Estuaries and Coasts

, Volume 42, Issue 1, pp 218–236 | Cite as

Spatial Subsidies and Mortality of an Estuarine Copepod Revealed Using a Box Model

  • Wim J. KimmererEmail author
  • Edward S. Gross
  • Anne M. Slaughter
  • John R. Durand


Mortality of planktonic populations is difficult to determine because assumptions of the methods are rarely met, more so in estuaries where tidal exchange ensures violation of the assumption of a closed or spatially uniform population. Estuarine plankton populations undergo losses through movement from productive regions, creating a corresponding subsidy to regions that are less productive. We estimated mortality rates of the copepod Pseudodiaptomus forbesi in the San Francisco Estuary using a vertical-life-table approach with a Bayesian estimation method, combined with estimates of spatial subsidies and losses using a spatial box model with salinity-based boundaries. Data came from a long-term monitoring program and from three sample sets for 1991–2007 and 2010–2012. A hydrodynamic model coupled with a particle-tracking model supplied exchange rates between boxes and from each box to several sinks. In situ mortality, i.e., mortality corrected for movement, was highly variable. In situ mortality of adults was high (means by box and sampling program 0.1–0.9 day−1) and appeared invariant with salinity or year. In situ mortality of nauplii and copepodites increased from fresh (~ 0) to brackish water (means 0.4–0.8 day−1), probably because of consumption by clams and predatory copepods in brackish water. High mortality in the low-salinity box was offset by a subsidy which increased after 1993, indicating an increase in mortality. Our results emphasize the importance of mortality and spatial subsidies in structuring populations. Mortality estimates of estuarine plankton are feasible with sufficient sampling to overcome high variability, provided adjustments are made to account for movement.


Pseudodiaptomus forbesi Population dynamics Estuarine circulation Gross Exchange Matrix Bayesian analysis San Francisco Estuary 



We thank K. Kayfetz, R. Vogt, M. Esgro, R. duMais, and V. Greene for assistance in the field, R. Baxter at CDFW for providing boats and operators, A. Hennessy and K. Hieb at CDFW for providing IEP Zooplankton Monitoring Program samples for re-analysis, M. MacWilliams for providing hydrodynamic model output, and M. Weaver, A. Hirst, and an anonymous reviewer for helpful comments.

Funding Information

Financial support was provided by Delta Science Program Grant SCI-05-C107, California Department of Water Resources Agreement 4600007494 and U.S. Bureau of Reclamation Agreement R10AC20074.

Supplementary material

12237_2018_436_MOESM1_ESM.docx (41 kb)
ESM 1 (DOCX 41 kb)


