Oecologia

, Volume 163, Issue 1, pp 181–191 | Cite as

Abiotic stress mediates top-down and bottom-up control in a Southwestern Atlantic salt marsh

  • Juan Alberti
  • Agustina Méndez Casariego
  • Pedro Daleo
  • Eugenia Fanjul
  • Brian Silliman
  • Mark Bertness
  • Oscar Iribarne
Community ecology - Original paper

Abstract

Increasing evidence has shown that nutrients and consumers interact to control primary productivity in natural systems, but how abiotic stress affects this interaction is unclear. Moreover, while herbivores can strongly impact zonation patterns in a variety of systems, there are few examples of this in salt marshes. We evaluated the effect of nutrients and herbivores on the productivity and distribution of the cordgrass Spartinadensiflora along an intertidal stress gradient, in a Southwestern Atlantic salt marsh. We characterized abiotic stresses (salinity, ammonium concentration, and anoxia) and manipulated nutrients and the presence of the herbivorous crab Neohelice (Chasmagnathus) granulata, at different tidal heights with a factorial experiment. Abiotic stress increased at both ends of the tidal gradient. Salinity and anoxia were highest at the upper and lower edge of the intertidal, respectively. Nutrients and herbivory interacted to control cordgrass biomass, but their relative importance varied with environmental context. Herbivory increased at lower tidal heights to the point that cordgrass transplants onto bare mud substrate were entirely consumed unless crabs were excluded, while nutrients were most important where abiotic stress was reduced. Our results show how the impact of herbivores and nutrients on plant productivity can be dependent on environmental conditions and that the lower intertidal limits of marsh plants can be controlled by herbivory.

Keywords

Herbivory Neohelice granulata Nutrients Spartina densiflora Tidal stress gradient 

Supplementary material

442_2009_1504_MOESM1_ESM.pdf (9 kb)
Supplementary material 1 (PDF 9 kb)
442_2009_1504_MOESM2_ESM.pdf (16 kb)
Supplementary material 2 (PDF 16 kb)
442_2009_1504_MOESM3_ESM.pdf (16 kb)
Supplementary material 3 (PDF 16 kb)
442_2009_1504_MOESM4_ESM.pdf (16 kb)
Supplementary material 4 (PDF 15 kb)

