, Volume 129, Issue 1, pp 121–138

Time scales of change in the San Francisco Bay benthos

  • Frederic H. Nichols
  • Janet K. Thompson


Results from multi-year investigations in the San Francisco Bay estuary show that large abundance fluctuations within benthic macroinvertebrate populations reflect both (1) within-year periodicity of reproduction, recruitment, and mortality that is not necessarily coincident with seasonal changes of the environment (e.g., the annual temperature cycle), and (2) aperiodic density changes (often larger than within-year fluctuations) following random perturbations of the environment.

Density peaks of the small, short-lived estuarine invertebrates that comprise the vast majority of individuals in the bay's relatively homogeneous benthic community normally occur between spring and autumn depending on the species, in large part a reflection of reproductive periodicity. However, because mild winters permit reproductive activity in some of the common species throughout much of the year, other factors are important to within-year density fluctuations in the community. Seasonally predictable changes in freshwater inflow, wind and tidal mixing, microalgal biomass, and sediment erosion/deposition patterns all contribute to observed seasonal changes in abundance. For example, the commonly observed decline in abundance during winter reflects both short-lived species that die after reproducing and the stress of winter conditions (e.g., inundation by less saline, sediment-laden water and the decline in both planktonic and benthic algal biomass — a direct source of food for the shallow-water benthos). On the other hand, data from several studies suggest that observed ‘recruitment’ and ‘mortality’ may in fact be the migration of juveniles and adults to and from study sites. For example, the common amphipod Ampelisca abdita apparently moves from shallow to deep water, or from up-estuary to down-estuary locations, coincident with periods of high river runoff in winter. Growth of individuals within the few studied species populations is also highly seasonal, and appears to be coincident with seasonal increases in the abundance of planktonic and/or benthic microalgae.

Two multi-year studies have shown that, in addition to within-year periodicity, major restructuring of the benthic community can occur as a result of anomalous (usually climate-related) perturbations of the benthic habitat. For example, during wet years freshwater-intolerant species disappear from the upper part of the estuary and from shallow areas of the bay. During a two-year drought these same species colonized the extreme upper end of the estuary in large numbers. Other aperiodic perturbations include localized instances of sediment erosion or deposition and algal mat accumulations that greatly depress abundance. Additionally, there is evidence (observations that the clam Macoma balthica establishes large populations only when the amphipod A. abdita is not abundant) that species interactions can contribute greatly to interannual variations. Thus, while community composition may change little over the long term, year-to-year predictability of species abundances is low.


