Advertisement

Tidal Wetlands Associated with Foraging Success of Delta Smelt

  • Bruce G. HammockEmail author
  • Rosemary Hartman
  • Steven B. Slater
  • April Hennessy
  • Swee J. Teh
Article

Abstract

Delta smelt (Hypomesus transpacificus), an annual fish endemic to the San Francisco Estuary (SFE), is imperiled. One recovery strategy is to restore tidal wetlands, thereby increasing productivity and prey abundance. However, the link between tidal wetlands and foraging of delta smelt is not yet established. Using GIS, we quantified the area of tidal wetlands (km2) within a 2-km radius around sampling stations from which 1380 delta smelt were collected over 4 years (2011–2015). We quantified stomach fullness, a metric of foraging success, for each fish and regressed it against tidal wetland area, turbidity, water temperature, and other factors known to influence foraging success of delta smelt. Stomach fullness increased with both increasing tidal wetland area and increasing water temperature and was reduced at turbidities > 80 NTU. Model estimates show that stomach fullness increased twofold from the minimum (0 km2) to the maximum (4.89 km2) tidal wetland area. Of this increase, 60% was due to increased predation on larval fish, while 40% was due to increased predation on zooplankton. Delta smelt collected from areas with the highest tidal wetland area were six times more likely to have a larval fish in their guts than those collected from areas with the lowest. Thus, tidal wetland appears to confer substantial benefits to the foraging success of delta smelt, mainly via increased predation on larval fish.

Keywords

GIS Stomach fullness Zooplankton Turbidity Temperature Tidal marsh 

Notes

Acknowledgements

We are grateful to the many people who contributed to this study, including CDFW boat crews, UCD AHP dissection teams, and the Interagency Ecological Program. We thank Randy Baxter for facilitating the Diet and Condition Study, Tricia Bippus for leading the CDFW Fish Diet Lab, and Sally Skelton for processing zooplankton samples. We also thank Ted Sommer, Andrew Shultz, and an anonymous reviewer for comments that greatly improved the paper.

Funding Information

Partial funding for this study was provided by US Bureau of Reclamation R17AC00129, US Geological Survey G15AS00018, and CDFW Ecosystem Restoration Program E1183004.

Supplementary material

12237_2019_521_MOESM1_ESM.docx (59 kb)
ESM 1 (DOCX 59 kb)

