Skip to main content
Log in

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

  • Community ecology - Original paper
  • Published:
Oecologia Aims and scope Submit manuscript

An Erratum to this article was published on 06 August 2011

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 Spartina densiflora 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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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 349:235–243

    Article  Google Scholar 

  • 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 353:126–133

    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 

  • Bertness MD (1984) Habitat and community modification by an introduced herbivorous snail. Ecology 65:370–381

    Google Scholar 

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

    Article  Google Scholar 

  • Bertness MD (1991b) Zonation of Spartina patens and Spartina alterniflora in New England salt marsh. Ecology 72:138–148

    Article  Google Scholar 

  • Bertness MD, Hacker SD (1994) Physical stress and positive associations among marsh plants. Am Nat 144:363–372

    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, Leonard GH, Levine JM, Schmidt PR, Ingraham AO (1999) Testing the relative contribution of positive and negative interactions in rocky intertidal communities. Ecology 80:2711–2726

    Article  Google Scholar 

  • Bertness M, Silliman BR, Jefferies R (2004) Salt marshes under siege. Am Sci 92:54–61

    Google Scholar 

  • Bertness MD, Crain C, Holdredge C, Sala N (2008) Eutrophication and consumer control of New England salt marsh primary productivity. Conserv Biol 22:131–139

    Article  PubMed  Google Scholar 

  • Bockelmann AC, Neuhaus R (1999) Competitive exclusion of Elymus athericus from a high-stress habitat in a European salt marsh. J Ecol 87:503–513

    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 

  • Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139

    Article  PubMed  Google Scholar 

  • Callaway RM et al (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848

    Article  CAS  PubMed  Google Scholar 

  • 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 353:180–190

    Article  Google Scholar 

  • 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 29:751–764

    Google Scholar 

  • 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 88:801–812

    Article  Google Scholar 

  • Clarke PJ, Kerrigan RA (2002) The effects of seed predators on the recruitment of mangroves. J Ecol 90:728–736

    Article  Google Scholar 

  • 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 18:307–315

    Article  Google Scholar 

  • Connell JH (1972) Community interactions on marine rocky intertidal shores. Annu Rev Ecol Syst 3:169–192

    Article  Google Scholar 

  • Conover WJ (1980) Practical nonparametric statistics, 2nd edn. Wiley, New York

    Google Scholar 

  • 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 187–203

    Google Scholar 

  • Cubit JD (1984) Herbivory and the seasonal abundance of algae on a high intertidal rocky shore. Ecology 65:1904–1917

    Article  Google Scholar 

  • Dai T, Wiegert RG (1996) Ramet population dynamics and net aerial primary productivity of Spartina alterniflora. Ecology 77:276–288

    Article  Google Scholar 

  • 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 373:66–71

    Article  Google Scholar 

  • 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 291:255–267

    Google Scholar 

  • 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 96:431–437

    Article  Google Scholar 

  • 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

  • Dudt CF, Shure DJ (1994) The influence of light and nutrients on foliar phenolics and insect herbivory. Ecology 75:86–98

    Article  Google Scholar 

  • Duke NC, Ball MC, Ellison JC (1998) Factors influencing biodiversity and distributional gradients in mangroves. Global Ecol Biogeogr Lett 7:27–47

    Article  Google Scholar 

  • Ellison AM, Farnsworth EJ (2001) Mangrove communities. In: Bertness MD, Gaines SD, Hay M (eds) Marine community ecology. Sinauer, Sunderland, pp 423–442

    Google Scholar 

  • Emery NC, Ewanchuk PJ, Bertness MD (2001) Competition and salt-marsh plant zonation: stress tolerators may be dominant competitors. Ecology 82:2471–2485

    Article  Google Scholar 

  • 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 27:120–131

    Article  Google Scholar 

  • Feller IC (1995) Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecol Monogr 65:477–505

