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Herbivory affects salt marsh succession dynamics by suppressing the recovery of dominant species

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Abstract

Disturbance can generate heterogeneous environments and profoundly influence plant diversity by creating patches at different successional stages. Herbivores, in turn, can govern plant succession dynamics by determining the rate of species replacement, ultimately affecting plant community structure. In a south-western Atlantic salt marsh, we experimentally evaluated the role of herbivory in the recovery following disturbance of the plant community and assessed whether herbivory affects the relative importance of sexual and clonal reproduction on these dynamics. Our results show that herbivory strongly affects salt marsh secondary succession by suppressing seedlings and limiting clonal colonization of the dominant marsh grass, allowing subordinate species to dominate disturbed patches. These results demonstrate that herbivores can have an important role in salt marsh community structure and function, and can be a key force during succession dynamics.

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References

  • Abrahamson WG (1980) Demography and vegetative reproduction. In: Solbrig OT (ed) Demography and evolution of plant populations. Blackwell, Oxford, pp 89–106

    Google Scholar 

  • Adam P (1993) Saltmarsh ecology. Cambridge University Press, Cambridge

    Google Scholar 

  • Alberti J, Montemayor D, Álvarez F, Méndez Casariego A, Luppi T, Canepuccia A, Isacch JP, Iribarne O (2007) Changes in rainfall pattern affect crab herbivory rates in a SW Atlantic salt marsh. J Exp Mar Biol Ecol 353:126–133

    Article  Google Scholar 

  • Alberti J, Escapa M, Iribarne O, Silliman B, Bertness M (2008) Crab herbivory regulates plant facilitative and competitive processes in Argentinean marshes. Ecology 89:155–164

    Article  PubMed  Google Scholar 

  • Alberti J, Escapa M, Daleo P, Mendez Casariego A, Iribarne O (2010a) Crab bioturbation and herbivory reduce pre- and post-germination success of Sarcocornia perennis in bare patches of SW Atlantic salt marshes. Mar Ecol Prog Ser 400:55–61

    Article  Google Scholar 

  • Alberti J, Mendez Casariego A, Daleo P, Fanjul E, Silliman BR, Bertness M, Iribarne O (2010b) Abiotic stress mediates top-down and bottom-up control in a Southwestern Atlantic saltmarsh. Oecologia 163:181–191

    Article  PubMed  Google Scholar 

  • Alberti J, Canepuccia A, Pascual J, Pérez C, Iribarne O (2011) Joint control of rodent herbivory and nutrient availability on plant diversity in a salt marsh-salty steppe transition zone. Veg Sci 22:216–224

    Article  Google Scholar 

  • Al-Mufti MM, Sydes CL, Furness SB, Grime JP, Band SR (1977) A quantitative analysis of shoot phenology and dominance in herbaceous vegetation. J Ecol 65:759–791

    Article  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: Guide to software and statistical methods. PRIMER-E, Plymouth

    Google Scholar 

  • Angelini C, Silliman BR (2012) Patch size-dependent community recovery after massive disturbance. Ecology 93:101–110

    Article  PubMed  Google Scholar 

  • Bazzaz FA (1979) The physiological ecology of plant succession. Annu Rev Ecol Syst 10:351–371

    Article  Google Scholar 

  • Berendse F (1998) Effects of dominant plant species on soils during succession in nutrient-poor ecosystems. Biogeochemistry 42:73–88

    Article  Google Scholar 

  • Bertness MD (1991) Interespecific interactions among high marsh perennials in a New England salt marsh. Ecology 72:125–137

    Article  Google Scholar 

  • Bertness MD (1999) The ecology of Atlantic shorelines. Sinauer, Sunderland

    Google Scholar 

  • Bertness MD, Ellison AM (1987) Determinants of pattern in a New England salt marsh plant community. Ecol Monogr 57:129–147

    Article  Google Scholar 

  • Bertness MD, Leonard GH (1997) The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78:1976–1989

    Article  Google Scholar 

  • Bertness MD, Shumway SW (1993) Competition and facilitation in marsh plants. Am Nat 142:718–724

    Article  CAS  PubMed  Google Scholar 

  • Bertness MD, Wise C, Ellison AM (1987) Consumer pressure and seed set in a salt marsh perennial plant community. Oecologia 71:190–200

    Article  Google Scholar 

  • Bertness MD, Trussell GC, Ewanchuk PJ, Silliman BR (2002) Do alternate stable community states exist in the Gulf of Maine rocky intertidal zone? Ecology 83:3434–3448

    Article  Google Scholar 

  • Bortolus A, Iribarne OO (1999) The effect of the southwestern Atlantic burrowing crab Chasmagnathus granulata on a Spartina salt-marsh. Mar Ecol Prog Ser 178:79–88

    Article  Google Scholar 

  • Bortolus A, Laterra P, Iribarne O (2004) Crab-mediated phenotypic changes in Spartina densiflora Brong. Estuar Coast Shelf Sci 59:97–107

