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Biological Invasions

, Volume 19, Issue 9, pp 2693–2710 | Cite as

Habitat partitioning by native and alien fishes and decapods in novel habitats of the upper San Francisco Estuary

  • Matthew J. Young
  • Kathleen A. Berridge
  • Teejay O’Rear
  • Peter B. Moyle
  • John R. DurandEmail author
Original Paper

Abstract

The rate of alien species introductions is increasing in aquatic ecosystems, but many invaders appear to co-exist with previous residents, resulting in persistent mixed assemblages of non-coevolved organisms. This study focuses on species’ habitat partitioning of edge habitats in the San Francisco Estuary, a highly altered novel ecosystem that supports mixed assemblages of native and alien fishes and macroinvertebrates. We used minnow traps to address two questions about the demersal assemblage along levees in large tidal sloughs: (1) What is the relative abundance of demersal fish and macroinvertebrate species in shallow water adjacent to levee edges? and (2) Do native and alien species occupy different habitat types? We used our findings to address the broader question: do native and non-native species show habitat segregation, suggesting development of assemblage structure similar to that of co-evolved assemblages? Results indicate that habitat partitioning occurs among some clusters of species, but not all. Native Prickly Sculpin was found most often near riprapped levee edges, while alien Yellowfin Goby occupied adjacent muddy habitat, and the alien Shimofuri Goby showed no preference. Where two non-native species of caridean shrimp co-occurred, Siberian Prawn occupied unvegetated mud, while Oriental Grass Shrimp used primarily riprap. However, when only Siberian Prawn was present, it showed no preference for habitat type. Habitat associations changed slightly in response to seasonal shifts in habitat and spawning requirements. This study demonstrates that non-coevolved assemblages of organisms can develop resource partitioning to assist co-existence in novel habitats.

Keywords

Benthic fish Caridean shrimp Habitat partitioning Suisun Marsh Novel species assembly Estuaries Biological invasions 

Notes

Acknowledgements

The authors thank Jacob Montgomery, Kousei Martin Perales, Denise DeCarion, and Amy Chandos for support with data collection. Three anonymous reviewers provided valuable feedback and led to a much improved manuscript, for which we are grateful. This research was funded by California Department of Fish and Wildlife (CDFW) Ecosystem Restoration Program Grant #E1183013, CDFW Delta Water Quality and Ecosystem Restoration Grant #P1596025, and by a Grant from the State and Federal Contractors Water Agency.

Supplementary material

10530_2017_1477_MOESM1_ESM.jpg (122 kb)
Supplementary material 1 (JPEG 122 kb)

