Estuaries and Coasts

, Volume 41, Issue 7, pp 1848–1867 | Cite as

Recruitment Ecology of Burrowing Shrimps in US Pacific Coast Estuaries

  • Brett R. Dumbauld
  • Katelyn M. Bosley
Management Applications


Recruitment is a strong determinant of year class strength and adult population density especially for sessile benthic invertebrates where post-settlement mortality and competition are low or relatively stable over time. A series of surveys were undertaken to characterize recruitment and post-settlement processes for two species of burrowing shrimps, Neotrypaea californiensis and Upogebia pugettensis in order to determine how they influenced broader adult populations in US west coast estuaries. On average, U. pugettensis decapodids settled earlier (April–July), recruited almost exclusively to areas with conspecific adults, and grew more rapidly during their first summer than N. californiensis. Neotrypaea californiensis decapodids settled and recruited over a longer period (June–November) and were distributed across the tidal flat. While initially more abundant in areas with conspecific adults, they also either survived better or redistributed as small juvenile shrimp to areas where adults were absent. Linear relationships were found between abundance of newly recruited (0+ age class) shrimp and that of older 1+ shrimp a year later. Positive slopes were close to one for N. californiensis but less than one for U. pugettensis, suggesting lower survival. Annual recruitment varied dramatically but was more consistent for both species in Yaquina Bay. Patterns in strong recruitment years amongst estuaries, particularly for U. pugettensis, suggest the presence of multi-estuary metapopulations linked via larval dispersal. These results have important implications for shrimp population management including control for shellfish aquaculture, but also conservation of estuarine habitats due to the strong influence of these ecosystem engineers on the benthic community.


Ecosystem engineers Estuary Neotrypaea californiensis Mortality Recruitment limitation Settlement Upogebia pugettensis 



The authors especially thank Lee McCoy and John Chapman for their dedicated assistance and help with field work, data analysis, and interpretation particularly during the 2010–2012 surveys in Yaquina Bay. We are grateful to a host of field assistants that are too numerous to mention that assisted with the long-term monitoring program but include most significantly Kristine Feldman who served over most of the program’s life and in more recent years efforts by Daniel Sund, Dacey Mercer, Jonathan Minch, Samantha Bund, Cara Fritz, Roy Hildenbrand, and Roxanna Hintzman. The Willapa Bay/Grays Harbor Shellfish growers provided significant in-kind assistance including use of their beds and consultation including assistance from integrated pest management coordinators Steve Booth, Jacob Moore, and David Beugli. We also frequently collaborated with and acknowledge similar Willapa Bay surveys and support from Kim Patten at the Washington State University extension station in Long Beach. Previous versions of the manuscript were greatly improved by comments from several reviewers including Dany de Oliveira, Dacey Mercer, and one anonymous reviewer. Mention of trade names or commercial products does not constitute endorsement or recommendation for use.

Funding Information

This research was funded by the U.S. Department of Agriculture, Agricultural Research Service (CRIS Project 2072-63000-004-00D) and several other institutions and granting agencies over the life of the long-term monitoring program including the Washington State Department of Fisheries, the Western Regional Aquaculture Center and Washington Sea Grant.