References

  1. Aasen, G.A. 1999. Juvenile delta smelt use of shallow-water and channel habitats in California’s Sacramento-San Joaquin estuary. California Fish and Game 85: 161–169.Google Scholar
  2. Allan, J.D., and M.M. Castillo. 2007. Stream ecology: Structure and function of running waters. Springer Verlag.Google Scholar
  3. Allen, E.A., P.E. Fell, M.A. Peck, J.A. Gieg, C.R. Guthke, and M.D. Newkirk. 1994. Gut contents of common mummichogs, Fundulus heteroclitus L., in a restored impounded marsh and in natural reference marshes. Estuaries and Coasts 17 (2): 462–471.CrossRefGoogle Scholar
  4. 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 (5): 946–955.CrossRefGoogle Scholar
  5. Baltz, D.M., C. Rakocinski, and J.W. Fleeger. 1993. Microhabitat use by marsh-edge fishes in a Louisiana estuary. Environmental Biology of Fishes 36 (2): 109–126.CrossRefGoogle Scholar
  6. Beck, M.W., K.L. Heck Jr., K.W. Able, D.L. Childers, D.B. Eggleston, B.M. Gillanders, B. Halpern, C.G. Hays, K. Hoshino, and T.J. Minello. 2001. The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates: A better understanding of the habitats that serve as nurseries for marine species and the factors that create site-specific variability in nursery quality will improve conservation and management of these areas. Bioscience 51: 633–641.CrossRefGoogle Scholar
  7. Bennett, W.A. 2005. Critical assessment of the delta smelt population in the San Francisco Estuary, California. San Francisco Estuary and Watershed Science 3 (2).Google Scholar
  8. Bennett, W., and J.R. Burau. 2015. Riders on the storm: Selective tidal movements facilitate the spawning migration of threatened delta smelt in the San Francisco Estuary. Estuaries and Coasts 38 (3): 826–835.CrossRefGoogle Scholar
  9. Booth, D. 1990. Effect of water temperature on stomach evacuation rates, and estimation of daily food intake of bluegill sunfish (Lepomis macrochirus Rafinesque). Canadian Journal of Zoology 68 (3): 591–595.CrossRefGoogle Scholar
  10. Bolker, B. 2010. bbmle: Tools for general maximum likelihood estimation. R package version 1.0.15.Google Scholar
  11. Breheny, P., and W. Burchett. 2013. Visualization of regression models using visreg. R Package version 2: 1–1.Google Scholar
  12. Brown, J.H., J.F. Gillooly, A.P. Allen, V.M. Savage, and G.B. West. 2004. Toward a metabolic theory of ecology. Ecology 85 (7): 1771–1789.CrossRefGoogle Scholar
  13. Burnham, K.P., and D.R. Anderson. 2002. Model selection and multi-model inference: A practical information-theoretic approach. New York: Springer Verlag.Google Scholar
  14. California Natural Resource Agency. 2017. Delta Smelt resiliency strategy. Progress update. [Internet]. [accessed 2017 Jul 17]; Available from: http://resources.ca.gov/docs/Delta-Smelt-ResiliencyStrategy-Update.pdf. Accessed 17 July 2017.
  15. Cloern, J.E., and A.D. Jassby. 2012. Drivers of change in estuarine-coastal ecosystems: Discoveries from four decades of study in San Francisco Bay. Reviews of Geophysics 50 (4): RG4001.  https://doi.org/10.1029/2012RG000397.
  16. Cloern, J.E., S. Foster, and A. Kleckner. 2014. Phytoplankton primary production in the world’s estuarine-coastal ecosystems. Biogeosciences 11 (9): 2477–2501.CrossRefGoogle Scholar
  17. Conway-Cranos, L., P. Kiffney, N. Banas, M. Plummer, S. Naman, P. MacCready, J. Bucci, and M. Ruckelshaus. 2015. Stable isotopes and oceanographic modeling reveal spatial and trophic connectivity among terrestrial, estuarine, and marine environments. Marine Ecology Progress Series 533: 15–28.CrossRefGoogle Scholar
  18. Cribari-Neto, F., and A. Zeileis. 2009. Beta regression in R.Google Scholar
  19. Damon, L.J., S.B. Slater, R.D. Baxter, and R.W. Fujimura. 2016. Fecundity and reproductive potential of wild female delta smelt in the upper San Francisco Estuary, California. California Fish and Game 102: 188–210.Google Scholar
  20. Dean, A.F., S.M. Bollens, C. Simenstad, and J. Cordell. 2005. Marshes as sources or sinks of an estuarine mysid: Demographic patterns and tidal flux of Neomysis kadiakensis at China Camp marsh, San Francisco estuary. Estuarine, Coastal and Shelf Science 63 (1-2): 1–11.CrossRefGoogle Scholar
  21. Dagorn, L., P. Bach, and E. Josse. 2000. Movement patterns of large bigeye tuna (Thunnus obesus) in the open ocean, determined using ultrasonic telemetry. Marine Biology 136 (2): 361–371.CrossRefGoogle Scholar
