Biogeographic gradients in ecosystem processes of the invasive ecosystem engineer Phragmites australis

Abstract

Latitudinal gradients in ecosystem patterns arise from complex interactions between biotic and abiotic forces operating at a range of spatial and temporal scales. Widespread invasive species, particularly invasive ecosystem engineers with large effects on their environment, may alter these gradients. We sampled 3–5 stands of the invasive common reed, Phragmites australis, in eight coastal wetlands ranging from Massachusetts (42°N) to South Carolina (32°N) to document geographic variation in P. australis primary production, associated plant and animal species diversity, and sediment carbon storage and to examine how local-, regional-, and large-scale environmental factors contribute to these patterns. Latitude best explained variation in P. australis density, but contrary to expectations, density increased with increasing latitude across our sites. Latitude also predicted macroinvertebrate species richness, which increased with latitude in a manner similar to P. australis density. In addition to latitude, P. australis leaf carbon:nitrogen ratios, distance to the open coast, and sediment oxygen levels were most important for explaining variation in P. australis production, as well as community (plant or animal species richness) and ecosystem (carbon storage) variables. The percent of developed land was positively associated with P. australis density, yet this variable had relatively low predictive power in our study. Our study provides an important biogeographic perspective for documenting and understanding variation in invasive P. australis that is fundamental both for managing the invasion and for understanding latitudinal gradients in ecosystem structure and function.

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References

  1. Berke SK, Jablonski D, Krug AZ, Valentine JW (2014) Origination and immigration drive latitudinal gradients in marine functional diversity. PLoS ONE 9:e101494

    Article  PubMed  PubMed Central  Google Scholar 

  2. Bertness MD, Ewanchuk PJ, Silliman BR (2002) Anthropogenic modification of New England salt marsh landscapes. Proc Natl Acad Sci USA 99:1395–1398

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Breiman L (2001) Random forests. Mach Learn 45:5–32

    Article  Google Scholar 

  4. Breiman L, Friedman J, Stone CJ, Olshen RA (1984) Classification and regression trees. Chapman and Hall, London

    Google Scholar 

  5. Caplan JS, Wheaton CN, Mozdzer TJ (2014) Belowground advantages in construction costs facilitate a cryptic plant invasion. AoB Plants 6:plu020

    Article  PubMed  PubMed Central  Google Scholar 

  6. Christian JM, Wilson SD (1999) Long-term ecosystem impacts of an introduced grass in the northern Great Plains. Ecology 80:2397–2407

    Article  Google Scholar 

  7. Crain CM, Silliman BR, Bertness SL, Bertness MD (2004) Physical and biotic drivers of plant distribution across estuarine salinity gradients. Ecology 85:2539–2549

    Article  Google Scholar 

  8. Cronin JT, Bhattarai GP, Allen WJ, Meyerson LA (2015) Biogeography of a plant invasion: plant-herbivore interactions. Ecology 96:1115–1127

    Article  PubMed  Google Scholar 

  9. Cutler DR, Edwards TC, Beard KH, Cutler A, Hess KT, Gibson J, Lawler JJ (2007) Random forests for classification in ecology. Ecology 88:2783–2792

    Article  PubMed  Google Scholar 

  10. Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carre G, Garcia Marquez JR, Gruber B, Lafourcade B, Leitao PJ, Munkemuller T, McClean C, Osborne PE, Reineking B, Schroder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46

    Article  Google Scholar 

  11. Fenberg PB, Menge BA, Raimondi PT, Rivadeneira MM (2015) Biogeographic structure of the northeastern Pacific rocky intertidal: the role of upwelling and dispersal to drive patterns. Ecography 38:83–95

    Article  Google Scholar 

  12. Finke DL, Denno RF (2006) Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades. Oecologia 149:265–275

    Article  PubMed  Google Scholar 

  13. Gilchrist GW, Huey RB, Balanya J, Pascual M, Serra L (2004) A time series of evolution in action: a latitudinal cline in wing size in South American Drosophila subobscura. Evolution 58:768–780

    Article  PubMed  Google Scholar 

  14. Gotelli NJ, Graves GR, Rahbek C (2010) Macroecological signals of species interactions in the Danish avifauna. Proc Natl Acad Sci 107:5030–5035

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Gouhier TC, Guichard F, Menge BA (2010) Ecological processes can synchronize marine population dynamics over continental scales. Proc Natl Acad Sci 107:8281–8286