Supplementary material

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  1. Armstrong, J.L., D.A. Armstrong, and S.B. Mathews. 1995. Food habits of estuarine staghorn sculpin, Leptocottus armatus, with focus on consumption of juvenile Dungeness crab, Cancer magister. Fishery Bulletin 93: 456–470.Google Scholar
  2. Asson, D., J.W. Chapman, and B.R. Dumbauld. 2017. No evidence that the introduced parasite Orthione griffenis Markham, 2004 causes sex change or differential mortality in the native mud shrimp, Upogebia pugettensis (Dana, 1852). Aquatic Invasions 12 (2): 213–224.CrossRefGoogle Scholar
  3. Bird, E.M. 1982. Population dynamics of thalassinidean shrimps and community effects through sediment modification. Ph. D. dissertation, University of Maryland, College Park, Maryland.Google Scholar
  4. Borin, J., M.L. Moser, A. Hansen, D.A. Beauchamp, S. Corbett, B.R. Dumbauld, C. Pruitt, J. Ruesink, and C. Donohue. 2017. Energetic requirements of green sturgeon (Acipensier medirostris) feeding on burrowing shrimp (Neotrypaea californiensis) in estuaries: importance of temperature, reproductive investment, and residence time. Environmental Biology of Fishes 100 (12): 1561–1573.CrossRefGoogle Scholar
  5. Bosley, K. 2016. An integrated approach to the investigation of age, growth and population dynamics of burrowing thalassinidean shrimps in a US West Coast estuary, Ph. D. dissertation, Oregon State University, Corvallis, Oregon.Google Scholar
  6. Bosley, K.M., L.A. Copeman, B.R. Dumbauld, and K.L. Bosley. 2017. Identification of burrowing shrimp food sources along an estuarine gradient using fatty acid analysis and stable isotope ratios. Estuaries and Coasts 40 (4): 1113–1130.CrossRefGoogle Scholar
  7. Bosley, K.M., and B.R. Dumbauld. 2011. Use of extractable lipofuscin to estimate age structure of ghost shrimp populations in west coast estuaries of the USA. Marine Ecology-Progress Series 428: 161–176.CrossRefGoogle Scholar
  8. Breckenridge, J.K., and S.M. Bollens. 2010. Biological thin layer formation: interactions between the larval decapod, Neotrypaea californiensis, haloclines and light. Journal of Plankton Research 32 (7): 1097–1102.CrossRefGoogle Scholar
  9. Broitman, B.R., C.A. Blanchette, B.A. Menge, J. Lubchenco, C. Krenz, M. Foley, P.T. Raimondi, D. Lohse, and S.D. Gaines. 2008. Spatial and temporal patterns of invertebrate recruitment along the West Coast of the United States. Ecological Monographs 78 (3): 403–421.CrossRefGoogle Scholar
  10. Camus, P.A., and M. Lima. 2002. Populations, metapopulations, and the open-closed dilemma: the conflict between operational and natural population concepts. Oikos 97 (3): 433–437.CrossRefGoogle Scholar
  11. Castorani, M.C.N., K.A. Hovel, S.L. Williams, and M.L. Baskett. 2014. Disturbance facilitates the coexistence of antagonistic ecosystem engineers in California estuaries. Ecology 95 (8): 2277–2288.CrossRefGoogle Scholar
  12. Chapman, J.W., and C.S. Carter. 2014. A rapid intertidal megafauna survey method applied to Upogebia pugettensis, and its introduced parasite, Orthione griffensis. Journal of Crustacean Biology 34 (3): 349–356.CrossRefGoogle Scholar
  13. Chapman, J.W., B.R. Dumbauld, G. Itani, and J.C. Markham. 2012. An introduced Asian parasite threatens northeastern Pacific estuarine ecosystems. Biological Invasions 14 (6): 1221–1236.CrossRefGoogle Scholar
  14. Connolly, S.R., and J. Roughgarden. 1998. A latitudinal gradient in northeast Pacific intertidal community structure: evidence for an oceanographically based synthesis of marine community theory. American Naturalist 151 (4): 311–326.CrossRefGoogle Scholar
