Abstract
Spartina anglica (hereafter Spartina) is an invasive perennial marsh grass shifting hydrodynamic regime and sediment characteristics in invaded area, thereby reducing macrobenthic diversity. There have been only a few studies focusing on the patch structure of Spartina according to size and its effects on macrofauna. A field experiment was conducted to identify effects of Spartina patches where they have been introduced no later than 5 years after invasion occurred on macrofauna assemblages in Ganghwa Island, South Korea. The survey area was divided into two sections according to vegetation: (1) Suaeda japonica vegetation from 0 to 60 m away from the levee, and (2) bare mudflat from 60 to 90 m away from the levee. The patch sizes of Spartina were categorized into small (1–4 m2), medium (5–11 m2), and large (13–40 m2) in area with four replicates for each section. The biomass ratio of the belowground and aboveground in the small size patch of Spartina was significantly higher than those in the medium and large size patch of Spartina. It indicated that more resource was allocated to rhizomes in small size patch with short invasion history (1 ~ 2 years). After Spartina invaded, macrofauna richness (70%), Shannon–Wiener diversity (80%), and density (67%) were decreased. However, infaunal deposit-feeding polychaete Perinereis linea and epifaunal gastropods Batillaria cumingi and Lactiforis takii increased by Spartina. Ordination of macroinvertebrate assemblages separated the habitat with Spartina invasion from the adjacent uninvaded tidal flat and Suaeda japonica habitats. This study offers a significant insight into early invasion strategies of an aggressive plant invader, Spartina for management of coastal wetlands and its impacts on macrofaunal assemblages.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data produced in this study are available upon requests from the corresponding author.
Code availability
‘Not applicable’ for that section.
References
Amsberry L, Baker MA, Ewanchuk PJ, Bertness MD (2000) Clonal integration and the expansion of Phragmites australis. Ecol Appl 10:1110–1118. https://doi.org/10.1890/1051-0761(2000)010[1110:CIATEO]2.0.CO;2
Ayres DR, Strong DR (2002) The Spartina invasion of san francisco bay. Aquat Nuis Species Digest 4:37–39
Balke T, Klaassen PC, Garbutt A, Van der Wal D, Herman PM, Bouma TJ (2012) Conditional outcome of ecosystem engineering: a case study on tussocks of the salt marsh pioneer Spartina anglica. Geomorphology 153:232–238. https://doi.org/10.1016/j.geomorph.2012.03.002
Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193. https://doi.org/10.1890/10-1510.1
Baumel A, Ainouche M, Kalendar R, Schulman AH (2002) Retrotransposons and genomic stability in populations of the young allopolyploid species Spartina anglica C.E. Hubbard (Poaceae). Mol Biol Evol 19:1218–1227. https://doi.org/10.1093/oxfordjournals.molbev.a004182
Boorman LA (1999) Salt marshes: present functioning and future change. Mangrove Salt Marshes 3:227–241. https://doi.org/10.1023/A:1009998812838
Bouma TJ, Ortells V, Ysebaert T (2009) Comparing biodiversity effects among ecosystem engineers of contrasting strength: macrofauna diversity in Zostera noltii and Spartina anglica vegetation. Helgol Mar Res 63:3–18. https://doi.org/10.1007/s10152-008-0133-8
Bouma TJ, De Vries MB, Herman PM (2010) Comparing ecosystem engineering efficiency of two plant species with contrasting growth strategies. Ecology 91:2696–2704. https://doi.org/10.1890/09-0690.1
Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–46. https://doi.org/10.1097/00010694-194501000-00006
Brusati ED, Grosholz ED (2006) Native and introduced ecosystem engineers produce contrasting effects on estuarine infaunal communities. Biol Invasions 8:683–695. https://doi.org/10.1007/s10530-005-2889-y
