Skip to main content
SpringerLink
Log in

An introduced Asian parasite threatens northeastern Pacific estuarine ecosystems

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The introduced Asian parasitic bopyrid isopod, Orthione griffenis, was first discovered on the Pacific coast of North America in Washington in 1988 and next in California in 1992. The range of Orthione presently extends from British Columbia to Baja California, where it infests at least two species of the native estuary mud shrimp, Upogebia. Intense Orthione infestations are associated with the apparent demise of many local populations of Upogebia pugettensis yet nonindigenous origins of Orthione in North America and thus the ecological significance of its impacts have remained in doubt. Six criteria reveal that Orthione is introduced to North America: its conspecificity with disjunct Asian populations, its earliest (1950s) collections in Asia, its late discovery among symbiotic species associated with Upogebia, its historical absence, and its appearance in North America coincident with extensive new ballast water traffic from Asia. Orthione is the first recognized bopyrid isopod invasion globally. Coexistence of U. pugettensis, which are ecosystem engineers, with its newly acquired parasite cannot be assumed. Orthione threatens eastern Pacific estuary ecosystems where Upogebia were previously abundant.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • An J, Williams JD, Yu H (2009) The Bopyridae (Crustacea: Isopoda) parasitic on thalassinideans (Crustacea: Decapoda) from China. Proc Biol Soc Wash 122:225–246

    Article  Google Scholar 

  • Boots M, Sasaki A (2001) Parasite-driven extinction in spatially explicit host-parasite systems. Am Nat 34:706–713

    Google Scholar 

  • Bourdon R (1987) Suborder Epicarida. In: Kozloff E, Price M (eds) Marine invertebrates of the Pacific Northwest. Univ Washington Press, Seattle, p 342

    Google Scholar 

  • Brusca RC, Coelho VR, Taiti S (2007) Isopoda. In: Carlton JT (ed) The light and smith manual: intertidal invertebrates from central California to Oregon, 4th edn. UC Press, Berkeley, pp 503–542

    Google Scholar 

  • Carlton JT (1985) Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr Mar Biol Ann Rev 23:313–371

    Google Scholar 

  • Carlton JT (1996) Biological invasions and cryptogenic species. Ecology 77:1653–1655

    Article  Google Scholar 

  • Carlton JT (2003) Community assembly and historical biogeography in the North Atlantic Ocean: the potential role of human-mediated dispersal vectors. Hydrobiologia 503:1–8

    Article  Google Scholar 

  • Carlton JT (2007) Acknowledgments. In: Carlton JT. (ed) The light and smith manual: intertidal invertebrates from central california to oregon, 4th edn. UC Press, Berkeley, pp xiii–xvii

  • Carlton JT (2009) Deep invasion ecology and the assembly of communities in historical time. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 13–56

    Chapter  Google Scholar 

  • Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82

    Article  Google Scholar 

  • Carter CA and Rozelle S (2002) Will China’s agricultural trade reflect its comparative advantage? In: Gale F, Tuan F, Lohmar B, Hsu H–H, Gilmour B (eds) China’s food and agriculture: issues for the 21st century agricultural information bulletin No. (AIB775), Econ Res Serv, USDA, pp 27–30

  • Chapman JW (2000) Climate effects on nonindigenous peracaridan crustacean introductions in estuaries. In: Pederson J (ed) Marine Bioinvasions: Proceedings of a Conference, January 24–27, 1999 MIT Sea Grant College Program, Cambridge, MA, pp 66–80

  • Chapman JW, Carlton JT (1991) A test of criteria for introduced species: the global invasion by the isopod Synidotea laevidorsalis (Miers, 1881). J Crust Biol 11:386–400

    Article  Google Scholar 

  • Cohen AN and Carlton JT (1995) Biological study. Nonindigenous aquatic species in a United States Estuary: a case study of the biological invasions of the San Francisco Bay and Delta. A Report for the United States Fish and Wildlife Service, Washington, D.C. and National Sea Grant College Program, Connecticut Sea Grant, NTIS Rep No PB96-166525, 246 pp. + Appendices

  • Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558

    Article  PubMed  CAS  Google Scholar 

  • D’Andrea AF, DeWitt TH (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. Limnol Oceanogr 54:1911–1932

    Article  Google Scholar 

  • Dumbauld BR, Chapman JW (2008) Could burrowing shrimp host populations with pelagic larval dispersal be controlled by an invading parasite? In: 37th Annual Benthic Ecology Meeting, Providence, RI April 9–13, 2008

  • Dumbauld BR, Chapman JW, Torchin ME, Kuris AM (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)? Estuar Coast 34:336–350