  15. D'Andrea, A.F., and T.H. DeWitt. 2009. Geochemical ecosystem engineering by the mud shrimp Upogebia pugettensis (Crustacea: Thalassinidae) in Yaquina Bay, Oregon: density-dependent effects on organic matter remineralization and nutrient cycling. Limnology and Oceanography 54 (6): 1911–1932.CrossRefGoogle Scholar
  16. de Oliveira, D.B., J.M. Martinelli-Lemos, A.S. de Souza, J.R. da Costa, and F.A. Abrunhosa. 2016. Does retention or exportation occur in the larvae of the mud shrimp Upogebia vasquezi (Decapoda, Gebiidea)? Implications for the reproductive strategy of the species on the Amazon coast. Hydrobiologia 773 (1): 241–252.CrossRefGoogle Scholar
  17. de Oliveira, D.B., D.C. Silva, and J.M. Martinelli. 2012. Density of larval and adult forms of the burrowing crustaceans Lepidophthalmus siriboia (Callianassidae) and Upogebia vasquezi (Upogebiidae) in an Amazon estuary, northern Brazil. Journal of the Marine Biological Association of the United Kingdom 92 (02): 295–303.CrossRefGoogle Scholar
  18. DeWitt, T.H., A.F. D'Andrea, C.A. Brown, B.D. Griffen, and P.M. Eldridge. 2004. Impact of burrowing shrimp populations on nitrogen cycling and water quality in western north American temperate estuaries. In Symposium on “Ecology of large bioturbators in tidal flats and shallow sublittoral sediments-from individual behavior to their role as ecosystem engineers”, ed. A. Tamaki, 107–118. Nagasaki: Nagasaki University.Google Scholar
  19. Dudas, S.E., B.A. Grantham, A.R. Kirincich, B.A. Menge, J. Lubchenco, and J.A. Barth. 2009. Current reversals as determinants of intertidal recruitment on the central Oregon coast. ICES Journal of Marine Science 66: 396–407.CrossRefGoogle Scholar
  20. Dumbauld, B.R., D.A. Armstrong, and K.L. Feldman. 1996. Life-history characteristics of two sympatric thalassinidean shrimps, Neotrypaea californiensis and Upogebia pugettensis, with implications for oyster culture. Journal of Crustacean Biology 16 (4): 689–708.CrossRefGoogle Scholar
  21. Dumbauld, B.R., S. Booth, D. Cheney, A. Suhrbier, and H. Beltran. 2006. An integrated pest management program for burrowing shrimp control in oyster aquaculture. Aquaculture 261 (3): 976–992.CrossRefGoogle Scholar
  22. Dumbauld, B.R., K.M. Brooks, and M.H. Posey. 2001. Response of an estuarine benthic community to application of the pesticide carbaryl and cultivation of Pacific oysters (Crassostrea gigas) in Willapa Bay, Washington. Marine Pollution Bulletin 42 (10): 826–844.CrossRefGoogle Scholar
  23. Dumbauld, B.R., J.W. Chapman, A.M. Kuris, and M.E. Torchin. 2011. Is the collapse of mud shrimp (Upogebia pugettensis) populations along the Pacific coast of North America caused by outbreaks of a previously unknown bopyrid isopod parasite (Orthione griffenis)? Estuaries and Coasts 34 (2): 336–350.CrossRefGoogle Scholar
  24. Dumbauld, B.R., K. Feldman, and D. Armstrong. 2004. A comparison of the ecology and effects of two species of thalassinidean shrimps on oyster aquaculture operations in the eastern North Pacific. In Symposium on “Ecology of large bioturbators in tidal flats and shallow sublittoral sediments-from individual behavior to their role as ecosystem engineers”, ed. A. Tamaki, 53–61. Nagasaki: Nagasaki University.Google Scholar
  25. Dumbauld, B.R., D.L. Holden, and O.P. Langness. 2008. Do sturgeon limit burrowing shrimp populations in Pacific Northwest estuaries. Environmental Biology of Fishes 83 (3): 283–296.CrossRefGoogle Scholar
  26. Dumbauld, B.R., and L.M. McCoy. 2015. The effect of oyster aquaculture on seagrass (Zostera marina) at the estuarine landscape scale in Willapa Bay, Washington (USA). Aquaculture Environment Interactions 7 (1): 29–47.CrossRefGoogle Scholar