  22. Dame, R., T. Chrzanowski, K. Bildstein, B. Kjerfve, H. McKellar, D. Nelson, J. Spurrier, S. Stancyk, H. Stevenson, and J. Vernberg. 1986. The outwelling hypothesis and north inlet, South Carolina. Marine Ecology Progress Series 33: 217–229.CrossRefGoogle Scholar
  23. 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 (3): 277–288.CrossRefGoogle Scholar
  24. Feyrer, F., M.L. Nobriga, and T.R. Sommer. 2007. Multidecadal trends for three declining fish species: Habitat patterns and mechanisms in the San Francisco Estuary, California, USA. Canadian Journal of Fisheries and Aquatic Sciences 64 (4): 723–734.CrossRefGoogle Scholar
  25. Feyrer, F., K. Newman, M. Nobriga, and T. Sommer. 2011. Modeling the effects of future outflow on the abiotic habitat of an imperiled estuarine fish. Estuaries and Coasts 34 (1): 120–128.CrossRefGoogle Scholar
  26. Fonds, M., R. Cronie, A. Vethaak, and P. Van der Puyl. 1992. Metabolism, food consumption and growth of plaice (Pleuronectes platessa) and flounder (Platichthys flesus) in relation to fish size and temperature. Netherlands Journal of Sea Research 29 (1-3): 127–143.CrossRefGoogle Scholar
  27. Gewant, D., and S.M. Bollens. 2012. Fish assemblages of interior tidal marsh channels in relation to environmental variables in the upper San Francisco Estuary. Environmental Biology of Fishes 94 (2): 483–499.CrossRefGoogle Scholar
  28. Glibert, P.M., D. Fullerton, J.M. Burkholder, J.C. Cornwell, and T.M. Kana. 2011. Ecological stoichiometry, biogeochemical cycling, invasive species, and aquatic food webs: San Francisco Estuary and comparative systems. Reviews in Fisheries Science 19 (4): 358–417.CrossRefGoogle Scholar
  29. Grimaldo, L.F., R.E. Miller, C.M. Peregrin, and Z.P. Hymanson. 2004. Spatial and temporal distribution of native and alien ichthyoplankton in three habitat types of the Sacramento-San Joaquin Delta. American Fisheries Society Symposium 39: 81–96.Google Scholar
  30. Grimaldo, L.F., T. Sommer, N. Van Ark, G. Jones, E. Holland, P.B. Moyle, B. Herbold, and P. Smith. 2009. Factors affecting fish entrainment into massive water diversions in a tidal freshwater estuary: Can fish losses be managed? North American Journal of Fisheries Management 29 (5): 1253–1270.CrossRefGoogle Scholar
  31. Grimaldo, L., F. Feyrer, J. Burns, and D. Maniscalco. 2017. Sampling uncharted waters: Examining rearing habitat of larval longfin smelt (Spirinchus thaleichthys) in the upper San Francisco Estuary. Estuaries and Coasts: 1–14.Google Scholar
  32. Hammock, B.G., J.A. Hobbs, S.B. Slater, S. Acuña, 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
  33. Hammock, B.G., S.B. Slater, R.D. Baxter, N.A. Fangue, D. Cocherell, A. Hennessy, T. Kurobe, C.Y. Tai, and S.J. Teh. 2017. Foraging and metabolic consequences of semi-anadromy for an endangered estuarine fish. PLoS One 12 (3): e0173497.CrossRefGoogle Scholar
  34. Handeland, S.O., A.K. Imsland, and S.O. Stefansson. 2008. The effect of temperature and fish size on growth, feed intake, food conversion efficiency and stomach evacuation rate of Atlantic salmon post-smolts. Aquaculture 283 (1-4): 36–42.CrossRefGoogle Scholar
  35. Hasenbein, M., L.M. Komoroske, R.E. Connon, J. Geist, and N.A. Fangue. 2013. Turbidity and salinity affect feeding performance and physiological stress in the endangered delta smelt. Integrative and Comparative Biology 53 (4): 620–634.CrossRefGoogle Scholar
  36. Hasenbein, M., N.A. Fangue, J. Geist, L.M. Komoroske, J. Truong, R. McPherson, and R.E. Connon. 2016. Assessments at multiple levels of biological organization allow for an integrative determination of physiological tolerances to turbidity in an endangered fish species. Conservation Physiology 4 (1): cow004.  https://doi.org/10.1093/conphys/cow004.
  37. Herbold, B., D.M. Baltz, L. Brown, R. Grossinger, W. Kimmerer, P. Lehman, C.S. Simenstad, C. Wilcox, and M. Nobriga. 2014. The role of tidal marsh restoration in fish management in the San Francisco Estuary. San Francisco Estuary and Watershed Science 12 (1).Google Scholar
  38. Hobbs, J., P.B. Moyle, N. Fangue, and R.E. Connon. 2017. Is extinction inevitable for delta smelt and longfin smelt? An opinion and recommendations for recovery. San Francisco Estuary and Watershed Science 15 (2).Google Scholar
  39. Howe, E.R., C.A. Simenstad, J.D. Toft, J.R. Cordell, and S.M. Bollens. 2014. Macroinvertebrate prey availability and fish diet selectivity in relation to environmental variables in natural and restoring North San Francisco Bay tidal marsh channels. San Francisco Estuary and Watershed Science 12 (1).Google Scholar