References

  1. Alberti J, Escapa M, Daleo P, Iribarne O, Silliman BR, Bertness M (2007a) Local and geographic variation in grazing intensity by herbivorous crabs in SW Atlantic salt marshes. Mar Ecol Prog Ser 349:235–243CrossRefGoogle Scholar
  2. Alberti J, Montemayor D, Álvarez F, Méndez Casariego A, Luppi T, Canepuccia A, Isacch JP, Iribarne O (2007b) Changes in rainfall pattern affect crab herbivory rates in a SW Atlantic salt marsh. J Exp Mar Biol Ecol 353:126–133CrossRefGoogle Scholar
  3. Alberti J, Escapa M, Iribarne O, Silliman B, Bertness M (2008) Crab herbivory regulates plant facilitative and competitive processes in Argentinean marshes. Ecology 89:155–164CrossRefPubMedGoogle Scholar
  4. Bertness MD (1984) Habitat and community modification by an introduced herbivorous snail. Ecology 65:370–381Google Scholar
  5. Bertness MD (1991a) Interespecific interactions among high marsh perennials in a New England salt marsh. Ecology 72:125–137CrossRefGoogle Scholar
  6. Bertness MD (1991b) Zonation of Spartina patens and Spartina alterniflora in New England salt marsh. Ecology 72:138–148CrossRefGoogle Scholar
  7. Bertness MD, Hacker SD (1994) Physical stress and positive associations among marsh plants. Am Nat 144:363–372CrossRefGoogle Scholar
  8. Bertness MD, Leonard GH (1997) The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78:1976–1989CrossRefGoogle Scholar
  9. Bertness MD, Leonard GH, Levine JM, Schmidt PR, Ingraham AO (1999) Testing the relative contribution of positive and negative interactions in rocky intertidal communities. Ecology 80:2711–2726CrossRefGoogle Scholar
  10. Bertness M, Silliman BR, Jefferies R (2004) Salt marshes under siege. Am Sci 92:54–61Google Scholar
  11. Bertness MD, Crain C, Holdredge C, Sala N (2008) Eutrophication and consumer control of New England salt marsh primary productivity. Conserv Biol 22:131–139CrossRefPubMedGoogle Scholar
  12. Bockelmann AC, Neuhaus R (1999) Competitive exclusion of Elymus athericus from a high-stress habitat in a European salt marsh. J Ecol 87:503–513CrossRefGoogle Scholar
  13. 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
  14. Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139CrossRefPubMedGoogle Scholar
  15. Callaway RM et al (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848CrossRefPubMedGoogle Scholar
  16. Canepuccia A, Escapa M, Daleo P, Alberti J, Botto F, Iribarne OO (2007) Positive interactions of the smooth cordgrass Spartina alterniflora on the mud snail Heleobia australis, in South Western Atlantic salt marshes. J Exp Mar Biol Ecol 353:180–190CrossRefGoogle Scholar
  17. Castañeda-Moya E, Rivera-Monroy VH, Twilley RR (2006) Mangrove zonation in the dry life zone of the gulf of Fonseca, Honduras. Estuaries and Coasts 29:751–764Google Scholar
  18. Castillo JM, Fernández-Baco L, Castellanos EM, Luque CJ, Figueroa ME, Davy AJ (2000) Lower limits of Spartina densiflora and S. maritima in a Mediterranean salt marsh determined by different ecophysiological tolerances. J Ecol 88:801–812CrossRefGoogle Scholar
  19. Clarke PJ, Kerrigan RA (2002) The effects of seed predators on the recruitment of mangroves. J Ecol 90:728–736CrossRefGoogle Scholar
  20. Clarke PJ, Myerscough PJ (1993) The intertidal distribution of the grey mangrove (Avicennia marina) in southeastern Australia: the effects of physical conditions, interspecific competition, and predation on propagule establishment and survival. Aust J Ecol 18:307–315CrossRefGoogle Scholar
  21. Connell JH (1972) Community interactions on marine rocky intertidal shores. Annu Rev Ecol Syst 3:169–192CrossRefGoogle Scholar
  22. Conover WJ (1980) Practical nonparametric statistics, 2nd edn. Wiley, New YorkGoogle Scholar
  23. Cousseau MB, Días de Astarloa JM, Figueroa DE (2001) La ictiofauna de la laguna Mar Chiquita. In: Iribarne O (ed) Reserva de biosfera Mar Chiquita: características físicas, biológicas y ecológicas. Martín, Mar del Plata, pp 187–203Google Scholar