References

  1. Baxter R, Breuer R, Brown L, Chotkowski M, Feyrer F, Herbold B, Hrodey P, Muller-Solger A, Nobriga M, Sommer T, Souza K (2008) Workplan to evaluate the decline of pelagic species in the upper San Francisco Estuary [Internet]. Sacramento: interagency ecological program for the San Francisco Bay/Delta Estuary.http://cdm16658.contentdm.oclc.org/cdm/ref/collection/p267501ccp2/id/2072
  2. Blumenshine SC, Tsukimura B, Rice A, Rudnick DA et al. (2012) Environmental factors influencing the dynamics of Chinese mitten crab zoeae in the San Francisco Bay-Delta [Internet].https://repository.library.fresnostate.edu/handle/10211.3/163252. Accessed 27 Apr 2017
  3. Brown LR (2003) Will tidal wetland restoration enhance populations of native fishes? San Franc Estuary Watershed Sci [Internet]. 1. http://escholarship.org/uc/item/2cp4d8wk
  4. Brown T, Hieb KA (2014) Status of the Siberian Prawn, in the San Francisco Estuary. San Franc Estuary Watershed Sci [Internet]. 12. https://escholarship.org/uc/item/36t046cq. Accessed 16 Sep 2016
  5. Brown LR, Michniuk D (2007) Littoral fish assemblages of the alien-dominated Sacramento-San Joaquin Delta, California, 1980–1983 and 2001–2003. Estuaries Coasts. 30:186–200. doi: 10.1007/BF02782979 CrossRefGoogle Scholar
  6. Brown LR, Matern SA, Moyle PB (1995) Comparative ecology of prickly sculpin, Cottus asper, and coastrange sculpin, C. aleuticus, in the Eel River, California. Environ Biol Fishes 42:329–343CrossRefGoogle Scholar
  7. Carlton JT, Thompson JK, Schemel LE, Nichols FH (1990) Remarkable invasion of San Francisco Bay (California, USA) by the Asian clam Potamocorbula amurensis. 1. Introduction and dispersal. Mar Ecol Prog Ser 66:81–94CrossRefGoogle Scholar
  8. Carpenter B, Gelman A, Hoffman M, Lee D, Goodrich B, Betancourt M, Brubaker MA, Guo J, Li P, Riddell A (2016) Stan: a probabilistic programming language. J Stat Softw [Internet]. 20. http://www.uvm.edu/~bbeckage/Teaching/DataAnalysis/Manuals/stan-resubmit-JSS1293.pdf. Accessed 08 Apr 2017
  9. Coen LD, Heck KL, Abele LG (1981) Experiments on competition and predation among shrimps of seagrass meadows. Ecology 62:1484–1493CrossRefGoogle Scholar
  10. Cohen AN, Carlton J (1995) Nonindigenous aquatic species in a United States Estuary: a case study of the biological invasions of the San Francisco Bay and Delta [Internet]. Washington,: U. S. Fish and Wildlife Service. http://nsgl.gso.uri.edu/conn/connt95002/connt95002index.html
  11. Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558. doi: 10.1126/science.279.5350.555 CrossRefPubMedGoogle Scholar
  12. Conrad JL, Bibian AJ, Weinersmith KL, Carion DD, Young MJ, Crain P, Hestir EL, Santos MJ, Sih A (2016) Novel species interactions in a highly modified estuary: association of Largemouth Bass with Brazilian waterweed Egeria densa. Trans Am Fish Soc 145:249–263. doi: 10.1080/00028487.2015.1114521 CrossRefGoogle Scholar
  13. Craig JF (1992) Human-induced changes in the composition of fish communities in the African Great Lakes. Rev Fish Biol Fish 2:93–124CrossRefGoogle Scholar
  14. Dudgeon D, Arthington AH, Gessner MO, Kawabata Z-I, Knowler DJ, Lévêque C, Naiman RJ, Prieur-Richard A-H, Soto D, Stiassny ML et al (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182CrossRefPubMedGoogle Scholar
  15. Durand J, Fleenor W, McElreath R, Santos MJ, Moyle P (2016) Physical controls on the distribution of the submersed aquatic weed egeria densa in the Sacramento-San Joaquin Delta, California and implications for habitat restoration. San Franc Estuary Watershed Sci [Internet]. 14. doi: 10.15447/sfews.2016v14iss1art4 http://escholarship.org/uc/item/85c9h479. Accessed 14 Apr 2016
