Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-23T03:01:46.608Z Has data issue: false hasContentIssue false

Invasion by Ammophila arenaria alters soil chemistry, leaving lasting legacy effects on restored coastal dunes in California

Published online by Cambridge University Press:  17 May 2021

Lorraine S. Parsons*
Affiliation:
Vegetation/Wetland Ecologist, Point Reyes National Seashore, National Park Service, Point Reyes Station, CA, USA
Benjamin H. Becker
Affiliation:
Science Adviser/Research Coordinator, Californian Cooperative Ecosystems Studies Unit, National Park Service, University of California Berkeley, Berkeley, CA, USA
*
Author for correspondence: Lorraine Parsons, Point Reyes National Seashore, 1 Bear Valley Road, Point Reyes Station, CA94956. (Email: [email protected])

Abstract

Many restoration projects rely on invasive plant removal to restore ecosystems. However, success of restoration efforts relying on invasive removal can be jeopardized, because in addition to displacing native plants, invasives can also dramatically impact soils. Many studies have documented invasives’ effects on soil chemistry and microbiota. While European beachgrass [Ammophila arenaria (L.) Link] is a worldwide invasive problem in coastal dunes outside northern Europe, little attention has been paid to effects of this species on soil chemistry following invasion, even though it establishes persistent, dense monocultures. In our study, we evaluated effects of A. arenaria invasion on soil chemistry of coastal dunes at Point Reyes National Seashore (PRNS); persistence of effects following removal by mechanical or herbicide treatment (legacy effects); and effects of treatment independent of invasion. Dune restoration efforts at PRNS have met with mixed success, especially in herbicide-treated backdunes, where decomposition of dead A. arenaria has been greatly delayed. Based on results, invasion impacted 74% of 19 variables assessed, although there was a significant interaction in many cases with successional status (earlier vs. later). Almost 60% of invasion effects persisted after restoration, with legacy effects prevalent in herbicide-treated backdunes where sand deposition from adjacent beaches could not mitigate effects as it could in herbicide-treated foredunes. Mechanical removal—or inversion of invaded surface soils with less-contaminated subsoils—resulted in fewer legacy effects, but more treatment effects, primarily in backdunes. Soil chemistry may decelerate decomposition of A. arenaria due to the limited nitrogen (N) available to enable microbial breakdown of the high carbon(C):N (70.8:1) material, but microbial factors probably play a more important role. Success of restoration at PRNS may not be fully realized until legacy effects are resolved through additional actions such as inoculation with healthy microbiomes or necromass reduction through controlled burning.

Type
Research Article
Creative Commons
This is a work of the US Government and is not subject to copyright protection within the United States.
Copyright
© U.S. National Park Service, 2021. Published by Cambridge University Press on behalf of Weed Science Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Associate Editor: Edith Allen, University of California, Riverside

