, Volume 139, Issue 4, pp 560–567 | Cite as

Upward cascading effects of nutrients: shifts in a benthic microalgal community and a negative herbivore response

  • Anna R. Armitage
  • Peggy Fong
Community Ecology


We evaluated the effects of nutrient addition on interactions between the benthic microalgal community and a dominant herbivorous gastropod, Cerithidea californica (California horn snail), on tidal flats in Mugu Lagoon, southern California, USA. We crossed snail and nutrient (N and P) addition treatments in enclosures on two tidal flats varying from 71 to 92% sand content in a temporally replicated experiment (summer 2000, fall 2000, spring 2001). Diatom biomass increased slightly (~30%) in response to nutrient treatments but was not affected by snails. Blooms of cyanobacteria (up to 200%) and purple sulfur bacteria (up to 400%) occurred in response to nutrient enrichment, particularly in the sandier site, but only cyanobacterial biomass decreased in response to snail grazing. Snail mortality was 2–5 times higher in response to nutrient addition, especially in the sandier site, corresponding to a relative increase in cyanobacterial biomass. Nutrient-related snail mortality occurred only in the spring and summer, when the snails were most actively feeding on the microalgal community. Inactive snails in the fall showed no response to nutrient-induced cyanobacterial growths. This study demonstrated strongly negative upward cascading effects of nutrient enrichment through the food chain. The strength of this upward cascade was closely linked to sediment type and microalgal community composition.


Cerithidea californica Cyanobacteria Diatom Trophic cascade 



We thank Thomas Keeney and the US Navy for providing access to the research site and Brian Dolan and numerous others for field and laboratory assistance. We are indebted to James L. Pinckney and Alyce R. Lee at Texas A&M University for their generosity and time in the use of J. Pinckney’s HPLC apparatus and pigment standards. Many thanks to Richard R. Vance, Richard R. Ambrose, and two anonymous reviewers for helpful comments on an earlier version of the manuscript. This project was funded in part by a UC Coastal Environmental Quality Initiative Graduate Fellowship to A.A. and a grant from the EPA (#R827637) to P.F.