  27. Dumbauld, B.R., J.L. Ruesink, and S.S. Rumrill. 2009. The ecological role of bivalve shellfish aquaculture in the estuarine environment: a review with application to oyster and clam culture in West Coast (USA) estuaries. Aquaculture 290 (3-4): 196–223.CrossRefGoogle Scholar
  28. Dumbauld, B.R., and S. Wyllie-Echeverria. 2003. The influence of burrowing thalassinid shrimps on the distribution of intertidal seagrasses in Willapa Bay, Washington, USA. Aquatic Botany 77 (1): 27–42.CrossRefGoogle Scholar
  29. Etherington, L., and D. Eggleston. 2000. Large-scale blue crab recruitment: linking postlarval transport, post-settlement planktonic dispersal, and multiple nursery habitats. Marine Ecology Progress Series 204: 179–198.CrossRefGoogle Scholar
  30. Feldman, K. 2001. Contrasting patterns of habitat-specific recruitment success in sympatric species of thalassinidean shrimp: effects of epibenthic bivalve shell with implications for population control in areas with commercial oyster aquaculture. Ph. D. Thesis, University of Washington Seattle, Washington.Google Scholar
  31. Feldman, K.L., D.A. Armstrong, B.R. Dumbauld, T.H. DeWitt, and D.C. Doty. 2000. Oysters, crabs, and burrowing shrimp: review of an environmental conflict over aquatic resources and pesticide use in Washington State's (USA) coastal estuaries. Estuaries 23 (2): 141–176.CrossRefGoogle Scholar
  32. Feldman, K.L., D.A. Armstrong, D.B. Eggleston, and B.R. Dumbauld. 1994. Ghost shrimp recruitment to intertidal shell and mud habitats: effects of substrate selection and post settlement survival on distribution of young-of-the-year5699.Google Scholar
  33. Feldman, K.L., D.A. Armstrong, D.B. Eggleston, and B.R. Dumbauld. 1997. Effects of substrate selection and post-settlement survival on recruitment success of the thalassinidean shrimp Neotrypaea californiensis to intertidal shell and mud habitats. Marine Ecology Progress Series 150: 121–136.CrossRefGoogle Scholar
  34. Ferraro, S.P., and F.A. Cole. 2010. Ecological periodic tables for nekton usage of four US Pacific Northwest estuarine habitats. Canadian Journal of Fisheries and Aquatic Sciences 67 (12): 1957–1967.CrossRefGoogle Scholar
  35. Ferraro, S.P., and F.A. Cole. 2011. Ecological periodic tables for benthic macrofaunal usage of estuarine habitats in the US Pacific Northwest. Estuarine Coastal and Shelf Science 94 (1): 36–47.CrossRefGoogle Scholar
  36. Fisher, J.L., W.T. Peterson, and S.G. Morgan. 2014. Does larval advection explain latitudinal differences in recruitment across upwelling regimes? Marine Ecology Progress Series 503: 123–137.CrossRefGoogle Scholar
  37. Gaines, S., and J. Roughgarden. 1985. Larval settlement rate—a leading determinant of structure in an ecological community of the marine intertidal zone. Proceedings of the National Academy of Sciences of the United States of America 82 (11): 3707–3711.CrossRefGoogle Scholar
  38. Garcia-Reyes, M., and J.L. Largier. 2012. Seasonality of coastal upwelling off central and northern California: new insights, including temporal and spatial variability. Journal of Geophysical Research-Oceans 117 (C3).CrossRefGoogle Scholar
  39. Hameed, S.O., M.L. Elliott, S.G. Morgan, and J. Jahnke. 2018. Interannual variation and spatial distribution of decapod larvae in a region of strong upwelling. Marine Ecology Progress Series 587: 55–71.CrossRefGoogle Scholar
  40. Hannah, R.W. 2011. Variation in the distribution of ocean shrimp (Pandalus jordani) recruits: links with coastal upwelling and climate change. Fisheries Oceanography 20 (4): 305–313.CrossRefGoogle Scholar