References

Abdel Wahab, AM, Wareing, PF (1980) Nitrogenase activity associated with the rhizosphere of Ammophila arenaria L. and effect of inoculation of seedlings with Azotobacter . New Phytol 84:711721 CrossRefGoogle Scholar
Art, HW, Bormann, FH, Voigt, GK, Woodwell, GM (1974) Barrier Island forest ecosystem: role of meteorologic nutrient inputs. Science 184:6062 CrossRefGoogle ScholarPubMed
Badalamenti, E, Gristino, L, Laudicina, VA, Novara, A, Pasta, S, La Mantia, T (2016) The impact of Carpobrotus cfr. acinaciformis (L.) L. Bolus on soil nutrients, microbial communities structure and native plant communities in Mediterranean ecosystems. Plant Soil 409:1934 CrossRefGoogle Scholar
Barbour, MG (1978) Salt spray as a microenvironmental factor in the distribution of beach plants at Point Reyes, California. Oecologia 32:213224 CrossRefGoogle ScholarPubMed
Barbour, MG, De Jong, TM, Johnson, AF (1976) Synecology of beach vegetation along the Pacific Coast of the United States of America: a first approximation. J Biogeogr 3:5569 CrossRefGoogle Scholar
Barbour, MG, De Jong, TM, Pavlik, BM (1985) Marine beach and dune plant communities. Pages 296–322 in Chabot BF, Mooney HA, eds. Physiological Ecology of North American Plant Communities. Dordrecht, Netherlands, Springer Google Scholar
Bastow, JL, Preisser, EL, Strong, DR (2008) Wood decomposition following a perennial lupine die-off: a 3-year litterbag study. Ecosystems 11:442453 CrossRefGoogle Scholar
Bates, D, Maechler, M, Bolker, B, Walker, S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:148 CrossRefGoogle Scholar
Benjamini, Y, Hochberg, Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B 57:289300 Google Scholar
Brady, NC, Weil, RR (1999) The Nature and Properties of Soils. 12th ed. Englewood Cliffs, NJ: Prentice-Hall. 881 pGoogle Scholar
Buck-Diaz, J, Sikes, K, Evens, JM (2021) Vegetation Classification of Alliances and Associations in Marin County, California. Draft. Sacramento: California Native Plant Society. 73 pGoogle Scholar
Clayton, JL (1972) Salt spray and mineral cycling in two California coastal ecosystems. Ecology 53:7481 CrossRefGoogle Scholar
Conser, C, Connor, EF (2009) Assessing the residual effects of Carpobrotus edulis invasion, implications for restoration. Biol Invasions 11:349358 CrossRefGoogle Scholar
Corbin, JD, D’Antonio, CM (2011) Abundance and productivity mediate invader effects on nitrogen dynamics in a California grassland. Ecosphere 2:ar32:1–20CrossRefGoogle Scholar
Corbin, JD, D’Antonio, CM (2012) Gone but not forgotten? Invasive plants’ legacies on community and ecosystem properties. Invasive Plant Sci Manag 5:117–124CrossRefGoogle Scholar
Dalton, DA, Kramer, S, Azios, N, Fusaro, S, Cahill, E, Kennedy, C (2004) Endophytic nitrogen fixation in dune grasses (Ammophila arenaria and Elymus mollis) from Oregon. FEMS Microbiol Ecol 49:469479 CrossRefGoogle ScholarPubMed
Dangremond, EM, Pardini, EA, Knight, TM (2010) Apparent competition with an invasive plant hastens the extinction of an endangered lupine. Ecology 91:22612271 CrossRefGoogle ScholarPubMed
D’Antonio, CM, Mahall, BE (1991) Root profiles and competition between the invasive, exotic perennial, Carpobrotus edulis, and two native shrub species in California coastal scrub. Am J Bot 78:885894 CrossRefGoogle Scholar
de la Peña, E, de Clercq, N, Bonte, D, Roiloa, S, Rodríguez-Echeverría, S, Freitas, H (2010) Plant-soil feedback as a mechanism of invasion by Carpobrotus edulis . Biol Invasions 12:3637–3648CrossRefGoogle Scholar
Ehrenfeld, JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503523 CrossRefGoogle Scholar