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. 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, Grosholz ED, Bertness MD (eds) Human impacts on salt marshes: a global perspective. University of California Press, Berkeley

    Google Scholar 

  17. Guo W-Y, Lambertini C, Li X-Z, Meyerson LA, Brix H (2013) Invasion of Old World Phragmites australis in the New World: precipitation and temperature patterns combined with human influences redesign the invasive niche. Glob Change Biol 19:3406–3422

    Google Scholar 

  18. Hillebrand H (2004) On the generality of the latitudinal diversity gradient. Am Nat 163:192–211

    Article  PubMed  Google Scholar 

  19. Holdredge C, Bertness MD, Von Wettberg E, Silliman BR (2011) Nutrient enrichment enhances hidden differences in phenotype to drive a cryptic plant invasion. Oikos 119:1776–1784

    Article  Google Scholar 

  20. Homer CG et al (2015) National Land Cover Database for the conterminous United States—representing a decade of land cover change information. Photogramm Eng Remote Sens 81:345–354

    Google Scholar 

  21. Howard J, Hoyt S, Isensee K, Telszewski M, Pidgeon E (eds) (2014) Coastal blue carbon: methods for assessing carbon stocks and emissions factors in mangroves, tidal salt marshes, and seagrasses. Conservation International, Intergovernmental Oceanographic Commission of UNESCO, International Union for Conservation of Nature. Arlington, VA

  22. Jones CG, Lawton JH, Shachak M (1996) Organisms as ecosystem engineers. In: Samson FB, Knopf FL (eds) Ecosystem management. Springer, New York, pp 130–147

    Google Scholar 

  23. Kettenring KM, McCormick MK, Baron HM, Whigham DF (2011) Mechanisms of Phragmites australis invasion: feedbacks among genetic diversity, nutrients, and sexual reproduction. J Appl Ecol 48:1305–1313

    Article  Google Scholar 

  24. King RS, Deluca WV, Whigham DF, Marra PP (2007) Threshold effects of coastal urbanization on Phragmites australis (common reed) abundance and foliar nitrogen in Chesapeake Bay. Estuaries Coasts 30:469–481

    CAS  Article  Google Scholar 

  25. Kirwan ML, Guntenspergen GR, Morris JT (2009) Latitudinal trends in Spartina alterniflora productivity and the response of coastal marshes to global change. Glob Change Biol 15:1982–1989

    Article  Google Scholar 

  26. Kirwan ML, Guntenspergen GR, Langley JA (2014) Temperature sensitivity of organic-matter decay in tidal marshes. Biogeosciences 11:4801–4808

    Article  Google Scholar 

  27. Kleinhesselink AR, Magnoli SM, Cushman JH (2014) Shrubs as ecosystem engineers across an environmental gradient: effects on species richness and exotic plant invasion. Oecologia 175:1277–1290

    Article  PubMed  Google Scholar 

  28. Lambertini C, Gustafsson MHG, Frydenberg J, Lissner J, Speranza M, Brix H (2006) A phylogeographic study of the cosmpolitan genus Phragmites (Poaceae) based on AFLPs. Plant Syst Evol 258:161–182

    Article  Google Scholar 

  29. Lambertini C, Mendelssohn IA, Gustafsson MHG, Olesen B, Riis T, Sorrell BK, Brix H (2012) Tracing the origin of the Gulf Coast Phragmites (Poaceae): a story of long-distance dispersal and hybridization. Am J Bot 99:538–551

    CAS  Article  PubMed  Google Scholar 

  30. Lavergne S, Molofsky J (2010) Reed Canary Grass (Phalaris arundinacea) as a biological model in the study of plant invasions. Crit Rev Plant Sci 23:415–429

    Article  Google Scholar 

  31. Liao CZ, Luo YQ, Fang CM, Chen JK, Li B (2008) Litter pool sizes, decomposition, and nitrogen dynamics in Spartina alterniflora-invaded and native coastal marshlands of the Yangtze Estuary. Oecologia 156:589–600

    Article  PubMed  Google Scholar 

  32. McCormick MK, Kettenring KM, Baron HM, Whigham DF (2010) Spread of invasive Phragmites australis in estuaries with differing degrees of development: genetic patterns Allee effects, and interpretation. J Ecol 98:1369–1378