  24. Cubit JD (1984) Herbivory and the seasonal abundance of algae on a high intertidal rocky shore. Ecology 65:1904–1917CrossRefGoogle Scholar
  25. Dai T, Wiegert RG (1996) Ramet population dynamics and net aerial primary productivity of Spartina alterniflora. Ecology 77:276–288CrossRefGoogle Scholar
  26. Daleo P, Iribarne O (2009) The burrowing crab Neohelice granulata affects the root strategies of the cordgrass Spartina densiflora in SW Atlantic salt marshes. J Exp Mar Biol Ecol 373:66–71CrossRefGoogle Scholar
  27. Daleo P, Ribeiro P, Iribarne O (2003) The SW Atlantic burrowing crab Chasmagnathus granulatus Dana affects the distribution and survival of the fiddler crab Uca uruguayensis Nobili. J Exp Mar Biol Ecol 291:255–267Google Scholar
  28. Daleo P, Alberti J, Canepuccia A, Escapa M, Fanjul E, Silliman BR, Bertness MD, Iribarne O (2008) Mycorrhizal fungi determine salt-marsh plant zonation depending on nutrient supply. J Ecol 96:431–437CrossRefGoogle Scholar
  29. Darwin CR (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life, 1st edition. Murray, London. http://darwin-online.org.uk/pdf/1859_Origin_F373.pdf
  30. Dudt CF, Shure DJ (1994) The influence of light and nutrients on foliar phenolics and insect herbivory. Ecology 75:86–98CrossRefGoogle Scholar
  31. Duke NC, Ball MC, Ellison JC (1998) Factors influencing biodiversity and distributional gradients in mangroves. Global Ecol Biogeogr Lett 7:27–47CrossRefGoogle Scholar
  32. Ellison AM, Farnsworth EJ (2001) Mangrove communities. In: Bertness MD, Gaines SD, Hay M (eds) Marine community ecology. Sinauer, Sunderland, pp 423–442Google Scholar
  33. Emery NC, Ewanchuk PJ, Bertness MD (2001) Competition and salt-marsh plant zonation: stress tolerators may be dominant competitors. Ecology 82:2471–2485CrossRefGoogle Scholar
  34. Escapa M, Iribarne O, Navarro D (2004) Effects of the intertidal burrowing crab Chasmagnathus granulatus on infaunal zonation patterns, tidal behavior, and risk of mortality. Estuaries 27:120–131CrossRefGoogle Scholar
  35. Feller IC (1995) Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecol Monogr 65:477–505CrossRefGoogle Scholar
  36. Feller IC, Whigham DF, McKee KL, Lovelock CE (2003) Nitrogen limitation of growth and nutrient dynamics in a disturbed mangrove forest, Indian River Lagoon, Florida. Oecologia 134:405–414PubMedGoogle Scholar
  37. Furbish CE, Albano M (1994) Selective herbivory and plant community structure in a mid-Atlantic salt marsh. Ecology 75:1015–1022CrossRefGoogle Scholar
  38. Goranson CE, Ho C, Pennings SC (2004) Environmental gradients and herbivore feeding preferences in coastal salt marshes. Oecologia 140:591–600CrossRefPubMedGoogle Scholar
  39. Gough L, Grace JB (1998) Effects of flooding, salinity and herbivory on coastal plant communities, Louisiana, United States. Oecologia 117:527–535CrossRefGoogle Scholar
  40. Halpern BS, Cottenie K, Broitman BR (2006) Strong top-down control in Southern California kelp forest ecosystems. Science 312:1230–1232CrossRefPubMedGoogle Scholar
  41. Harley CDG (2003) Abiotic stress and herbivory interact to set range limits across a two-dimensional stress gradient. Ecology 84:1477–1488CrossRefGoogle Scholar
  42. Hillebrand H (2002) Top-down versus bottom-up control of autotrophic biomass: a meta-analysis on experiments with periphyton. J North Am Benthol Soc 21:349–369CrossRefGoogle Scholar
  43. Holmgren M, Scheffer M, Huston MA (1997) The interplay of facilitation and competition in plant communities. Ecology 78:1966–1975CrossRefGoogle Scholar
  44. Howes BL, Howarth RW, Teal JM, Valiela I (1981) Oxidation-reduction potentials in a salt marsh: spatial patterns and interactions with primary production. Limnol Oceanogr 26:350–360CrossRefGoogle Scholar
  45. Huckle JM, Potter JA, Marrs RH (2000) Influence of environmental factors on the growth and interactions between salt marsh plants: effects of salinity, sediment and waterlogging. J Ecol 88:492–505CrossRefGoogle Scholar