Ehrenfeld, JG (2004) Implications of invasive species for belowground community and nutrient processes. Weed Technol 18:12321235 CrossRefGoogle Scholar
Ehrenfeld, JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol System 41:5980 CrossRefGoogle Scholar
Ehrenfeld, JG, Kourtev, P, Huang, W (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11:12871300 CrossRefGoogle Scholar
Eppinga, MB, Rietkerk, M, Dekker, S, De Ruiter, P, van der Putten, WH (2006) Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions. Oikos 114:168176 CrossRefGoogle Scholar
Espejel, I (1992) Coastal sand dune communities and soil relationships in the Yucatan Peninsula, Mexico. Pages 323–335 in Seeliger U, ed. Coastal Plant Communities of Latin America (Physiological Ecology). San Diego: AcademicCrossRefGoogle Scholar
Etherington, JR (1967) Studies of nutrient cycling and productivity in oligotrophic ecosystems: I. Soil potassium and wind-blown sea-spray in a South Wales dune grassland. J Ecol 55:743752 CrossRefGoogle Scholar
Godoy, O, Castro-Díez, P, Van Logtestijn, RSP, Cornelissen, JHC, Valladares, F (2010) Leaf litter traits of invasive species slow down decomposition compared to Spanish natives: a broad phylogenetic comparison. Oecologia 162:781790 CrossRefGoogle ScholarPubMed
Goodman, J (1982) Water Potential from Advected Fog. San Jose, CA: Department of Meteorology, San Jose State University Progress Report 1. 45 pGoogle Scholar
Gornish, ES, Franklin, K, Rowe, J, Barberán (2020) Buffelgrass invasion and glyphosate effects on desert soil microbiome communities. Biol Invasions 22:25872597 CrossRefGoogle Scholar
Hesp, PA (1991) Ecological processes and plant adaptations on coastal dunes. J Arid Environ 21:165191 CrossRefGoogle Scholar
Hetherington, JK, Wilson, JB (2019) Short-term soil nutrient and plant community responses to the eradication of a nitrogen fixing tree, Lupinus arboreus . J Coastal Conserv 23:49–58CrossRefGoogle Scholar
Holton, B, Barbour, MG, Martens, SN (1991) Some aspects of the nitrogen cycle in a Californian strand ecosystem. Madroño 38:170184 Google Scholar
Holton, B, Johnson, AF (1979) Dune scrub communities and their correlation with environmental factors at Point Reyes National Seashore, California. J Biogeogr 6:317328 CrossRefGoogle Scholar
Inderjit, , Seastedt, TR, Callaway, RM, Pollock, JL, Kaur, J (2008) Allelopathy and plant invasions: traditional, congeneric, and bio-geographical approaches. Biol Invasions 10:875890 10.1007/s10530-008-9239-9CrossRefGoogle Scholar
Inderjit, van der Putten WH (2010) Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol 25:512519 CrossRefGoogle ScholarPubMed
Ingraham, NL, Matthews, RA (1995) The importance of fog-drip water to vegetation: Point Reyes Peninsula, California. J Hydrol 164:269285 CrossRefGoogle Scholar
Jacob, DJ, Waldman, TJM, Monger, JW, Hoffmann, MR (1985) Chemical composition of fogwater collected along the California coast. Environ Sci Technol 19:730736 CrossRefGoogle ScholarPubMed
Jo, I, Fridley, JD, Frank, DA (2016) More of the same? In situ leaf and root decomposition rates do not vary between 80 native and nonnative deciduous forest species. New Phytol 209:115122 CrossRefGoogle Scholar
Jones, MLM, Sowerby, A, Williams, DL, Jones, RE (2008) Factors controlling soil development in sand dunes: evidence from a coastal dune soil chronosequence. Plant Soil 307:219234 CrossRefGoogle Scholar
Kardol, P, Wardle, DA (2010) How understanding aboveground–belowground linkages can assist restoration ecology. Trends Ecol Evol 25:670679 CrossRefGoogle ScholarPubMed