San Francisco Bay Benthos estuarine estuarine fauna long term changes river flow 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anderlini, V. C., J. W. Chapman, D. C. Girvin, S. J. McCormick, A. S. Newton & R. W. Risebrough, 1975. Heavy metal uptake study, final report, Appendix H, Pollutant uptake study, U.S. Army Corps of Engineers dredge disposal study, San Francisco Bay and estuary. San Francisco, Calif., 89 pp.Google Scholar
  2. Anderson, F. E., L. Black, L. M. Mayer & L. E.Watling, 1981a. A temporal and spatial study of mudflat texture. Northeastern Geol. 3: 184–191.Google Scholar
  3. Anderson, F. E., L. Black, L. E. Watling, W. Mook & L. M.Mayer, 1981b. A temporal and spatial study of mudflat erosion and deposition. J. sed. Petrol. 51: 729–736.Google Scholar
  4. Andrews, M. J. & D. G. Rickard, 1980. Rehabilitation of the inner Thames estuary. Mar. Pollution Bull. 11: 327–332.Google Scholar
  5. Arntz, W. E. & H. Rumohr, 1982. An experimental study of macrobenthic colonization and succession, and the importance of seasonal variation in temperate latitudes. J. exp. mar. Biol. Ecol. 64: 17–45.Google Scholar
  6. Ball, M. D. & J. F. Arthur, 1981. Phytoplankton settling rates — a major factor in determining estuarine dominance (abs.). Estuaries 4: 246.Google Scholar
  7. Beukema, J. J., G. C. Cadee & J. J. M. Jansen, 1977. Variability of growth rate of Macoma balthica (L.) in the Wadden Sea in relation to availability of food. In B. F. Keegan, P. O. Ceidigh & P. J. S. Boaden(eds.), Biology of benthic organisms. Pergamon Press, Oxford: 69–77.Google Scholar
  8. Beukema, J. J., 1979. Biomass and species richness of the macrobenthic animals living on a tidal flat area in the Dutch Wadden Sea: effects of a severe winter. Neth. J. Sea Res. 13: 203–223.Google Scholar
  9. Boesch, D. F., R. J. Diaz & R. W. Virnstein, 1976a. Effects of tropical storm Agnes on soft-bottom macrobenthic communities of the James and York estuaries and the lower Chesapeake Bay. Chesapeake Sci. 17: 246–259.Google Scholar
  10. Boesch, D. F., M. L. Wass & R. W. Virnstein, 1976b. The dynamics of estuarine benthic communities. In M. Wiley (ed.), Estuarine processes, V. 1. Academic Press, New York: 177–196.Google Scholar
  11. Boesch, D. F. & R. Rosenberg, 1982. Response to stress in marine benthic communities. In G. W. Barrett & R. Rosenberg (eds.), Stress effects on natural ecosystems. John Wiley, New York: 179–200.Google Scholar
  12. Buchanan, J. B., M. Sheader & P. F. Kingston, 1978. Sources of variability in the benthic macrofauna off the south Northumberland coast, 1971–1976. J. mar. biol. Ass. U.K. 58: 191–209.Google Scholar
  13. California Department of Water Resources, 1982. Sacramento — San Joaquin Delta water quality surveillance program 1981 — monitoring results pursuant to conditions set forth in Delta Water Rights Decision 1485. v. 3, Sacramento, Calif. 313 pp.Google Scholar
  14. Carlton, J. T., 1979a. Introduced invertebrates of San Francisco Bay. In T. J.Conomos (ed.), San Francisco Bay — the urbanized estuary. Pacific Division, Am. Ass. Adv. Sci., San Francisco, Calif: 427–444.Google Scholar
  15. Carlton, J. T., 1979b. History, biogeography, and ecology of the introduced marine and estuarine invertebrates of the Pacific coast of North America. Ph.D. Thesis, Univ. California, Davis, 904 pp.Google Scholar
  16. Cloern, J. E., 1982. Does the benthos control phytoplankton biomass in south San Francisco Bay?Mar. Ecol. Prog. Ser. 9: 191–202.Google Scholar
  17. Cloern, J. E., A. E. Alpine, B. E. Cole, R. L. J. Wong, J. F. Arthur & M. D. Ball, 1983. River discharge controls phytoplankton dynamics in the northern San Francisco Bay Estuary. Estuar. coast. shelf Sci. 16: 415–429.Google Scholar
  18. Cloern, J. E., B. E. Cole, R. L. J. Wong & A. E. Alpine, 1985. Temporal dynamics of estuarine phytoplankton: a case study of San Francisco Bay. Hydrobiologia (this volume).Google Scholar