  16. Enright C (2014) Physical processes and geomorphic features. In: Moyle PB, Manfree AD, Fiedler PL (eds) Suisun Marsh. University of California Press, Berkeley, pp 45–64CrossRefGoogle Scholar
  17. Fahnenstiel GL, Lang GA, Nalepa TF, Johengen TH (1995) Effects of zebra mussel (Dreissena polymorpha) colonization on water quality parameters in Saginaw Bay, Lake Huron. J Gt Lakes Res 21:435–448CrossRefGoogle Scholar
  18. Feyrer F, Healey MP (2003) Fish community structure and environmental correlates in the highly altered southern Sacramento-San Joaquin Delta. Environ Biol Fishes 66:123–132. doi: 10.1023/A:1023670404997 CrossRefGoogle Scholar
  19. Feyrer F, Herbold B, Matern SA, Moyle PB (2003) Dietary shifts in a stressed fish assemblage: consequences of a bivalve invasion in the San Francisco Estuary. Environ Biol Fishes 67:277–288. doi: 10.1023/A:1025839132274 CrossRefGoogle Scholar
  20. Feyrer F, Sommer T, Slater SB (2009) Old school vs. new school: status of threadfin shad (Dorosoma petenense) five decades after its introduction to the Sacramento-San Joaquin Delta. San Franc Estuary Watershed Sci [Internet]. 7. http://escholarship.ucop.edu/uc/item/4dt6p4bv
  21. Gelman A, Carlin JB, Stern HS, Rubin DB (2014) Bayesian data analysis [Internet]. [place unknown]: Chapman and Hall/CRC, Boca Raton. http://amstat.tandfonline.com/doi/full/10.1080/01621459.2014.963405. Accessed 08 Apr 2017
  22. Goldschmidt T, Witte F, Wanink J (1993) Cascading effects of the introduced Nile perch on the detritivorous/phytoplanktivorous species in the sublittoral areas of Lake Victoria. Conserv Biol 7:686–700. doi: 10.1046/j.1523-1739.1993.07030686.x CrossRefGoogle Scholar
  23. Grewell BJ, Baye PR, Fiedler PL (2014) Shifting mosaics: vegetation of Suisun Marsh. In: Moyle PB, Manfree AD, Fiedler PL (eds) Suisun Marsh ecological history and possible futures. University of California Press, Berkeley, pp 65–102CrossRefGoogle Scholar
  24. Grosholz ED (2005) Recent biological invasion may hasten invasional meltdown by accelerating historical introductions. Proc Natl Acad Sci U S A 102:1088–1091. doi: 10.1073/pnas.0308547102 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Grosholz ED, Ruiz GM (1996) Predicting the impact of introduced marine species: lessons from the multiple invasions of the European green crab Carcinus maenas. Biol Conserv 78:59–66. doi: 10.1016/0006-3207(94)00018-2 CrossRefGoogle Scholar
  26. Hatfield SE (1985) Seasonal and interannual variation in distribution and population abundance of the shrimp Crangon franciscorum in San Francisco Bay. In: Temporal dyn estuary San Francisco Bay [Internet]. Springer, Berlin p 199–210. http://link.springer.com/chapter/10.1007/978-94-009-5528-8_12. Accessed 03 Feb 2014
  27. He X, Lodge DM (1990) Using minnow traps to estimate fish population size: the importance of spatial distribution and relative species abundance. Hydrobiologia 190:9–14CrossRefGoogle Scholar
  28. Herbold B, Moyle PB (1986) Introduced species and vacant niches. Am Nat 128:751–760CrossRefGoogle Scholar
  29. Herbold B, Baltz DM, Brown L, Grossinger R, Kimmerer W, Lehman P, Simenstad CS, Wilcox C, Nobriga M (2014) The role of tidal marsh restoration in fish management in the San Francisco Estuary. San Franc Estuary Watershed Sci [Internet]. 12. http://escholarship.org/uc/item/1147j4nz
  30. Hestir EL (2010) Trends in estuarine water quality and submerged aquatic vegetation invasion [Internet]. University of California, Davis. http://gradworks.umi.com/34/22/3422770.html. Accessed 22 Oct 2012