Konlechner, TM, Lord, JM (2015) Plant community response following the removal of the invasive Lupinus arboreus in a coastal dune system: community response following L. arboreus removal. Restor Ecol 23:607614 CrossRefGoogle Scholar
Kooijman, A, Morriën, E, Jagers op Akkerhuis G, Missong A, Bol R, Klumpp E, van Hall R, van Til M, Kalbitz K, Bloem J (2020) Resilience in coastal dune grasslands: pH and soil organic matter effects on P nutrition, plant strategies, and soil communities. Ecosphere 11:e03112 CrossRefGoogle Scholar
Koske, RE, Polson, WR (1984) Are VA mycorrhizae required for sand dune stabilization? BioScience 34:420424 CrossRefGoogle Scholar
Kueffer, C, Klingler, G, Zirfass, K, Schumacher, E, Edwards, PJ, Güsewell, S (2008) Invasive trees show only weak potential to impact nutrient dynamics in phosphorus-poor tropical forests in the Seychelles. Funct Ecol 22:359366 CrossRefGoogle Scholar
Lebassi, B, González, J, Fabris, D, Maurer, E, Miller, N, Milesi, C, Switzer, P, Bornstein, R (2009) Observed 1970–2005 cooling of summer daytime temperatures in coastal California. J Climate 22(13), 10.1175/2008JCLI2111.1 CrossRefGoogle Scholar
Lekberg, Y, Gibbons, SM, Rosendahl, S, Ramsey, PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. ISME J 7:14241433 CrossRefGoogle ScholarPubMed
Liao, C, Peng, R, Luo, Y, Zhou, X, Wu, X, Fang, C, Chen, J, Li, B (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706714 CrossRefGoogle ScholarPubMed
Mack, MC, D’Antonio, CM, Ley, RE (2001) Alteration of ecosystem nitrogen dynamics by exotic plants: a case study of C4 grasses in Hawaii. Ecol Appl 11:13231335 Google Scholar
Maloney, E, Camargo, SJ, Chang, E, Colle, B, Fu, R, Geil, KL, Hu, Q, Jiang, X, Johnson, N, Karnauskas, KB, Kinter, J, Kirtman, B, Kumar, S, Langenbrunner, B, Lombardo, K, et al. (2014) North American climate in CMIP5 experiments: Part III: assessment of twenty-first-century projections. J Climate 27:22302270 CrossRefGoogle Scholar
Maron, JL, Connors, PG (1996) A native nitrogen-fixing shrub facilitates weed invasion. Oecologia 105:302312 CrossRefGoogle ScholarPubMed
Maron, JL, Jefferies, RL (1999) Bush lupine mortality, altered resource availability, and alternative vegetation states. Ecology 80:443454 CrossRefGoogle Scholar
Maron, JL, Jefferies, RL (2001) Restoring enriched grasslands: effects of mowing on species richness, productivity, and nitrogen retention. Ecol Appl 11:10881100 CrossRefGoogle Scholar
Muir, JJ, Colwell, MA (2010) Snowy plovers select open habitats for courtship scrapes and nests. The Condor 112:507510 CrossRefGoogle Scholar
[NPS] National Park Service (2009) Abbotts Lagoon Area Dune Restoration Plan Environmental Assessment. Point Reyes Station, CA: Point Reyes National Seashore, National Park Service. 198 pGoogle Scholar
Niu, H, Liu, W, Wan, F, Liu, B (2007) An invasive aster (Ageratina adenophora) invades and dominates forest understories in China: altered soil microbial communities facilitate the invader and inhibit natives. Plant Soil 294:7385 CrossRefGoogle Scholar
Novoa, A, González, L (2014) Impacts of Carpobrotus edulis (L.) N.E.Br. on the germination, establishment and survival of native plants: a clue for assessing its competitive strength. PLoS ONE 9(9):e107557 CrossRefGoogle ScholarPubMed
Novoa, A, González, L, Moravcová, L, Pyšek, P (2012) Effects of soil characteristics, allelopathy and frugivory on establishment of the invasive plant Carpobrotus edulis and a co-occurring native, Malcolmia littorea . PLoS ONE 7(12):e53166 CrossRefGoogle Scholar
Novoa, A, González, L, Moravcová, L, Pyšek, P (2013) Constraints to native plant species establishment in coastal dune communities invaded by Carpobrotus edulis: implications for restoration. Biol Conserv 164:19 CrossRefGoogle Scholar