    Article  Google Scholar 

  33. McGill B (2010) Matters of scale. Science 328:575–576

    CAS  Article  PubMed  Google Scholar 

  34. Meyerson LA (2000) Ecosystem-level effects of invasive species: a Phragmites case study in two freshwater tidal marsh ecosystems on the Connecticut River. Ph.D. Thesis, Yale University

  35. Meyerson LA, Cronin JT (2013) Evidence for multiple introductions of Phragmites australis to North America: detection of a new non-native haplotype. Biol Invasions 15:2605–2608

    Article  Google Scholar 

  36. Meyerson LA, Saltonstall K, Chambers RM, Silliman BR, Bertness MD, Strong D (2009) Phragmites australis in Eastern North America: a historical and ecological perspective. In: Silliman BR, Grosholz ED, Bertness MD (eds) Human impacts on salt marshes: a global perspective. University of California Press, Berkeley

    Google Scholar 

  37. Middelburg JJ, Klaver G, Nieuwenhuize J, Wielemaker A, de Haas W, Vlug T, van der Nat JFWA (1996) Organic matter mineralization in intertidal sediments along an estuarine gradient. Mar Ecol Prog Ser 132:157–168

    CAS  Article  Google Scholar 

  38. Minchinton TE, Bertness MD (2003) Disturbance-mediated competition and the spread of Phragmites australis in a coastal marsh. Ecol Appl 13:1400–1416

    Article  Google Scholar 

  39. Minchinton TE, Simpson JC, Bertness MD (2006) Mechanisms of exclusion of native coastal marsh plants by an invasive grass. J Ecol 94:342–354

    Article  Google Scholar 

  40. Mozdzer TJ, Megonigal JP (2012) Jack-and-Master trait responses to elevated CO2 and N: a comparison of native and introduced Phragmites australis. PLoS ONE 7:e42794

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Mozdzer TJ, Megonigal JP (2013) Increased methane emissions by an introduced Phragmites australis lineage under global change. Wetlands 33:609–615

    Article  Google Scholar 

  42. Mozdzer TJ, Zieman JC (2010) Ecophysiological differences between genetic lineages facilitate the invasion of non-native Phragmites australis in North American Atlantic coast wetlands. J Ecol 98:451–458

    Article  Google Scholar 

  43. Mozdzer TJ, Zieman JC, McGlathery KJ (2010) Nitrogen uptake by native and invasive temperate coastal macrophytes: importance of dissolved organic nitrogen. Estuaries Coasts 33:784–797

    CAS  Article  Google Scholar 

  44. Mozdzer TJ, McGlathery KJ, Mills AL, Zieman JC (2014) Latitudinal variation in the availability and use of dissolved organic nitrogen in Atlantic coast salt marshes. Ecology 95:3293–3303

    Article  Google Scholar 

  45. 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

    Article  PubMed  Google Scholar 

  46. Neubauer SC, Miller WD, Anderson IC (2000) Carbon cycling in a tidal freshwater marsh ecosystem: a carbon gas flux study. Mar Ecol Prog Ser 199:13–30

    CAS  Article  Google Scholar 

  47. Pennings SC, Bertness MD (2001) Salt marsh communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland

    Google Scholar 

  48. Pennings SC, Silliman BR (2005) Linking biogeography and community ecology: latitudinal variation in plant-herbivore interaction strength. Ecology 86:2310–2319

    Article  Google Scholar 

  49. Pennings SC, Ho C-K, Salgado CS, Wieski K, Dave N, Kunza AE, Wason EL (2009) Latitudinal variation in herbivore pressure in Atlantic Coast salt marshes. Ecology 90:183–195

    Article  PubMed  Google Scholar 

  50. Prasad AM, Iverson LR, Liaw A (2006) Newer classification and regression tree techniques: bagging and random forests for ecological prediction. Ecosystems 9:181–199

    Article  Google Scholar 

  51. R Development Core Team (2015) R: a language and environment for statistical computing. Vienna, Austria

  52. Rohde K (1992) Latitudinal gradients in species diversity: the search for the primary cause. Oikos 65:514–527

    Article  Google Scholar 

  53. Romero GQ, Goncalves-Souza T, Vieira C, Koricheva J (2014) Ecosystem engineering effects on species diversity across ecosystems: a meta-analysis. Biol Rev. doi:10.1111/brv.12138

    PubMed  Google Scholar 

  54. Rooth JE, Stevenson JC, Cornwell JC (2003) Increased sediment accretion rates following invasion by Phragmites australis: the role of litter. Estuaries 26:475–483

