Advertisement

Oecologia

, Volume 175, Issue 1, pp 335–343 | Cite as

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

  • Pedro DaleoEmail author
  • Juan Alberti
  • Jesús Pascual
  • Alejandro Canepuccia
  • Oscar Iribarne
Community ecology - Original research

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.

Keywords

Community structure Secondary succession Colonization Spartina 

Notes

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.

Supplementary material

442_2014_2903_MOESM1_ESM.doc (88 kb)
Supplementary material 1 (DOC 88 kb)

References

  1. Abrahamson WG (1980) Demography and vegetative reproduction. In: Solbrig OT (ed) Demography and evolution of plant populations. Blackwell, Oxford, pp 89–106Google Scholar
  2. Adam P (1993) Saltmarsh ecology. Cambridge University Press, CambridgeGoogle Scholar
  3. 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 353:126–133CrossRefGoogle Scholar
  4. Alberti J, Escapa M, Iribarne O, Silliman B, Bertness M (2008) Crab herbivory regulates plant facilitative and competitive processes in Argentinean marshes. Ecology 89:155–164PubMedCrossRefGoogle Scholar
  5. 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 400:55–61CrossRefGoogle Scholar
  6. 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 163:181–191PubMedCrossRefGoogle Scholar
  7. 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 22:216–224CrossRefGoogle Scholar
  8. 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 65:759–791CrossRefGoogle Scholar
  9. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  10. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: Guide to software and statistical methods. PRIMER-E, PlymouthGoogle Scholar
  11. Angelini C, Silliman BR (2012) Patch size-dependent community recovery after massive disturbance. Ecology 93:101–110PubMedCrossRefGoogle Scholar
  12. Bazzaz FA (1979) The physiological ecology of plant succession. Annu Rev Ecol Syst 10:351–371CrossRefGoogle Scholar
  13. Berendse F (1998) Effects of dominant plant species on soils during succession in nutrient-poor ecosystems. Biogeochemistry 42:73–88CrossRefGoogle Scholar
  14. Bertness MD (1991) Interespecific interactions among high marsh perennials in a New England salt marsh. Ecology 72:125–137CrossRefGoogle Scholar
  15. Bertness MD (1999) The ecology of Atlantic shorelines. Sinauer, SunderlandGoogle Scholar
  16. Bertness MD, Ellison AM (1987) Determinants of pattern in a New England salt marsh plant community. Ecol Monogr 57:129–147CrossRefGoogle Scholar
  17. Bertness MD, Leonard GH (1997) The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78:1976–1989CrossRefGoogle Scholar
  18. Bertness MD, Shumway SW (1993) Competition and facilitation in marsh plants. Am Nat 142:718–724PubMedCrossRefGoogle Scholar
  19. Bertness MD, Wise C, Ellison AM (1987) Consumer pressure and seed set in a salt marsh perennial plant community. Oecologia 71:190–200CrossRefGoogle Scholar
  20. Bertness MD, Trussell GC, Ewanchuk PJ, Silliman BR (2002) Do alternate stable community states exist in the Gulf of Maine rocky intertidal zone? Ecology 83:3434–3448CrossRefGoogle Scholar
  21. Bortolus A, Iribarne OO (1999) The effect of the southwestern Atlantic burrowing crab Chasmagnathus granulata on a Spartina salt-marsh. Mar Ecol Prog Ser 178:79–88CrossRefGoogle Scholar
  22. Bortolus A, Laterra P, Iribarne O (2004) Crab-mediated phenotypic changes in Spartina densiflora Brong. Estuar Coast Shelf Sci 59:97–107CrossRefGoogle Scholar
  23. Brewer JS, Bertness MD (1996) Disturbance and intraspecific variation in the clonal morphology of salt marsh perennials. Oikos 77:107–116CrossRefGoogle Scholar
  24. 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 86:125–136CrossRefGoogle Scholar
  25. Bromberg Gedan K, Crain CM, Bertness MD (2009) Small-mammal herbivore control of secondary succession in New England tidal marshes. Ecology 90:430–440CrossRefGoogle Scholar
  26. 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 19:291–298CrossRefGoogle Scholar
  27. 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 396:42–47CrossRefGoogle Scholar
  28. Cates RG, Orians GH (1975) Successional status and the palatability of plants to generalized herbivores. Ecology 56:410–418CrossRefGoogle Scholar
  29. Chapin FS III, Matson PA, Mooney HA (2002) Principles of terrestrial ecosystem ecology. Springer, New YorkGoogle Scholar
  30. Connell J, Slatyer R (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1143CrossRefGoogle Scholar
  31. Crain CM (2008) Interactions between marsh plant species vary in direction and strength depending on environmental and consumer context. J Ecol 96:166–173Google Scholar
  32. Crain CM, Albertson LK, Bertness MD (2008) Secondary succession dynamics in estuarine marshes across landscape-scale salinity gradients. Ecology 89:2889–2899PubMedCrossRefGoogle Scholar
  33. Daleo P, Alberti J, Iribarne O (2011) Crab herbivory regulates re-colonization of disturbed patches in a southwestern Atlantic salt marsh. Oikos 120:842–847CrossRefGoogle Scholar
  34. Dayton PK (1971) Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41:351–389CrossRefGoogle Scholar
  35. 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 422:711–713PubMedCrossRefGoogle Scholar
  36. Dorken ME, Eckert CG (2001) Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J Ecol 89:339–350CrossRefGoogle Scholar
  37. Ellison AM (1987) Effects of competition, disturbance, and herbivory on Salicornia europaea. Ecology 68:576–586CrossRefGoogle Scholar
  38. Ewanchuk PJ, Bertness MD (2004) Structure and organization of a northern New England salt marsh. J Ecol 92:72–85CrossRefGoogle Scholar
