Impacts of plant invasions can be reversed through restoration: A regional meta-analysis of faunal communities

Biological Invasions

Volumn 15, Issue 8, 2013, Pages 1725-1737

  Dibble, Kimberly L ^a   Pooler, Penelope S ^a   Meyerson, Laura A ^a,b  

^a UNIVERSITY OF RHODE ISLAND   (United States)

^b INSTITUTE OF MATHEMATICS   (Czech Republic)

Author keywords

Bootstrapping; Log response ratio; Non native; Phragmites; Salt marsh; Spartina

Indexed keywords

BIOLOGICAL INVASION; BOOTSTRAPPING; INVASIVE SPECIES; LIFE HISTORY; META-ANALYSIS; NEKTON; RESTORATION ECOLOGY; SALTMARSH; TAXONOMY; TIMESCALE;

NEW ENGLAND; UNITED STATES;

INVERTEBRATA; PHRAGMITES; PHRAGMITES AUSTRALIS; SPARTINA; TRACHEOPHYTA;

EID: 84879793517     PISSN: 13873547     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10530-012-0404-9     Document Type: Article

References (106)

1. Able KW, Hagan SM (2000) Effects of common reed (Phragmites australis) invasion on marsh surface macrofauna: response of fishes and decapod crustaceans. Estuaries 23(5): 633-646.
2. Able KW, Hagan SM (2003) Impact of common reed, Phragmites australis, on essential fish habitat: influence on reproduction, embryological development, and larval abundance of mummichog (Fundulus heteroclitus). Estuaries 26(1): 40-50.
3. Able KW, Hagan SM, Brown SA (2003) Mechanisms of marsh habitat alteration due to Phragmites: response of young-of-the-year mummichog (Fundulus heteroclitus) to treatment for Phragmites removal. Estuaries 26(2B): 484-494.
4. Adams DC, Gurevitch J, Rosenberg MS (1997) Resampling tests for meta-analysis of ecological data. Ecology 78(5): 1277-1283.
5. Allen EA, Fell PE, Peck MA, Gieg JA, Gutiike CR, Newkirk MD (1994) Gut contents of common mummichogs, Fundulus heteroclitus L., in a restored impounded marsh and in natural reference marshes. Estuaries 17(2): 462-471.
6. Angradi TR, Hagan SM, Able KW (2001) Vegetation type and the intertidal macroinvertebrate fauna of a brackish marsh: Phragmites vs. Spartina. Wetlands 21(1): 75-92.
7. Arnqvist G, Wooster D (1995) Meta-analysis: synthesizing research findings in ecology and evolution. Trends Ecol Evol 10(6): 236-240.
8. Benoit LK, Askins RA (1999) Impact of the spread of Phragmites on the distribution of birds in Connecticut tidal marshes. Wetlands 19(1): 194-208.
9. Brawley AH, Warren RS, Askins RA (1998) Bird use of restoration and reference marshes within the Barn Island wildlife management area, Stonington, Connecticut, USA. Environ Manage 22(4): 625-633.
10. Brittain RA, Schimmelmann A, Parkhurst DF, Craft CB (2012) Habitat use by coastal birds inferred from stable carbon and nitrogen isotopes. Estuaries Coast 35: 633-645.
11. Buchsbaum RN, Catena J, Hutchins E, James-Pirri MJ (2006) Changes in salt marsh vegetation, Phragmites australis, and nekton in response to increased tidal flushing in a New England salt marsh. Wetlands 26(2): 544-557.
12. Burdick DM, Dionne M, Boumans RM, Short FT (1997) Ecological responses to tidal restorations of two northern New England salt marshes. Wetl Ecol Manag 4(2): 129-144.
13. Burk I (1877) List of plants recently collected on ship's ballast in the neighborhood of Philadelphia. P Acad Nat Sci Phila 29: 105-109.
14. Bushaw-Newton KL, Kreeger DA, Doaty S, Velinsky DJ (2008) Utilization of Spartina- and Phragmites-derived dissolved organic matter by bacteria and ribbed mussels (Geukensia demissa) from Delaware Bay salt marshes. Estuaries Coast 31: 694-703.