  1. Aksnes, D.L., and M.D. Ohman. 1996. A vertical- life- table approach to zooplankton mortality estimation. Limnology and Oceanography 41: 1461–1469.CrossRefGoogle Scholar
  2. Alpine, A.E., and J.E. Cloern. 1992. Trophic interactions and direct physical effects control phytoplankton biomass and production in an estuary. Limnology and Oceanography 37: 946–955.CrossRefGoogle Scholar
  3. Barlow, J.P. 1955. Physical and biological processes determining the distribution of zooplankton in a tidal estuary. Biological Bulletin 109: 211–225.CrossRefGoogle Scholar
  4. Batchelder, H.P., C.A. Edwards, and T.M. Powell. 2002. Individual-based models of copepod populations in coastal upwelling regions: implications of physiologically and environmentally influenced diel vertical migration on demographic success and nearshore retention. Progress in Oceanography 53: 307–333.CrossRefGoogle Scholar
  5. Baxter, R., R. Breuer, L. Brown, L. Conrad, F. Feyrer, S. Fong, K. Gehrts, et al. 2010. 2010 Pelagic organism decline work plan and synthesis of results. Sacramento: Interagency Ecological Program for the San Francisco Estuary.Google Scholar
  6. Bryant, M.E., and J.D. Arnold. 2007. Diets of age-0 striped bass in the San Francisco Estuary, 1973–2002. California Fish and Game 93: 1–22.Google Scholar
  7. Cloern, J.E. 2007. Habitat connectivity and ecosystem productivity: implications from a simple model. American Naturalist 169: E21–E33.CrossRefGoogle Scholar
  8. Cowen, R.K., C.B. Paris, and A. Srinivasan. 2006. Scaling of connectivity in marine populations. Science 311: 522–527.CrossRefGoogle Scholar
  9. Cronin, T.W., and R.B. Forward Jr. 1979. Tidal vertical migration: an endogenous rhythm in estuarine crab larvae. Science 205: 1020–1022.CrossRefGoogle Scholar
  10. Dam, H.G., and K.W. Tang. 2001. Affordable egg mortality: constraining copepod egg mortality with life history traits. Journal of Plankton Research 23: 633–640.CrossRefGoogle Scholar
  11. Drinkwater, K.F., and K.T. Frank. 1994. Effects of river regulation and diversion on marine fish and invertebrates. Aquatic Conservation: Marine and Freshwater Ecosystems 4: 135–151.CrossRefGoogle Scholar
  12. Durand, J.R. 2010. Determinants of seasonal abundance in key zooplankton of the San Francisco Estuary. Master’s thesis, San Francisco State University, San Francisco, CA.Google Scholar
  13. Eiane, K., D.L. Aksnes, M.D. Ohman, S. Wood, and M.B. Martinussen. 2002. Stage-specific mortality of Calanus spp. under different predation regimes. Limnology and Oceanography 47: 636–645.CrossRefGoogle Scholar
  14. Feyrer, F., B. Herbold, S.A. Matern, and P.B. Moyle. 2003. Dietary shifts in a stressed fish assemblage: consequences of a bivalve invasion in the San Francisco Estuary. Environmental Biology of Fishes 67: 277–288.CrossRefGoogle Scholar
  15. Genin, A., L. Haury, and P. Greenblatt. 1988. Interactions of migrating zooplankton with shallow topography: predation by rockfishes and intensification of patchiness. Deep-Sea Research Part II 35: 151–175.CrossRefGoogle Scholar
  16. Gentleman, W.C., P. Pepin, and S. Doucette. 2012. Estimating mortality: clarifying assumptions and sources of uncertainty in vertical methods. Journal of Marine Systems 105: 1–19.CrossRefGoogle Scholar
  17. Greene, V.E., L.J. Sullivan, J.K. Thompson, and W.J. Kimmerer. 2011. Grazing impact of the invasive clam Corbula amurensis on the microplankton assemblage of the northern San Francisco Estuary. Marine Ecology Progress Series 431: 183–193.CrossRefGoogle Scholar
  18. Gross, E.S., M.S. MacWilliams, C.D. Holleman, and T.A. Hervier. 2010. POD 3–D particle tracking modeling study. Particle tracking model testing and applications report. Report to the Interagency Ecological Program. Available from: Accessed 26 April 2018.