  46. Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732Google Scholar
  47. Iribarne O (ed) (2001) Reserva de biosfera Mar Chiquita: características físicas, biológicas y ecológicas. Martín, Mar del PlataGoogle Scholar
  48. Iribarne O, Bortolus A, Botto F (1997) Between-habitat differences in burrow characteristics and trophic modes in the southwestern Atlantic burrowing crab Chasmagnathus granulata. Mar Ecol Prog Ser 155:137–145CrossRefGoogle Scholar
  49. Iribarne O, Bruschetti M, Escapa M, Bava J, Botto F, Gutiérrez J, Palomo G, Delhey K, Petracci P, Gagliardini A (2005) Small- and large-scale effect of the SW Atlantic burrowing crab Chasmagnathus granulatus on habitat use by migratory shorebirds. J Exp Mar Biol Ecol 315:87–101CrossRefGoogle 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 on the south-west Atlantic coast. J Biogeogr 33:888–900CrossRefGoogle Scholar
  51. 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
  52. Kautsky N, Kautsky H, Kautsky U, Waern M (1986) Decreased depth penetration of Fucus vesiculosus (L.) since the 1940’s indicates eutrophication of the Baltic Sea. Mar Ecol Prog Ser 28:1–8CrossRefGoogle Scholar
  53. Levine JM, Brewer JS, Bertness MD (1998) Nutrients, competition and plant zonation in a New England salt marsh. J Ecol 86:285–292CrossRefGoogle Scholar
  54. Linthurst RA, Seneca ED (1981) Aeration, nitrogen and salinity as determinants of Spartina alferniflora Loisel. growth response. Estuaries 4:53–63CrossRefGoogle Scholar
  55. Louda SM (1989) Differential predation pressure: a general mechanism for structuring plant communities along complex environmetal gradients? Trends Ecol Evol 4:158–159CrossRefGoogle Scholar
  56. Lubchenco J (1980) Algal zonation in the New England rocky intertidal community: an experimental analysis. Ecology 61:333–344CrossRefGoogle Scholar
  57. Martinetto P, Iribarne O, Palomo G (2005) Effect of fish predation on intertidal benthic fauna is modified by crab bioturbation. J Exp Mar Biol Ecol 318:71–84CrossRefGoogle Scholar
  58. Méndez Casariego A, Alberti J, Luppi T, Iribarne O (2009) Stage-dependent interactions between intertidal crabs: from facilitation to predation. J Mar Biol Assoc UK 89:781–788CrossRefGoogle Scholar
  59. Menge BA, Farrell TM (1989) Community structure and interaction webs in shallow marine hard-bottom communities: test of an environmental stress model. Adv Ecol Res 19:189–262CrossRefGoogle Scholar
  60. Menge BA, Sutherland JP (1976) Species diversity gradients: synthesis of the roles of predation, competition, and temporal heterogeneity. Am Nat 110:351–369CrossRefGoogle Scholar
  61. Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757CrossRefGoogle Scholar
  62. Moran MD, Scheidler AR (2002) Effects of nutrients and predators on an old-field food chain: interactions of top-down and bottom-up processes. Oikos 98:116–124CrossRefGoogle Scholar
  63. Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850CrossRefPubMedGoogle Scholar
  64. Nixon SW, Buckley BA (2002) “A strikingly rich zone”—nutrient enrichment and secondary production in coastal marine ecosystems. Estuaries 25:782–796CrossRefGoogle Scholar
  65. Pennings SC, Bertness MD (2001) Salt marsh communities. In: Bertness MD, Gaines SD, Hay M (eds) Marine community ecology. Sinauer, Sunderland, pp 289–316Google Scholar
  66. Pennings SC, Callaway RM (1992) Salt marsh plant zonation: the relative importance of competition and physical factors. Ecology 73:681–690CrossRefGoogle Scholar
  67. Peterson BJ et al (1993) Biological responses of a tundra river to fertilization. Ecology 74:653–672CrossRefGoogle Scholar
  68. Power ME (1992) Top-down and bottom-up forces in food webs: do plants have primacy? Ecology 73:733–746CrossRefGoogle Scholar
  69. Pugnaire FI, Luque MT (2001) Changes in plant interactions along a gradient of environmental stress. Oikos 93:42–49CrossRefGoogle Scholar
  70. Rand TA (2002) Variation in insect herbivory across a salt marsh tidal gradient influences plant survival and distribution. Oecologia 132:549–558CrossRefGoogle Scholar