    Article  Google Scholar 

  • Frick WE, Khangaonkar T, Sigleo AC, Yang Z (2007) Estuarine-ocean exchange in a North Pacific estuary: comparison of steady state and dynamic models. Estuar Coast Shelf Sci 74:1–11

    Article  Google Scholar 

  • Griffen BD (2009) Effects of a newly invasive parasite on the burrowing mud shrimp, a widespread ecosystem engineer. Mar Ecol Prog Ser 391:73–83

    Article  Google Scholar 

  • Griffen BD, DeWitt TH, Langdon C (2004) Particle removal rates by the mud shrimp Upogebia pugettensis, its burrow, and a commensal clam: effects on estuarine phytoplankton abundance. Mar Ecol Prog Ser 269:223–236

    Article  Google Scholar 

  • Hailstone TS, Stephenson W (1961) The biology of Callianassa (Trypaea) australiensis Dana 1852 (Crustacea, Thalassinidea). Univ Qld Dept Zool Pap 1:257–286

    Google Scholar 

  • Hart JL (1982) Crabs and their relatives of British Columbia. British Columbia Prov Handb 40:226

    Google Scholar 

  • Hatch MH (1947) The Chelifera and Isopoda of Washington and adjacent regions. Univ Wash Publ 10:155–274

    Google Scholar 

  • Hickey BM (1998) Coastal oceanography of western North America from the tip of Baja California to Vancouver Island; coastal segment. Sea 11:345–393

    Google Scholar 

  • Hoof RC, Peterson WT (2006) Copepod biodiversity as an indicator of changes in ocean and climate conditions of the northern California current ecosystem. Limnol Oceanogr 51:2607–2620

    Article  Google Scholar 

  • Itani G (2004) Host specialization in symbiotic animals associated with thalassinidean shrimps of Japan. In: Tamaki A (ed) Proceedings of the symposium on “Ecology of large bioturbators in tidal flats and shallow sublittoral sediments—from individual behavior to their role as ecosystem engineers”. November 1–2, 2003, Nagasaki Univ, Nagasaki, Japan, pp 33–43

  • Jensen GC (1995) Pacific coast crabs and shrimps. Sea challengers, Monterey, p 87

    Google Scholar 

  • Johnson ME, Snook HJ (1927) Seashore animals of the Pacific coast. Dover Publ, New York, p 659

    Google Scholar 

  • Kozloff E (1973) Seashore life of the northern Pacific coast: an illustrated guide to the Northern California, Oregon. Washington, and British Columbia, Univ Washington Press, p 370

    Google Scholar 

  • Kozloff E, Price M (1987) Marine invertebrates of the Pacific Northwest. Univ Washington Press, Seattle, p 511

    Google Scholar 

  • Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, Lorda J, Mababa L, Mancini FT, Mora AB, Pickering AM, Talhouk NL, Torchin ME, Lafferty KD (2008) Ecosystem energetic implications of parasites and free-living biomass in three estuaries. Nature 454:515–518

    Article  PubMed  CAS  Google Scholar 

  • Lafferty KD, Kuris AM (2002) Trophic strategies, animal diversity and body size. Trend Ecol Evol 17:507–513

    Article  Google Scholar 

  • Lamb A, Hanby BP (2005) Marine life of the Pacific Northwest: a photographic encyclopedia of invertebrates, seaweeds and selected fishes. Harbour Publishing, Madiera Park, p 398

    Google Scholar 

  • Lockington WN (1878) Remarks upon the Thalassinidea and Astacidea of the Pacific coast of North America, with the description of a new species. Ann Mag Nat Hist 5:299–300

    Article  Google Scholar 

  • Long JD, Trussell GC, Elliman T (2009) Linking invasions and biogeography: isolation differentially affects exotic and native plant diversity. Ecology 90:863–868

    Article  PubMed  Google Scholar 

  • Lund N (2011) The plight of the blue mud shrimp. Sandbar 3:4–6

    Google Scholar 

  • MacGinitie G (1930) Natural history of mudshrimp, Upogebia. Ann Mag Nat Hist Ser 10(6):36–44

    Article  Google Scholar 

  • MacGinitie GE (1935) Ecological aspects of a California marine estuary. Am Midl Nat 16:629–765

    Article  Google Scholar 

  • MacGinitie GE, MacGinitie N (1949) Natural history of marine animals. McGraw-Hill Book Co., New York, p 373

    Google Scholar 

  • Markham JC (1992) The Isopoda Bopyridae of the eastern Pacific—missing or just hiding? Proc S Diego Soc Nat Hist 17:1–4

    Google Scholar 

  • Markham JC (2001) A review of the bopyrid isopods parasitic on thalassinidean decapods. In: Kensley B, Brusca RC (eds) Isopod systematics and evolution, Crust Issues 13:195–204