Brusati ED, Grosholz ED (2009) Does invasion of hybrid cordgrass change estuarine food webs? Biol Invasions 11:917–926. https://doi.org/10.1007/s10530-008-9304-4
Castellanos EM, Figueroa ME, Davy AJ (1994) Nucleation and facilitation in saltmarsh succession: interactions between Spartina maritima and Arthrocnemum perenne. J Ecol. https://doi.org/10.2307/2261292
Castillo JM, Grewell BJ, Pickart AJ, Figueroa E, Sytsma M (2016) Variation in tussock architecture of the invasive cordgrass Spartina densiflora along the Pacific Coast of North America. Biol Invasions 18:2159–2174. https://doi.org/10.1007/s10530-015-0991-3
Chen H, Li B, Hu J, Chen J, Wu J (2007) Effects of Spartina alterniflora invasion on benthic nematode communities in the Yangtze Estuary. Mar Ecol Prog Ser 336:99–110. https://doi.org/10.3354/meps336099
Chen Z, Guo L, Jin B, Wu J, Zheng G (2009) Effect of the exotic plant Spartina alterniflora on macrobenthos communities in salt marshes of the Yangtze River Estuary, China. Estuar Coast Shelf Sci 82:265–272. https://doi.org/10.1016/j.ecss.2009.01.014
Choi KH, Walton M, Park GS (2010) Benthic habitat quality change as measured by macroinfauna community in a tidal flat on the west coast of Korea. J Oceanogr 66:307–317. https://doi.org/10.1007/s10872-010-0027-7
Chung CH (1993) Thirty years of ecological engineering with Spartina plantations in China. Ecol Eng 2:261–289. https://doi.org/10.1016/0925-8574(93)90019-C
Compton TJ, Holthuijsen S, Koolhaas A, Dekinga A, Horn TJ, Smith J, Galama Y, Brugge M, Wal DVD, Meer J, Veer HW, Piersma T (2013) Distinctly variable mudscapes: distribution gradients of intertidal macrofauna across the Dutch Wadden Sea. J Sea Res 82:103–116. https://doi.org/10.1016/j.seares.2013.02.002
Connor R, Chmura GL (2000) Dynamics of above-and belowground organic matter in a high latitude macrotidal saltmarsh. Mar Ecol Prog Ser 204:101–110. https://doi.org/10.3354/meps204101
Costa CSB, Marangoni JC, Azevedo AMG (2003) Plant zonation in irregularly flooded salt marshes: relative importance of stress tolerance and biological interactions. J Ecol 91:951–965. https://doi.org/10.1046/j.1365-2745.2003.00821.x
Costanza R, d’Arge R, de Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, O’Neill RV, Paruelo J, Raskin RG, Sutton P, van den Belt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260. https://doi.org/10.1038/387253a0
Cottet M, de Montaudouin X, Blanchet H, Lebleu P (2007) Spartina anglica eradication experiment and in situ monitoring assess structuring strength of habitat complexity on marine macrofauna at high tidal level. Estuar Coast Shelf Sci 71(3–4):629–640. https://doi.org/10.1016/j.ecss.2006.09.014
Curado G, Sanchez-Moyano JE, Figueroa E, Castillo JM (2014) Do Spartina maritima plantations enhance the macroinvertebrate community in European salt marshes? Estuar Coast 37:589–601. https://doi.org/10.1007/s12237-013-9713-1
Cutajar J, Shimeta J, Nugegoda D (2012) Impacts of the invasive grass Spartina anglica on benthic macrofaunal assemblages in a temperate Australian saltmarsh. Mar Ecol Prog Ser. https://doi.org/10.3354/meps09826
Daehler CC, Strong DR (1996) Status, prediction and prevention of introduced cordgrass Spartina spp. invasions in Pacific estuaries, USA. Biol Conserv 78:1–2. https://doi.org/10.1016/0006-3207(96)00017-1
Dame RF, Kenny PD (1986) Variability of Spartina alterniflora primary production in the euhaline North Inlet estuary. Mar Ecol Prog Ser 32:71–80. https://doi.org/10.3354/MEPS032071
Darby FA, Turner RE (2008) Below- and aboveground Spartina alterniflora production in a Louisiana salt marsh. Estuar Coasts 31:223–231. https://doi.org/10.1007/s12237-007-9014-7