  1. Armitage AR (2003) Community structure and trophic interactions in restored and natural estuarine mudflats: complex trophic cascades and positive and negative effects of nutrients. Ph.D. thesis. University of California, Los AngelesGoogle Scholar
  2. Berman-Frank I, et al (2001) Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 294:1534–1537CrossRefPubMedGoogle Scholar
  3. Byers JE (2000) Differential susceptibility to hypoxia aids estuarine invasion. Mar Ecol Prog Ser 203:123–132Google Scholar
  4. Carpenter SR, Kitchell JF, Hodgson JR (1985) Cascading trophic interactions and lake productivity. Bioscience 35:634–639Google Scholar
  5. Carrick HJ, Lowe RL (1988) Response of Lake Michigan benthic algae to in situ enrichment with silicon, nitrogen, and phosphorus. Can J Fish Aquat Sci 45:271–279Google Scholar
  6. Childs CR, Rabalais NN, Turner RE, Proctor LM (2002) Sediment denitrification in the Gulf of Mexico zone of hypoxia. Mar Ecol Prog Ser 240:285–290Google Scholar
  7. Clarke KD, Knoechel R, Ryan PM (1997) Influence of trophic role and life-cycle duration on timing and magnitude of benthic macroinvertebrate response to whole-lake enrichment. Can J Fish Aquat Sci 54:89–95CrossRefGoogle Scholar
  8. Currin CA, Joye SB, Paerl HW (1996) Diel rates of N2-fixation and denitrification in a transplanted Spartina alterniflora marsh: implications for N-flux dynamics. Estuarine Coastal Shelf Sci 42:597–616CrossRefGoogle Scholar
  9. Decho AW, Castenholz RW (1986) Spatial patterns and feeding of meiobenthic harpacticoid copepods in relation to resident microbial flora. Hydrobiologia 131:87–96Google Scholar
  10. Ferrão-Filho AS, Azevedo SMFO, DeMott WR (2000) Effects of toxic and non-toxic cyanobacteria on the life history of tropical and temperate cladocerans. Freshwater Biol 45:1–19CrossRefGoogle Scholar
  11. Fong P, Donohoe RM, Zedler JB (1993) Competition with macroalgae and benthic cyanobacterial mats limits phytoplankton abundance in experimental microcosms. Mar Ecol Prog Ser 100:97–102Google Scholar
  12. Fulton RS III, Paerl HW (1987) Effects of colonial morphology on zooplankton utilization of algal resources during blue-green algal (Microcystis aeruginosa) blooms. Limnol Oceanogr 32:634–644Google Scholar
  13. Geddes P, Trexler JC (2003) Uncoupling of omnivore-mediated positive and negative effects on periphyton mats. Oecologia 136:585–595CrossRefPubMedGoogle Scholar
  14. Goldfinch AC, Carman KR (2000) Chironomid grazing on benthic microalgae in a Louisiana salt marsh. Estuaries 23:536–547Google Scholar
  15. Hann BJ, Mundy CJ, Goldsborough LG (2001) Snail-periphyton interactions in a prairie lacustrine wetland. Hydrobiology 457:167–175CrossRefGoogle Scholar
  16. Hauxwell J, McClelland J, Behr PJ, Valiela I (1998) Relative importance of grazing and nutrient controls of macroalgal biomass in three temperate shallow estuaries. Estuaries 21:347–360Google Scholar
  17. Javor BJ, Castenholz RW (1984) Invertebrate grazers of microbial mats, Laguna Guerrero Negro, Mexico. In: Cohen Y, Castenholz RW, Halvorson HO (eds) Microbial mats: stromatolites, vol 3. Alan R. Liss, New York, pp 85–94Google Scholar
  18. Keating KI (1978) Blue-green algal inhibition of diatom growth transition from mesotrophic to eutrophic community structure. Science 199:971–973Google Scholar
  19. Kuffner IB, Paul VJ (2001) Effects of nitrate, phosphate and iron on the growth of macroalgae and benthic cyanobacteria from Cocos Lagoon, Guam. Mar Ecol Prog Ser 222:63–72Google Scholar
  20. Lafferty KD (1993) Effects of parasitic castration on growth, reproduction and population dynamics of the marine snail Cerithidea californica. Mar Ecol Prog Ser 96:229–237Google Scholar
  21. Lafferty KD, Morris AK (1996) Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77:1390–1397Google Scholar
  22. Lorenzen CJ (1967) Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol Oceanogr 12:343–346Google Scholar
  23. McQueen DJ, Post JR, Mills EL (1986) Trophic relationships in freshwater pelagic ecosystems. Can J Fish Aquat Sci 43:1571–1581Google Scholar
  24. Menge BA (1992) Community regulation: under what conditions are bottom-up factors important on rocky shores? Ecology 73:755–765Google Scholar
  25. Menge BA (2000) Top-down and bottom-up community regulation in marine rocky intertidal habitats. J Exp Mar Biol Ecol 250:257–289CrossRefPubMedGoogle Scholar
  26. Meyer-Reil L-A, Köster M (2000) Eutrophication of marine waters: effects on benthic microbial communities. Mar Pollut Bull 41:255–263CrossRefGoogle Scholar
  27. Micheli F (1999) Eutrophication, fisheries, and consumer-resource dynamics in marine pelagic ecosystems. Science 285:1396–1398CrossRefPubMedGoogle Scholar
  28. Miller MW, Hay ME, Miller SL, Malone D, Sotka EE, Szmant AM (1999) Effects of nutrients versus herbivores on reef algae: a new method for manipulating nutrients on coral reefs. Limnol Oceanogr 44:1847–1861Google Scholar
  29. O’Neil JM (1999) Grazer interactions with nitrogen-fixing marine cyanobacteria: adaptation for N-acquisition? Bull Inst Oceanogr 19:293–317Google Scholar