  41. Harada, K., and A. Tamaki. 2004. Assessment of the predation impact of the stingray Dasytis akajei (Muller and Henle, 1841) on the population of the ghost shrimp Nihonotrypaea harmandi (Bouvier, 1901) on and intertidal sandflat (preliminary report). In Symposium on “Ecology of large bioturbators in tidal flats and shallow sublittoral sediments-from individual behavior to their role as ecosystem engineers”, ed. A. Tamaki, 81–85. Nagasaki: Nagasaki University.Google Scholar
  42. Hart, J.F.L. 1937. Larval and adult stages of British Columbia Anomura. Canadian Journal of Research 15: 179–219.CrossRefGoogle Scholar
  43. Hernaez, P., E. Villegas-Jimenez, F. Villalobos-Rojas, and I.S. Wehrtmann. 2012. Reproductive biology of the ghost shrimp Lepidophthalmus bocourti (A. Milne-Edwards, 1870) (Decapoda: Axiidea: Callianassidae): a tropical species with a seasonal reproduction. Marine Biology Research 8 (7): 635–643.CrossRefGoogle Scholar
  44. Houde. 2008. Emerging from Hjort’s shadow. Journal of Northwest Atlantic Fisheries Science 41: 53–70.CrossRefGoogle Scholar
  45. Johnson, G.E., and J.J. Gonor. 1982. The tidal exchange of Callianassa californiensis (Crustacea, Decapoda) larvae between the ocean and Salmon River estuary, Oregon. Estuarine, Coastal and Shelf Science 14 (5): 501–516.CrossRefGoogle Scholar
  46. Kogan, M. 1998. Integrated pest management: historical perspectives and contemporary developments. Annual Review of Entomology 43 (1): 243–270.CrossRefGoogle Scholar
  47. Kritzer, J.P., and P.F. Sale. 2004. Metapopulation ecology in the sea: from Levins’ model to marine ecology and fisheries science. Fish and Fisheries 5 (2): 131–140.CrossRefGoogle Scholar
  48. Kunze, H.B., S.G. Morgan, and K.M. Lwiza. 2013. Field test of the behavioral regulation of larval transport. Marine Ecology Progress Series 487: 71–87.CrossRefGoogle Scholar
  49. Lefebvre, M., S.R.H. Langrell, and S. Gomez-Y-Paloma. 2015. Incentives and policies for integrated pest management in Europe: a review. Agronomy for Sustainable Development 35 (1): 27–45.CrossRefGoogle Scholar
  50. Leslie, H.M., E.N. Breck, F. Chan, J. Lubchenco, and B.A. Menge. 2005. Barnacle reproductive hotspots linked to nearshore ocean conditions. Proceedings of the National Academy of Sciences of the United States of America 102 (30): 10534–10539.CrossRefGoogle Scholar
  51. Lipcius, R.N., D.B. Eggleston, S.J. Schreiber, R.D. Seitz, J. Shen, M. Sisson, W.T. Stockhausen, and H.V. Wang. 2008. Importance of metapopulation connectivity to restocking and restoration of marine species. Reviews in Fisheries Science 16 (1-3): 101–110.CrossRefGoogle Scholar
  52. MacDonald, P. 2015. Mixdist: finite mixture distribution models. R package version 0.5–4
  53. Menge, B.A., T.C. Gouhier, T. Freidenburg, and J. Lubchenco. 2011. Linking long-term, large-scale climatic and environmental variability to patterns of marine invertebrate recruitment: toward explaining “unexplained” variation. Journal of Experimental Marine Biology and Ecology 400 (1-2): 236–249.CrossRefGoogle Scholar
  54. Morgan, S.G., and J.L. Fisher. 2010. Larval behavior regulates nearshore retention and offshore migration in an upwelling shadow and along the open coast. Marine Ecology-Progress Series 404: 109–126.CrossRefGoogle Scholar
  55. Morgan, S.G., J.L. Fisher, S.T. McAfee, J.L. Largier, and C.M. Halle. 2012. Limited recruitment during relaxation events: larval advection and behavior in an upwelling system. Limnology and Oceanography 57 (2): 457–470.CrossRefGoogle Scholar
  56. Morgan, S.G., J.L. Fisher, S.T. McAfee, J.L. Largier, S.H. Miller, M.M. Sheridan, and J.E. Neigel. 2014. Transport of crustacean larvae between a low-inflow estuary and coastal waters. Estuaries and Coasts 37 (5): 1269–1283.CrossRefGoogle Scholar
  57. Morgan, S.G., J.L. Fisher, S.H. Miller, S.T. McAfee, and J.L. Largier. 2009. Nearshore larval retention in a region of strong upwelling and recruitment limitation. Ecology 90 (12): 3489–3502.CrossRefGoogle Scholar