Ellison AM, Bertness MD, Miller T (1986) Seasonal patterns in the belowground biomass of Spartina alterniflora (Gramineae) across a tidal gradient. Am J Bot 73:1548–1554. https://doi.org/10.1002/j.1537-2197.1986.tb10905.x
Figueroa ME, Castillo JM, Redondo S, Luque T, Castellanos EM, Nieva FJ, Luque CJ, Rubio-Casal AE, Davy AJ (2003) Facilitated invasion by hybridization of Sarcocornia species in a salt-marsh succession. J Ecol 91(4):616–626. https://doi.org/10.1046/j.1365-2745.2003.00794.x
Forbes TL, Lopez GR (1990) The effect of food concentration, body size, and environmental oxygen tension on the growth of the deposit-feeding polycheate, Capitella species 1. Limnol Oceanogr 35:1535–1544. https://doi.org/10.4319/lo.1990.35.7.1535
Gallego-Tévar B, Infante-Izquierdo MD, Figueroa E, Nieva FJ, Muñoz-Rodríguez AF, Grewell BJ, Castillo JM (2019) Some like it hot: maternal-switching with climate change modifies formation of invasive Spartina hybrids. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00484
Ganju NK, Kirwan ML, Dickhudt PJ, Guntenspergen GR, Cahoon DR, Kroeger KD (2015) Sediment transport-based metrics of wetland stability. Geophys Res Lett 42:7992–8000. https://doi.org/10.1002/2015GL065980
Ge BM, Bao YX, Cheng HY, Zhang DZ, Hu ZY (2012) Influence of Spartina alterniflora invasion stages on macrobenthic communities on a tidal flat in Wenzhou Bay, China. Braz J Oceanogr 60:441–448. https://doi.org/10.1590/S1679-87592012000300014
Gray AJ, Marshall DF, Raybould AF (1991) A century of evolution in Spartina anglica. Adv Ecol Res 21:1–62. https://doi.org/10.1016/S0065-2504(08)60096-3
Grosholz ED, Levin LA, Tyler AC, Neira C (2009) Changes in community structure and ecosystem function following Spartina alterniflora invasion of Pacific estuaries. In: Silliman BR, Bertness M, Grosholz E (eds) Human impacts on salt marshes: a global perspective. University of California Press, Berkeley, CA, pp 23–40
Hacker SD, Heimer D, Hellquist CE, Reeder TG, Reeves B, Riordan TJ, Dethier MN (2001) A marine plant (Spartina anglica) invades widely varying habitats: potential mechanisms of invasion and control. Biol Invasions 3:211–217. https://doi.org/10.1023/A:1014555516373
Hedge P, Kriwoken LK (2000) Evidence for effects of Spartina anglica invasion on benthic macrofauna in Little Swanport estuary, Tasmania. Austral Ecol 25:150–159. https://doi.org/10.1046/j.1442-9993.2000.01016.x
Hedge P, Kriwoken LK, Patten K (2003) A review of Spartina management in Washington State, US. J Aquat Plant Manag 41:82–90
Hosack GR, Dumbauld BR, Ruesink JL, Armstrong DA (2006) Habitat associations of estuarine species: comparisons of intertidal mudflat, seagrass (Zostera marina), and oyster (Crassostrea gigas) habitats. Estuar Coasts 29:1150–1160. https://doi.org/10.1007/BF02781816
Hubbard JCE, Stebbings RE (1968) Spartina marshes in Southern England: VII. Stratigraphy of the Keysworth marsh. Poole Harb J Ecol 56:707–722. https://doi.org/10.2307/2258102
Hubbard JCE, Partridge TR (1981) Tidal immersion and the growth of Spartina anglica marshes in the Waihopai River Estuary, New Zealand. NZ J Bot 19:5–121. https://doi.org/10.1080/0028825X.1981.10425195
Kanaya G, Takagi S, Kikuchi E (2008) Dietary contribution of the microphytobenthos to infaunal deposit feeders in an estuarine mudflat in Japan. Mar Biol 155:543–553. https://doi.org/10.1007/s00227-008-1053-5
Kang CK, Kim JB, Lee KS, Kim JB, Lee PY, Hong JS (2003) Trophic importance of benthic microalgae to macrozoobenthos in coastal bay systems in Korea: Dual stable C and N isotope analyses. Mar Ecol Prog Ser 259:79–92. https://doi.org/10.3354/meps259079
Kim S, Hong JS, Kim DW (2019) Effective initiation diffusion model based on data of patches growing in smooth cordgrass Spartina alterniflora. In: The Fourth Asian Mar Biol Symposium. Taiwan.