15. Canty A, Ripley B (2011) Boot: bootstrap R (S-Plus) functions. R package version 1. 3-3.
16. Chambers RM, Meyerson LA, Saltonstall K (1999) Expansion of Phragmites australis into tidal wetlands of North America. Aquat Bot 64: 261-273.
17. Chambers RM, Havens KJ, Killeen S, Berman M (2008) Common reed Phragmitesaustralis occurrence and adjacent land use along estuarine shoreline in Chesapeake Bay. Wetlands 28(4): 1097-1103.
18. Chambers RM, Meyerson LA, Dibble KL (2012) Ecology of Phragmites australis and responses to tidal restoration. In: Roman C, Burdick D (eds) Tidal marsh restoration: a synthesis of science and management. Island Press, Washington, DC.
19. Currin CA, Wainright SC, Able KW, Weinstein MP, Fuller CM (2003) Determination of food web support and trophic position of the mummichog, Fundulus heteroclitus, in New Jersey smooth cordgrass (Spartina alterniflora), common reed (Phragmites australis), and restored salt marshes. Estuaries 26: 495-510.
20. Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol Lett 14: 419-431.
21. Davison AC, Hinkley DV (1997) Bootstrap methods and their applications. Cambridge Univ Press, Cambridge.
22. Deegan LA, Garritt RH (1997) Evidence for spatial variability in estuarine food webs. Mar Ecol Prog Ser 147: 31-47.
23. Deegan LA, Bowen JL, Drake D, Fleeger JW, Friedrichs CT, Galván KA, Hobbie JE, Hopkinson C, Johnson DS, Johnson JM, LeMay LE, Miller E, Peterson BJ, Picard C, Sheldon S, Sutherland M, Vallino J, Warren RS (2007) Susceptibility of salt marshes to nutrient enrichment and predator removal. Ecol Appl 17(5): S42-S63.
24. Dibble KL, Meyerson LA (2012) Tidal flushing restores the physiological condition of fish residing in degraded salt marshes. PLoS ONE 7(9): e46161.
25. Dionne M, Short FT, Burdick DM (1999) Fish utilization of restored, created, and reference salt-marsh habitat in the Gulf of Maine. Am Fish Soc Symp S22: 384-404.
26. Eberhardt AL, Burdick DM, Dionne M (2010) The effects of road culverts on nekton in New England salt marshes: implications for tidal restoration. Restor Ecol 19. doi: 10. 1111/j. 1526-100X. 2010. 00721. x.
27. Efron B (1987) Better bootstrap confidence intervals (with discussion). J Am Stat Assoc 82: 171-200.
28. Fell PE, Weissbach SP, Jones DA, Fallon MA, Zeppieri JA, Faison EK, Lennon KA, Newberry KJ, Reddington LK (1998) Does invasion of oligohaline tidal marshes by reed grass, Phragmites australis (Cav.) Trin. ex Steud., affect the availability of prey resources for the mummichog, Fundulus heteroclitus L.? J Exp Mar Biol Ecol 222: 59-77.
29. Fry B (2006) Stable isotope ecology. Springer, USA.
30. Gaertner M, Den Breeyen A, Hui C, Richardson DM (2009) Impacts of alien plant invasions on species richness in Mediterranean-type ecosystems: a meta-analysis. Prog Phys Geogr 33(3): 319-338.
31. Galván K, Fleeger JW, Fry B (2008) Stable isotope addition reveals dietary importance of phytoplankton and microphytobenthos to saltmarsh infauna. Mar Ecol Prog Ser 359: 37-49.
32. Galván K, Fleeger JW, Peterson B, Drake D, Deegan LA, Johnson DS (2011) Natural abundance stable isotopes and dual isotope tracer additions help to resolve resources supporting a salt marsh food web. J Exp Mar Biol Ecol 410: 1-11.