  19. Hammock, B.G., J.A. Hobbs, S.B. Slater, S. Acuna, and S.J. Teh. 2015. Contaminant and food limitation stress in an endangered estuarine fish. Science of the Total Environment 532: 316–326.CrossRefGoogle Scholar
  20. Harding, J.M.S., M.R. Segal, and J.D. Reynolds. 2015. Location is everything: evaluating the effects of terrestrial and marine resource subsidies on an estuarine bivalve. PLoS One 10.Google Scholar
  21. Hirst, A.G., and A.J. Bunker. 2003. Growth of marine planktonic copepods: global rates and patterns in relation to chlorophyll a, temperature, and body weight. Limnology and Oceanography 48: 1988–2010.CrossRefGoogle Scholar
  22. Hirst, A.G., and T. Kiørboe. 2002. Mortality of marine planktonic copepods: global rates and patterns. Marine Ecology Progress Series 230: 195–209.CrossRefGoogle Scholar
  23. Hirst, A.G., D. Bonnet, D.V.P. Conway, and T. Kiørboe. 2010. Does predation control adult sex ratios and longevities in marine pelagic copepods? Limnology and Oceanography 55: 2193–2206.CrossRefGoogle Scholar
  24. Hook, S.E., and N.S. Fisher. 2001. Reproductive toxicity of metals in calanoid copepods. Marine Biology 138: 1131–1140.CrossRefGoogle Scholar
  25. Jassby, A.D., W.J. Kimmerer, S.G. Monismith, C. Armor, J.E. Cloern, T.M. Powell, J.R. Schubel, and T.J. Vendlinski. 1995. Isohaline position as a habitat indicator for estuarine populations. Ecological Applications 5: 272–289.CrossRefGoogle Scholar
  26. Johnson, J.K. 1980. Effects of temperature and salinity on production and hatching of dormant eggs of Acartia californiensis (Copepoda) in an Oregon estuary. Fishery Bulletin 77: 567–581.Google Scholar
  27. Jumars, P.A. 2007. Habitat coupling by mid-latitude, subtidal, marine mysids: import-subsidised omnivores. Oceanography and Marine Biology: An Annual Review 45: 89–138.CrossRefGoogle Scholar
  28. Kayfetz, K., and W. Kimmerer. 2017. Abiotic and biotic controls on the copepod Pseudodiaptomus forbesi in the upper San Francisco Estuary. Marine Ecology Progress Series 581: 85–101.CrossRefGoogle Scholar
  29. Ketchum, B.H. 1954. Relation between circulation and planktonic populations in estuaries. Ecology 35: 191–200.CrossRefGoogle Scholar
  30. Kimmerer, W.J. 2006. Response of anchovies dampens effects of the invasive bivalve Corbula amurensis on the San Francisco Estuary foodweb. Marine Ecology Progress Series 324: 207–218.CrossRefGoogle Scholar
  31. Kimmerer, W.J. 2015. Mortality estimates of stage-structured populations must include uncertainty in stage duration and relative abundance. Journal of Plankton Research 37: 939–952.CrossRefGoogle Scholar
  32. Kimmerer, W.J., and L.A. Lougee. 2015. Bivalve grazing causes substantial mortality to an estuarine copepod population. Journal of Experimental Marine Biology and Ecology 473: 53–63.CrossRefGoogle Scholar
  33. Kimmerer, W.J., and A.D. McKinnon. 1987. Growth, mortality, and secondary production of the copepod Acartia tranteri in Westernport Bay, Australia. Limnology and Oceanography 32: 14–28.CrossRefGoogle Scholar
  34. Kimmerer, W.J., and A.D. McKinnon. 1990. High mortality in a copepod population caused by a parasitic dinoflagellate. Marine Biology 107: 449–452.CrossRefGoogle Scholar
  35. Kimmerer, W.J., and K.A. Rose. 2018. Individual-based modeling of delta smelt population dynamics in the upper San Francisco Estuary III. Effects of entrainment mortality and changes in prey. Transactions of the American Fisheries Society 147: 223–243.CrossRefGoogle Scholar
  36. Kimmerer, W., and A. Slaughter. 2016. Fine-scale distributions of zooplankton in the northern San Francisco Estuary. San Francisco Estuary and Watershed Science 14 (3) Article 2).
