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Biological Invasions

, Volume 20, Issue 1, pp 105–119 | Cite as

Factors affecting distribution and abundance of jellyfish medusae in a temperate estuary: a multi-decadal study

  • Jason Baumsteiger
  • Teejay A. O’Rear
  • Jonathan D. Cook
  • Amber D. Manfree
  • Peter B. Moyle
Original Paper

Abstract

Three hydrozoan species, reputedly from the Black Sea (Maeotias marginata, Blackfordia virginica, Moerisia lyonsi), are now found throughout the San Francisco Estuary, California, but long-term and seasonal patterns of distribution and abundance have been poorly documented. We evaluated trends from 35 years of monthly otter trawl data and from a 2-year macrozooplankton survey in Suisun Marsh, a brackish region with extensive tidal sloughs and channels that is part of the San Francisco Estuary. Medusae of all three hydrozoans occurred primarily during the dry season (summer–fall). Abundance of M. marginata medusae significantly increased since the 1980s. Moerisia lyonsi was the most abundant hydrozoan in the macrozooplankton medusa survey followed by M. marginata and B. virginica. Salinity and temperature were strongly positively associated with medusa abundance. Maeotias marginata occurred in the lowest salinity range (2.3–9.1 ppt), while M. lyonsi (2.8–9.9 ppt) and B. virginica (5.6–10.3 ppt) occupied slightly higher salinities. Overall, abundance and distribution of medusae of these three hydrozoans in Suisun Marsh depended on seasonal stability of environmental conditions that favored blooms. While harmful effects have yet to be demonstrated, they could become more of a problem as both sea level and water temperatures rise, especially given the combined range of environmental conditions at which the three species occur.

Keywords

Hydrozoans Medusa Non-native species Generalized linear model 

Notes

Acknowledgements

Sampling in Suisun Marsh has been the responsibility of many graduate students and others over the years, especially Donald Baltz, Robert Daniels, Bruce Herbold, Lesa Meng, Scott Matern, Patrick Crain, John Durand, Alpa Wintzer, and Sabra Purdy. We have also been assisted by literally hundreds of volun-teers and student assistants. Special thanks to Robert Schroeter for collecting much of the jellyfish data and conducting some preliminary analyses. A final thank you goes to subject editor Jim Carlton and two anonymous reviewers for their helpful comments and suggestions which made for a better overall manuscript.

Supplementary material

10530_2017_1518_MOESM1_ESM.pdf (578 kb)
Supplementary material 1 (PDF 578 kb)