  31. Hooten MB, Hobbs NT (2015) A guide to Bayesian model selection for ecologists. Ecol Monogr 85:3–28CrossRefGoogle Scholar
  32. Jackson DA, Harvey HH (1997) Qualitative and quantitative sampling of lake fish communities. Can J Fish Aquat Sci 54:2807–2813CrossRefGoogle Scholar
  33. Kanou K, Sano M, Kohno H (2007) Relationships between short-term variations in density of juvenile yellowfin goby Acanthogobius flavimanus and environmental variables on an estuarine mudflat. Fish Sci 73:38–45CrossRefGoogle Scholar
  34. Kimmerer WJ, Orsi JJ (1996) Causes of long-term declines in zooplankton in the San Francisco Bay estuary since 1987. In: Hollibaugh JT (ed) San Francisco Bay the ecosystem. American Association for the Advancement of Science, San Francisco, pp 403–424Google Scholar
  35. Leach JH (1993) Impacts of the Zebra Mussel (Dreissena polymorpha) on water quality and fish spawning reefs in western Lake Erie. In: Nalepa TF, Schloesser DW (eds) Zebra Mussels: biology, impacts, and control. Lewis Publishers, Boca Raton, pp 381–397Google Scholar
  36. Leidy RA, Moyle PB (1998) Conservation status of the world’s fish fauna: an overview. In: Fiedler PL, Kareiva PM (eds) Conservation biology for the coming decade. Chapman & Hall, New York, pp 187–227Google Scholar
  37. Light SF, Carlton JT (eds) (2007) The Light and Smith manual: intertidal invertebrates from central California to Oregon. University of California Press, BerkeleyGoogle Scholar
  38. Light T, Moyle PB (2015) Assembly rules and novel assemblages in aquatic ecosystems. In: Canning-Clode J (ed) Biol invasions chang ecosyst vectors ecol impacts manag predict. De Gruyter Open, Warsaw, Berlin, pp 432–457Google Scholar
  39. Lund J, Hanak E, Fleenor W, Bennett W, Howitt R (2010) Comparing futures for the Sacramento-San Joaquin delta. University of California Press, Berkeley. http://www.ppic.org/main/publication.asp?i=810
  40. MacIsaac HJ (1996) Potential abiotic and biotic impacts of zebra mussels on the inland waters of North America. Am Zool 36:287–299CrossRefGoogle Scholar
  41. Madsen JD, Chambers PA, James WF, Koch EW, Westlake DF (2001) The interaction between water movement, sediment dynamics and submersed macrophytes. Hydrobiologia 444:71–84CrossRefGoogle Scholar
  42. Malavasi S, Franco A, Fiorin R, Franzoi P, Torricelli P, Mainardi D (2005) The shallow water gobiid assemblage of the Venice Lagoon: abundance, seasonal variation and habitat partitioning. J Fish Biol 67:146–165CrossRefGoogle Scholar
  43. Marchetti MP (1999) An experimental study of competition between the native Sacramento perch (Archoplites interruptus) and introduced bluegill (Lepomis macrochirus). Biol Invasions 1:55–65CrossRefGoogle Scholar
  44. Marchetti MP, Light T, Feliciano J, Armstrong T, Hogan Z, Viers J, Moyle PB (2001) Homogenization of California’s fish fauna through abiotic change. In: Biot Homog [Internet]. p. 259–278. http://link.springer.com/chapter/10.1007/978-1-4615-1261-5_13. Accessed 27 Apr 2017
  45. Matern SA, Brown LR (2005) Invaders eating invaders: exploitation of novel alien prey by the alien shimofuri goby in the San Francisco Estuary, California. Biol Invasions 7:497–507CrossRefGoogle Scholar
  46. Matern SA, Moyle PB, Pierce LC (2002) Native and alien fishes in a California estuarine marsh: twenty-one years of changing assemblages. Trans Am Fish Soc 131:797–816. doi: 10.1577/1548-8659(2002)131<0797:NAAFIA>2.0.CO;2 CrossRefGoogle Scholar
  47. McElreath R (2015) Rethinking: an R package for fitting and manipulating Bayesian models [Internet]. [place unknown]. https://github.com/rmcelreath/rethinking
