, et al. Hybridization between invasive Spartina densiflora (Poaceae) and native S. foliosa in San Francisco Bay, California, USA. American Journal of Botany, 2008, 95: 713-719
[54]	赵彩云, 李俊生, 赵相健. 中国沿海互花米草入侵与防控管理. 北京: 科学出版社, 2015: 63-100 [Zhao C-Y, Li J-S, Zhao X-J. Invasion and Prevention and Control Management of Spartina alterniflora in Coastal Areas of China. Beijing: Science Press, 2015: 63-100]
[55]	Evin LA, Talley TS. Influences of vegetation and abiotic environmental factors on salt marsh invertebrates// Weinstein MP, Kreeger DA, eds. Concepts and Controversies in Tidal Marsh Ecology. Dordrecht: Springer, 2002: 661-707
[56]	江旷, 陈小南, 鲍毅新, 等. 互花米草入侵对大型底栖动物群落垂直结构的影响. 生态学报, 2016, 36(2): 535-544 [Jiang K, Chen X-N, Bao Y-X, et al. The effect of the invasion of Spartina alterniflora on the vertical structure of macrobenthos community. Acta Ecologica Sinica, 2016, 36(2): 535-544]
[57]	Fu S, Cai L, Cao J, et al. Nematode responses to the invasion of exotic Spartina in mangrove wetlands in Southern China. Estuaries and Coasts, 2017, 40: 1437-1449
[58]	Chen HL, Li B, Hu JK, et al. Effects of Spartina alternifora invasion on benthic nematode communities in the Yangtze Estuary. Marine Ecology Progress Series, 2007, 336: 99-110
[59]	仇乐, 刘金娥, 陈建琴, 等. 互花米草扩张对江苏海滨湿地大型底栖动物的影响. 海洋科学, 2010, 34(8): 50-55 [Qiu L, Liu J-E, Chen J-Q, et al. Impacts of Spartina alterniflora invasion on the macro-benthos communities of Jiangsu’s coastal wetlands. Marine Sciences, 2010, 34(8): 50-55]
[60]	Chen P, Zhang Y, Zhu XJ, et al. Distribution of crabs along a habitat gradient on the Yellow Sea coast after Spartina alterniflora invasion. PeerJ, 2019, 7: e6775
[61]	Hedge P, Kriwoken LK. Evidence for effects of Spartina anglica invasion on benthic macrofauna in Little Swanport estuary, Tasmania. Austral Ecology, 2000, 25: 150-159
[62]	冯建祥, 黄茜, 陈卉, 等. 互花米草入侵对盐沼和红树林滨海湿地底栖动物群落的影响. 生态学杂志, 2018, 37(3): 943-951 [Feng J-X, Huang Q, Chen H, et al. Effects of Spartina alterniflora invasion on benthic faunal community in saltmarsh and mangrove wetland. Chinese Journal of Ecology, 2018, 37(3): 943-951]
[63]	Taylor CM, Davis HG, Civille JC, et al. Consequences of an Allee effect in the invasion of a Pacific estuary by Spartina alterniflora. Ecology, 2004, 85: 3254-3266
[64]	Quan WM, Fu CZ, Jin BS, et al. Tidal marshes as energy sources for commercially important nektonic organisms: Stable isotope analysis. Marine Ecology Progress Series, 2007, 352: 89-99
[65]	Hindel J, Wary F. Nutritional support of estuary perch (Macquaria colononmam) in a temperate Australian inlet: Evaluating the relative importance of invasive Spartina. Estuarine, Coastal and Shelf Science, 2010, 90: 159-167
[66]	Simenstad CA, Thom RM. Spartina alterniflora (smooth cordgrass) as an invasive halophyte in Pacific Northwest estuaries. Hortus Northwest, 1995, 6(12): 38-40
[67]	Tallamy DW. Do alien plants reduce insect biomass? Conservation Biology, 2004, 18: 1689-1692
[68]	Bernays E, Graham M. On the evolution of host specificity in phytophagous arthropods. Ecology, 1988, 69: 886-892
[69]	潘卉, 陈秀芝, 吴捷, 等. 互花米草入侵对长江口九段沙湿地昆虫功能群组成特征及季节动态的影响.昆虫学报, 2017, 60(1): 67-83 [Pan H, Chen X-Z, Wu J, et al. Effects of Spartina alterniflora invasion on the structural characteristics and seasonal dynamics of insect functional groups in Jiuduansha wetland of the Yangtze River Estuary, East China. Acta Entomologica Sinica, 2017, 60(1): 67-83]
[70]	童春富. 长江河口潮间带盐沼植被分布区及邻近光滩鱼类组成特征. 生态学报, 2012, 32(20): 6501-6510 [Tong C-F. Characteristics of the fish assemblages in the intertidal salt marsh zone and adjacent mudflat in the Yangtze Estuary. Acta Ecologica Sinica, 2012, 32(20): 6501-6510]
[71]	Streever WJ. Spartina alterniflora marshes on dredged material: A critical review of the ongoing debate over success. Wetlands Ecology and Management, 2000, 8: 295-316
[72]	Jacques D. Shorebird status and effects of Spartina alterniflora at Willapa National Wildlife Refuge. Naselle, WA: Progress Report to the Willapa Bay National Wildlife Refuge, 2002
[73]	Nordby JC, Cohen AN, Beissinger SR. Effect of a habitat-altering invader on nesting sparrows: An ecological trap? Biological Invasions, 2009, 11: 565-575
[74]	Wang J, Liu HY, Li YF, et al. Effects of Spartina alterniflora invasion on quality of the red-crowned crane (Grus japonensis) wintering habitat. Environmental Science and Pollution Research, 2019, 26: 21546-21555
[75]	Delach A. Invasive species in the northwestern United States: Threats to wildlife, and defenders of wildlife. Northwestern Naturalist, 2006, 87: 43-55