A global synthesis of the effectiveness and ecological impacts of management interventions for Spartina species
Shengyu Wang, Philip A. Martin, Yan Hao, William J. Sutherland, Gorm E. Shackelford, Jihua Wu, Ruiting Ju, Wenneng Zhou, Bo Li
A global synthesis of the effectiveness and ecological impacts of management interventions for Spartina species
● Spartina abundance decreases over time by chemical control. ● Integrated control is the most efficient method to control Spartina . ● Biodiversity sometimes decreases after Spartina management.
Invasions by Spartina species pose serious threats to global coastal ecosystems. Although many studies have examined the effectiveness and ecological impacts of invasive Spartina management, no comprehensive global synthesis has been conducted to assess the effects of management on Spartina per se and on wider non-targets. Here, we conducted a global meta-analysis of 3,459 observations from 102 studies to quantify the effects of different management interventions (physical, chemical, biological, and integrated control) on Spartina per se and native biodiversity and environments. We found that physical measures quickly suppressed Spartina but that their effectiveness declined over time. By contrast, chemical measures decreased the abundance and growth of Spartina to a lesser degree in the early stage, but the effectiveness increased over time. Different management measures did not significantly decrease the diversity of native biota on the whole, but native-plant diversity significantly decreased with time after physical control. Different management measures did not affect abiotic factors differently. These results support the use of chemical measures to control invasive Spartina, although their effectiveness would depend on the time since the management intervention. Addressing the problem of Spartina regrowth following physical control requires improved techniques. We hold that initial states of invaders and subsequent environmental changes after management interventions should be weighed in evaluating control efficacy.
Plant invasion / Biodiversity / Meta-analysis / Restoration / Salt marshes / Treatment timing
[1] |
Adams C R, Hovick S M, Anderson N O, Kettenring K M. (2021). We can better manage ecosystems by connecting solutions to constraints: learning from wetland plant invasions. Frontiers in Environmental Science, 9: 715350
CrossRef
Google scholar
|
[2] |
Adams J, van Wyk E, Riddin T. (2016). First record of Spartina alterniflora in southern Africa indicates adaptive potential of this saline grass. Biological Invasions, 18(8): 2153–2158
CrossRef
Google scholar
|
[3] |
An S Q, Gu B H, Zhou C F, Wang Z S, Deng Z F, Zhi Y B, Li H L, Chen L, Yu D H, Liu Y H. (2007). Spartina invasion in China: implications for invasive species management and future research. Weed Research, 47(3): 183–191
CrossRef
Google scholar
|
[4] |
Augustinus B A, Gentili R, Horvath D, Naderi R, Sun Y, Tournet A, Schaffner U, Muller-Scharer H. (2020). Assessing the risks of non-target feeding by the accidentally introduced ragweed leaf beetle, Ophraella communa, to native European plant species. Biological Control, 150: 104356
CrossRef
Google scholar
|
[5] |
Baker C M, Bode M. (2016). Placing invasive species management in a spatiotemporal context. Ecological Applications, 26(3): 712–725
CrossRef
Google scholar
|
[6] |
Burge O R, Bodmin K A, Clarkson B R, Bartlam S, Watts C H, Tanner C C. (2017). Glyphosate redirects wetland vegetation trajectory following willow invasion. Applied Vegetation Science, 20(4): 620–630
CrossRef
Google scholar
|
[7] |
Chen H, Liao B W, Liu B E, Peng C H, Zhang Y, Guan W, Zhu Q A, Yang G. (2014). Eradicating invasive Spartina alterniflora with alien Sonneratia apetala and its implications for invasion controls. Ecological Engineering, 73: 367–372
CrossRef
Google scholar
|
[8] |
Clewley G D, Eschen R, Shaw R H, Wright D J. (2012). The effectiveness of classical biological control of invasive plants. Journal of Applied Ecology, 49(6): 1287–1295
