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Co-occurrence of habitat-modifying invertebrates: effects on structural and functional properties of a created salt marsh

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Abstract

The roles of co-occurring herbivores that modify habitat structure and ecosystem processes have seldom been examined in manipulative experiments or explored in early successional communities. In a created marsh in southern California (USA), we tested the individual and combined effects of two epibenthic invertebrates on nutrient and biomass pools, community structure, and physical habitat features. We manipulated snail (Cerithidea californica) and crab (Pachygrapsus crassipes) presence in field enclosures planted with pickleweed (Salicornia virginica) at elevations matching the plant’s lower extent in an adjacent natural marsh. In the 4-month experiment, C. californica altered habitat structure by reducing sediment surface heterogeneity and shear strength (a measure of sediment stability) markedly throughout the enclosures. Both invertebrates had strong negative effects on a group of correlated sediment physicochemical characteristics, including nitrogen and organic matter concentrations and soil moisture. In addition, both invertebrates greatly reduced benthic chlorophyll a, a proxy for biomass of microphytobenthos. Compared to controls, macroalgal cover was up to sixfold lower with crabs present, while snails increased cover at low elevations of enclosures. Unexpectedly, macroalgal cover was eliminated with both species present, perhaps through P. crassipes consumption of larger thalli and C. californica reduction in cover of recruits. Neither species influenced the S. virginica canopy (quantified with an index of branch length and number); however, at the lower elevation of enclosures, the two species together negatively impacted the plant canopy. The two invertebrates’ modifications to our experimental marshes led to distinct suites of biotic and physicochemical features depending on their presence or co-occurrence, with the latter producing several unexpected results. We propose that the roles and interactions of habitat-modifying fauna deserve further attention, particularly in the context of efforts to conserve and restore the processes found in natural systems.

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References

  • Augustine DJ, Frelich LE, Jordon PA (1998) Evidence for two alternate stable states in an ungulate grazing system. Ecol Appl 8:1260–1269

    Article  Google Scholar 

  • Bakker ES, Olff H, Boekhoff M, Gleichman JM, Berendse F (2004) Impact of herbivores on nitrogen cycling: contrasting effects of small and large species. Oecologia 138:91–101

    Article  PubMed  CAS  Google Scholar 

  • Bertness MD (1985) Fiddler crab regulation of Spartina alterniflora production on a New England salt marsh. Ecology 66:1042–1055

    Article  Google Scholar 

  • Boag G, Yeates GW (2001) The potential impact of the New Zealand flatworm, a predator of earthworms, in Western Europe. Ecol Appl 11:1276–1286

    Article  Google Scholar 

  • Bohlen PJ, Groffman PM, Fahey TJ, Fisk MC, Suarez E, Pelletier DM, Fahey RT (2004) Ecosystem consequences of exotic earthworm invasion of north temperate forests. Ecosystems 7:1–12

    Article  Google Scholar 

  • Bruno JF, Bertness MD (2001) Habitat modification and facilitation in benthic marine communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer, Sunderland, pp 201–218

    Google Scholar 

  • Buchmann SL, Nabhan GP (1996) The forgotten pollinators. Island Press, Washington

    Google Scholar 

  • Byers JE (2000) Effects of body size and resource availability on dispersal in a native and a non-native estuarine snail. J Exp Mar Biol Ecol 248:133–150

    Article  PubMed  Google Scholar 

  • Cadée GC (2001) Sediment dynamics by bioturbating organisms. In: Reise K (ed) Ecological comparisons of sedimentary shores. Ecological studies 151. Springer, Berlin Heidelberg New York, pp 127–148

    Google Scholar 

  • Chapin FS, Walker BH, Hobbs RJ, Hooper JU, Lawton JH, Sala OE, Tilman D (1997) Biotic controls on the functioning of ecosystems. Science 277:500–503

    Article  CAS  Google Scholar 

  • Coleman FC, Williams SL (2002) Overexploiting marine ecosystem engineers: potential consequences for biodiversity. Trends Ecol Evol 17:40–44

    Article  Google Scholar 

  • Crooks JA (1998) Habitat alteration and community-level effects of an exotic mussel, Musculista senhousia. Mar Ecol Prog Ser 162:137–152