Kimura T, Hanai T, Kimura S, Fujioka E (2016) Identification of invasive alien species Spartina alterniflora in Japan using morphological characteristics as compared with native species Phragmites australis. Jpn J Benthol 70:91–94 ((In Japanese with English summary))
Kriwoken LK, Hedge P (2000) Exotic species and estuaries: Managing Spartina anglica in Tasmania, Australia. Ocean Coast Manag 43:573–584. https://doi.org/10.1016/S0964-5691(00)00047-8
Lee AK, Ayres DR, Pakenham-Walsh MR, Strong DR (2016) Responses to salinity of Spartina hybrids formed in San Francisco Bay, California (S. alterniflora × foliosa and S. densiflora × foliosa). Biol Invasions 18:2207–2219. https://doi.org/10.1007/s10530-015-1011-3
Levin LA, Neira C, Grosholz ED (2006) Invasive cordgrass modifies wetland trophic function. Ecology 87:419–432. https://doi.org/10.1890/04-1752
Linthurst RA, Blum U (1981) Growth modifications of Spartina alterniflora Loisel. by the interaction of pH and salinity under controlled conditions. J Exp Mar Biol Ecol 55:207–218. https://doi.org/10.1016/0022-0981(81)90112-X
Lodge DM (1993) Biol Invasions: lessons for ecology. Trends Ecol Evol 8:133–137. https://doi.org/10.1016/0169-5347(93)90025-K
Möller I, Kudella M, Rupprecht F, Spencer T, Paul M, van Wesenbeeck BK, Wolters G, Jensen K, Bouma TJ, Miranda-Lange M, Schimmels S (2014) Wave attenuation over coastal salt marshes under storm surge conditions. Nat Geosci 7:727–731. https://doi.org/10.1038/NGEO2287
Morris JT, Sundareshwar PV, Nietch CT, Kjerfve B, Cahoon DR (2002) Responses of coastal wetlands to rising sea level. Ecology 83:2869–2877. https://doi.org/10.1890/0012-9658(2002)083[2869:ROCWTR]2.0.CO;2
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36. https://doi.org/10.1016/S0003-2670(00)88444-5
Neira C, Grosholz ED, Levin LA, Blake R (2006) Mechanisms generating modification of benthos following tidal flat invasion by a Spartina hybrid. Ecol Appl 16:1391–1404. https://doi.org/10.1890/1051-0761(2006)016
Neira C, Levin LA, Grosholz ED (2005) Benthic macrofaunal communities of three sites in San Francisco Bay invaded by hybrid Spartina, with comparison to uninvaded habitats. Mar Ecol Prog Ser 292:111–126. https://doi.org/10.3354/MEPS292111
Neira C, Levin LA, Grosholz ED, Mendoza G (2007) Influence of invasive Spartina growth stages on associated macrofaunal communities. Biol Invasions 9:975–993. https://doi.org/10.1007/s10530-007-9097-x
Netto SA, Lana PC (1997) Influence of Spartina alterniflora on superficial sediment characteristics of tidal flats in Paranagua Bay (southeastern Brazil). Estuar Coast Shelf Sci 44:641–648. https://doi.org/10.1006/ecss.1996.0154
Netto SA, Lana PC (1999) The role of above- and below-ground components of Spartina alterniflora (Loisel) and detritus biomass in structuring macrobenthic associations of Paranagua Bay (SE, Brazil). Hydrobiologia 400:167–177. https://doi.org/10.1023/A:1003753001411
Petrone RM, Waddington JM, Price JS (2001) Ecosystem scale evapotranspiration and net CO2 exchange from a restored peatland. Hydrol Process 15:2839–2845. https://doi.org/10.1002/hyp.475
Pielou EC (1966) The measurement of diversity in different types of biological collections. J Theor Biol 13:131–144. https://doi.org/10.1016/0022-5193(66)90013-0
Prieur-Richard AH, Lavorel S, Grigulis K, Dos Santos A (2000) Plant community diversity and invasibility by exotics: Invasion of Mediterranean old fields by Conyza bonariensis and Conyza canadensis. Ecol Lett 3:412–422. https://doi.org/10.1046/j.1461-0248.2000.00157.x
Quan W, Zhang H, Wu Z, Jin S, Tang F, Dong J (2016) Does invasion of Spartina alterniflora alter microhabitats and benthic communities of salt marshes in Yangtze River estuary? Ecol Eng 88:153–164. https://doi.org/10.1016/j.ecoleng.2015.12.026
Raybould AF, Gray AJ, Lawrence MJ, Marshall DF (1991) The evolution of Spartina anglica C.E. Hubbard (Gramineae): origin and genetic variability. Biol J Linn Soc 43:111–126. https://doi.org/10.1111/j.1095-8312.1991.tb00588.x
Roman CT, Daiber FC (1984) Aboveground and belowground primary production dynamics of two Delaware Bay tidal marshes. Bull Torrey Bot Club. https://doi.org/10.2307/2996208
Schirmel J, Bundschuh M, Entling MH et al (2016) Impacts of invasive plants on resident animals across ecosystems, taxa, and feeding types: a global assessment. Glob Change Biol 22:594–603. https://doi.org/10.1111/gcb.13093
Schubauer JP, Hopkinson CS (1984) Above- and belowground emergent macrophyte production and turnover in a coastal marsh ecosystem, Georgia. Limnol Oceanogr 29:1052–1065. https://doi.org/10.4319/lo.1984.29.5.1052