33. Gratton C, Denno RF (2005) Restoration of arthropod assemblages in a Spartina salt marsh following removal of the invasive plant Phragmites australis. Restor Ecol 13(2): 358-372.
34. Gratton C, Denno RF (2006) Arthropod food web restoration following removal of an invasive wetland plant. Ecol Appl 16: 622-631.
35. Grothues TM, Able KW (2003a) Discerning vegetation and environmental correlates with subtidal marsh fish assemblage dynamics during Phragmites eradication efforts: interannual Trend Measures. Estuaries 26(2B): 574-586.
36. Grothues TM, Able KW (2003b) Response of juvenile fish assemblages in tidal salt marsh creeks treated for Phragmites removal. Estuaries 26(2B): 563-573.
37. Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analyses. Ecology 80(4): 1142-1149.
38. Hagan SM, Brown SA, Able KW (2007) Production of mummichog (Fundulus heteroclitus): response in marshes treated for common reed (Phragmites australis) removal. Wetlands 27(1): 54-67.
39. Hauber DP, Saltonstall K, White DA, Hood CS (2011) Genetic variation in the common reed, Phragmites australis, in the Mississippi River Delta marshes: evidence for multiple introductions. Estuaries Coast 34: 851-862.
40. Hedges LV, Olkin I (1985) Statistical methods for meta-analysis. Academic Press, Florida.
41. Hedges LV, Gurevitch J, Curtis P (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80: 1150-1156.
42. Hendricks LG, Mossop HE, Kicklighter CE (2011) Palatability and chemical defense of Phragmites australis to the marsh periwinkle snail Littoraria irrorata. J Chem Ecol. doi: 10. 1007/s10886-011-9990-8.
43. Hesterberg T, Moore DS, Monaghan S, Clipson A, Epstein R (2005) Bootstrap methods and permutation tests, 2nd edn. W. H. Freeman, New York.
44. Holt ER, Buchsbaum R (2000) Bird use of Phragmites australis in coastal marshes of northern Massachusetts. In: Pederson J (ed) Marine bioinvasions: proceedings of a conference, January 24-27, 1999. MIT Sea Grant College Program vol 2, pp 232-240.
45. Hunter KL, Fox DA, Brown LM, Able KW (2006) Responses of resident marsh fishes to stages of Phragmites australis invasion in three mid Atlantic estuaries. Estuaries Coast 29(3): 487-498.
46. James-Pirri MJ, Raposa KB, Catena JG (2001) Diet composition of mummichogs, Fundulus heteroclitus, from restoring and unrestricted regions of a New England (U. S. A.) salt marsh. Estuar Coast Shelf Sci 53: 205-213.
47. Jivoff PR, Able KW (2003) Blue crab, Callinectes sapidus, response to the invasive common reed, Phragmites australis: abundance, size, sex ratio, and molting frequency. Estuaries 26(2B): 587-595.
48. Kalies EL, Chambers CL, Covington WW (2010) Wildlife responses to thinning and burning treatments in southwestern conifer forests: a meta-analysis. For Ecol Manag 259: 333-342.
49. Kettenring KM, Reinhardt Adams C (2011) Lessons learned from invasive plant control experiments: a systematic review and meta-analysis. J Appl Ecol 48: 970-979.
50. Kimball ME, Able KW (2007) Nekton utilization of intertidal salt marsh creeks: tidal influences in natural Spartina, invasive Phragmites, and marshes treated for Phragmites removal. J Exp Mar Biol Ecol 346: 87-101.
51. Kimball ME, Able KW, Grothues TM (2010) Evaluation of long-term response of intertidal creek nekton to Phragmites australis (common reed) removal in oligohaline Delaware Bay salt marshes. Restor Ecol 18(5): 772-779.
52. Kneib RT (1986) The role of Fundulus heteroclitus in salt marsh trophodynamics. Am Zool 26: 259-269.