CrossRef
Google scholar
|
[9] |
Cohen J. (1960). A coefficient of agreement for nominal scales. Educational and Psychological Measurement, 20(1): 37–46
CrossRef
Google scholar
|
[10] |
CottetM, De Montaudouin X, BlanchetH, LebleuP (2007). Spartina anglica eradication experiment and in situ monitoring assess structuring strength of habitat complexity on marine macrofauna at high tidal level. Estuarine, Coastal and Shelf Science, 71(3–4): 629–640
CrossRef
Google scholar
|
[11] |
Cousins M M, Briggs J, Whitwell T, Gresham C, Whetstone J. (2010). Reestablishment potential of beach Vitex (Vitex rotundifolia) after removal and control efforts. Invasive Plant Science and Management, 3(3): 327–333
CrossRef
Google scholar
|
[12] |
Cui B S, He Q, An Y. (2011). Spartina alterniflora invasions and effects on crab communities in a western Pacific estuary. Ecological Engineering, 37(11): 1920–1924
CrossRef
Google scholar
|
[13] |
Culliney T W. (2005). Benefits of classical biological control for managing invasive plants. Critical Reviews in Plant Sciences, 24(2): 131–150
CrossRef
Google scholar
|
[14] |
Davoren M J, Schiestl R H. (2018). Glyphosate-based herbicides and cancer risk: a post-IARC decision review of potential mechanisms, policy and avenues of research. Carcinogenesis, 39(10): 1207–1215
CrossRef
Google scholar
|
[15] |
Diagne C, Leroy B, Gozlan R E, Vaissiere A C, Assailly C, Nuninger L, Roiz D, Jourdain F, Jaric I, Courchamp F. (2020). InvaCost, a public database of the economic costs of biological invasions worldwide. Scientific Data, 7(1): 277
CrossRef
Google scholar
|
[16] |
Dibble K L, Pooler P S, Meyerson L A. (2013). Impacts of plant invasions can be reversed through restoration: a regional meta-analysis of faunal communities. Biological Invasions, 15(8): 1725–1737
CrossRef
Google scholar
|
[17] |
Frank J H, McCoy E D. (2007). The risk of classical biological control in Florida. Biological Control, 41(2): 151–174
CrossRef
Google scholar
|
[18] |
Gao Y, Tang L, Wang J Q, Wang C H, Liang Z S, Li B, Chen J K, Zhao B. (2009). Clipping at early florescence is more efficient for controlling the invasive plant Spartina alterniflora. Ecological Research, 24(5): 1033–1041
CrossRef
Google scholar
|
[19] |
Grevstad F S, Strong D R, Garcia-Rossi D, Switzer R W, Wecker M S. (2003). Biological control of Spartina alterniflora in Willapa Bay, Washington using the planthopper Prokelisia marginata: agent specificity and early results. Biological Control, 27(1): 32–42
CrossRef
Google scholar
|
[20] |
He Q, Silliman B R. (2016). Consumer control as a common driver of coastal vegetation worldwide. Ecological Monographs, 86(3): 278–294
CrossRef
Google scholar
|
[21] |
Hedge P, Kriwoken L K, Patten K. (2003). A review of Spartina management in Washington State, US. Journal of Aquatic Plant Management, 41: 82–90
|
[22] |
Hedges L V, Gurevitch J, Curtis P S. (1999). The meta-analysis of response ratios in experimental ecology. Ecology, 80(4): 1150–1156
CrossRef
Google scholar
|
[23] |
Hopkinson P, Hammond M, Bartolome J W, Macaulay L. (2020). Using consecutive prescribed fires to reduce shrub encroachment in grassland by increasing shrub mortality. Restoration Ecology, 28(4): 850–858
CrossRef
Google scholar
|
[24] |
JennionsM D, Lortie C J, RosenbergM S, RothsteinH R (2013). Handbook of Meta-analysis in Ecology and Evolution. Koricheva J, Gurevitch J, Mengersen K, eds. Princeton: Princeton University Press
|
[25] |
Kettenring K M, Adams C R. (2011). Lessons learned from invasive plant control experiments: a systematic review and meta-analysis. Journal of Applied Ecology, 48: 970–979
CrossRef
Google scholar
|
[26] |
Lee S Y, Khim J S. (2017). Hard science is essential to restoring soft-sediment intertidal habitats in burgeoning East Asia. Chemosphere, 168: 765–776
CrossRef
Google scholar
|
[27] |
Li B, Liao C H, Zhang X D, Chen H L, Wang Q, Chen Z Y, Gan X J, Wu J H, Zhao B, Ma Z J.