    Article  Google Scholar 

  55. Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis into North America. Proc Natl Acad Sci USA 99:2445–2449

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  56. Saltonstall K (2003) Microsatellite variation within and among North American lineages of Phragmites australis. Mol Ecol 12:1689–1702

    CAS  Article  PubMed  Google Scholar 

  57. Sax DF, Stachowicz JJ, Gaines SD (eds) (2005) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Associates, Sunderland

    Google Scholar 

  58. Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K (2009) Is there a latitudinal gradient in the importance of biotic interactions? Annu Rev Ecol Evol Syst 40:245–269

    Article  Google Scholar 

  59. Silliman BR, Bertness MD (2004) Shoreline development drives invasion of Phragmites australis and the loss of plant diversity in New England salt marshes. Conserv Biol 18:1424–1434

    Article  Google Scholar 

  60. Simley J, Doumbouya A (2012) National hydrography dataset—linear referencing. US Geological Survey Fact Sheet 3068

  61. Strayer DL, Beighley RE, Thomopson LC, Brooks S, Nilsson C, Pinay G, Naiman RJ (2003) Effects of land cover on stream ecosystems: roles of empirical models and scaling isues. Ecosystems 6:407–423

    Article  Google Scholar 

  62. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845

    CAS  Article  PubMed  Google Scholar 

  63. Turner RE (1976) Geographic variations in salt marsh marcrophyte production: a review. Contrib Mar Sci 20:47–68

    Google Scholar 

  64. Vitousek PM, Walker LR (1989) Biological invasion by Myrica faya in Hawaii: plant demography, nitrogen fixation, ecosystem effects. Ecol Monogr 59:247–265

    Article  Google Scholar 

  65. 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 Phragmites control on vegetation, macroinvertebrates, and fish within tidelands of the lower Connecticut River. Estuaries 24:90–107

    Article  Google Scholar 

  66. Willig MR, Kaufman DM, Stevens RD (2003) Latitudinal gradients of biodiversity: pattern, process, scale and synthesis. Annu Rev Ecol Evol Syst 34:273–309

    Article  Google Scholar 

  67. Windham L (2001) Comparison of biomass production and decomposition between Phragmites australis (Common Reed) and Spartina patens (Salt Hay Grass) in brackish tidal marshes of New Jersey, USA. Wetlands 21:179–188

    Article  Google Scholar 

  68. Windham L, Ehrenfeld JG (2003) Net impact of a plant invasion on nitrogen-cycling processes within a brackish tidal marsh. Ecol Appl 13:883–896

    Article  Google Scholar 

  69. 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 22:927–935

    Article  Google Scholar 

  70. Wright JP, Jones CG (2004) Predicting effects of ecosystem engineers on patch-scale species richness from primary productivity. Ecology 85:2071–2081

    Article  Google Scholar 

  71. Zhang D, Hui D, Luo Y, Zhou G (2008) Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. J Plant Ecol 1:85–93

    Article  Google Scholar 

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Acknowledgments

This study would not have been possible without the support of reserve managers and research coordinators at each of our sites, including A. Giblin, K. Raposa, M. Kennish, M. De Luca, K. Cole, L. Hice-Dunton, J. Allen, J. Raulin, S. Lerberg, K. Moore, R. Ellin, H. Wells, P. Maier, J. Leffler, D. Hurley, and B. Sullivan. E. Grape, A. Halverstadt, E. Podbielski, D. von Staats, A. Thau, and A. Weiss assisted with sample processing in the lab. M. Piehler provided helpful feedback on the study. We thank L. Meyerson and 3 anonymous reviewers for constructive comments on the manuscript. This project was funded by a Northeastern University Tier1 grant to E. Beighley, D. Kimbro, and R. Hughes. This is contribution 333 from the Northeastern University Marine Science Center.

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Correspondence to A. Randall Hughes.

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Guest editors: Laura A. Meyerson and Kristin Saltonstall/Phragmites invasion.

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Hughes, A.R., Schenck, F.R., Bloomberg, J. et al. Biogeographic gradients in ecosystem processes of the invasive ecosystem engineer Phragmites australis . Biol Invasions 18, 2577–2595 (2016). https://doi.org/10.1007/s10530-016-1143-0

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Keywords

  • Blue carbon
  • Foundation species
  • Latitudinal gradients
  • Primary production
  • Salt marsh
  • Species diversity