53. Kneib RT (1997) The role of tidal marshes in the ecology of estuarine nekton. Oceanogr Mar Biol Annu Rev 35: 163-220.
54. Kneib RT (2003) Bioenergetic and landscape considerations for scaling expectations of nekton production from intertidal marshes. Mar Ecol Prog Ser 264: 279-296.
55. Kulmatiski A, Beard KH, Meyerson LA, Gibson JC, Mock KE (2010) Nonnative Phragmites australis invasion into Utah wetlands. West N Am Nat 70(4): 541-552.
56. Lambertini C, Mendelssohn IA, Gustafsson MHG, Olesen B, Riis T, Sorrell BK, Brix H (2012) Tracing the origin of Gulf coast Phragmites (Poaceae): a story of long distance dispersal and hybridization. Am J Bot 99(3): 538-551.
57. Litvin SY, Weinstein MP (2003) Life history strategies of estuarine nekton: the role of marsh macrophytes, benthic microalgae, and phytoplankton in the trophic spectrum. Estuaries 26(2B): 552-562.
58. Litvin SY, Weinstein MP (2004) Multivariate analysis of stable-isotope ratios to infer movements and utilization of estuarine organic matter by juvenile weakfish (Cynoscion regalis). Can J Fish Aquat Sci 61: 1851-1861.
59. McClary M Jr (2004) Spartina alterniflora and Phragmites australis as habitat for the ribbed mussel, Geukensia demissa (Dillwyn), in Saw Mill Creek of New Jersey's Hackensack Meadowlands. Urban Habitats 2(1): 83-90.
60. Meadows RE, Saltonstall K (2007) Distribution of native and introduced Phragmites australis in freshwater and oligohaline tidal marshes of the Delmarva Peninsula and southern New Jersey. J Torrey Bot Soc 134(1): 99-107.
61. Meyer DL, Johnson JM, Gill JW (2001) Comparison of nekton use of Phragmites australis and Spartina alterniflora marshes in the Chesapeake Bay, USA. Mar Ecol Prog Ser 209: 71-84.
62. Meyerson LA, Cronin JT (in revision) Evidence for multiple introductions of Phragmites australis to North America: detection of a new non-native haplotype. Biol Invasions.
63. Meyerson LA, Chambers RM, Vogt KA (1999) The effects of Phragmites removal on nutrient pools in a freshwater tidal marsh ecosystem. Biol Invasions 1: 129-136.
64. Meyerson LA, Saltonstall K, Windham L, Kiviat E, Findlay S (2000) A comparison of Phragmites australis in freshwater and brackish marsh environments in North America. Wetl Ecol Manage 8: 89-103.
65. Meyerson LA, Saltonstall K, Chambers RM (2009) Phragmites australis in Eastern North America: a historical and ecological perspective. In: Silliman BR, Grosholz E, Bertness MD (eds) Salt Marshes under global siege. University of California Press, Berkeley, pp 57-82.
66. Molloy PP, Reynolds JD, Gage MJG, Mosqueira I, Cote IM (2008) Links between sex change and fish densities in marine protected areas. Biol Conserv 141: 187-197.
67. Moreno-Mateos D, Power ME, Comin FA, Yockteng R (2012) Structural and functional loss in restored wetland ecosystems. PLoS Biol 10(1). doi: 10. 1371/journal. pbio. 1001247.
68. Osgood DT, Yozzo DJ, Chambers RM, Jacobson D, Hoffman T, Wnek J (2003) Tidal hydrology and habitat utilization by resident nekton in Phragmites and non-Phragmites marshes. Estuaries 26(2B): 522-533.
69. Peterson BJ (1999) Stable isotopes as tracers of organic matter input and transfer in benthic food webs: a review. Acta Oecol 20(4): 479-487.
70. Posey MH, Alphin TD, Meyer DL, Johnson JM (2003) Benthic communities of common reed Phragmites australis and marsh cordgrass Spartina alterniflora marshes in Chesapeake Bay. Mar Ecol Prog Ser 261: 51-61.