  37. Kimmerer, W.J., and J.K. Thompson. 2014. Phytoplankton growth balanced by clam and zooplankton grazing and net transport into the low-salinity zone of the San Francisco Estuary. Estuaries and Coasts 37: 1202–1218.CrossRefGoogle Scholar
  38. Kimmerer, W.J., W.A. Bennett, and J.R. Burau. 2002. Persistence of tidally-oriented vertical migration by zooplankton in a temperate estuary. Estuaries 25: 359–371.CrossRefGoogle Scholar
  39. Kimmerer, W.J., M.L. MacWilliams, and E.S. Gross. 2013. Variation of fish habitat and extent of the low-salinity zone with freshwater flow in the San Francisco Estuary. San Francisco Estuary and Watershed Science.Google Scholar
  40. Kimmerer, W.J., E.S. Gross, and M.L. MacWilliams. 2014. Tidal migration and retention of estuarine zooplankton investigated using a particle-tracking model. Limnology and Oceanography 59: 901–906.CrossRefGoogle Scholar
  41. Kimmerer, W.J., T.R. Ignoffo, K.R. Kayfetz, and A.M. Slaughter. 2017. Effects of freshwater flow and phytoplankton biomass on growth, reproduction, and spatial subsidies of the estuarine copepod Pseudodiaptomus forbesi. Hydrobiologia 807: 113–130.CrossRefGoogle Scholar
  42. Kneib, R.T. 1997. The role of tidal marshes in the ecology of estuarine nekton. Oceanography and Marine Biology Annual Review 35: 163–220.Google Scholar
  43. Koslow, J.A. 1981. Feeding selectivity of schools of northern anchovy, Engraulis mordax, in the Southern California Bight. Fishery Bulletin 79: 131–142.Google Scholar
  44. Kremer, J.N., J.M.P. Vaudrey, D.S. Ullman, D.L. Bergondo, N. LaSota, C. Kincaid, D.L. Codiga, and M.J. Brush. 2010. Simulating property exchange in estuarine ecosystem models at ecologically appropriate scales. Ecological Modelling 221: 1080–1088.CrossRefGoogle Scholar
  45. LaBolle, E.M., J. Quastel, G.E. Fogg, and J. Gravner. 2000. Diffusion processes in composite porous media and their numerical integration by random walks: generalized stochastic differential equations with discontinuous coefficients. Water Resources Research 36: 651–662.CrossRefGoogle Scholar
  46. Laprise, R., and J.J. Dodson. 1993. Nature of environmental variability experienced by benthic and pelagic animals in the St. Lawrence Estuary, Canada. Marine Ecology Progress Series 94: 129–139.CrossRefGoogle Scholar
  47. Longhurst, A.R., A.W. Bedo, W.G. Harrison, E.J.H. Head, and D.D. Sameoto. 1990. Vertical flux of respiratory carbon by oceanic diel migrant biota. Deep-Sea Research Part II 37: 685–694.CrossRefGoogle Scholar
  48. Lopez, C.B., J.E. Cloern, T.S. Schraga, A.J. Little, L.V. Lucas, J.K. Thompson, and J.R. Burau. 2006. Ecological values of shallow-water habitats: implications for the restoration of disturbed ecosystems. Ecosystems 9: 422–440.CrossRefGoogle Scholar
  49. Lund, J., E. Hanak, W. Fleenor, R. Howitt, J. Mount, and P. Moyle. 2007. Envisioning futures for the Sacramento-San Joaquin Delta. San Francisco: Public Policy Institute of California, San Francisco.Google Scholar
  50. Mac Nally, R., J. Thomson, W. Kimmerer, F. Feyrer, K. Newman, A. Sih, W. Bennett, et al. 2010. An analysis of pelagic species decline in the upper San Francisco Estuary using Multivariate Autoregressive modelling (MAR). Ecological Applications 20: 1417–1430.CrossRefGoogle Scholar
  51. MacIsaac, H.J., W.G. Sprules, and J.H. Leach. 1991. Ingestion of small-bodied zooplankton by zebra mussels (Dreissena polymorpha)—can cannibalism on larvae influence population dynamics? Canadian Journal of Fisheries and Aquatic Sciences 48: 2051–2060.CrossRefGoogle Scholar
  52. MacWilliams, M.L., and E.S. Gross. 2013. Hydrodynamic simulation of circulation and residence time in Clifton Court Forebay. San Francisco Estuary and Watershed Science.