  • Markham JC (2003) A worldwide list of hermit crabs and their relatives (Anomura: Paguridea) reported as hosts of Isopoda Bopyridae. Mem Mus Vic 60:71–77

    Google Scholar 

  • Markham JC (2004) New species and records of Bopyridae (Crustacea: Isopoda) infesting species of the genus Upogebia (Crustacea: Decapoda: Upogebiidae): the genera Orthione Markham, 1988, and Gyge Cornalia & Panceri, 1861. Proc Biol Soc Wash 117:186–198

    Google Scholar 

  • Markham JC (2008) New records of pseudionine bopyrid isopods, including two new species and one new genus, infesting porcellanid crabs (Decapoda: Anomura) on the Pacific coast of North and Central America. Bull South Calif Acad Sci 107:145–157

    Google Scholar 

  • McArdle BH (1990) When are rare species not there? Oikos 57:276–277

    Article  Google Scholar 

  • Miller MA (1975) Phylum Arthropoda: Crustacea, Tanaidacea and Isopoda. In: Smith RI, Carlton JT (eds) Light’s manual: intertidal invertebrates of the central California coast, 3rd edn. UC Press, Berkeley, pp 277–312

  • Morgan SG, Fisher JL, Miller SH, McAffee ST, Largier JL (2009) Nearshore larval retention in a region of strong upwelling and recruitment limitation. Ecology 90:3489–3502

    Article  PubMed  Google Scholar 

  • Pernet B, Deconinck A, Llaban A, Archie J (2008) Evaluating risks associated with transport of the ghost shrimp Neotrypaea californiensis as live bait. Mar Biol 153:1127–1140

    Article  Google Scholar 

  • Peterson W (1998) Life cycle strategies of copepods in coastal upwelling zones. J Mar Syst 15:313–326

    Article  Google Scholar 

  • Posey MH (1986) Predation on a burrowing shrimp: distribution and community consequences. J Exper Mar Bio Ecol 103:143–161

    Article  Google Scholar 

  • Posey MH, Dumbauld BR, Armstrong DA (1991) Effects of a burrowing mud shrimp, Upogebia pugettensis (Dana), on abundances of macro-infauna. J Exper Mar Biol Ecol 148:283–294

    Article  Google Scholar 

  • Queiroga H, Blanton J (2005) Interactions between behavior and physical forcing in the control of horizontal transport of decapod crustacean larvae. Adv Mar Biol 47:107–214

    Article  PubMed  Google Scholar 

  • Richardson H (1905) A monograph on the isopods of North America. Bull US Nat Mus 54:1–727

    Google Scholar 

  • Rongfen W, Guozheng Y (2007) The open port system in northeast China. Chin Geogr Sci 7:270–277

    Google Scholar 

  • Ruiz GM, Carlton JT (2003) Invasion vectors: a conceptual framework for management. In: Ruiz GM, Carlton JT (eds) Invasive species: vectors and management strategies. Island Press, Washington, DC, pp 459–504

    Google Scholar 

  • Ruiz GM, Fofonoff P, Carlton JT, Wonham MJ, Hines AH (2000) Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Ann Rev Ecol Syst 31:481–531

    Article  Google Scholar 

  • Saito N (2002) A list of crustacean hosts of the epicaridean isopods (Crustacea: Peracarida) in the Japanese waters. Takusa 13:18–31

    Google Scholar 

  • Saito N, Itani G, Nunomura N (2000) A preliminary checklist of isopod crustaceans in Japan. Bull Toyama Sci Mus 3:11–107

    Google Scholar 

  • Schultz GA (1969) How to know the marine Isopod Crustaceans. W. C. Brown, Dubuque, vii + p 359

  • Sept JD (2008) Common seashore creatures of the Pacific Northwest. Calypso Publishing, Sechelt, BC, p 95

  • Shanks AL, Roegner GC (2007) Recruitment limitation in Dungeness crab populations is driven by atmospheric forcing. Ecology 88:1726–1737

    Article  PubMed  Google Scholar 

  • Smith AE, Chapman JW, Dumbauld BR (2008) Population structure and energetics of the bopyrid isopod parasite Orthione griffenis in mud shrimp Upogebia pugettensis. J Crust Biol 28:228–233

    Article  Google Scholar 

  • Sterman JD (2008) Risk communication on climate: mental models and mass balance. Science 322:532–533

    Article  PubMed  CAS  Google Scholar 

  • Stimpson W (1857) The Crustacea and Echinodermata of the Pacific shores of North America. Boston J Nat Hist 6:444–532

    Google Scholar 

  • Swinbanks DD, Luternauer JL (1987) Burrow distribution of thalassinidean shrimp on a Fraser Delta tidal flat, British Columbia. J Paleontol 61:315–332