Novoa, A, Rodríguez, R, Richardson, D, González, L (2014) Soil quality: a key factor in understanding plant invasion? The case of Carpobrotus edulis (L.) N.E.Br. Biol Invasions 16:429443 CrossRefGoogle Scholar
O’Brien, TA (2011) The Recent Past and Possible Future Decline of California Coastal Fog. Ph.D thesis. Santa Cruz: University of California, Santa Cruz. 193 pGoogle Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O’Hara, RB, Simpson, GB, Solymos, P, Henry, M, Stevens, H, Szoecs, E, Wagner, H (2019) Vegan: Community Ecology Package. R Package v. 2.5-6. https://CRAN.R-project.org/package=vegan. Accessed: January 16, 2020Google Scholar
Parsons, L, Ender, C, Ryan, A (2020a) Coastal Dune Restoration Vegetation Monitoring Report. Point Reyes Station, CA: Point Reyes National Seashore, National Park Service. 128 pGoogle Scholar
Parsons, L, Sayre, J, Ender, C, Rodrigues, JLM, Barberán, A (2020b) Soil microbial communities in restored and unrestored coastal dune ecosystems in California. Restor Ecol 28(S4):S311S321 CrossRefGoogle Scholar
Pearson, DE, Ortega, YK, Runyon, JB, Butler, JL (2016) Secondary invasion: the bane of weed management. Biol Conserv 197:817 CrossRefGoogle Scholar
Peterson, RA (2019) Ordered quantile normalization: a semiparametric transformation built for the cross-validation era. J Appl Stat 47:23122327 CrossRefGoogle Scholar
Pickart, AJ, Sawyer, JO (1998) Ecology and Restoration of Northern California Coastal Dunes. Sacramento: California Native Plant Society. 152 pGoogle Scholar
Polade, SD, Gershunov, A, Cayan, DR, Dettinger, MD, Pierce, DW (2017) Precipitation in a warming world: assessing projected hydro-climate changes in California and other Mediterranean climate regions. Sci Rep 7:10783 CrossRefGoogle Scholar
Pozo Buil, M, Jacox, MG, Fiechter, J, Alexander, MA, Bograd, SJ, Curchitser, EN, Edwards, CA, Rykaczewski, RR, Stock, CA (2021) A dynamically downscaled ensemble of future projections for the California Current System. Front Mar Sci 8:612874 CrossRefGoogle Scholar
Prescott, CE, Zukswert, JM (2016) Invasive plant species and litter decomposition: time to challenge assumptions. New Phytol 209:57 CrossRefGoogle ScholarPubMed
Pringle, A, Rillig, MC, Gardes, M, Klironomos, J (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699715 CrossRefGoogle Scholar
R Core Team (2020) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org Google Scholar
Randall, RE (1973) Calcium carbonate in dune soils: evidence for geomorphic change. Area 5:308310 Google Scholar
Reinhart, KO, Callaway, RM (2006) Soil biota and invasive plants. New Phytol 170:445457 CrossRefGoogle ScholarPubMed
Rose, SL (1988) Above and belowground community development in sand dunes. Plant Soil 109:215226 CrossRefGoogle Scholar
Ruppel, S (1989) Isolation and characterization of dinitrogen-fixing bacteria from the rhizosphere of Triticum aestivum and Ammophila arenaria. Dev Soil Sci 18:253262 Google Scholar
Santoro, R, Jucker, T, Carboni, M, Acosta, ATR (2012) Patterns of plant community assembly in invaded and non-invaded communities along a natural environmental gradient. J Veg Sci 23:483494 CrossRefGoogle Scholar
Santoro, R, Jucker, T, Carranza, ML, Acosta, ATR (2011) Assessing the effects of Carpobrotus invasion on coastal dune soils. Does the nature of the invaded habitat matter? Commun Ecol 12:234240 CrossRefGoogle Scholar
Smith, SM, Allen, RB, Daly, BK (1985) Soil-vegetation relationships on a sequence of sand dunes, Tautuku Beach, South-East Otago, New Zealand. J R Soc NZ 15:295312 CrossRefGoogle Scholar