  39. Fahrig L, Coffin DP, Lauenroth WK, Shugart HH (1994) The advantage of long-distance clonal spreading in highly disturbed habitats. Evol Ecol 8:172–187CrossRefGoogle Scholar
  40. 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 19:413–422PubMedCrossRefGoogle Scholar
  41. Farrell TM (1991) Models and mechanisms of succession: an example from a rocky intertidal community. Ecol Monogr 6:95–113Google Scholar
  42. Foster BL, Tilman D (2000) Dynamic and static views of succession: testing the descriptive power of the chronosequence approach. Plant Ecol 146:1–10CrossRefGoogle Scholar
  43. Gardner SN, Mangel M (1999) Modeling investments in seeds, clonal offspring, and translocation in a clonal plant. Ecology 80:1202–1220CrossRefGoogle Scholar
  44. 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 85:2630–2637CrossRefGoogle Scholar
  45. Grime JP (2001) Plant strategies, vegetation processes, and ecosystem properties, 2nd edn. Wiley, ChichesterGoogle Scholar
  46. Harris LG, Ebeling AW, Laur DR, Rowley RJ (1984) Community recovery after storm damage: a case of facilitation in primary succession. Science 224:1336–1338PubMedCrossRefGoogle Scholar
  47. Hättenschwiler S, Tiunov AV, Schev S (2005) Biodiveristy and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218CrossRefGoogle Scholar
  48. Hobbie SE (1996) Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–522CrossRefGoogle Scholar
  49. Horn SH (1974) The ecology of secondary succession. Annu Rev Ecol Syst 5:25–37CrossRefGoogle Scholar
  50. 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 33:888–900CrossRefGoogle Scholar
  51. Isla FI (1997) Seasonal behavior of Mar Chiquita tidal inlet in relation to adjacent beaches, Argentina. J Coast Res 13:1221–1232Google Scholar
  52. Jefferies RL, Jano AP, Abraham KF (2006) A biotic agent promotes large-scale catastrophic change in the coastal marshes of Hudson Bay. J Ecol 94:234–242CrossRefGoogle Scholar
  53. Kuijper DPJ, Nijhoff DJ, Bakker JP (2004) Herbivory and competition slow down invasion of a tall grass along a productivity gradient. Oecologia 141:452–459PubMedCrossRefGoogle Scholar
  54. Levine JM, HilleRisLambers J (2009) The importance of niches for the maintenance of species diversity. Nature 461:254–257PubMedCrossRefGoogle Scholar
  55. Mellinger MV, McNaughton SJ (1975) Structure and function of successional vascular plant communities in Central New York. Ecol Monogr 45:161–182CrossRefGoogle Scholar
  56. 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:e35448PubMedCentralPubMedCrossRefGoogle Scholar
  57. 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 2.0-4Google Scholar
  58. Olff H, Ritchie ME (1998) Effects of herbivores on grassland plant diversity. Trends Ecol Evol 13:261–265PubMedCrossRefGoogle Scholar
  59. Pennings SC, Bertness MD (2001) Salt marsh communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer, Sunderland, pp 289–316Google Scholar
  60. Pennings SC, Callaway RM (2000) The advantages of clonal integration under different ecological conditions: a community-wide test. Ecology 81:709–716CrossRefGoogle Scholar
  61. Pennings SC, Selig ER, Houser LT, Bertness MD (2003) Geographic variation in positive and negative interactions among salt marsh plants. Ecology 84:1527–1538CrossRefGoogle Scholar
  62. 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 95:698–706CrossRefGoogle Scholar
  63. Pomeroy LR, Wiegert RG (1981) The ecology of a salt marsh. Springer, New YorkCrossRefGoogle Scholar
  64. Richards AJ (1986) Plant breeding systems. Allen & Unwin, LondonGoogle Scholar
  65. Rousset O, Lepart J (2000) Positive and negative interactions at different life stages of a colonizing species (Quercus humilis). J Ecol 88:401–412CrossRefGoogle Scholar
  66. Schmitz OJ, Kalies EL, Booth MG (2006) Alternative dynamic regimes and trophic control of plant succession. Ecosystems 9:659–672CrossRefGoogle Scholar
  67. Shumway SW (1995) Physiological integration among clonal ramets during invasion of disturbance patches in a New England salt marsh. Ann Bot 76:225–233CrossRefGoogle Scholar
  68. Shumway SW, Bertness MD (1992) Salt stress limitation of seedling recruitment in a salt marsh plant community. Oecologia 92:490–497CrossRefGoogle Scholar
  69. 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 310:1803–1806PubMedCrossRefGoogle Scholar
  70. Tilman D (1987) Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecol Monogr 57:189–214CrossRefGoogle Scholar
  71. Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Princeton University Press, PrincetonGoogle Scholar
  72. Vallejo-Marín M, Dorke ME, Barrett SCH (2010) The ecological and evolutionary consequences of clonality for plant mating. Annu Rev Ecol Evol Syst 41:193–213CrossRefGoogle Scholar
  73. Wardle DA (2002) Communities and ecosystems.Linking the aboveground and belowground componentsLinking the aboveground and belowground components. Princeton University Press, Princeton, New JerseyGoogle Scholar
  74. Warwick RM, Clarke KR (1991) A comparison of some methods for analyzing changes in benthic community structure. J Mar Biol Ass UK 71:225–244CrossRefGoogle Scholar
  75. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle RiverGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Pedro Daleo
    • 1
    Email author
  • Juan Alberti
    • 1
  • Jesús Pascual
    • 1
  • Alejandro Canepuccia
    • 1
  • Oscar Iribarne
    • 1
  1. 1.Instituto de Investigaciones Marinas y Costeras, CONICET-UNMDPMar del PlataArgentina

Personalised recommendations