CrossRef
Google scholar
|
[28] |
Li H P, Zhang L Q. (2008). An experimental study on physical controls of an exotic plant Spartina alterniflora in Shanghai, China. Ecological Engineering, 32(1): 11–21
CrossRef
Google scholar
|
[29] |
Li T Y, Zhang C W, Zhang J Y, Yan S, Qin C Y. (2021). Remediation of 2,4-dichlorophenol-contaminated groundwater using nano-sized CaO2 in a two-dimensional scale tank. Frontiers of Environmental Science & Engineering, 15(5): 87
CrossRef
Google scholar
|
[30] |
LiuY J, Oduor A M O, ZhangZ, ManeaA, ToothI M, LeishmanM R, Xu X L, Van KleunenM (2017). Do invasive alien plants benefit more from global environmental change than native plants? Global Change Biology, 23(8): 3363–3370
CrossRef
Google scholar
|
[31] |
Major W W, Grue C E, Grassley J M, Conquest L L. (2003). Mechanical and chemical control of smooth cordgrass in Willapa Bay, Washington. Journal of Aquatic Plant Management, 41: 6–12
|
[32] |
Mobberley D G. (1953). Taxonomy and distribution of the genus Spartina. Iowa State College Journal of Science, 30: 471–574
|
[33] |
Neira C, Levin L A, Grosholz E D, Mendoza G. (2007). Influence of invasive Spartina growth stages on associated macrofaunal communities. Biological Invasions, 9(8): 975–993
CrossRef
Google scholar
|
[34] |
Ning Z H, Chen C, Xie T, Zhu Z C, Wang Q, Cui B S, Bai J H. (2021). Can the native faunal communities be restored from removal of invasive plants in coastal ecosystems? A global meta-analysis. Global Change Biology, 27(19): 4644–4656
CrossRef
Google scholar
|
[35] |
Ning Z H, Xie T, Liu Z Z, Bai J H, Cui B S. (2019). Native herbivores enhance the resistance of an anthropogenically disturbed salt marsh to Spartina alterniflora invasion. Ecosphere, 10(1): e02565
CrossRef
Google scholar
|
[36] |
Patten K. (2002). Smooth cordgrass (Spartina alterniflora) control with imazapyr. Weed Technology, 16(4): 826–832
CrossRef
Google scholar
|
[37] |
Pearson D E, Ortega Y K, Runyon J B, Butler J L. (2016). Secondary invasion: the bane of weed management. Biological Conservation, 197: 8–17
CrossRef
Google scholar
|
[38] |
Pejchar L, Mooney H A. (2009). Invasive species, ecosystem services and human well-being. Trends in Ecology & Evolution, 24(9): 497–504
CrossRef
Google scholar
|
[39] |
PingY, Zhang L Q (2010). Study on long-term effects of physical control measures on Spartina alterniflora. Marine Environmental Science, 29(1): 32–35 (in Chinese)
|
[40] |
QuanW M, Zhang H, WuZ L, JinS F, TangF H, DongJ B (2016). Does invasion of Spartina alterniflora alter microhabitats and benthic communities of salt marshes in Yangtze River estuary? Ecological Engineering, 88: 153–164
CrossRef
Google scholar
|
[41] |
R Core Team (2021). A language and environment for statistical computing. Available access at the website of R-project.org
|
[42] |
Reeder T G, Hacker S D. (2004). Factors contributing to the removal of a marine grass invader (Spartina anglica) and subsequent potential for habitat restoration. Estuaries, 27(2): 244–252
CrossRef
Google scholar
|
[43] |
ReidA M, Morin L, DowneyP O, FrenchK, VirtueJ G (2009). Does invasive plant management aid the restoration of natural ecosystems? Biological Conservation, 142(10): 2342–2349
CrossRef
Google scholar
|
[44] |
Ren J L, Chen J S, Xu C L, Van De Koppel J, Thomsen M S, Qiu S Y, Cheng F Y, Song W J, Liu Q X, Xu C.
CrossRef
Google scholar
|
[45] |
Roberts P D, Pullin A S. (2008). The effectiveness of management interventions for the control of Spartina species: a systematic review and meta-analysis. Aquatic Conservation, 18(5): 592–618
CrossRef
Google scholar
|
[46] |
RohatgiA (2017). Web Plot Digitizer. Austin, TX, USA
|
[47] |
Sardain A, Sardain E, Leung B. (2019). Global forecasts of shipping traffic and biological invasions to 2050. Nature Sustainability, 2(4): 274–282
CrossRef
Google scholar
|
[48] |
Seebens H, Blackburn T M, Dyer E E, Genovesi P, Hulme P E, Jeschke J M, Pagad S, Pyšek P, Winter M, Arianoutsou M.
CrossRef
Google scholar
|
[49] |
Seebens H, Essl F, Dawson W, Fuentes N, Moser D, Pergl J, Pyšek P, Van Kleunen M, Weber E, Winter M.