  58. Ogburn, M.B., H. Diaz, and R.B. Forward. 2009. Mechanisms regulating estuarine ingress of blue crab Callinectes sapidus megalopae. Marine Ecology-Progress Series 389: 181–192.CrossRefGoogle Scholar
  59. Olafsson, E.B., C.H. Peterson, and W.G.J. Ambrose. 1994. Does recruitment limitation structure populations and communities of macro-invertebrates in marine soft sediments: the relative significance of pre- and post-settlement processes. Oceanography and Marine Biology: An Annual Review 32: 65–109.Google Scholar
  60. Patten, K., and S. Norelius. 2016. Burrowing shrimp recruitment survey for Willapa Bay late summer 2016. Progress report to the Washington Department of Fish and Wildlife, from Washington State University, Long Beach Research and Extension Unit, 6p.Google Scholar
  61. Peteiro, L.G., and A.L. Shanks. 2015. Up and down or how to stay in the bay: retentive strategies of Olympia oyster larvae in a shallow estuary. Marine Ecology Progress Series 530: 103–117.CrossRefGoogle Scholar
  62. Pilditch, C.A., S. Valanko, J. Norkko, and A. Norkko. 2015. Post-settlement dispersal: the neglected link in maintenance of soft-sediment biodiversity. Biology Letters 11 (2): 20140795.CrossRefGoogle Scholar
  63. Pillay, D., and G.M. Branch. 2011. Bioengineering effects of burrowing thalassinidean shrimps on marine soft-bottom ecosystems. Oceanography and Marine Biology: An Annual Review 49: 137–191.Google Scholar
  64. Pillay, D., G.M. Branch, and A.T. Forbes. 2007. The influence of bioturbation by the sandprawn Callianassa kraussi on feeding and survival of the bivalve Eumarcia paupercula and the gastropod Nassarius kraussianus. Journal of Experimental Marine Biology and Ecology 344 (1): 1–9.CrossRefGoogle Scholar
  65. Pineda, J., F. Porri, V. Starczak, and J. Blythe. 2010. Causes of decoupling between larval supply and settlement and consequences for understanding recruitment and population connectivity. Journal of Experimental Marine Biology and Ecology 392 (1-2): 9–21.CrossRefGoogle Scholar
  66. Posey, M.H. 1986. Predation on burrowing shrimp: distribution and community consequences. Journal of Experimental Marine Biology and Ecology 103 (1-3): 143–161.CrossRefGoogle Scholar
  67. Develoment Core Team, R. 2015. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  68. Rae, G.H. 2002. Sea louse control in Scotland, past and present. Pest Management Science 58 (6): 515–520.CrossRefGoogle Scholar
  69. Repetto, M., and B.D. Griffen. 2012. Physiological consequences of parasite infection in the burrowing mud shrimp, Upogebia pugettensis, a widespread ecosystem engineer. Marine and Freshwater Research 63 (1): 60–67.CrossRefGoogle Scholar
  70. Shanks, A., G.C. Roegner, and J. Miller. 2010. Using megalopae abundance to predict future commercial catches of Dungeness crabs (Cancer magister) in Oregon. California Cooperative Oceanic Fisheries Investigations Reports 51: 106–118.Google Scholar
  71. Shanks, A.L. 2013. Atmospheric forcing drives recruitment variation in the Dungeness crab (Cancer magister), revisited. Fisheries Oceanography 22 (4): 263–272.CrossRefGoogle Scholar
  72. Shanks, A.L., S.G. Morgan, J. MacMahan, A.J.H.M. Reniers, M. Jarvis, J. Brown, A. Fujimura, and C. Griesemer. 2014. Onshore transport of plankton by internal tides and upwelling-relaxation events. Marine Ecology Progress Series 502: 39–51.CrossRefGoogle Scholar
  73. Shanks, A.L., and R.K. Shearman. 2009. Paradigm lost? Cross-shelf distributions of intertidal invertebrate larvae are unaffected by upwelling or downwelling. Marine Ecology-Progress Series 385: 189–204.CrossRefGoogle Scholar