  19. Cole, B. E. & J. E. Cloern, 1984. Significance of biomass and light availability to phytoplankton productivity in San Francisco Bay. Mar. Ecol. Prog. Ser. 17: 15–24.Google Scholar
  20. Conomos, T. J. & D. H. Peterson, 1977. Suspended-particle transport and circulation in San Francisco Bay: an overview. In M. Wiley (ed.), Estuarine Processes 2. Academic Press, New York: 82–97.Google Scholar
  21. Crisp, D. J., 1964. The effects of the severe ice winter of 1962–1963 on marine life in Britain. J. Anim. Ecol. 33: 165–210.Google Scholar
  22. Crisp, D. J., 1971. Energy flow measurements. In N. A. Holme & A. D. McIntyre (eds.), Methods for the study of marine benthos. Int. Biol. Prog. Handbook 16: 197–279.Google Scholar
  23. Cullinane, J. P. & P. M. Whelan, 1983. An example of drastic natural changes in the intertidal biota and the implications for monitoring programmes. Estuar. coast. shelf Sci. 17: 479–481.Google Scholar
  24. Dauer, D. M., 1984. High resilience to disturbance of an estuarine polychaete community. Bull. mar. Sci. 34: 170–174.Google Scholar
  25. DeWilde, P. A. W. J., 1975. Influence of temperature on behavior, energy metabolism, and growth of Macoma balthica (L.). In H. Barnes (ed.), Proc. 9th Europ. Mar. Biol. Symp.: 239–256.Google Scholar
  26. Diaz, R. J., 1984. Short term dynamics of the dominant annelids in a polyhaline temperate estuary. Hydrobiologia115: 153–158.Google Scholar
  27. Eagle, R. A., 1975. Natural fluctuations in a soft bottom benthic community. J. mar. biol. Ass. U.K. 55: 865–878.Google Scholar
  28. Eckman, J. E., 1979. Small-scale patterns and processes in a soft-substratum, intertidal community. J. mar. Res. 37: 437–457.Google Scholar
  29. Eckman, J. E., 1983. Hydrodynamic processes affecting benthic recruitment. Limnol. Oceanogr. 28: 241–257.Google Scholar
  30. Einstein, H. A. & R. B. Krone, 1961. Estuarial sediment transport patterns. J. am. Soc. civil Eng. H 12: 51–59.Google Scholar
  31. Filice, F. P., 1958. Invertebrates from the estuarine portion of San Francisco Bay and some factors influencing their distributions. Wasmann J. Biol. 16: 159–211.Google Scholar
  32. Foe, C. & A. Knight, 1985. A thermal energy budget for juvenile Corbicula fluminea. Hydrobiologia (in press).Google Scholar
  33. Fuller, C. C., 1982. The use of Pb-210, Th-234 and Cs-137 as tracers of sedimentary processes in San Francisco Bay, California. M.S. Thesis, Univ. Southern California, Los Angeles, 251 pp.Google Scholar
  34. Gallagher, E. D., P. A. Jumars & D. D. Trueblood, 1983. Facilitation of soft-bottom benthic succession by tube builders. Ecology 64: 1200–1216.Google Scholar
  35. Giese, A. C., 1959. Comparative physiology: annual reproductive cycles of marine invertebrates. Ann. Rev. Physiol. 21: 547–576.Google Scholar
  36. Goldman, H. B., 1967. Salt, sand and shells — mineral resources of San Francisco Bay. San Francisco Bay Conservation and Development Commission Rep. San Francisco, Calif. 28 pp.Google Scholar
  37. Grant, J., 1981. Sediment transport and disturbance on an intertidal sandflat: infaunal distribution and recolonization. Mar. Ecol. Prog. Ser. 6: 249–255.Google Scholar
  38. Grassle, J. F. & J. P. Grassle, 1974. Opportunistic life histories and genetic systems in marine benthic polychaetes. J. mar. Res. 32: 253–284.Google Scholar
  39. Hammond, D. E. & C. Fuller, 1979. The use of radon-222 to estimate benthic exchange and atmospheric exchange rates in San Francisco Bay. In T. J. Conomos (ed.), San Francisco Bay-the urbanized estuary. Pacific Division, Am. Ass. Adv. Sci., San Francisco, Calif: 213–230.Google Scholar
  40. Henderson, A. R., 1984. Long term monitoring of the macrobenthos of the upper Clyde estuary. Wat. Sci. Tech. 16: 359–373.Google Scholar