Sheehan MR, Ellison JC (2014) Intertidal morphology change following Spartina anglica introduction, Tamar Estuary, Tasmania. Estuar Coast Shelf Sci 149:24–37. https://doi.org/10.1016/j.ecss.2014.07.006
Shin WH, Kim JH, Lee EJ (2020) Effect of native Suaeda japonica structure on the initial seed settlement of an invasive plant Spartina anglica. Aquat Bot 161:103175. https://doi.org/10.1016/j.aquabot.2019.103175
Snelgrove PVR (1998) The biodiversity of macrofaunal organisms in marine sediments. Biodivers Conserv 7:1123–1132. https://doi.org/10.1023/A:1008867313340
Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method 1. Limnol Oceanogr 14:799–801. https://doi.org/10.4319/lo.1969.14.5.0799
Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993. https://doi.org/10.1111/j.1461-0248.2006.00950.x
Tang M, Kristensen E (2010) Associations between macrobenthos and invasive cordgrass, Spartina anglica, in the Danish Wadden Sea. Helgol Mar Res 64:321–329. https://doi.org/10.1007/s10152-009-0187-2
Temmerman S, Govers G, Wartel S, Meire P (2004) Modelling estuarine variations in tidal marsh sedimentation: response to changing sea level and suspended sediment concentrations. Mar Geol 212:1–19. https://doi.org/10.1016/j.margeo.2004.10.021
Thompson JD, McNeilly T, Gay AJ (1991) Population variation in Spartina anglica CE Hubbard: I. Evidence from a common garden experiment. New Phytol 117(1):115–128. https://doi.org/10.1111/j.1469-8137.1991.tb00951.x
Tripathee R, Schafer KVR (2014) Above- and belowground biomass allocation in four dominant salt marsh species of the eastern United States. Wetlands 35:21–30. https://doi.org/10.1007/s13157-014-0589-z
Valiela I, Teal JM, Persson NY (1976) Production and dynamics of experimentally enriched salt marsh vegetation: Belowground biomass 1. Limnol Oceanogr 21(2):245–252. https://doi.org/10.4319/lo.1976.21.2.0245
Wang R, Yuan L, Zhang L (2010) Impacts of Spartina alterniflora invasion on the benthic communities of salt marshes in the Yangtze Estuary, China. Ecol Eng 36:799–806. https://doi.org/10.1016/j.ecoleng.2010.02.005
Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern B, Jackson J, Lotze H, Micheli F, Palumbi S, Sala E, Selkoe K, Stachowicz J, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790. https://doi.org/10.1126/science.1132294
Wu YT, Wang CH, Zhang XD et al (2009) Effects of saltmarsh invasion by Spartina alterniflora on arthropod community structure and diets. Biol Invasions 11:635–649. https://doi.org/10.1007/s10530-008-9279-1
Xiao Y, Tang J, Qing H, Ouyang Y, Zhao Y, Zhou C, An S (2010) Clonal integration enhances flood tolerance of Spartina alterniflora daughter ramets. Aquat Bot 92:9–13. https://doi.org/10.1016/j.aquabot.2009.09.001
Zuo P, Zhao S, Liu C, Wang C, Liang Y (2012) Distribution of Spartina spp. along China’s coast. Ecol Eng 40:160–166. https://doi.org/10.1016/j.ecoleng.2011.12.014
Acknowledgments
The authors would like to thank the member of Laboratory of Plant Ecology, including Jeong Hwan Bang, Saeromi Moon, Seung-Kyung Lee, Hyunyoung Yang, Shinyeong Park, Minjin Choi, Youngeun Kim for assistance with the vegetation survey. We also thank Tai Yang Lim and Yong Hwan Kim for their assistance in data acquisition using UAV. We would like to express a great appreciation to the anonymous reviewers for their valuable comments on previous versions of this manuscript.
Funding
This work was supported by the Korea Environment Industry and Technology Institute (KEITI) through the Urban Ecological Health Promotion Technology Development Project, funded by the Korea Ministry of Environment (MOE) (no. 2020002770002). This work is financially supported by Korea Ministry of Land, Infrastructure and Transport(MOLIT) as Innovative Talent Education Program for Smart City. This work was supported by the National Research Foundation of Korea (NRF) Grant funded by the Korea government. (MSIT) (2022R1A2C1003504). Wonhyeop Shin is grateful for financial support from Hyundai Motor Chung Mong-Koo Foundation.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interests nor competing interests.
Ethical approval
Sampling protocols were established in compliance with the ethical standards.
Consent to participate
All persons entitled to authorship have been so named and have agreed to participate.
Consent for publication
All authors have seen and agreed to the submitted version of the manuscript.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Shin, W., Oh, M., Hong, JS. et al. Early invasion of common cordgrass (Spartina anglica) increases belowground biomass and decreases macrofaunal density and diversity in a tidal flat marsh. Biol Invasions 24, 3615–3629 (2022). https://doi.org/10.1007/s10530-022-02866-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-022-02866-8