    Article  Google Scholar 

  • Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166

    Article  Google Scholar 

  • Crowl TA, McDowell WH, Covich AP, Johnson SL (2001) Freshwater shrimp effects on detrital processing and nutrients in a tropical headwater stream. Ecology 82:775–783

    Google Scholar 

  • Dhillion S (1999) Environmental heterogeneity, animal disturbances, microsite characteristics, and seedling establishment in a Quercus havardii community. Rest Ecol 7:399–406

    Article  Google Scholar 

  • Duffy JE (2002) Biodiversity and ecosystem function: the consumer connection. Oikos 99:201–219

    Article  Google Scholar 

  • Duffy JE, Richardson JP, Canuel EA (2003) Grazer diversity effects on ecosystem functioning in seagrass beds. Ecol Lett 6:637–645

    Article  Google Scholar 

  • Edwards CA (2004) Earthworm ecology, 2nd edn. CRC, Boca Raton

    Google Scholar 

  • Emmerson M, Huxham M (2002) How can marine ecology contribute to the biodiversity-ecosystem functioning debate? In: Loreau M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning. Oxford, New York, pp 139–146

    Google Scholar 

  • Emmerson MC, Solan M, Emes C, Paterson DM, Raffaelli D (2001) Consistent patterns and the idiosyncratic effects of biodiversity in marine ecosystems. Nature 411:73–77

    Article  PubMed  CAS  Google Scholar 

  • Ernest SKM, Brown JH (2001) Homeostasis and compensation: the role of species and resources in ecosystem stability. Ecology 82:2118–2132

    Article  Google Scholar 

  • Flecker AS (1996) Ecosystem engineering by a dominant detritivore in a diverse tropical stream. Ecology 77:1845–1854

    Article  Google Scholar 

  • Fong P, Desmond JS, Zedler JB (1997) The effect of a horn snail on Ulva expansa (Chlorophyta): consumer or facilitator of growth? J Phycol 33:353–359

    Article  Google Scholar 

  • Fournier C, Rosenheim JA, Brodeur J, Laney LO, Johnson MW (2003) Herbivorous mites as ecological engineers: indirect effects on arthropods inhabiting papaya foliage. Oecologia 135:442–450

    PubMed  Google Scholar 

  • Frank DA, Juns MM, Guido DR (2002) Consumer control of grassland plant production. Ecology 83:602–606

    Google Scholar 

  • Gerdol V, Hughes RG (1994) Effect of Corophium volutator on the abundance of benthic diatoms, bacteria and sediment stability in two estuaries in southeastern England. Mar Ecol Prog Ser 114:109–115

    Article  Google Scholar 

  • Grant J, Bathmann UV, Mills EL (1986) The interaction between diatom films and sediment transport. Estuar Coast Shelf Sci 23:225–238

    Article  CAS  Google Scholar 

  • Heck KL Jr, Pennock JR, Valentine JF, Coen LD, Sklenar SA (2000) Effects of nutrient enrichment and small predator density on seagrass ecosystems: an experimental assessment. Limnol Oceanogr 45:1041–1057

    CAS  Google Scholar 

  • Hiatt RW (1948) Biology of the lined shore crab, Pachygrapsus crassipes Randall. Pac Sci 2:134–213

    Google Scholar 

  • Hunt-Joshi TR, Blossey B, Root RB (2004) Root and leaf herbivory on Lythrum salicaria: implications for plant performance and communities. Ecol Appl 14:1574–1589

    Article  Google Scholar 

  • Jensen GC (1995) Pacific coast crabs and shrimps, 2nd edn. Sea Challengers, Petaluma

    Google Scholar 

  • Jones CG, Lawton JH (1995) Linking species and ecosystems. Chapman and Hall, New York

    Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386

    Article  Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957

    Article  Google Scholar 

  • Lee RF, Dornselif B, Gonsoulin F, Tenore K, Hanson R (1981) Fate and effects of a heavy fuel oil spill on a Georgia salt marsh. Mar Environ Res 5:125–143