CrossRef
Google scholar
|
[50] |
Shackelford G E, Kelsey R, Dicks L V. (2019). Effects of cover crops on multiple ecosystem services: ten meta-analyses of data from arable farmland in California and the Mediterranean. Land Use Policy, 88: 104204
CrossRef
Google scholar
|
[51] |
Sheng Q, Zhao B, Huang M Y, Wang L, Quan Z X, Fang C M, Li B, Wu J H. (2014). Greenhouse gas emissions following an invasive plant eradication program. Ecological Engineering, 73: 229–237
CrossRef
Google scholar
|
[52] |
Shimeta J, Saint L, Verspaandonk E R, Nugegoda D, Howe S. (2016). Long-term ecological consequences of herbicide treatment to control the invasive grass, Spartina anglica, in an Australian saltmarsh. Estuarine, Coastal and Shelf Science, 176: 58–66
CrossRef
Google scholar
|
[53] |
Silliman B R, Zieman J C. (2001). Top-down control of Spartina alterniflora production by periwinkle grazing in a Virginia salt marsh. Ecology, 82(10): 2830–2845
CrossRef
Google scholar
|
[54] |
StrongD R, Ayres D A (2009). Human Impacts on Salt Marshes: A Global Perspective. University of California Press: Berkeley and Los Angeles
|
[55] |
Strong D R, Ayres D A. (2016). Control and consequences of Spartina spp. invasions with focus upon San Francisco Bay. Biological Invasions, 18(8): 2237–2246
CrossRef
Google scholar
|
[56] |
Strong D R, Ayres D R. (2013). Ecological and evolutionary misadventures of Spartina. Annual Review of Ecology, Evolution, and Systematics, 44(1): 389–410
CrossRef
Google scholar
|
[57] |
Tang L, Gao Y, Wang C H, Wang J Q, Li B, Chen J K, Zhao B. (2010). How tidal regime and treatment timing influence the clipping frequency for controlling invasive Spartina alterniflora: implications for reducing management costs. Biological Invasions, 12(3): 593–601
CrossRef
Google scholar
|
[58] |
Tataridas A, Jabran K, Kanatas P, Oliveira R S, Freitas H, Travlos I. (2022). Early detection, herbicide resistance screening, and integrated management of invasive plant species: a review. Pest Management Science, 78(10): 3957–3972
CrossRef
Google scholar
|
[59] |
Van BruggenA H C, HeM M, ShinK, MaiV, JeongK C, FinckhM R, Morris J G Jr (2018). Environmental and health effects of the herbicide glyphosate. Science of the Total Environment, 616–617: 255–268
CrossRef
Google scholar
|
[60] |
van Wilgen B W, Raghu S, Sheppard A W, Schaffner U. (2020). Quantifying the social and economic benefits of the biological control of invasive alien plants in natural ecosystems. Current Opinion in Insect Science, 38: 1–5
CrossRef
Google scholar
|
[61] |
Viechtbauer W. (2010). Conducting meta-analyses in R with the metafor package. Journal of Statistical Software, 36(3): 1–48
CrossRef
Google scholar
|
[62] |
WangQ, An S Q, MaZ J, ZhaoB, ChenJ K, LiB (2006). Invasive Spartina alterniflora: biology, ecology and management. Journal of Systematics and Evolution, 44(5): 559–588 (in Chinese)
CrossRef
Google scholar
|
[63] |
WangS Y, Martin P A, HaoY, SutherlandW J, LiB (2021). Management of invasive Spartina species: a systematic review protocol. OSF, DOI: 10.17605/OSF.IO/A6BR5
|
[64] |
Williams S L, Grosholz E D. (2008). The invasive species challenge in estuarine and coastal environments: marrying management and science. Estuaries and Coasts, 31(1): 3–20
CrossRef
Google scholar
|
[65] |
XieB H, Han G X (2018). Control of invasive Spartina alterniflora: a review. Chinese Journal of Applied Ecology, 29(10): 3464–3476 (in Chinese)
|
[66] |
Xie B H, Han G X, Qiao P Y, Mei B L, Wang Q, Zhou Y F, Zhang A F, Song W M, Guan B. (2019). Effects of mechanical and chemical control on invasive Spartina alterniflora in the Yellow River Delta, China. PeerJ, 7: e7655
CrossRef
Google scholar
|
[67] |
Yuan L, Zhang L Q, Xiao D R, Huang H M. (2011). The application of cutting plus waterlogging to control Spartina alterniflora on saltmarshes in the Yangtze Estuary, China. Estuarine, Coastal and Shelf Science, 92(1): 103–110
CrossRef
Google scholar
|
[68] |
Zhang Y, Peng Z, Dong Z M, Wang M J, Jiang C. (2022). Twenty years of achievements in China’s implementation of the Stockholm Convention. Frontiers of Environmental Science & Engineering, 16(12): 152
CrossRef
Google scholar
|
[69] |
Zhang Y H, Meng H Y, Wang Y, He Q. (2018). Herbivory enhances the resistance of mangrove forest to cordgrass invasion. Ecology, 99(6): 1382–1390
CrossRef
Google scholar
|
[70] |
Zhao C Y, Li J S, Zhao X J. (2019). Mowing plus shading as an effective method to control the invasive plant Spartina alterniflora. Flora (Jena), 257: 151408
CrossRef
Google scholar
|
[71] |
Zhu Z Q, Zhang L Q, Wang N, Schwarz C, Ysebaert T. (2012). Interactions between the range expansion of saltmarsh vegetation and hydrodynamic regimes in the Yangtze Estuary, China. Estuarine, Coastal and Shelf Science, 96: 273–279
CrossRef
Google scholar
|
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