  53. MacWilliams, M.L., A.J. Bever, E.S. Gross, G.S. Ketefian, and W.J. Kimmerer. 2015. Three-dimensional modeling of hydrodynamics and salinity in the San Francisco Estuary: an evaluation of model accuracy, X2, and the low-salinity zone. San Francisco Estuary and Watershed Science.
  54. Meyer, M., A. Barr, H. Lee, and M. Desbrun. 2002. Generalized barycentric coordinates on irregular polygons. Journal of Graphics Tools 7: 13–22.CrossRefGoogle Scholar
  55. Miller, C.B., J.K. Johnson, and D.R. Heinle. 1977. Growth rules in the marine copepod genus Acartia. Limnology and Oceanography 22: 326–335.CrossRefGoogle Scholar
  56. Monismith, S.G., W.J. Kimmerer, J.R. Burau, and M.T. Stacey. 2002. Structure and flow-induced variability of the subtidal salinity field in northern San Francisco Bay. Journal of Physical Oceanography 32: 3003–3019.CrossRefGoogle Scholar
  57. Mullin, M.M., and E.R. Brooks. 1970. Production of the planktonic copepod, Calanus helgolandicus. Bulletin of the Scripps Institution Oceanography 17: 89–103.Google Scholar
  58. Nichols, F.H., J.K. Thompson, and L.E. Schemel. 1990. Remarkable invasion of San Francisco Bay (California, USA) by the Asian clam Potamocorbula amurensis .2. Displacement of a former community. Marine Ecology Progress Series 66: 95–101.CrossRefGoogle Scholar
  59. Nixon, S.W., C.A. Oviatt, J. Frithsen, and B. Sullivan. 1986. Nutrients and the productivity of estuarine and coastal marine systems. Journal of the Limnological Society of South Africa 12: 43–71.CrossRefGoogle Scholar
  60. Odum, E.P. 1980. The status of three ecosystem-level hypotheses regarding salt marsh estuaries: tidal subsidy, outwelling and detritus-based food chains. In Estuarine perspectives, ed. V.S. Kennedy, 485–495. Academic Press.Google Scholar
  61. Ohman, M.D. 2012. Estimation of mortality for stage-structured zooplankton populations: what is to be done? Journal of Marine Systems 93: 4–10.CrossRefGoogle Scholar
  62. Ohman, M.D., and S.N. Wood. 1995. The inevitability of mortality. ICES Journal of Marine Science 52: 517–522.CrossRefGoogle Scholar
  63. Orsi, J., and W. Mecum. 1986. Zooplankton distribution and abundance in the Sacramento-san Joaquin Delta in relation to certain environmental factors. Estuaries 9: 326–339.CrossRefGoogle Scholar
  64. Orsi, J.J., and T.C. Walter. 1991. Pseudodiaptomus forbesi and P. marinus (Copepoda: Calanoida), the latest copepod immigrants to California’s Sacramento-San Joaquin Estuary. In Proceedings of the Fourth International Conference on Copepoda, ed. S.-I. Uye, S. Nishida, and J.-S. Ho, 553–562. Hiroshima.Google Scholar
  65. Polis, G.A., W.B. Anderson, and R.D. Holt. 1997. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annual Review of Ecology and Systematics 28: 289–316.CrossRefGoogle Scholar
  66. R Development Core Team. 2015. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. doi.Google Scholar
  67. Rogers, H. 1940. Occurrence and retention of plankton within an estuary. Journal of the Fisheries Research Board of Canada 5: 164–171.CrossRefGoogle Scholar
  68. Schmitt, F.G., D. Devreker, G. Dur, and S. Souissi. 2011. Direct evidence of tidally oriented behavior of the copepod Eurytemora affinis in the Seine estuary. Ecological Research 26: 773–780.CrossRefGoogle Scholar
  69. Slater, S.B., and R.D. Baxter. 2014. Diet, prey selection, and body condition of age-0 delta smelt, Hypomesus transpacificus, in the upper San Francisco Estuary. San Francisco Estuary and Watershed Science.
  70. Slaughter, A.M., T.R. Ignoffo, and W. Kimmerer. 2016. Predation impact of Acartiella sinensis, an introduced predatory copepod in the San Francisco Estuary, USA. Marine Ecology Progress Series 547: 47–60.CrossRefGoogle Scholar