71. Powell KI, Chase JM, Knight TM (2011) A synthesis of plant invasion effects on biodiversity across spatial scales. Am J Bot 98(3): 539-548.
72. Pyšek P, Jarosik V, Hulme PE, Pergl J, Hejda M, Schaffner U, Vilà M (2012) A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species' traits and environment. Glob Change Biol. doi: 10. 1111/j. 1365-2486. 2011. 02636. x.
73. Raichel DL, Able KW, Hartman JM (2003) The influence of Phragmites (common reed) on the distribution, abundance, and potential prey of a resident marsh fish in the Hackensack Meadowlands, New Jersey. Estuaries 26(2B): 511-521.
74. Raposa K (2002) Early responses of fishes and crustaceans to restoration of a tidally restricted New England salt marsh. Restor Ecol 10(4): 665-676.
75. Raposa K (2008) Early ecological responses to hydrologic restoration of a tidal pond and salt marsh complex in Narragansett Bay, Rhode Island. J Coast Res 55: 180-192.
76. Raposa KB, Roman CT (2001) Seasonal habitat-use patterns of nekton in a tide-restricted and unrestricted New England salt marsh. Wetlands 21(4): 451-461.
77. Raposa KB, Roman CT (2003) Using gradients in tidal restriction to evaluate nekton community responses to salt marsh restoration. Estuaries 26(1): 98-105.
78. Rey Benayas JM, Newton AC, Diaz A, Bullock JM (2009) Enhancement of biodiversity and ecosystem services by ecological restoration: a meta-analysis. Science 325: 1121-1124.
79. Robertson TL, Weis JS (2005) A comparison of epifaunal communities associated with the stems of salt marsh grasses Phragmites australis and Spartina alterniflora. Wetlands 25(1): 1-7.
80. Robertson TL, Weis JS (2007) Interactions between the grass shrimp Palaemonetes pugio and the salt marsh grasses Phragmites australis and Spartina alterniflora. Biol Invasions 9: 25-30.
81. Roman CT, Niering WA, Warren RS (1984) Salt marsh vegetation change in response to tidal restriction. Environ Manage 8: 141-150.
82. Roman CT, Raposa KB, Adamowicz SC, James-Pirri MJ, Catena JG (2002) Quantifying vegetation and nekton response to tidal restoration of a New England salt marsh. Restor Ecol 10(3): 450-460.
83. Rooth JE, Court Stevenson J, Cornwell JC (2003) Increased sediment accretion rates following invasion by Phragmites australis: the role of litter. Estuaries 26(2B): 475-483.
84. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0, URL: http://www.R-project.org/.
85. Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. P Natl Acad Sci 99: 2445-2449.
86. Silliman BR, Bertness MD (2004) Shoreline development drives invasion of Phragmites australis and the loss of plant diversity on New England salt marshes. Conserv Biol 18(5): 1424-1434.
87. Stribling JM, Cornwell JC (1997) Identification of important primary producers in a Chesapeake Bay tidal creek system using stable isotopes of carbon and sulfur. Estuaries 20(1): 77-85.
88. Talley TS, Levin LA (2001) Modification of sediments and macrofauna by an invasive marsh plant. Biol Invasions 3: 51-68.
89. Vasquez EA, Glenn EP, Brown JJ, Guntenspergen GR, Nelson SG (2005) Salt tolerance underlies the cryptic invasion of North American salt marshes by an introduced haplotype of the common reed Phragmites australis(Poaceae). Mar Ecol Prog Ser 298: 1-8.
90. Vilà M, Espinar J, Hejda M, Hulme PE, Jarosik V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities, and ecosystems. Ecol Lett 14: 702-708.