    Google Scholar 

  • Tamaki A, Mandal S, Yohihiro A, Aoki I, Suzuki T, Kanehara H, Aoshima T, Fukuda Y, Tsukamoto H, Yanagi T (2010) Complex vertical migration of larvae of the ghost shrimp, Nihonotrypaea harmandi, in inner shelf waters of western Kyushu. Jpn Mar Ecol Prog Ser 86:125–136

    CAS  Google Scholar 

  • Telnack J and Phipps M (2005) Intertidal marine invertebrates of the south Puget Sound. http://www.nwmarinelife.com/webgallery/pages/U_pugettensis.htm (see Appendix A)

  • Thompson RK (1972) Functional morphology of the hindgut gland of Upogebia pugettensis (Crustacea, Thalassinidea) and its role in burrow construction. PhD Dissertation, Zool, Univ California Berkeley, Berkeley, CA p 202

  • Williams AB (1986) Mud shrimps, Upogebia, from the eastern Pacific (Thalassinoidea: Upogebiidae). San Diego Soc Nat Hist Mem 14:2–60

    Google Scholar 

  • Williams JD, An J (2009) The cryptogenic parasitic isopod Orthione griffenis Markham, 2004 from the eastern and western Pacific. Integrat Compar Biol 49:114–126

    Article  Google Scholar 

  • Wooldridge TH, Loubser H (1996) Larval release rhythms and tidal exchange in the estuarine mudprawn, Upogebia africana. Hydrobiologia 337:113–121

    Article  Google Scholar 

  • Yamada SB, Kosro PM (2010) Linking ocean conditions to year class strength of the European green crab, Carcinus maenas. Biol Invas 12:1791–1804

    Article  Google Scholar 

  • Yuji I, Ono T, Matsui T, Miyasaka J, Kinoshita Y, Ihn H (2008) Epidemiological survey of Vibrio vulnificus infection in Japan between 1999 and 2003. J Dermatol 35:129–213

    Article  Google Scholar 

  • Zimmer RL (2007) Phoronida. In: Carlton JT (ed) The Light and Smith Manual: Intertidal Invertebrates from Central California to Oregon, 4th edn. University of California Press, Berkeley, pp 860–863

    Google Scholar 

Download references

Acknowledgments

Washington State contingency funds for biological control of burrowing shrimp partially funded this research. James Carlton, Alan Shanks, and Kathy Hieb forwarded zooplankton samples and notes. Ardis Johnston (Harvard University Museum of Comparative Zoology), Bob Van Syoc (California Academy of Sciences), Eric Hochberg (Santa Barbara Museum of Natural History) and Leslie Harris and Regina Wetzer (Los Angeles County Museum of Natural History) assisted with their respective collections. We thank George Boehlert, Ryan Hechinger, Armand Kuris, Bill Peterson and Alan Shanks for insightful comments and advice. Mary Jo Adams, Ernesto Campos, Francis Choi, Andy Cohen, Anthony D’Andrea, Rusty Fairey, Tom Gaumer, Travis Goodman, Greg Jensen, Eugene Kozloff, Michael McGowan, Todd Newberry, John Pearse, Bruno Pernet, Martin Posey, Austin Pritchard, Jerry Rudy, Erik Thuesen, Cynthia Trowbridge, Kristen Wasson and Jason Williams provided pre- and post 1990 s data, specimens, or accounts of eastern Pacific Upogebia and Orthione populations. Susan Swarbrick, Jeff Crooks, Ralph Breitenstein, Eric Robbins, Carol Cole, Lee McCoy, and Cara Fritz helped with sampling, data and analyses. We thank Sylvia Yamada, Jennifer Ruesink and James Carlton for their critical reviews of the manuscript.

Author information

Authors and Affiliations

  1. Fisheries and Wildlife, Hatfield Marine Science Center, Oregon State University, Newport, OR, 97365-5296, USA

    John W. Chapman

  2. Agricultural Research Service, US Department of Agriculture, Hatfield Marine Science Center, Newport, OR, 97365, USA

    Brett R. Dumbauld

  3. Laboratory of Marine Symbiotic Biology, Faculty of Education, Kochi University, 2-5-1 Akebono, Kochi, 780-8520, Japan

    Gyo Itani

  4. Arch Cape Marine Laboratory, Arch Cape, OR, 97102, USA

    John C. Markham

Authors
  1. John W. Chapman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brett R. Dumbauld
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gyo Itani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. John C. Markham
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John W. Chapman.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 645 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chapman, J.W., Dumbauld, B.R., Itani, G. et al. An introduced Asian parasite threatens northeastern Pacific estuarine ecosystems. Biol Invasions 14, 1221–1236 (2012). https://doi.org/10.1007/s10530-011-0151-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-011-0151-3

Keywords

Search

Navigation