  71. Rozas LP, Minello TJ (1998) Nekton use of salt marsh, seagrass, and nonvegetated habitats in a South Texas (USA) estuary. Bull Mar Sci 63:481–501Google Scholar
  72. Russell BD, Connell SD (2005) A novel interaction between nutrients and grazers alters relative dominance of marine habitats. Mar Ecol Prog Ser 289:5–11CrossRefGoogle Scholar
  73. Sala NM, Bertness MD, Silliman BR (2008) The dynamics of bottom-up and top-down control in a New England salt marsh. Oikos 117:1050–1056CrossRefGoogle Scholar
  74. Silliman BR, Bortolus A (2003) Underestimation of Spartina productivity in western Atlantic marshes: marsh invertebrates eat more than just detritus. Oikos 101:549–554CrossRefGoogle Scholar
  75. Silliman BR, Zieman JC (2001) Top-down control of Spartina alterniflora production by periwinkle grazing in a Virginia salt marsh. Ecology 82:2830–2845Google Scholar
  76. Silliman BR, van de Koppel J, Bertness MD, Stanton LE, Mendelssohn IA (2005) Drought, snails, and large-scale die-off of Southern US salt marshes. Science 310:1803–1806CrossRefPubMedGoogle Scholar
  77. Smith TJ III (1987) Seed predation in relation to tree dominance and distribution in mangrove forests. Ecology 68:266–273CrossRefGoogle Scholar
  78. Solórzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801CrossRefGoogle Scholar
  79. Sousa WP, Kennedy PG, Mitchell BJ, Ordóñez LBM (2007) Supply-side ecology in mangroves: do propagule dispersal and seedling establishment explain forest structure? Ecol Monogr 77:53–76CrossRefGoogle Scholar
  80. Terborgh J, Lopez L, Nuñez P, Rao M, Shahabuddin G, Orihuela G, Riveros M, Ascanio R, Adler GH, Lambert TD, Balbas L (2001) Ecological meltdown in predator-free forest fragments. Science 294:1923–1926CrossRefPubMedGoogle Scholar
  81. Underwood AJ (1980) The effects of grazing by gastropods and physical factors on the upper limits of distribution of intertidal macroalgae. Oecologia 46:201–213CrossRefGoogle Scholar
  82. Underwood AJ, Denley EJ (1984) Paradigms, explanations, and generalizations in models for the structure of intertidal communities on rocky shores. In: Strong DR, Simberloff D, Abele LG, Thistle AB (eds) Ecological communities. Conceptual issues and the evidence. Princeton University Press, Princeton, pp 151–180Google Scholar
  83. Valiela I, Teal JM, Persson NY (1976) Production and dynamics of experimentally enriched salt marsh vegetation: belowground biomass. Limnol Oceanogr 21:245–252CrossRefGoogle Scholar
  84. van Katwijk MM, Schmitz GHW, Gasseling AP, van Avesaath PH (1999) Effects of salinity and nutrient load and their interaction on Zostera marina. Mar Ecol Prog Ser 190:155–165CrossRefGoogle Scholar
  85. Vicari RL, Fischer S, Madanes N, Bonaventura SM, Pancotto V (2002) Tiller population dynamics and production on Spartina densiflora (Brong) on the floodplain of the Paraná river, Argentina. Wetlands 22:347–354CrossRefGoogle Scholar
  86. Vince SW, Valiela I, Teal JM (1981) An experimental study of the structure of herbivorous insect communities in a salt marsh. Ecology 62:1662–1678CrossRefGoogle Scholar
  87. White TCR (2007) Flooded forests: death by drowning, not herbivory. J Veg Sci 18:147–148CrossRefGoogle Scholar
  88. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle RiverGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Juan Alberti
    • 1
    • 2
  • Agustina Méndez Casariego
    • 1
    • 2
  • Pedro Daleo
    • 1
    • 2
  • Eugenia Fanjul
    • 1
    • 2
  • Brian Silliman
    • 3
  • Mark Bertness
    • 4
  • Oscar Iribarne
    • 1
    • 2
  1. 1.Laboratorio de Ecología, Departamento de Biología (FCEyN)Universidad Nacional de Mar del PlataMar del PlataArgentina
  2. 2.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Ciudad de Buenos AiresArgentina
  3. 3.Department of BiologyUniversity of FloridaGainesvilleUSA
  4. 4.Department of Ecology and Evolutionary BiologyBrown UniversityProvidenceUSA

Personalised recommendations