91. Wainright SC, Weinstein MP, Able KW, Currin CA (2000) Relative importance of benthic microalgae, phytoplankton, and the detritus of smooth cordgrass Spartina alterniflora and the common reed Phragmites australis to brackish-marsh food webs. Mar Ecol Prog Ser 200: 77-91.
92. Warren RS, Fell PE, Grimsby JL, Buck EL, Rilling GC, Fertik RA (2001) Rates, patterns, and impacts of Phragmites australis expansion and effects of experimental control on vegetation, macroinvertebrates, and fish within tidelands of the Lower Connecticut River. Estuaries 24(1): 90-107.
93. Warren RS, Fell PE, Rozsa R, Brawley AH, Orsted AC, Olson ET, Swamy V, Niering WA (2002) Salt marsh restoration in Connecticut: 20 years of science and management. Restor Ecol 10(3): 497-513.
94. Weinstein MP, Litvin SY, Bosley KL, Fuller CM, Wainright SC (2000) The role of tidal marsh as an energy source for marine transient and resident finishes: a stable isotope approach. T Am Fish Soc 129: 797-810.
95. Weinstein MP, Keough JR, Gutenspergen GR, Litvin SY (2003) Phragmites australis: a sheep in wolf's clothing? Estuaries 26(2B): 397.
96. Weinstein MP, Litvin SY, Guida VG (2009) Essential Fish Habitat and wetland restoration success: a tier III approach to the biochemical condition of common mummichog Fundulus heteroclitus in common reed Phragmites australis and smooth cordgrass Spartina alterniflora-dominated salt marshes. Estuaries Coast 32: 1011-1022.
97. Weis JS (2005) Diet and food web support of the white perch, Morone americana, in the Hackensack Meadowlands of New Jersey. Environ Biol Fishes 74: 109-113.
98. Weis JS, Butler CA (2009) Salt marshes: a natural and unnatural history. Rutgers Univ Press, New Jersey.
99. Weis JS, Weis P (2000) Behavioral responses and interactions of estuarine animals with an invasive marsh plant: a laboratory analysis. Biol Invasions 2: 305-314.
100. Weis JS, Windham L, Santiago-Bass C, Weis P (2002) Growth, survival, and metal content of marsh invertebrates fed diets of detritus from Spartina alterniflora Loisel. and Phragmites australis Cav. Trin. ex Steud. from metal-contaminated and clean sites. Wetl Ecol Manag 10: 71-84.
101. Weisberg SB, Lotrich VA (1982) The importance of an infrequently flooded intertidal marsh surface as an energy source for the mummichog Fundulus heteroclitus: an experimental approach. Mar Biol 66: 307-310.
102. Windham L, Lathrop RG Jr (1999) Effects of Phragmites australis (common reed) invasion on aboveground biomass and soil properties in brackish tidal marsh of the Mullica River, New Jersey. Estuaries 22(4): 927-935.
103. Windham L, Meyerson LA (2003) Effects of common reed (Phragmites australis) expansions on nitrogen dynamics of tidal marshes in the Northeastern U. S. Estuaries 26(2B): 452-464.
104. Woolcott CA (2005) Nekton use of Spartina alterniflora and Phragmites australis in the Hackensack Meadowlands. MS Thesis, Rutgers.
105. Wozniak AS, Roman CT, Wainright SC, McKinney RA, James-Pirri MJ (2006) Monitoring food web changes in tide-restored salt marshes: a carbon stable isotope approach. Estuaries Coast 29(4): 568-578.
106. Yuhas CE, Hartman JM, Weis JS (2005) Benthic communities in Spartina alterniflora-and Phragmites australis-dominated salt marshes in the Hackensack Meadowlands, New Jersey. Urban Habitats 3(1): 158-191.