  41. Holland, A. F., 1985. Long-term variation of macrobenthos in a mesohaline region of Chesapeake Bay. Estuaries (in press)Google Scholar
  42. Horne, A. J. & A. Nonomura, 1976. Drifting macroalgae in estuarine water: interactions with salt marsh and human communities. Univ. California (Berkeley) Sanitary Engineering Research Laboratory Rep. 76-3, 76 pp.Google Scholar
  43. Jones, M. L., 1961. A quantitative evaluation of the benthic fauna off Point Richmond, California. Univ. California Publ. Zool. 67: 219–320.Google Scholar
  44. Jones and Stokes Associates, Inc. 1980. Chapter 4, Population — life history survey. In Predischarge phase of the local effects monitoring program, final report. Prepared for West Contra Costa County Sanitary District. Sacramento, Calif.: 91–107.Google Scholar
  45. Josselyn, M. N. & J. A. West, 1985. The distribution and temporal dynamics of the estuarine macroalgal community of San Francisco Bay. Hydrobiologia (this volume).Google Scholar
  46. Kinnetic Laboratories Inc., 1983. Life history analysis of Ampelisca milleri. Final Report — Predischarge Monitoring Program. East Bay Dischargers Authority, San Lorenzo, Calif., 173 pp.Google Scholar
  47. Klingeman, P. C. & W. J. Kaufman, 1963. Transport of radionuclides with San Francisco Bay sediments, progress report, 1961–62 water year. Univ. California (Berkeley) Sanitary Engineering Research Laboratory, Berkeley, Calif., 70 pp.Google Scholar
  48. Klingeman, P. C. & W. J. Kaufman, 1965. Transport of radionuclides with suspended sediment in estuarine systems. Univ. California (Berkeley) Sanitary Engineering Research Laboratory Rep. 65-17, 222 pp.Google Scholar
  49. Knight, A. W., J. W. Sharp & R. M. Sitts, 1980. Trophic relationships of detritus in the Sacramento — San Joaquin Delta Estuary. Univ. California (Davis) Department of Land, Air and Water Resources, Water Science and Engineering Paper 4510, 185 pp.Google Scholar
  50. Langlois, G. W., 1980. Aspects of the population biology of the ribbed mussel, Ischadium demissum, in a South Francisco Bay salt marsh. M.S. Thesis, Calif. State Univ. Hayward. 95 pp.Google Scholar
  51. Laws, R. A., 1983. Quaternary diatom floras and Pleistocene paleogeography of San Francisco Bay. Ph.D. Thesis, Univ. California, Berkeley. 352 pp.Google Scholar
  52. Levin, L. A., 1981. Dispersion, feeding behavior and competition in two spionid polychaetes. J. mar. Res. 39: 99–117.Google Scholar
  53. Liu, D. H. W., K. D. Martin & C. R. Norwood, 1975. San Francisco Bay benthic community study — technical evaluation, final report. Appendix D, biological community study, U.S. Army Corps of Engineers dredge disposal study, San Francisco Bay and estuary. San Francisco, Calif., 244 pp.Google Scholar
  54. Luoma, S. N., D. Cain & C. Johansson, 1985. Temporal fluctuations of silver, copper and zinc in the bivalve Macoma balthica in South San Francisco Bay. Hydrobiologia (this volume).Google Scholar
  55. McCall, P. L., 1977. Community patterns and adaptive strategies of the infaunal benthos of Long Island Sound. J. mar. Res. 35: 221–266.Google Scholar
  56. Miller, D. C., P. A. Jumars & A. R. M. Norwell, 1984. Effects of sediment transport on deposit feeding: scaling arguments. Limnol. Oceanogr. 29: 1202–1217.Google Scholar
  57. Mills, E. L., 1967. The biology of an ampeliscid amphipod crustacean sibling species pair. J. Fish Res. Bd Can. 24: 305–355.Google Scholar
  58. Naylor, E. & R. G. Hartnoll, 1979. Cyclic phenomena in marine plants and animals. Oxford, Pergamon Press, 477 pp.Google Scholar
  59. Nichols, F. H., 1975. Dynamics and energetics of three deposit-feeding benthic invertebrate populations in Puget Sound, Washington. Ecol. Monogr. 45: 57–82.Google Scholar
  60. Nichols, F. H., 1979. Natural and anthropogenic influences on benthic community structure in San Francisco Bay. In T. J. Conomos (ed.), San Francisco Bay — the urbanized estuary. Pacific Division, Am. Ass. Adv. Sci., San Francisco, Calif. 409–426.Google Scholar