  48. Meng L, Matern SA (2001) Native and introduced larval fishes of Suisun Marsh, California: the effects of freshwater flow. Trans Am Fish Soc 130:750–765CrossRefGoogle Scholar
  49. Meng L, Moyle PB, Herbold B (1994) Changes in abundance and distribution of native and introduced fishes of Suisun Marsh. Trans Am Fish Soc 123:498–507CrossRefGoogle Scholar
  50. Miyazaki Y, Terui A (2016) Difference in habitat use between the two related goby species of Gymnogobius opperiens and Gymnogobius urotaenia: a case study in the Shubuto River System, Hokkaido, Japan. Ichthyol Res.:1–7Google Scholar
  51. Moyle PB (2002) Inland fishes of California. University of California Press, BerkeleyGoogle Scholar
  52. Moyle PB, Leidy RA (1992) Loss of biodiversity in aquatic ecosystems: evidence from fish faunas. In: Fiedler PL, Jain SK (eds) Conservation biology the theory and practice of nature conservation preservation and management. Chapman and Hall, New York, pp 127–170Google Scholar
  53. Moyle PB, Light T (1996a) Fish invasions in California: do abiotic factors determine success? Ecology 77:1666–16670CrossRefGoogle Scholar
  54. Moyle PB, Light T (1996b) Biological invasions of fresh water: empirical rules and assembly theory. Biol Conserv 78:149–161CrossRefGoogle Scholar
  55. Moyle PB, Marchetti MP (2006) Predicting invasion success: freshwater fishes in California as a model. Bioscience 56:515–524CrossRefGoogle Scholar
  56. Moyle PB, Bennett WA, Dahm C, Durand JR, Enright C, Fleenor WE, Kimmerer W, Lund JR (2010) Changing ecosystems: a brief ecological history of the Delta. Report to the California State Water Resource Control Board Sacram CA FebrGoogle Scholar
  57. Moyle P, Bennett W, Durand J, Fleenor W, Gray B, Hanak E, Lund JR, Mount J (2012) Where the wild things aren’t: making the delta a better place for native species [Internet]. Public Policy Institute of California, San Francisco. http://www.ppic.org/main/publication.asp?i=1025. Accessed 06 May 2016
  58. Moyle PB, Manfree AD, Fiedler PL (2014) Suisun Marsh: ecological history and possible futures. University of California Press, BerkeleyCrossRefGoogle Scholar
  59. Nichols FH, Thompson JK, Schemel LE (1990) Remarkable invasion of San Francisco Bay (California, USA) by the Asian clam Potamocorbula amurensis. 2. Displacement of a former community. Mar Ecol Prog Ser 66:95–101CrossRefGoogle Scholar
  60. Nobriga ML, Feyrer F (2007) Shallow-water piscivore-prey dynamics in California’s Sacramento-San Joaquin Delta. San Francisco Estuary Watershed Sci [Internet]. 5. http://escholarship.org/uc/item/387603c0. Accessed 28 April 2017
  61. O’Rear TA (2012) Diet of an introduced estuarine population of white catfish in California [M.S. Thesis]. University of California, Davis, DavisGoogle Scholar
  62. O'Rear TA, Moyle PB (2015) Trends in fish and invertebrate populations of Suisun Marsh January 2013-December 2013. Annual Report for the California Department of Water Resources, Sacramento, CAGoogle Scholar
  63. Pianka ER (1969) Sympatry of desert lizards (Ctenotus) in Western Australia. Ecology 50:1012–1030CrossRefGoogle Scholar
  64. Pratt AE, Lauer TE (2013) Habitat use and separation among congeneric darter species. Trans Am Fish Soc 142:568–577CrossRefGoogle Scholar
  65. R Development Core Team. 2015. R: A language and environment for statistical computing [Internet]. [place unknown]: R Foundation for Statistical Computing, Vienna. http://www.R-project.org
  66. Rahel FJ (2002) Homogenization of freshwater faunas. Annu Rev Ecol Syst 33:291–315CrossRefGoogle Scholar
  67. Ross ST (1986) Resource partitioning in fish assemblages: a review of field studies. Copeia 1986(2):352–388CrossRefGoogle Scholar