    Article  CAS  Google Scholar 

  • Lill JT, Marquis RJ (2003) Ecosystem engineering by caterpillars increases insect herbivore diversity on white oak. Ecology 84:682–690

    Article  Google Scholar 

  • Lorenzen CJ (1967) Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol Oceanogr 12:343–346

    CAS  Google Scholar 

  • Machicote M, Branch LC, Villarreal D (2004) Burrowing owls and burrowing mammals: are ecosystem engineers interchangeable as facilitators? Oikos 106:527–535

    Article  Google Scholar 

  • Mahall BE, Park RB (1976) The ecotone between Spartina foliosa Trin. and Salicornia virginica L. in salt marshes of northern San Francisco Bay III Soil aeration and tidal immersion. J Ecol 64:811–820

    Article  Google Scholar 

  • McCloy MJ (1979) Population regulation in the deposit-feeding mesogastropod Cerithidea californica as it occurs in a San Diego salt marsh. MS Thesis, San Diego State University, San Diego

  • Morris RJ, Abbott DP, Haderlie EC (1980) Intertidal invertebrates of California. Stanford University Press, Stanford

    Google Scholar 

  • Page HM (1997) Importance of vascular plant and algal production to macro-invertebrate consumers in a southern California salt marsh. Estuar Coast Shelf Sci 45:823–834

    Article  Google Scholar 

  • Palmer MA, Ambrose RF, Poff NL (1997) Ecological theory and community restoration ecology. Rest Ecol 5:291–300

    Article  Google Scholar 

  • Parsons TR, Strickland JDH (1963) Discussion of spectrophotometric determination of marine plant pigments with revised equations for ascertaining chlorophylls and carotenoids. J Mar Res 21:155–163

    CAS  Google Scholar 

  • Paterson DM (1994) Microbiological mediation of sediment structure and behaviour. In: Stal LJ, Caumette P (eds) Microbial Mats. Nato ASI Series, vol G35. Springer, Berlin Heidelberg New York

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

    Google Scholar 

  • Peterson BJ, Heck KL (1999) The potential for suspension feeding bivalves to increase seagrass productivity. J Exp Mar Biol Ecol 240:37–52

    Article  Google Scholar 

  • Pringle CM, Hemphill N, McDowell WH, Bednarek A, March JG (1999) Linking species and ecosystems: different biotic assemblages cause interstream differences in organic matter. Ecology 80:1860–1872

    Google Scholar 

  • Quammen ML (1984) Predation by shorebirds, fish, and crabs on invertebrates in intertidal mudflats: an experimental test. Ecology 65:529–537

    Article  Google Scholar 

  • Race MS (1982) Competitive displacement and predation between introduced and native mud snails. Oecologia 54:337–347

    Article  Google Scholar 

  • Raffaelli D, Emmerson M, Solan M, Biles C, Paterson D (2003) Biodiversity and ecosystem processes in shallow coastal waters: an experimental approach. J Sea Res 49:133–141

    Article  Google Scholar 

  • Reed CC (1995) Insects surveyed on flowers in native and reconstructed prairies (Minnesota). Restorat Manag Notes 13:210–213

    Google Scholar 

  • Richardson JS, Jackson MJ (2002) Aquatic invertebrates. In: Perrow MR, Davey AJ (eds) Handbook of ecological restoration. Cambridge University Press, Cambridge, pp 300–323

    Google Scholar 

  • Richardson AMM, Swain R, Wong V (1998) Relationship between the crustacean and molluscan assemblages of Tasmanian saltmarshes and the vegetation and soil conditions. Mar Freshwater Res 49:785–799

    Article  Google Scholar 

  • Riera P, Stal LJ, Nieuwenhuize J, Richard P, Blanchard G, Gentil F (1999) Determination of food sources for benthic invertebrates in a salt marsh (Aiguillon Bay, France) by carbon and nitrogen stable isotopes: importance of locally produced sources. Mar Ecol Prog Ser 187:301–307

    Article  CAS  Google Scholar 

  • Ritchie ME, Tilman D, Knops JMH (1998) Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79:165–177