  40. Jassby, A.D., and T.M. Powell. 1994. Hydrodynamic influences on interannual chlorophyll variability in an estuary: Upper San Francisco Bay-Delta (California, USA). Estuarine, Coastal and Shelf Science 39 (6): 595–618.CrossRefGoogle Scholar
  41. Jassby, A.D., J.E. Cloern, and B.E. Cole. 2002. Annual primary production: Patterns and mechanisms of change in a nutrient-rich tidal ecosystem. Limnology and Oceanography 47 (3): 698–712.CrossRefGoogle Scholar
  42. Kalff, J. 2002. Limnology: Inland water ecosystems. Upper Saddle River, NJ: Prentice Hall.Google Scholar
  43. Kimmerer, W., J. Burau, and W. Bennett. 1998. Tidally oriented vertical migration and position maintenance of zooplankton in a temperate estuary. Limnology and Oceanography 43 (7): 1697–1709.CrossRefGoogle Scholar
  44. 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).Google Scholar
  45. Komoroske, L., R. Connon, J. Lindberg, B. Cheng, G. Castillo, M. Hasenbein, and N. Fangue. 2014. Ontogeny influences sensitivity to climate change stressors in an endangered fish. Conservation Physiology 2 (1): cou008.CrossRefGoogle Scholar
  46. Kurobe T, P.M., Javidmehr A, Teh FC, Acuña SC, Corbin CJ, Conley A, Bennett WA, Teh SJ. 2016. Assessing oocyte development and maturation in the threatened delta smelt, Hypomesus transpacificus.Environmental Biology of Fishes 99: 423–432, 4.Google Scholar
  47. Lehman, P., S. Mayr, L. Mecum, and C. Enright. 2010. The freshwater tidal wetland Liberty Island, CA was both a source and sink of inorganic and organic material to the San Francisco Estuary. Aquatic Ecology 44 (2): 359–372.CrossRefGoogle Scholar
  48. Lindberg, J.C., G. Tigan, L. Ellison, T. Rettinghouse, M.M. Nagel, and K.M. Fisch. 2013. Aquaculture methods for a genetically managed population of endangered delta smelt. North American Journal of Aquaculture 75 (2): 186–196.CrossRefGoogle Scholar
  49. Lucas, L.V., D.M. Sereno, J.R. Burau, T.S. Schraga, C.B. Lopez, M.T. Stacey, K.V. Parchevsky, and V.P. Parchevsky. 2006. Intradaily variability of water quality in a shallow tidal lagoon: Mechanisms and implications. Estuaries and Coasts 29 (5): 711–730.CrossRefGoogle Scholar
  50. Mahardja, B., N. Ikemiyagi, and B. Schreier. 2015. Evidence for increased utilization of the Yolo Bypass by delta smelt. IEP newsletter [internet].[accessed 2016 Sep 27]; 28 (1): 13–18.Google Scholar
  51. Marsac, F., and P. Cayré. 1998. Telemetry applied to behaviour analysis of yellowfin tuna (Thunnus albacares, Bonnaterre, 1788) movements in a network of fish aggregating devices. Hydrobiologia 371 (372): 155–171.CrossRefGoogle Scholar
  52. Matern, S.A., P.B. Moyle, and L.C. Pierce. 2002. Native and alien fishes in a California estuarine marsh: Twenty-one years of changing assemblages. Transactions of the American Fisheries Society 131 (5): 797–816.CrossRefGoogle Scholar
  53. McElreath, R. 2016. Statistical rethinking: A Bayesian course with examples in R and Stan. CRC Press.Google Scholar
  54. Merz, J.E., S. Hamilton, P.S. Bergman, and B. Cavallo. 2011. Spatial perspective for delta smelt: A summary of contemporary survey data. California Fish and Game 97: 164–189.Google Scholar
  55. Miller, W.J., B.F. Manly, D.D. Murphy, D. Fullerton, and R.R. Ramey. 2012. An investigation of factors affecting the decline of delta smelt (Hypomesus transpacificus) in the Sacramento-San Joaquin Estuary. Reviews in Fisheries Science 20 (1): 1–19.CrossRefGoogle Scholar
  56. Nobriga, M.L. 2002. Larval delta smelt diet composition and feeding incidence: environmental and ontogenetic influences. California Fish and Game 88: 149–164.Google Scholar
  57. Odum, E.P., and A.A. de la Cruz. 1967. Particulate organic detritus in a Georgia salt marsh-estuarine ecosystem. In Estuaries. AAAS, Publ, ed. G.H. Lauff, vol. 83, 383–388. Washington: DC.Google Scholar
  58. Parker, A.E., R.C. Dugdale, and F.P. Wilkerson. 2012. Elevated ammonium concentrations from wastewater discharge depress primary productivity in the Sacramento River and the northern San Francisco Estuary. Marine Pollution Bulletin 64 (3): 574–586.CrossRefGoogle Scholar
  59. Persson, L. 1981. The effects of temperature and meal size on the rate of gastric evacuation in perch (Perca fluviatilis) fed on fish larvae. Freshwater Biology 11 (2): 131–138.CrossRefGoogle Scholar