    Article  Google Scholar 

  • 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 134:405–414

    PubMed  Google Scholar 

  • Furbish CE, Albano M (1994) Selective herbivory and plant community structure in a mid-Atlantic salt marsh. Ecology 75:1015–1022

    Article  Google Scholar 

  • Goranson CE, Ho C, Pennings SC (2004) Environmental gradients and herbivore feeding preferences in coastal salt marshes. Oecologia 140:591–600

    Article  PubMed  Google Scholar 

  • Gough L, Grace JB (1998) Effects of flooding, salinity and herbivory on coastal plant communities, Louisiana, United States. Oecologia 117:527–535

    Article  Google Scholar 

  • Halpern BS, Cottenie K, Broitman BR (2006) Strong top-down control in Southern California kelp forest ecosystems. Science 312:1230–1232

    Article  CAS  PubMed  Google Scholar 

  • Harley CDG (2003) Abiotic stress and herbivory interact to set range limits across a two-dimensional stress gradient. Ecology 84:1477–1488

    Article  Google Scholar 

  • Hillebrand H (2002) Top-down versus bottom-up control of autotrophic biomass: a meta-analysis on experiments with periphyton. J North Am Benthol Soc 21:349–369

    Article  Google Scholar 

  • Holmgren M, Scheffer M, Huston MA (1997) The interplay of facilitation and competition in plant communities. Ecology 78:1966–1975

    Article  Google Scholar 

  • 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 26:350–360

    Article  Google Scholar 

  • 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 88:492–505

    Article  Google Scholar 

  • 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 73:724–732

    Google Scholar 

  • Iribarne O (ed) (2001) Reserva de biosfera Mar Chiquita: características físicas, biológicas y ecológicas. Martín, Mar del Plata

    Google Scholar 

  • 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 155:137–145

    Article  Google Scholar 

  • 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 315:87–101

    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 on the south-west Atlantic coast. J Biogeogr 33:888–900

    Article  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 

  • 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 28:1–8

    Article  Google Scholar 

  • Levine JM, Brewer JS, Bertness MD (1998) Nutrients, competition and plant zonation in a New England salt marsh. J Ecol 86:285–292

    Article  Google Scholar 

  • Linthurst RA, Seneca ED (1981) Aeration, nitrogen and salinity as determinants of Spartina alferniflora Loisel. growth response. Estuaries 4:53–63

    Article  Google Scholar 

  • Louda SM (1989) Differential predation pressure: a general mechanism for structuring plant communities along complex environmetal gradients? Trends Ecol Evol 4:158–159

    Article  Google Scholar 

  • Lubchenco J (1980) Algal zonation in the New England rocky intertidal community: an experimental analysis. Ecology 61:333–344

    Article  Google Scholar 

  • 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 318:71–84

    Article  Google Scholar 

  • 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 89:781–788

    Article  Google Scholar 

  • 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 19:189–262

    Article  Google Scholar 

  • Menge BA, Sutherland JP (1976) Species diversity gradients: synthesis of the roles of predation, competition, and temporal heterogeneity. Am Nat 110:351–369

    Article  Google Scholar 

  • Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757

    Article  Google Scholar 

  • 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 98:116–124

    Article  Google Scholar 

  • 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 315:1846–1850

    Article  CAS  PubMed  Google Scholar 

  • Nixon SW, Buckley BA (2002) “A strikingly rich zone”—nutrient enrichment and secondary production in coastal marine ecosystems. Estuaries 25:782–796

    Article  Google Scholar 

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

    Google Scholar 

  • Pennings SC, Callaway RM (1992) Salt marsh plant zonation: the relative importance of competition and physical factors. Ecology 73:681–690

    Article  Google Scholar 

  • Peterson BJ et al (1993) Biological responses of a tundra river to fertilization. Ecology 74:653–672

    Article  CAS  Google Scholar 

  • Power ME (1992) Top-down and bottom-up forces in food webs: do plants have primacy? Ecology 73:733–746

