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
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
Bertness MD (1985) Fiddler crab regulation of Spartina alterniflora production on a New England salt marsh. Ecology 66:1042–1055
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
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
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
Buchmann SL, Nabhan GP (1996) The forgotten pollinators. Island Press, Washington
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
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
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
Coleman FC, Williams SL (2002) Overexploiting marine ecosystem engineers: potential consequences for biodiversity. Trends Ecol Evol 17:40–44
Crooks JA (1998) Habitat alteration and community-level effects of an exotic mussel, Musculista senhousia. Mar Ecol Prog Ser 162:137–152
Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166
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
Dhillion S (1999) Environmental heterogeneity, animal disturbances, microsite characteristics, and seedling establishment in a Quercus havardii community. Rest Ecol 7:399–406
Duffy JE (2002) Biodiversity and ecosystem function: the consumer connection. Oikos 99:201–219
Duffy JE, Richardson JP, Canuel EA (2003) Grazer diversity effects on ecosystem functioning in seagrass beds. Ecol Lett 6:637–645
Edwards CA (2004) Earthworm ecology, 2nd edn. CRC, Boca Raton
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
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
Ernest SKM, Brown JH (2001) Homeostasis and compensation: the role of species and resources in ecosystem stability. Ecology 82:2118–2132
Flecker AS (1996) Ecosystem engineering by a dominant detritivore in a diverse tropical stream. Ecology 77:1845–1854
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
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
Frank DA, Juns MM, Guido DR (2002) Consumer control of grassland plant production. Ecology 83:602–606
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
Grant J, Bathmann UV, Mills EL (1986) The interaction between diatom films and sediment transport. Estuar Coast Shelf Sci 23:225–238
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
Hiatt RW (1948) Biology of the lined shore crab, Pachygrapsus crassipes Randall. Pac Sci 2:134–213
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
Jensen GC (1995) Pacific coast crabs and shrimps, 2nd edn. Sea Challengers, Petaluma
Jones CG, Lawton JH (1995) Linking species and ecosystems. Chapman and Hall, New York
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386
Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957
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
Lill JT, Marquis RJ (2003) Ecosystem engineering by caterpillars increases insect herbivore diversity on white oak. Ecology 84:682–690
Lorenzen CJ (1967) Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol Oceanogr 12:343–346
Machicote M, Branch LC, Villarreal D (2004) Burrowing owls and burrowing mammals: are ecosystem engineers interchangeable as facilitators? Oikos 106:527–535
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
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
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
Palmer MA, Ambrose RF, Poff NL (1997) Ecological theory and community restoration ecology. Rest Ecol 5:291–300
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
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
Peterson BJ, Heck KL (1999) The potential for suspension feeding bivalves to increase seagrass productivity. J Exp Mar Biol Ecol 240:37–52
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
Quammen ML (1984) Predation by shorebirds, fish, and crabs on invertebrates in intertidal mudflats: an experimental test. Ecology 65:529–537
Race MS (1982) Competitive displacement and predation between introduced and native mud snails. Oecologia 54:337–347
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
Reed CC (1995) Insects surveyed on flowers in native and reconstructed prairies (Minnesota). Restorat Manag Notes 13:210–213
Richardson JS, Jackson MJ (2002) Aquatic invertebrates. In: Perrow MR, Davey AJ (eds) Handbook of ecological restoration. Cambridge University Press, Cambridge, pp 300–323
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
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
Ritchie ME, Tilman D, Knops JMH (1998) Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79:165–177
Schläpfer F, Schmid B (1999) Ecosystem effects of biodiversity: a classification of hypotheses and exploration of empirical results. Ecol Appl 9:893–912
Sousa WP (1993) Size-dependent predation on the salt-marsh snail Cerithidea californica Haldeman. J Exp Mar Biol Ecol 166:19–37
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
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
Talley TS, Levin LA (1999) Macrofaunal succession and community structure in Salicornia marshes of southern California. Estuar Coast Shelf Sci 49:713–731
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
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
Underwood GJC (1997) Microalgal colonization in a saltmarsh restoration scheme. Estuar Coast Shelf Sci 44:471–481
Whicker AD, Detling JK (1988) Ecological consequences of prairie dog disturbances. BioScience 38:778–785
Whitlach RB, Obrebski S (1980) Feeding selectivity and coexistence in two deposit-feeding gastropods. Mar Biol 58:219–225
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
Wilby A, Shachak M, Boeken B (2001) Integration of ecosystem engineering and trophic effects of herbivores. Oikos 92:436–444
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
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
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
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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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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DOI: https://doi.org/10.1007/s00442-005-0015-6