References

  1. Bardi J, Marques AC (2009) The invasive hydromedusae Blackfordia virginica Mayer, 1910 (Cnidaria: Blackfordiidae) in southern Brazil, with comments on taxonomy and distribution of the genus Blackfordia. Zootaxa 2198:41–50Google Scholar
  2. Berry WD, Felman S (1985) Multiple regression in practice. Sage Publications, Beverly HillsCrossRefGoogle Scholar
  3. Boulenger CA (1908) On Moerisia lyonsi, a new hydromedusan from Lake Qurun. Q J Microsc Sci 52:357–378Google Scholar
  4. Brewer RH, Feingold JS (1991) The effect of temperature on the benthic stages of Cyanea (Cnidaria:Schyphozoa), and their seasonal distribution in the Niantic River estuary, Connecticut. J Exper Mar Biol Ecol 152:49–60CrossRefGoogle Scholar
  5. Brown LR, Kimmerer W, Conrad JL, Lesmeister S, Muller-Solger A (2016) Food webs of the Delta, Suisun Bay, and Suisun Marsh: an update on current understanding and possibilities for management. SF Est. Water Sci. 14(3). doi: http://escholarship.org/uc/item/4mk5326r
  6. Chícharo A, Leitão T, Range P, Gutierrez C, Morales J, Morais P, Chícharo L (2009) Alien species in the Guadiana Estuary (SE-Portugal/SW-Spain): Blackfordia virginica (Cnidaria, Hydrozoa) and Palaemon macrodactylus (Crustacea, Decapoda): potential impacts and mitigation measures. Aquat Inv 4(3):501–506CrossRefGoogle Scholar
  7. Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558CrossRefPubMedGoogle Scholar
  8. Decker MB, Brown CW, Hood RR, Purcell JE, Gross TF, Matanoski JC, Bannon RO, Setzler-Hamilton EM (2007) Predicting the distribution of the scyphomedusa Chrysaora quinquecirrha in Chesapeake Bay. Mar Ecol Prog Ser 329:99–113CrossRefGoogle Scholar
  9. Feyrer F, Nobriga ML, Sommer TR (2007) Multidecadal trends for three declining fish species: habitat patterns and mechanisms in the San Francisco Estuary, California, USA. Can J Fish Aquat Sci 64:723–734CrossRefGoogle Scholar
  10. Greene VE, Sullivan LJ, Thompson JK, Kimmerer WJ (2011) Grazing impact of the invasive clam Corbula amurensis on the microplankton assemblage of the northern San Francisco Estuary. Mar Ecol Prog Ser 431:183–193CrossRefGoogle Scholar
  11. Guisan A, Edwards TC Jr, Hastie T (2002) Generalized linear and generalized additive models in studies of species distribution: setting the scene. Ecol Model 157:89–100CrossRefGoogle Scholar
  12. Helsel DR, Hirsch RM (1992) Statistical methods in water resources. Elsevier Science Publications, New YorkGoogle Scholar
  13. Hilbe JM (2007) Negative binomial regression, 2nd edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  14. Howat IM, Tulaczyk S (2005) Trends in spring snowpack over a half-century of climate warming in California, USA. Ann Glaciol 40:151–156CrossRefGoogle Scholar
  15. Kendall M, Gibbons JD (1990) Rank correlation methods, 5th edn. Oxford University Press, New YorkGoogle Scholar
  16. Knowles N, Cayan DR (2002) Potential effects of global warming on the Sacramento/San Joaquin watershed and the San Francisco estuary. Geophy Res Lett 29:38.1–38.4CrossRefGoogle Scholar
  17. Lucas CH (2001) Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment. Hydrobiologia 451:229–246CrossRefGoogle Scholar
  18. Lund J, Hanak E, Fleenor W, Bennet W, Howitt R, Mount J, Moyle PB (2010) Comparing futures for the Sacramento-San Joaquin Delta. University of California Press, BerkeleyCrossRefGoogle Scholar
  19. Ma X, Purcell JE (2005a) Effects of temperature, salinity and predators on mortality of and colonization by the invasive hydrozoan Moerisia lyonsi. Mar Biol 147:215–224CrossRefGoogle Scholar
  20. Ma X, Purcell JE (2005b) Temperature, salinity, and prey effects on the polyp versus medusa bud production of the invasive hydrozoan Moerisia lyonsi. Mar Biol 147:225–234CrossRefGoogle Scholar
  21. Marques F, Chainho P, Costa JL, Domingos I, Angélico MM (2015) Abundance, seasonal patterns and diet of the non-native jellyfish Blackfordia virginica in a Portuguese estuary. Estuar Coast Shelf Sci 167:212–219CrossRefGoogle Scholar
  22. 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 131:797–816CrossRefGoogle Scholar
  23. Mayer AG (1910) Genus Blackfordia, gen. nov. In: Mayor AG (ed) Medusae of the world, volume II, the hydromedusae. Carnegie Institution of Washington, Washington, pp 276–278Google Scholar
  24. McLeod AI (2011) Kendall: Kendall rank correlation and Mann-Kendall trend test. R package version 2.2. Available: https://CRAN.R-project.org/package=Kendall
  25. Meek MH, Wintzer AP, Wetzel WC, May B (2012) Climate Change likely to facilitate the invasion of the non-native hydroid, Cordylophora caspia, in the San Francisco Estuary. PLoS ONE 7(10):e46373. doi: 10.1371/journal.pone.0046373 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Meek MH, Wintzer AP, Sheperd N, May B (2013) Genetic diversity and reproductive mode in two non-native hydromedusae, Maeotias marginata and Moerisia sp., in the Upper San Francisco Estuary, California. Biol Invasions 15(1):199–212CrossRefGoogle Scholar
  27. 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
  28. Mills CE, Rees JT (2000) New observations and corrections concerning the trio of invasive hydromedusae Maeotias marginata (= M. inexpectata), Blackfordia virginica, and Moerisia sp. in the San Francisco Estuary. Sci Mar 64((Suppl. 1)):151–155CrossRefGoogle Scholar