  30. Onuf CP (1987) The ecology of Mugu Lagoon, California: an estuarine profile. 85 (7.15). U.S. Fish and Wildlife Service, Washington, D.C.Google Scholar
  31. Overmann J, Hall KJ, Northcote TG, Ebenhöh W, Chapman MA, Beatty T (1999) Structure of the aerobic food chain in a meromictic lake dominated by purple sulfur bacteria. Arch Hydrobiol 144:127–156Google Scholar
  32. Paerl HW (1996) A comparison of cyanobacterial bloom dynamics in freshwater, estuarine and marine environments. Phycologia 35:25–35Google Scholar
  33. Paerl HW, Fitzpatrick M, Bebout BM (1996) Seasonal nitrogen fixation dynamics in a marine microbial mat: potential roles of cyanobacteria and microheterotrophs. Limnol Oceanogr 41:419–427Google Scholar
  34. Page HM (1997) Importance of vascular plant and algal production to macro-invertebrate consumers in a southern California salt marsh. Estuarine Coastal Shelf Sci 45:823–834CrossRefGoogle Scholar
  35. Piehler MF, Currin CA, Cassanova R, Paerl HW (1998) Development and N2-fixing activity of the benthic microbial community in transplanted Spartina alterniflora marshes in North Carolina. Restor Ecol 6:290–296Google Scholar
  36. Pinckney J, Piceno Y, Lovell CR (1994) Short-term changes in the vertical distribution of benthic microalgal biomass in intertidal muddy sediments. Diatom Res 9:143–153Google Scholar
  37. Pinckney J, Paerl HW, Fitzpatrick M (1995) Impacts of seasonality and nutrients on microbial mat community structure and function. Mar Ecol Prog Ser 123:207–216Google Scholar
  38. Pinckney JL, Paerl HW, Harrington MB (1999) Responses of the phytoplankton community growth rate to nutrient pulses in variable estuarine environments. J Phycol 35:1455–1463CrossRefGoogle Scholar
  39. Posey M, Powell C, Cahoon L, Lindquist D (1995) Top down vs. bottom up control of benthic community composition on an intertidal tideflat. J Exp Mar Biol Ecol 185:19–31CrossRefGoogle Scholar
  40. Posey MH, Alphin TD, Cahoon LB, Lindquist DG, Mallin MA, Nevers MB (2002) Top-down versus bottom-up limitation in benthic infaunal communities: direct and indirect effects. Estuaries 25:999–1014Google Scholar
  41. Race MS (1981) Field ecology and natural history of Cerithidea californica (Gastropoda: Prosobranchia) in San Francisco Bay. Veliger 24:18–27Google Scholar
  42. Sardá R, Valiela I, Foreman K (1996) Decadal shifts in a salt marsh macroinfaunal community in response to sustained long-term experimental nutrient enrichment. J Exp Mar Biol Ecol 205:63–81CrossRefGoogle Scholar
  43. Sommer U (1997) Selectivity of Idothea chelipes (Crustacea: Isopoda) grazing on benthic microlagae. Limnol Oceanogr 42:1622–1628Google Scholar
  44. Sommer U (2001) Reversal of density dependence of juvenile Littorina littorea (Gastropoda) growth in response to periphyton nutrient status. J Sea Res 45:95–103CrossRefGoogle Scholar
  45. Sullivan MJ, Currin CA (2000) Community structure and functional dynamics of benthic microalgae in salt marshes. In: Weinstein MP, Kreeger DA (eds) Concepts and controversies in tidal marsh ecology. Kluwer Academic, Dordrecht, The Netherlands, pp 81–106Google Scholar
  46. Sullivan MJ, Moncreiff CA (1990) Edaphic algae are an important component of salt marsh food-webs: evidence from multiple stable isotope analyses. Mar Ecol Prog Ser 62:149–160Google Scholar
  47. Sweeney RA (1989) Generic combustion method for determination of crude protein in feeds: collaborative study. J Assoc Off Anal Chem 72:770–774PubMedGoogle Scholar
  48. Thacker RW, Ginsburg DW, Paul VJ (2001) Effects of herbivore exclusion and nutrient enrichment on coral reef macroalgae and cyanobacteria. Coral Reefs 19:318–329CrossRefGoogle Scholar
  49. Underwood GJC (1997) Microalgal colonization in a saltmarsh restoration scheme. Estuarine Coastal Shelf Sci 44:471–481CrossRefGoogle Scholar
  50. Valiela I, McClelland J, Hauxwell J, Behr PJ, Hersh D, Foreman K (1997) Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnol Oceanogr 42:1105–1118Google Scholar
  51. Van Raalte CD, Valiela I, Teal JM (1976) Production of epibenthic salt marsh algae: light and nutrient limitation. Limnol Oceanogr 21:862–872Google Scholar
  52. Whitlatch RB, Obrebski S (1980) Feeding selectivity and coexistence in two deposit feeding gastropods. Mar Biol 58:219–226Google Scholar
  53. Williams SL, Ruckelshaus MH (1993) Effects of nitrogen availability and herbivory on eelgrass (Zostera marina) and epiphytes. Ecology 74:904–918Google Scholar
  54. Wiltse WI, Foreman KH, Teal JT, Valiela I (1984) Effects of predators and food resources on the macrobenthos of salt marsh creeks. J Mar Res 42:923–942Google Scholar
  55. Zedler JB (1980) Algal mat productivity: comparisons in a salt marsh. Estuaries 3:122–131Google Scholar
  56. Zedler JB (1996) Coastal mitigation in southern California: the need for a regional restoration strategy. Ecol Appl 6:84–93Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of Organismic Biology, Ecology and EvolutionUniversity of California Los AngelesLos AngelesUSA
  2. 2.Southeast Environmental Research Center—OE 148Florida International UniversityMiamiUSA

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