  61. Nichols, F. H., 1985a. Abundance fluctuations among benthic invertebrates in two Pacific estuaries. Estuaries 8: 136–144.Google Scholar
  62. Nichols, F. H., 1985b. Increased benthic grazing: an alternative explanation for low phytoplankton biomass in northern San Francisco Bay during the 1976–77 drought. Estuar. coast. shelf Sci. (in press).Google Scholar
  63. Nichols, F. H. & J. K. Thompson, 1982. Seasonal growth in the bivalve Macoma balthica near the southern limit of its range Estuaries 5: 110–120.Google Scholar
  64. Nichols, F. H. & J. K. Thompson, 1985. Persistence of an introduced mudflat community in South San Francisco Bay, California. Mar. Ecol. Prog. Ser. (in press).Google Scholar
  65. Nixon, S. W., 1980. Between coastal marshes and coastal waters — a review of twenty years of speculation and research on the role of salt marshes in estuarine productivity and water chemistry. In P. Hamilton & K. B. MacDonald (eds.), Estuarined and wetland processes. Plenum, New York: 437–525.Google Scholar
  66. Officer, C. B., R. B. Biggs, J. L. Taft, L. E. Cronin, M. A. Tyler & W. R. Boynton, 1984. Chesapeake Bay anoxia: origin, development, and significance. Science 223: 22–27.Google Scholar
  67. Painter, R. E., 1966. Zoobenthos of San Pablo and Suisun Bays. Calif. Dept. Fish and Game, Fish Bull. 133: 40–56.Google Scholar
  68. Pearson, T. H. & R. Rosenberg, 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr. Mar. Biol. annu. Rev. 16: 229–311.Google Scholar
  69. Peterson, D. H., T. J. Conomos, W. W. Broenkow & P. C. Doherty, 1975. Location of the non-tidal current null zone in northern San Francisco Bay. Estuar. coast. mar. Sci. 3: 1–11.Google Scholar
  70. Rachor, E. & S. A. Gerlach, 1978. Changes of macrobenthos in a sublittoral sand area of the German Bight, 1967 to 1975. Rapp. P.-v. Reun. Cons. int. Explor. Mer 172: 418–431.Google Scholar
  71. Rees, E. I. S., A. Nicolaidou & P. Laskaridou, 1977. The effects of storms on the dynamics of shallow water benthic associations. In B. F. Keegan, P. O. Ceidigh & P. J. S. Boaden (eds.), Biology of benthic organisms. Pergamon, Oxford: 465–474.Google Scholar
  72. Rhoads, D. C., K. Tenore & M. Browne, 1975. The role of resuspended bottom mud in nutrient cycles of shallow embayments. In L. E. Cronin (ed.), Estuarine Research. I. Chemistry, biology, and the estuarine system. Academic Press, New York: 563–579.Google Scholar
  73. Roman, M. R. & K. R. Tenore, 1978. Tidal resuspension in Buzzards Bay, Massachusetts. I. Seasonal changes in the resuspension of organic carbon and chlorophyll a. Est. coast. mar. Sci. 6: 37–46.Google Scholar
  74. Rubin, D. M. & D. S. McCulloch, 1979. The movement and equilibrium of bedforms in central San Francisco Bay. In T. J.Conomos (ed.), San Francisco Bay —he urbanized estuary. Pacific Division, Am. Ass. Adv. Sci., San Francisco, Calif: 97–113.Google Scholar
  75. Santos, S. L. & S. A. Bloom, 1983. Evaluation of succession in an estuarine macrobenthic soft-bottom community near Tampa, Florida. Int. Revue ges. Hydrobiol. 68: 617–632.Google Scholar
  76. Sastry, A. N., 1975. Physiology and ecology of reproduction in marine invertebrates. In F. J. Vernberg (ed.), Physiological ecology of estuarine organisms. Belle W. Baruch Library in Marine Sci. 3. Univ. South Carolina Press: 279–299.Google Scholar
  77. Schneider, M. R., 1976. Population of the symbiotic marine isopods, Sphaeroma quoyana and Iais california. M.S. Thesis, San Francisco State Univ., Calif. 85 pp.Google Scholar
  78. Shulenberger, E., 1971. Responses of Gemma gemma (Mollusca: Pelecypoda) to a catastrophic burial. Veliger 13: 163–170.Google Scholar