  71. Smith, S.V., and J.T. Hollibaugh. 1997. Annual cycle and interannual variability of ecosystem metabolism in a temperate climate embayment. Ecological Monographs 67: 509–533.CrossRefGoogle Scholar
  72. Sobczak, W.V., J.E. Cloern, A.D. Jassby, B.E. Cole, T.S. Schraga, and A. Arnsberg. 2005. Detritus fuels ecosystem metabolism but not metazoan food webs in San Francisco Estuary’s freshwater Delta. Estuaries 28: 124–137.CrossRefGoogle Scholar
  73. Sommer, T., and F. Mejia. 2013. A place to call home: a synthesis of delta smelt habitat in the upper San Francisco Estuary. San Francisco Estuary and Watershed Science.Google Scholar
  74. Sommer, T., C. Armor, R. Baxter, R. Breuer, L. Brown, M. Chotkowski, S. Culberson, et al. 2007. The collapse of pelagic fishes in the upper San Francisco Estuary. Fisheries 32: 270–277.CrossRefGoogle Scholar
  75. Sommer, T., F. Mejia, K. Hieb, R. Baxter, E. Loboschefsky, and F. Loge. 2011. Long-term shifts in the lateral distribution of age-0 striped bass in the San Francisco Estuary. Transactions of the American Fisheries Society 140: 1451–1459.CrossRefGoogle Scholar
  76. Sullivan, L.J., and W.J. Kimmerer. 2013. Egg development times of Eurytemora affinis and Pseudodiaptomus forbesi (Copepoda, Calanoida) from the upper San Francisco Estuary with notes on methods. Journal of Plankton Research 35: 1331–1338.CrossRefGoogle Scholar
  77. Sullivan, L.J., T.R. Ignoffo, B. Baskerville-Bridges, D.J. Ostrach, and W.J. Kimmerer. 2016. Prey selection of larval and juvenile planktivorous fish: impacts of introduced prey. Environmental Biology of Fishes 99: 633–646.CrossRefGoogle Scholar
  78. Tang, K.W., C.S. Freund, and C.L. Schweitzer. 2006. Occurrence of copepod carcasses in the lower Chesapeake Bay and their decomposition by ambient microbes. Estuarine, Coastal and Shelf Science 68: 499–508.CrossRefGoogle Scholar
  79. Thomson, J., W. Kimmerer, L. Brown, K. Newman, R. Mac Nally, W. Bennett, F. Feyrer, and E. Fleishman. 2010. Bayesian change-point analysis of abundance trends for pelagic fishes in the upper San Francisco Estuary. Ecological Applications 20: 1431–1448.CrossRefGoogle Scholar
  80. Tiselius, P., C.M.A. Borg, B.W. Hansen, P.J. Hansen, T.G. Nielsen, and B. Vismann. 2008. High reproduction, but low biomass: mortality estimates of the copepod Acartia tonsa in a hyper-eutrophic estuary. Aquatic Biology 2: 93–103.CrossRefGoogle Scholar
  81. UNESCO. 1981. The practical salinity scale 1978 and the International Equation of State of seawater 1980, Tenth report of the Joint Panel on Oceanographic Tables and Standards. Sidney: UNESCO.Google Scholar
  82. Verheye, H.M., and J.G. Field. 1992. Vertical distribution and diel vertical migration of Calanoides carinatus (Krøyer, 1849) developmental stages in the southern Benguela upwelling region. Journal of Experimental Marine Biology and Ecology 158: 123–140.CrossRefGoogle Scholar
  83. Walter, T.C. 1989. Review of the new-world species of Pseudodiaptomus (Copepoda, Calanoida), with a key to the species. Bulletin of Marine Science 45: 590–628.Google Scholar
  84. Wang, B., G. Zhao, and O.B. Fringer. 2011. Reconstruction of vector fields for semi-Lagrangian advection on unstructured, staggered grids. Ocean Modelling 40: 52–71.CrossRefGoogle Scholar
  85. Wood, S.N. 1994. Obtaining birth and mortality patterns from structured population trajectories. Ecological Monographs 64: 23–44.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2018

Authors and Affiliations

  1. 1.Estuary & Ocean Science CenterSan Francisco State UniversityTiburonUSA
  2. 2.RMADavisUSA
  3. 3.Center for Watershed SciencesUniversity of CaliforniaDavisUSA
  4. 4.Department of Wildlife, Fish and Conservation BiologyUniversity of California, DavisDavisUSA

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