    Article  Google Scholar 

  • Brewer JS, Bertness MD (1996) Disturbance and intraspecific variation in the clonal morphology of salt marsh perennials. Oikos 77:107–116

    Article  Google Scholar 

  • Brewer JS, Levine JM, Bertness MD (1998) Interactive effects of elevation and burial with wrack on plant community structure in some Rhode Island salt marshes. J Ecol 86:125–136

    Article  Google Scholar 

  • Bromberg Gedan K, Crain CM, Bertness MD (2009) Small-mammal herbivore control of secondary succession in New England tidal marshes. Ecology 90:430–440

    Article  Google Scholar 

  • Buschmann H, Keller M, Porret N, Dietz H, Edwards PJ (2005) The effect of slug grazing on vegetation development and plant species diversity in an experimental grassland. Funct Ecol 19:291–298

    Article  Google Scholar 

  • Canepuccia A, Alberti A, Pascual J, Alvarez G, Cebrian J, Iribarne O (2010) ENSO episodes modify plant/terrestrial-herbivore interactions in a southwestern Atlantic salt marsh. J Exp Mar Biol Ecol 396:42–47

    Article  Google Scholar 

  • Cates RG, Orians GH (1975) Successional status and the palatability of plants to generalized herbivores. Ecology 56:410–418

    Article  Google Scholar 

  • Chapin FS III, Matson PA, Mooney HA (2002) Principles of terrestrial ecosystem ecology. Springer, New York

    Google Scholar 

  • Connell J, Slatyer R (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1143

    Article  Google Scholar 

  • Crain CM (2008) Interactions between marsh plant species vary in direction and strength depending on environmental and consumer context. J Ecol 96:166–173

    Google Scholar 

  • Crain CM, Albertson LK, Bertness MD (2008) Secondary succession dynamics in estuarine marshes across landscape-scale salinity gradients. Ecology 89:2889–2899

    Article  PubMed  Google Scholar 

  • Daleo P, Alberti J, Iribarne O (2011) Crab herbivory regulates re-colonization of disturbed patches in a southwestern Atlantic salt marsh. Oikos 120:842–847

    Article  Google Scholar 

  • Dayton PK (1971) Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41:351–389

    Article  Google Scholar 

  • De Deyn GB, Raaijmakers CE, Zoomer HR, Berg MP, de Ruiter PC, Verhoef HA, Bazemer TM, van der Putten WH (2003) Soil invertebrate fauna enhances grassland succession and diversity. Nature 422:711–713

    Article  PubMed  Google Scholar 

  • Dorken ME, Eckert CG (2001) Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J Ecol 89:339–350

    Article  Google Scholar 

  • Ellison AM (1987) Effects of competition, disturbance, and herbivory on Salicornia europaea. Ecology 68:576–586

    Article  Google Scholar 

  • Ewanchuk PJ, Bertness MD (2004) Structure and organization of a northern New England salt marsh. J Ecol 92:72–85

    Article  Google Scholar 

  • Fahrig L, Coffin DP, Lauenroth WK, Shugart HH (1994) The advantage of long-distance clonal spreading in highly disturbed habitats. Evol Ecol 8:172–187

    Article  Google Scholar 

  • Fariña JM, Silliman BR, Bertness MD (2009) Can conservation biologist rely on established community structure rules to manage novel systems?…Not in salt marshes. Ecol Appl 19:413–422

    Article  PubMed  Google Scholar 

  • Farrell TM (1991) Models and mechanisms of succession: an example from a rocky intertidal community. Ecol Monogr 6:95–113

    Google Scholar 

  • Foster BL, Tilman D (2000) Dynamic and static views of succession: testing the descriptive power of the chronosequence approach. Plant Ecol 146:1–10

    Article  Google Scholar 

  • Gardner SN, Mangel M (1999) Modeling investments in seeds, clonal offspring, and translocation in a clonal plant. Ecology 80:1202–1220

    Article  Google Scholar 

  • Garnier E, Cortez J, Billès G, Navas ML, Roumet C, Debussche M, Laurent G, Blanchard A, Aubry D, Bellman A, Neill C, Toussaint JP (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637

    Article  Google Scholar 

  • Grime JP (2001) Plant strategies, vegetation processes, and ecosystem properties, 2nd edn. Wiley, Chichester

  • Harris LG, Ebeling AW, Laur DR, Rowley RJ (1984) Community recovery after storm damage: a case of facilitation in primary succession. Science 224:1336–1338

    Article  CAS  PubMed  Google Scholar 

  • Hättenschwiler S, Tiunov AV, Schev S (2005) Biodiveristy and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218

    Article  Google Scholar 

  • Hobbie SE (1996) Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–522

    Article  Google Scholar 

  • Horn SH (1974) The ecology of secondary succession. Annu Rev Ecol Syst 5:25–37

    Article  Google Scholar 

  • Isacch JP, Costa CSB, Rodríguez-Gallego L, Conde D, Escapa M, Gagliardini DA, Iribarne OO (2006) Distribution of saltmarsh plant communities associated with environmental factors along a latitudinal gradient in the south-west Atlantic coast. J Biogeogr 33:888–900