  74. Shimoda, K., Y. Aramaki, J. Nasuda, H. Yokoyama, Y. Ishihi, and A. Tamaki. 2007. Food sources for three species of Nihonotrypaea (Decapoda: Thalassinidea: Callianassidae) from western Kyushu, Japan, as determined by carbon and nitrogen stable isotope analysis. Journal of Experimental Marine Biology and Ecology 342 (2): 292–312.CrossRefGoogle Scholar
  75. Strathmann, R.R. 1982. Selection for retention or export of larvae in estuaries. In Estuarine Comparisons, ed. V.S. Kennedy, 521–536. New York: Academic Press.CrossRefGoogle Scholar
  76. Sulkin, S.D., and W.V. Van Heukelem. 1982. Larval recruitment in the crab Callinectes sapidus Rathbun: amendment to the concept of larval retention in estuaries. In Estuarine comparisons, ed. V.S. Kennedy, 459–475. New York: Academic Press.CrossRefGoogle Scholar
  77. Takeuchi, S., Y. Takahara, Y. Agata, J. Nasuda, F. Yamada, and A. Tamaki. 2013. Response of suspension-feeding clams to natural removal of bioturbating shrimp on a large estuarine intertidal sandflat in western Kyushu, Japan. Journal of Experimental Marine Biology and Ecology 448: 308–320.CrossRefGoogle Scholar
  78. Tamaki, A., K. Ikebe, K. Muramatsu, and B. Ingole. 1992. Utilization of adult burrows by juveniles of the ghost shrimp, Callianassa japonica Ortmann: evidence from resin casts of burrows. Researches on Crustacea 217: 113–120.CrossRefGoogle Scholar
  79. Tamaki, A., and B. Ingole. 1993. Distribution of juvenile and adult ghost shrimps, Callianassa japonica Ortmann (Thalassinidea), on an intertidal sand flat: intraspecific facilitation as a possible pattern-generating factor. Journal of Crustacean Biology 13 (1): 175–183.CrossRefGoogle Scholar
  80. Tamaki, A., S. Mandal, Y. Agata, I. Aoki, T. Suzuki, H. Kanehara, T. Aoshima, Y. Fukuda, H. Tsukamoto, and T. Yanagi. 2010. Complex vertical migration of larvae of the ghost shrimp, Nihonotrypaea harmandi, in inner shelf waters of western Kyushu, Japan. Estuarine Coastal and Shelf Science 86 (1): 125–136.CrossRefGoogle Scholar
  81. Tamaki, A., Y. Saitoh, J. Itoh, Y. Hongo, S. Sen-Ju, S. Takeuchi, and S. Ohashi. 2013. Morphological character changes through decapodid-stage larva and juveniles in the ghost shrimp Nihonotrypaea harmandi from western Kyushu, Japan: clues for inferring pre- and post-settlement states and processes. Journal of Experimental Marine Biology and Ecology 443: 90–113.CrossRefGoogle Scholar
  82. Teske, P.R., I. Papadopoulos, B.K. Newman, P.C. Dworschak, C.D. McQuaid, and N.P. Barker. 2008. Oceanic dispersal barriers, adaptation and larval retention: an interdisciplinary assessment of potential factors maintaining a phylogeographic break between sister lineages of an African prawn. BMC Evolutionary Biology 8: 1–14.CrossRefGoogle Scholar
  83. Thorson, G. 1950. Reproductive and larval ecology of marine bottom invertebrates. Biological Reviews 25 (1): 1–45.CrossRefGoogle Scholar
  84. Thorson, G. 1966. Some factors influencing recruitment and establishment of marine benthic communities. Netherlands Journal of Sea Research 33: 267–293.CrossRefGoogle Scholar
  85. Thrush, S.F., J.E. Hewitt, and A.M. Lohrer. 2012. Interaction networks in coastal soft-sediments highlight the potential for change in ecological resilience. Ecological Applications 22 (4): 1213–1223.CrossRefGoogle Scholar
  86. Volkenborn, N., L. Polerecky, D.S. Wethey, T.H. DeWitt, and S.A. Woodin. 2012. Hydraulic activities by ghost shrimp Neotrypaea californiensis induce oxic-anoxic oscillations in sediments. Marine Ecology-Progress Series 455: 141–156.CrossRefGoogle Scholar
  87. Washington State Dept. of Ecology. 2015. Final environmental impact statement control of burrowing shrimp using imidacloprid on commercial oyster and clam beds in Willapa Bay and Grays Harbor, Washington, 389 p.