  60. R Core Team. R: A language and environment for statistical computing. version 3.0.2. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
  61. Rozas, L.P., and M.W. LaSalle. 1990. A comparison of the diets of Gulf killifish, Fundulus grandis Baird and Girard, entering and leaving a Mississippi brackish marsh. Estuaries and Coasts 13 (3): 332–336.CrossRefGoogle Scholar
  62. Shaffer, G.P., and M.J. Sullivan. 1988. Water column productivity attributable to displaced benthic diatoms in well-mixed shallow estuaries. Journal of Phycology 24 (2): 132–140.CrossRefGoogle Scholar
  63. Slater, S.B., and R.D. Baxter. 2014. Diet, prey selection, and body condition of age-0 delta smelt, in the upper San Francisco Estuary. San Francisco Estuary and Watershed Science 12 (3).Google Scholar
  64. Sommer, T.R., W.C. Harrell, R. Kurth, F. Feyrer, S.C. Zeug, and G. O Leary. 2004. Ecological patterns of early life stages of fishes in a large river-floodplain of the San Francisco estuary. In American Fisheries society symposium, 39: 111–123: American Fisheries Society.Google Scholar
  65. Sommer, T., C. Armor, R. Baxter, R. Breuer, L. Brown, M. Chotkowski, S. Culberson, F. Feyrer, M. Gingras, and B. Herbold. 2007. The collapse of pelagic fishes in the upper San Francisco Estuary. Fisheries 32 (6): 270–277.CrossRefGoogle Scholar
  66. Sommer, T., F.H. Mejia, M.L. Nobriga, F. Feyrer, and L. Grimaldo. 2011. The spawning migration of delta smelt in the upper San Francisco Estuary. San Francisco Estuary and Watershed Science 9 (2).Google Scholar
  67. 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 11 (2).Google Scholar
  68. Swanson, C., P.S. Young, and J. Cech. 1998. Swimming performance of delta smelt: Maximum performance, and behavioral and kinematic limitations on swimming at submaximal velocities. Journal of Experimental Biology 201 (3): 333–345.Google Scholar
  69. Teh, S.J., D.V. Baxa, B.G. Hammock, S.A. Gandhi, and T. Kurobe. 2016. A novel and versatile flash-freezing approach for evaluating the health of delta smelt. Aquatic Toxicology 170: 152–161.CrossRefGoogle Scholar
  70. United States Fish and Wildlife Service (USFWS). 2008. Formal Endangered Species Act consultation on the proposed coordinated operations of the Central Valley Project (CVP) and State Water Project (SWP). U.S. Fish and Wildlife Service, Sacramento, California.Google Scholar
  71. Vadeboncoeur, Y., P.B. McIntyre, and M.J. Vander Zanden. 2011. Borders of biodiversity: Life at the edge of the world’s large lakes. BioScience 61 (7): 526–537.CrossRefGoogle Scholar
  72. Vander Zanden, M.J., Y. Vadeboncoeur, and S. Chandra. 2011. Fish reliance on littoral–benthic resources and the distribution of primary production in lakes. Ecosystems 14 (6): 894–903.CrossRefGoogle Scholar
  73. Vinagre, C., A. Maia, and H. Cabral. 2007. Effect of temperature and salinity on the gastric evacuation of juvenile sole Solea solea and Solea senegalensis. Journal of Applied Ichthyology 23 (3): 240–245.CrossRefGoogle Scholar
  74. Visintainer, T.A., S.M. Bollens, and C. Simenstad. 2006. Community composition and diet of fishes as a function of tidal channel geomorphology. Marine Ecology Progress Series 321: 227–243.CrossRefGoogle Scholar
  75. West, J.M., and J.B. Zedler. 2000. Marsh-creek connectivity: Fish use of a tidal salt marsh in southern California. Estuaries and Coasts 23 (5): 699–710.CrossRefGoogle Scholar
  76. Wilkerson, F., and R. Dugdale. 2016. The ammonium paradox of an urban high-nutrient low-growth estuary. In Aquatic Microbial Ecology and Biogeochemistry: A Dual Perspective, 117–126: Springer.Google Scholar
  77. Whipple, A.A., R.M. Grossinger, D. Rankin, B. Stanford, and R.A. Askevold. 2012. Sacramento-San Joaquin Delta historical ecology investigation: Exploring pattern and process. CA: San Francisco Estuary Institute-Aquatic Science Center. Richmond.Google Scholar
  78. Whitley, S.N., and S.M. Bollens. 2014. Fish assemblages across a vegetation gradient in a restoring tidal freshwater wetland: Diets and potential for resource competition. Environmental Biology of Fishes 97 (6): 659–674.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2019

Authors and Affiliations

  1. 1.Aquatic Health Program, Department of Anatomy, Physiology, and Cell Biology, School of Veterinary MedicineUniversity of CaliforniaDavisUSA
  2. 2.California Department of Fish and WildlifeStocktonUSA

Personalised recommendations