  29. Mills CE, Sommer F (1995) Invertebrate introductions in marine habitats: two species of hydromedusae (Cnidaria) native to the Black Sea, Maeotias inexspectata and Blackfordia virginica, invade San Francisco Bay. Mar Biol 122:279–288Google Scholar
  30. Modeer A (1791) Tentamen systematis medusarum stabiliendi. Nova acta physico-medica Academiae Caesareae Leopoldino-Carolinae, Naturae Curiosum 8 (Appendix): 19–34. http://www.biodiversitylibrary.org/item/132020#page/443/mode/1up
  31. Moore SJ (1987) Redescription of the leptomedusan Blackfordia virginica. J Mar Biol Assoc U.K. 67:287–291CrossRefGoogle Scholar
  32. Moyle PB, Hobbs J, O’Rear T (2012) Fishes. In: Palaima A (ed) Ecology, conservation and restoration of tidal marshes: the San Francisco estuary. University of California Press, Berkeley, pp 161–173CrossRefGoogle Scholar
  33. Moyle PB, Manfree AD, Fiedler PL (2014) Suisun marsh: ecological history and possible futures. University of California Press, BerkeleyCrossRefGoogle Scholar
  34. Nowaczyk A, David V, Lepage M, Goarant A, de Oliveira E, Sautour B (2016) Spatial and temporal patterns of occurrence of three alien hydromedusae, Blackfordia virginica (Mayer, 1910), Nemopsis bachei (Agassiz, 1849) and Maeotias marginata (Modeer, 1791), in the Gironde Estuary (France). Aquat Inv 11(4):397–409CrossRefGoogle Scholar
  35. O’Rear T, Moyle PB (2014) In: Moyle PB, Manfree AD, Fiedler PL (eds) suisun marsh: ecological history and possible futures. University of California Press, BerkeleyGoogle Scholar
  36. Purcell JE (2005) Climate effects on formation of jellyfish and ctenophore blooms. J Mar Biol Assoc U.K. 85:461–476CrossRefGoogle Scholar
  37. Purcell JE, Båmstedt U, Båmstedt A (1999) Prey, feeding rates, and asexual reproduction rates of the introduced oligohaline hydrozoan Moerisia lyonsi. Mar Biol 134:317–325CrossRefGoogle Scholar
  38. Purcell JE, Uye S, Lo W (2007) Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Mar Ecol Prog Ser 350:153–174CrossRefGoogle Scholar
  39. Rees JT, Gershwin LA (2000) Non-indigenous hydromedusae in California’s upper San Francisco Estuary: life cycles, distribution, and potential environmental impacts. Sci Mar 64(Suppl. 1):73–86CrossRefGoogle Scholar
  40. Rees JT, Kitting CL (2002) Survey of gelatinous zooplankton (“Jellyfish”) in the San Francisco Estuary: initial field survey, annotated species checklist and field key. In: Interagency ecological program, Technical Report 70Google Scholar
  41. Santhakumari V, Ramaiah N, Nair VR (1997) Ecology of hydromedusae from Bombay Harbour—Thana and Bassein Creek estuarine complex. Ind J Mar Sci 26:162–168Google Scholar
  42. Schroeter RE (2008). Biology and long-term trends of alien hydromedusae and striped bass in a brackish tidal marsh in the San Francisco Estuary. Ph.D. Dissertation, University of California, DavisGoogle Scholar
  43. Schroeter RE, O’Rear TA, Young MJ, Moyle PB (2015) The aquatic trophic ecology of Suisun Marsh, San Francisco Estuary, California, during autumn in a wet year. SF Estuar Water Sci 13(3):1–18Google Scholar
  44. Vainola R, Oulasvirta P, Hoisater T (2001) The first record of Maeotias marginata (Cnidaria, Hydrozoa) from the Baltic Sea: a Pontocaspian invader. Sarsia 86:401–404CrossRefGoogle Scholar
  45. Winder M, Jassby AD (2011) Shifts in zooplankton community structure: implications for food web processes in the upper San Francisco Estuary. Estuar Coasts 34:675–690CrossRefGoogle Scholar
  46. Wintzer AP (2010) Ecology of the non-native hydrozoans in the San Francisco Estuary: implications for pelagic organism decline fishes. Ph.D. dissertation, University of California, Davis. http://gateway.proquest.com/openurl?url_ver=Z39.88-2004&res_dat=xri:pqdiss&rft_val_fmt=info:ofi/fmt:kev:mtx:dissertation&rft_dat=xri:pqdiss:3427453
  47. Wintzer AP, Meek MH, Moyle PB, May B (2011a) Ecological insights into the polyp stage of non-native hydrozoans in the San Francisco Estuary. Aquat Ecol 45:151–161CrossRefGoogle Scholar
  48. Wintzer AP, Meek MH, Moyle PB (2011b) Life history and population dynamics of Moerisia sp., a non-native hydrozoan, in the upper San Francisco Estuary (U.S.A.). Estuar Coast Shelf Sci 94(1):48–55CrossRefGoogle Scholar
  49. Wintzer AP, Meek MH, Moyle PB (2011c) Trophic ecology of two non-native hydrozoan medusae in the upper San Francisco Estuary. Mar Fresh Res 62:952–961CrossRefGoogle Scholar
  50. Wintzer AP, Meek MH, Moyle PB (2013) Abundance, size, and diel feeding ecology of Blackfordia virginica (Mayer, 1910), a non-native hydrozoan in the lower Napa and Petaluma Rivers, California (USA). Aquat Inv 8:147–156CrossRefGoogle Scholar
  51. Xia W, Kang B, Liu R (2005) Jellyfish blooms in the Yangtze Estuary. Science 307:41. doi: 10.1126/science.307.5706.41c Google Scholar
  52. Zhu T, Jenkins MW, Lund JR (2005) Estimated impacts of climate warming on California water availability under twelve future climate scenarios. J Am Water Res Assoc 41:1027–1038CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Jason Baumsteiger
    • 1
  • Teejay A. O’Rear
    • 1
  • Jonathan D. Cook
    • 2
  • Amber D. Manfree
    • 1
  • Peter B. Moyle
    • 1
    • 2
  1. 1.Center for Watershed SciencesUniversity of California-DavisDavisUSA
  2. 2.Department of Wildlife, Fish, and Conservation BiologyUniversity of California-DavisDavisUSA

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