  88. Washington State Dept. of Ecology. 2018. Final supplemental environmental impact statement control of burrowing shrimp using imidacloprid on commercial oyster and clam beds in Willapa Bay and Grays Harbor, Washington, 885 p.
  89. Wasson, K., B.B. Hughes, J.S. Berriman, A.L. Chang, A.K. Deck, P.A. Dinnel, C. Endris, M. Espinoza, S. Dudas, M.C. Ferner, E.D. Grosholz, D. Kimbro, J.L. Ruesink, A.C. Trimble, D.V. Schaaf, C.J. Zabin, and D.C. Zacherl. 2016. Coast-wide recruitment dynamics of Olympia oysters reveal limited synchrony and multiple predictors of failure. Ecology 97 (12): 3503–3516.CrossRefGoogle Scholar
  90. Watson, J.R., B.E. Kendall, D.A. Siegel, and S. Mitarai. 2012. Changing seascapes, stochastic connectivity, and marine metapopulation dynamics. American Naturalist 180 (1): 99–112.CrossRefGoogle Scholar
  91. Webb, A.P., and B.D. Eyre. 2004. Effect of natural populations of burrowing thalassinidean shrimp on sediment irrigation, benthic metabolism, nutrient fluxes and denitrification. Marine Ecology-Progress Series 268: 205–220.CrossRefGoogle Scholar
  92. Woodin, S.A. 1976. Adult-larval interactions in dense infaunal assemblages: patterns of abundance. Journal of Marine Research 34: 25–41.Google Scholar
  93. Woodin, S.A., S.M. Lindsay, and D.S. Wethey. 1995. Process-specific recruitment cues in marine sedimentary systems. Biological Bulletin 189 (1): 49–58.CrossRefGoogle Scholar
  94. Woodson, C.B., M.A. McManus, J.A. Tyburczy, J.A. Barth, L. Washburn, J.E. Caselle, M.H. Carr, D.P. Malone, P.T. Raimondi, B.A. Menge, and S.R. Palumbi. 2012. Coastal fronts set recruitment and connectivity patterns across multiple taxa. Limnology and Oceanography 57 (2): 582–596.CrossRefGoogle Scholar
  95. Wooldridge, T.H., and H. Loubser. 1996. Larval release rhythms and tidal exchange in the estuarine mudprawn, Upogebia africana. Hydrobiologia 337 (1-3): 113–121.CrossRefGoogle Scholar
  96. Yamada, S.B., and P.M. Kosro. 2010. Linking ocean conditions to year class strength of the invasive European green crab, Carcinus maenas. Biological Invasions 12 (6): 1791–1804.CrossRefGoogle Scholar
  97. Yannicelli, B., L.R. Castro, W. Schneider, and M. Sobarzo. 2006a. Crustacean larvae distribution in the coastal upwelling zone off Central Chile. Marine Ecology-Progress Series 319: 175–189.CrossRefGoogle Scholar
  98. Yannicelli, B., L.R. Castro, A. Valle-Levinson, L. Atkinson, and D. Figueroa. 2006b. Vertical distribution of decapod larvae in the entrance of an equatorward facing bay of central Chile: implications for transport. Journal of Plankton Research 28 (1): 19–37.CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection 2018

Authors and Affiliations

  1. 1.Agricultural Research Service, U.S. Department of AgricultureHatfield Marine Science CenterNewportUSA
  2. 2.Department of Fisheries and WildlifeOregon State University, Hatfield Marine Science CenterNewportUSA
  3. 3.NOAA Fisheries—NWFSCHatfield Marine Science CenterNewportUSA

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