Snyder, MA, Sloan, LC, Diffenbaugh, NS, Bell, JL (2003) Future climate change and upwelling in the California Current. Geophys Res Lett 30:1823 CrossRefGoogle Scholar
Soil Conservation Service (1985) Soil Survey of Marin County California. Washington, DC: Soil Conservation Service, U.S. Department of Agriculture. 229 pGoogle Scholar
Stinson, KA, Campbell, SA, Powell, JR, Wolfe, BE, Callaway, RM, Thelen, GC, Hallett, SG, Prati, D, Klironomos, JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4(5):e140 CrossRefGoogle ScholarPubMed
Suding, KN, Gross, KL, Houseman, GR (2004) Alternative states and positive feedbacks in restoration ecology. Trends Ecol Evol 19:4653 CrossRefGoogle ScholarPubMed
Sydeman, WJ, García-Reyes, M, Schoeman, DS, Rykaczewski, RR, Thompson, SA, Black, BA, Bograd, S (2014) Climate change and wind intensification in coastal upwelling ecosystems. Science 345:7780 CrossRefGoogle ScholarPubMed
van der Putten, WH, Yeates, GW, Duyts, H, Schreck Reis, C, Karssen, G (2005) Invasive plants and their escape from root herbivory: a worldwide comparison of the root feeding nematode communities of the dune grass Ammophila arenaria in natural and introduced ranges. Biol Invasions 7:733746 CrossRefGoogle Scholar
van der Valk, AG (1974) Mineral cycling in coastal foredune plant communities in Cape Hatteras National Seashore. Ecology 55:13491358 CrossRefGoogle Scholar
van der Watt, E, Pretorius, JC (2001) Purification and identification of active antibacterial components in Carpobrotus edulis L. J Ethnopharmacol 76:8791 CrossRefGoogle ScholarPubMed
Vilà, M, Tessier, M, Suehs, CM, Brundu, G, Carta, L, Galanidis, A, Lambdon, P, Manca, M, Médail, F, Moragues, E, Traveset, A, Troumbis, AY, Hulme, PE (2006) Local and regional assessments of the impacts of plant invaders on vegetation structure and soil properties of Mediterranean islands. J Biogeogr 33:853861 CrossRefGoogle Scholar
Vivrette, NJ, Muller, CH (1977) Mechanism of invasion and dominance of coastal grassland by Mesembryanthemum crystallinum . Ecol Monogr 47:301318 CrossRefGoogle Scholar
Weber, E (2003) Invasive Plant Species of the World: A Reference Guide to Environmental Weeds. Wallingford, UK: CAB International Publishing. 548 p Google Scholar
[WRCC] Western Regional Climate Center (2020) Climate Data from Point Reyes RCA CA Weather Station. https://wrcc.dri.edu/cgi-bin/rawMAIN.pl?nvprca. Accessed: December 15, 2020Google Scholar
Willis, JE, Yemm, EW (1961) Braunton Burrows: mineral nutrient status of the dune soils. J Ecol 49:377390 CrossRefGoogle Scholar
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 21:179188 CrossRefGoogle Scholar
Wolfe, BE, Klironomos, JN (2005) Breaking new ground: soil communities and exotic plant invasion. BioScience 55:477487 CrossRefGoogle Scholar
Woodhouse, WW, Hanes, RE (1967) Dune Stabilization with Vegetation on the Outer Banks of North Carolina. Washington, DC: U.S. Army Coastal Engineering Research Center Tech Memo No. 22. 53 pCrossRefGoogle Scholar
Xiong, S, Nilsson, C (1999) The effects of plant litter on vegetation: a meta-analysis. J Ecol 87:984994 CrossRefGoogle Scholar
Yelenik, SG, D’Antonio, CM (2013) Self-reinforcing impacts of plant invasions change over time. Nature 503:517521.CrossRefGoogle ScholarPubMed
Yelenik, SG, Levine, JM (2010) Processes limiting native shrub recovery in exotic grasslands after nonnative herbivore removal. Restor Ecol 18:418425 CrossRefGoogle Scholar
Supplementary material: File

Parsons and Becker supplementary material

Parsons and Becker supplementary material

Download Parsons and Becker supplementary material(File)
File 21.9 KB