    Article  Google Scholar 

  • Isla FI (1997) Seasonal behavior of Mar Chiquita tidal inlet in relation to adjacent beaches, Argentina. J Coast Res 13:1221–1232

    Google Scholar 

  • Jefferies RL, Jano AP, Abraham KF (2006) A biotic agent promotes large-scale catastrophic change in the coastal marshes of Hudson Bay. J Ecol 94:234–242

    Article  Google Scholar 

  • Kuijper DPJ, Nijhoff DJ, Bakker JP (2004) Herbivory and competition slow down invasion of a tall grass along a productivity gradient. Oecologia 141:452–459

    Article  CAS  PubMed  Google Scholar 

  • Levine JM, HilleRisLambers J (2009) The importance of niches for the maintenance of species diversity. Nature 461:254–257

    Article  CAS  PubMed  Google Scholar 

  • Mellinger MV, McNaughton SJ (1975) Structure and function of successional vascular plant communities in Central New York. Ecol Monogr 45:161–182

    Article  Google Scholar 

  • Niu K, Schmid B, Choler P, Du G (2012) Relationship between reproductive allocation and relative abundance among 32 species of a Tibetan alpine meadow: effects of fertilization and grazing. PLoS ONE 7:e35448

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymon P, Stevens MH, Wagner H (2012) vegan: Community Ecology Package. R package version 2.0-4

  • Olff H, Ritchie ME (1998) Effects of herbivores on grassland plant diversity. Trends Ecol Evol 13:261–265

    Article  CAS  PubMed  Google Scholar 

  • Pennings SC, Bertness MD (2001) Salt marsh communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer, Sunderland, pp 289–316

    Google Scholar 

  • Pennings SC, Callaway RM (2000) The advantages of clonal integration under different ecological conditions: a community-wide test. Ecology 81:709–716

    Article  Google Scholar 

  • Pennings SC, Selig ER, Houser LT, Bertness MD (2003) Geographic variation in positive and negative interactions among salt marsh plants. Ecology 84:1527–1538

    Article  Google Scholar 

  • Pierce S, Luzzaro A, Caccianiga M, Ceriani RM, Cerabolini B (2007) Disturbance is the principal α-scale filter determining niche differentiation, coexistence and biodiversity in an alpine community. J Ecol 95:698–706

    Article  Google Scholar 

  • Pomeroy LR, Wiegert RG (1981) The ecology of a salt marsh. Springer, New York

    Book  Google Scholar 

  • Richards AJ (1986) Plant breeding systems. Allen & Unwin, London

    Google Scholar 

  • Rousset O, Lepart J (2000) Positive and negative interactions at different life stages of a colonizing species (Quercus humilis). J Ecol 88:401–412

    Article  Google Scholar 

  • Schmitz OJ, Kalies EL, Booth MG (2006) Alternative dynamic regimes and trophic control of plant succession. Ecosystems 9:659–672

    Article  Google Scholar 

  • Shumway SW (1995) Physiological integration among clonal ramets during invasion of disturbance patches in a New England salt marsh. Ann Bot 76:225–233

    Article  Google Scholar 

  • Shumway SW, Bertness MD (1992) Salt stress limitation of seedling recruitment in a salt marsh plant community. Oecologia 92:490–497

    Article  Google Scholar 

  • Silliman BR, van de Koppel J, Bertness MD, Stanton L, Mendelsohn I (2005) Drought, snails, and large-scale die-off of southern U.S. salt marshes. Science 310:1803–1806

    Article  CAS  PubMed  Google Scholar 

  • Tilman D (1987) Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecol Monogr 57:189–214

    Article  Google Scholar 

  • Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton

    Google Scholar 

  • Vallejo-Marín M, Dorke ME, Barrett SCH (2010) The ecological and evolutionary consequences of clonality for plant mating. Annu Rev Ecol Evol Syst 41:193–213

    Article  Google Scholar 

  • Wardle DA (2002) Communities and ecosystems.Linking the aboveground and belowground componentsLinking the aboveground and belowground components. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Warwick RM, Clarke KR (1991) A comparison of some methods for analyzing changes in benthic community structure. J Mar Biol Ass UK 71:225–244

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle River

    Google Scholar 

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Acknowledgments

We are grateful to B. Silliman and three anonymous reviewers for helpful comments on the manuscript. The experiments comply with the current laws of the country, Argentina, in which the experiments were performed. This project was supported by grants from the Universidad Nacional de Mar del Plata, CONICET and ANPCyT.

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Correspondence to Pedro Daleo.

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Communicated by Laura Gough.

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Daleo, P., Alberti, J., Pascual, J. et al. Herbivory affects salt marsh succession dynamics by suppressing the recovery of dominant species. Oecologia 175, 335–343 (2014). https://doi.org/10.1007/s00442-014-2903-0

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