  68. Rudnick DA, Hieb K, Grimmer KF, Resh VH (2003) Patterns and processes of biological invasion: the Chinese mitten crab in San Francisco Bay. Basic Appl Ecol 4:249–262. http://dx.doi.org/10.1078/1439-1791-00152. Accessed 28 April 2017
  69. Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632CrossRefGoogle Scholar
  70. Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39CrossRefPubMedGoogle Scholar
  71. Sheaves MJ (1992) Patterns of distribution and abundance of fishes in different habitats of a mangrove-lined tropical estuary, as determined by fish trapping. Mar Freshw Res 43:1461–1479CrossRefGoogle Scholar
  72. Siegfried CA (1982) Trophic relations of Crangon franciscorum Stimpson and Palaemon macrodactylus Rathbum: predation on the opossum shrimp, Neomysis mercedis Holmes. Hydrobiologia 89:129–139CrossRefGoogle Scholar
  73. Szedlmayer ST, Able KW (1996) Patterns of seasonal availability and habitat use by fishes and decapod crustaceans in a Southern New Jersey Estuary. Estuaries 19:697. doi: 10.2307/1352529 CrossRefGoogle Scholar
  74. Thompson J (1957) The settlement geography of the Sacramento-San Joaquin Delta, California. Stanford University, Palo AltoGoogle Scholar
  75. van der Wegen M, Jaffe BE (2014) Processes governing decadal-scale depositional narrowing of the major tidal channel in San Pablo Bay, California, USA. J Geophys Res Earth Surf 119:1136–1154. http://dx.doi.org/10.1002/2013JF002824. Accessed 28 April 2017
  76. van Snik Gray E, Stauffer JR Jr (1999) Comparative microhabitat use of ecologically similar benthic fishes. Environ Biol Fishes 56:443–453CrossRefGoogle Scholar
  77. Whipple A, Grossinger RM, Rankin D, Stanford B, Askevold R (2012) Sacramento-San Joaquin Delta historical ecology investigation: exploring pattern and process [Internet]. San Francisco Estuary Institute–Aquatic Science Center, Richmond. http://www.sfei.org/DeltaHEStudy. Accessed 28 April 2017
  78. Whitcraft CR, Grewell BJ, Baye PR (2011) Estuarine vegetation at Rush Ranch Open Space preserve, San Franciso Bay national estuarine research reserve, California. San Franc Estuary Watershed Sci [Internet]. 9. http://escholarship.org/uc/item/6j89531r. Accessed 14 Feb 2015
  79. White JL, Harvey BC (1999) Habitat separation of prickly sculpin, Cottus asper, and coastrange sculpin, Cottus aleuticus, in the mainstem Smith River, northwestern California. Copeia 1999(2):371–375CrossRefGoogle Scholar
  80. Winder M, Jassby AD (2010) Shifts in zooplankton community structure: Implications for food web processes in the upper San Francisco Estuary. Estuaries Coast 34:675–690. doi: 10.1007/s12237-010-9342-x CrossRefGoogle Scholar
  81. Wright SA, Schoellhamer DH (2004) Trends in the sediment yield of the Sacramento River, California, 1957–2001. San Franc Estuary Watershed Sci [Internet]. 2. http://escholarship.org/uc/item/891144f4. Accessed 28 April 2017
  82. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Zero-truncated and Zero-inflated models for Count Data. In: Mixed effects models and extensions in ecology with R [Internet]. Springer, New York, p 261–293. http://link.springer.com/chapter/10.1007/978-0-387-87458-6_11http://dx.doi.org/10.1007/978-0-387-87458-6_11. Accessed 2017 Apr 8

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Matthew J. Young
    • 1
  • Kathleen A. Berridge
    • 1
  • Teejay O’Rear
    • 1
  • Peter B. Moyle
    • 1
  • John R. Durand
    • 1
    Email author
  1. 1.Center for Watershed SciencesUniversity of California, DavisDavisUSA

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