  79. Segerstråle, S. G., 1973. Results of bottom fauna sampling in certain localities in the Tvarminne area (inner Baltic), with special reference to the so-called Macoma-Pontoporeia theory. Commentationes Biologicae67: 3–12.Google Scholar
  80. Storrs, P. N., E. A. Pearson & R. E. Selleck, 1966. A comprehensive study of San Francisco Bay, final report. 5. Summary of physical, chemical, and biological water and sediment data. University of California (Berkeley) Sanitary Engineering Research Laboratory Rep. 67(2), 140 pp.Google Scholar
  81. Storrs, P. N., R. E. Selleck & E. A. Pearson, 1963. A comprehensive study of San Francisco Bay, 1961–62. Univ. California (Berkeley) Sanitary Engineering Research Laboratory Rep. 63-3, 221 pp.Google Scholar
  82. Storrs, P. N., R. E. Selleck & E. A. Pearson, 1965. A comprehensive study of San Francisco Bay 1963–64. Univ. California (Berkeley) Sanitary Engineering Research Laboratory Rep. 65-1, 181 pp.Google Scholar
  83. Taghon, G. L., A. R. M. Nowell & P. A. Jumars, 1980. Induction of suspension feeding in spionid polychaetes by high particulate fluxes. Science 210: 562–564.Google Scholar
  84. Thistle, D., 1981. Natural physical disturbances and communities of marine soft bottoms. Mar. Ecol. Prog. Ser. 6: 223–228.Google Scholar
  85. Thompson, J. K., 1979. Population dynamics and sediment relations of Gemma gemma in San Francisco Bay. M.S. Thesis, San Francisco State Univ., San Francisco, Calif., 139 pp.Google Scholar
  86. Thompson, J. K., 1982. Population structure of Gemma gemma in South San Francisco Bay, with a comparison to some northeastern United States estuarine populations. Veliger 24: 281–290.Google Scholar
  87. Thompson, J. K. & F. H. Nichols, 1981. Benthic macrofaunal biomass of San Francisco Bay, California: January/February and August 1973. U.S. geol. Survey Open-File Rep. 81–1331, Menlo Park, Calif. 39 pp.Google Scholar
  88. Thompson, J. K., F. H. Nichols & S. M. Wienke, 1981. Distribution of benthic chlorophyll in San Francisco Bay, California, February 1980–February 1981. U.S. geol. Survey Open File Rep. 81–1134, Menlo Park, Calif. 36 pp.Google Scholar
  89. Walters, R. A., R. T. Cheng & T. J. Conomos, 1985. Time scales of circulation and mixing processes of San Francisco Bay waters. Hydrobiologia (this volume).Google Scholar
  90. Watling, L., 1975. Analysis of structural variations in a shallow estuarine deposit-feeding community. J. exp. mar. Biol. Ecol. 19: 275–313.Google Scholar
  91. Whitlatch, R. B., 1980. Patterns of resource utilization and coexistence in marine intertidal deposit-feeding communities. J. mar. Res. 38: 743–765.Google Scholar
  92. Wilson, D. P., 1955. The role of micro-organisms in the settlement of Ophelia bicornis Savigny. J. mar. biol. Ass. U.K. 34: 531–543.Google Scholar
  93. Wolff, W. J., 1978. The degradation of ecosystems in the Rhine. In M. W. Holdgate & M. J. Woodman (eds.), the breakdown and restoration of ecosystems. Plenum Press, New York: 169–191.Google Scholar
  94. Woodin, S. A., 1976. Adult-larval interactions in dense infaunal assemblages: patterns of abundance. J. mar. Res. 34: 25–41.Google Scholar
  95. Zajac, R. N. & R. B. Whitlatch, 1982a. Responses of estuarine infauna to disturbance. I. Spatial and temporal variation in initial recolonization. Mar. Ecol. Prog. Ser. 10: 1–14.Google Scholar
  96. Zajac, R. N. & R. B. Whitlatch, 1982b. Responses of estuarine infauna to disturbance. II. Spatial and temporal variation of succession. Mar. Ecol. Prog. Ser. 10: 15–27.Google Scholar
  97. Ziegelmeier, E., 1978. Macrobenthos investigations in the eastern part of the German Bight from 1950 to 1974. Rapp. P.-v. Reun. Cons. int. Explor. Mer. 172: 432–444.Google Scholar

Copyright information

© Dr W. Junk Publishers 1985

Authors and Affiliations

  • Frederic H. Nichols
    • 1
  • Janet K. Thompson
    • 1
  1. 1.U.S. Geological SurveyMenlo ParkUSA

Personalised recommendations