    Google Scholar 

  • Schläpfer F, Schmid B (1999) Ecosystem effects of biodiversity: a classification of hypotheses and exploration of empirical results. Ecol Appl 9:893–912

    Article  Google Scholar 

  • Sousa WP (1993) Size-dependent predation on the salt-marsh snail Cerithidea californica Haldeman. J Exp Mar Biol Ecol 166:19–37

    Article  Google Scholar 

  • Statzner B, Fievet E, Champagne JY, Morel R, Herouin E (2000) Crayfish as geomorhpic agents and ecosystem engineers: biological behavior affects sand and gravel erosion in experimental streams. Limnol Oceanogr 45:1030–1040

    Article  Google Scholar 

  • Sullivan MJ (1999) Applied diatom studies in estuaries and shallow coastal environments. In: Stoermer EF, Smol JP (eds) The diatoms: applications for the environmental and earth sciences. Cambridge University Press, Cambridge, pp 334–351

    Google Scholar 

  • Talley TS, Levin LA (1999) Macrofaunal succession and community structure in Salicornia marshes of southern California. Estuar Coast Shelf Sci 49:713–731

    Article  Google Scholar 

  • Talley TS, Crooks JA, Levin LA (2001) Habitat utilization and alteration by the invasive burrowing isopod, Sphaeroma quoyanum, in California salt marshes. Mar Biol 138:561–573

    Article  Google Scholar 

  • Thompson L, Thomas CD, Radley JMA, Williamson S, Lawton JH (1993) The effect of earthworms and snails in a simple plant community. Oecologia 95:171–178

    Article  Google Scholar 

  • Underwood GJC (1997) Microalgal colonization in a saltmarsh restoration scheme. Estuar Coast Shelf Sci 44:471–481

    Article  CAS  Google Scholar 

  • Whicker AD, Detling JK (1988) Ecological consequences of prairie dog disturbances. BioScience 38:778–785

    Article  Google Scholar 

  • Whitlach RB, Obrebski S (1980) Feeding selectivity and coexistence in two deposit-feeding gastropods. Mar Biol 58:219–225

    Article  Google Scholar 

  • Widdecombe D, Austen MC (1998) Experimental evidence for the role of Brissopsis lyrifera as a critical species in the maintenance of benthic diversity and the modification of sediment chemistry. J Exp Mar Biol Ecol 228:241–255

    Article  Google Scholar 

  • Wilby A, Shachak M, Boeken B (2001) Integration of ecosystem engineering and trophic effects of herbivores. Oikos 92:436–444

    Article  Google Scholar 

  • Willason SW (1981) Factors influencing the distribution and coexistence of Pachygrapsus crassipes and Hemigrapsus oregonensis (Decapoda:Grapsidae) in a California salt marsh. Mar Biol 64:125–133

    Article  Google Scholar 

  • Zedler JB, Callaway JC, Desmond JS, Vivian-Smith G, Williams G, Sullivan G, Brewster AE, Bradshaw BK (1999) Californian salt-marsh vegetation: an improved model of spatial pattern. Ecosystems 2:19–35

    Article  Google Scholar 

  • Zedler JB, Callaway JC, Sullivan GD (2001) Declining biodiversity: why species matter and how their functions might be restored in Californian tidal marshes. Bioscience 51:1005–1017

    Article  Google Scholar 

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Acknowledgements

We thank Wayne Shipman for help with enclosure design, Rich Ambrose, Rick Vance, and Rachel Kennison for assistance with fieldwork, Tom Keeney for site access, and Steve Obrebski for statistical advice. Rick Vance, Rich Ambrose, Phil Rundel, John Bruno, Sarah Lee, and Anna Armitage provided helpful comments. This research was funded by the Association for Women in Science and the US Environmental Protection Agency (fellowship #U915399 to K. Boyer and grant #R827637 to P. Fong). The experiment described herein complied with current laws of the USA.

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Correspondence to Katharyn E. Boyer.

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Communicated by Jim Cronin

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Boyer, K.E., Fong, P. Co-occurrence of habitat-modifying invertebrates: effects on structural and functional properties of a created salt marsh. Oecologia 143, 619–628 (2005). https://doi.org/10.1007/s00442-005-0015-6

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