    Article  Google Scholar 

  • Pugnaire FI, Luque MT (2001) Changes in plant interactions along a gradient of environmental stress. Oikos 93:42–49

    Article  Google Scholar 

  • Rand TA (2002) Variation in insect herbivory across a salt marsh tidal gradient influences plant survival and distribution. Oecologia 132:549–558

    Article  Google Scholar 

  • Rozas LP, Minello TJ (1998) Nekton use of salt marsh, seagrass, and nonvegetated habitats in a South Texas (USA) estuary. Bull Mar Sci 63:481–501

    Google Scholar 

  • Russell BD, Connell SD (2005) A novel interaction between nutrients and grazers alters relative dominance of marine habitats. Mar Ecol Prog Ser 289:5–11

    Article  CAS  Google Scholar 

  • Sala NM, Bertness MD, Silliman BR (2008) The dynamics of bottom-up and top-down control in a New England salt marsh. Oikos 117:1050–1056

    Article  Google Scholar 

  • Silliman BR, Bortolus A (2003) Underestimation of Spartina productivity in western Atlantic marshes: marsh invertebrates eat more than just detritus. Oikos 101:549–554

    Article  Google Scholar 

  • Silliman BR, Zieman JC (2001) Top-down control of Spartina alterniflora production by periwinkle grazing in a Virginia salt marsh. Ecology 82:2830–2845

    Google Scholar 

  • 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 310:1803–1806

    Article  CAS  PubMed  Google Scholar 

  • Smith TJ III (1987) Seed predation in relation to tree dominance and distribution in mangrove forests. Ecology 68:266–273

    Article  Google Scholar 

  • Solórzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801

    Article  Google Scholar 

  • 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 77:53–76

    Article  Google Scholar 

  • 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 294:1923–1926

    Article  CAS  PubMed  Google Scholar 

  • Underwood AJ (1980) The effects of grazing by gastropods and physical factors on the upper limits of distribution of intertidal macroalgae. Oecologia 46:201–213

    Article  Google Scholar 

  • 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 151–180

    Google Scholar 

  • Valiela I, Teal JM, Persson NY (1976) Production and dynamics of experimentally enriched salt marsh vegetation: belowground biomass. Limnol Oceanogr 21:245–252

    Article  Google Scholar 

  • 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 190:155–165

    Article  Google Scholar 

  • 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 22:347–354

    Article  Google Scholar 

  • Vince SW, Valiela I, Teal JM (1981) An experimental study of the structure of herbivorous insect communities in a salt marsh. Ecology 62:1662–1678

    Article  Google Scholar 

  • White TCR (2007) Flooded forests: death by drowning, not herbivory. J Veg Sci 18:147–148

    Article  Google Scholar 

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

    Google Scholar 

Download references

Acknowledgments

We thank M. Escapa, M. Valiñas, M. Bruschetti, E. García, A. García Coni and A. Canepuccia for help in the field and processing samples. We also thank P. Clarke and two anonymous reviewers for kindly suggesting valuable corrections on previous versions of this manuscript, and for pointing out Darwin’s comments on species distributional patterns. This project was supported by Universidad Nacional de Mar del Plata, Fundación Antorchas (grant no. 13900-13), ANPCyT, and CONICET (all granted to O. I.) and a grant from the Andrew Mellon Foundation (to M. D. B.) and a Young Investigator grant from the Andrew Mellon Foundation to B. S. J. A., A. M. C., P. D. and E. F. were supported by post-doctoral scholarships from CONICET. Experiments comply with the current laws of Argentina, where they were performed.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan Alberti.

Additional information

Communicated by Peter Clarke.

An erratum to this article is available at http://dx.doi.org/10.1007/s00442-011-2101-2.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alberti, J., Méndez Casariego, A., Daleo, P. et al. Abiotic stress mediates top-down and bottom-up control in a Southwestern Atlantic salt marsh. Oecologia 163, 181–191 (2010). https://doi.org/10.1007/s00442-009-1504-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-009-1504-9

Keywords

Navigation