Advertisement

Marine Biology

, Volume 153, Issue 6, pp 1127–1140 | Cite as

Evaluating risks associated with transport of the ghost shrimp Neotrypaea californiensis as live bait

  • Bruno PernetEmail author
  • Aimee Deconinck
  • Angela Llaban
  • James W. Archie
Research Article

Abstract

The ghost shrimp Neotrypaea californiensis is imported into southern California from Oregon and Washington for use as live bait in recreational marine fisheries. We studied the population genetic structure of N. californiensis across much its range to assess the possibility that the transport of ghost shrimp across phylogeographic boundaries poses a risk of homogenizing existing genetic variation in the species. Analyses of two mitochondrial DNA markers showed little phylogeographic structure across the sampled range, suggesting that this risk is low. Unexpectedly, mitochondrial DNA analyses revealed that a second putative species of ghost shrimp frequently coexisted with N. californiensis in southern California intertidal habitats; almost all previous studies of soft-sediment communities in the region report the presence of N. californiensis only. We also assessed the possibility that the import of ghost shrimp might pose a risk of introduction of a parasitic castrator, the bopyrid isopod Ione cornuta, into southern California waters, where it does not appear to be native. Prevalence of living I. cornuta in samples purchased from bait shops was high (5.8%), suggesting that this is a real risk that merits further study.

Keywords

Intertidal Zone Carapace Length Ghost Shrimp Pairwise Sequence Divergence Gill Chamber 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We thank S. Anderson, R. Emlet, S. Fork, C. Gramlich, A. Hart, R. Hechinger, M. Jacobs, A. Krajewski, A. Kuris, F. Oyarzun, B. Passarelli, P. Reynolds, L. Rogers-Bennett, K. Wasson, and staff of the Cabrillo Marine Aquarium (K. Darrow, B. Higgins, M. Schaadt, and C. Webber) for assistance in collecting ghost shrimp. D. Wang assisted with preliminary surveys of parasites on ghost shrimp. J. Brusslan, A. Christensen, J. Dillon, and S. Malcomber provided advice or equipment useful in obtaining DNA sequences, and J. Zardus advised on analyses. Three anonymous reviewers provided useful comments on the manuscript. This publication was prepared by the authors under NOAA Grant #NA04OAR4170038, California Sea Grant College Program Project #R/FISH-204 (awarded to BP and JA), through NOAA’s National Sea Grant College Program, U.S. Department of Commerce. Additional support was provided by the Department of Biological Sciences and the College of Natural Sciences and Mathematics at CSULB, a Women in Philanthropy Undergraduate Scholarship (to AL), and a Provost’s Student Summer Stipend Award (to AD). The statements, findings, conclusions and recommendations are those of the authors and do not necessarily reflect the views of California Sea Grant or the U.S. Department of Commerce.

References

  1. Anderson G, Dale WE (1981) Probopyrus pandalicola: morphology and development of larvae in culture. Crustaceana 41:143–161Google Scholar
  2. Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer, SunderlandGoogle Scholar
  3. Beck JT (1979) Population interactions between a parasitic castrator, Probopyrus pandalicola, and one its freshwater shrimp hosts, Palaemonetes paludosus. Parasitology 79:431–449Google Scholar
  4. Berkenbusch K, Rowden A, Probert P (2000) Temporal and spatial variation in macrofauna community composition imposed by ghost shrimp Callianassa filholi bioturbation. Mar Ecol Prog Ser 192:249–257CrossRefGoogle Scholar
  5. Bilton DT, Paula J, Bishop JDD (2002) Dispersal, genetic differentiation and speciation in estuarine organisms. Est Coast Shelf Sci 55:937–952CrossRefGoogle Scholar
  6. Bird F, Ford P, Hancock G (1999) Effect of burrowing macrobenthos on the flux of dissolved substances across the sediment-water interface. Mar Freshw Res 50:523–532CrossRefGoogle Scholar
  7. Branch G, Pringle A (1987) The impact of the sand prawn Callianassa kraussi on sediment turnover and on bacteri, meiofauna, and benthic microflora. J Exp Mar Biol Ecol 107:219–235CrossRefGoogle Scholar
  8. Brusca RC, Coelho V, Taiti S (2001) A guide to the coastal Isopods of California. Internet address: http://tolweb.org/notes/?note_id=3004.x
  9. Burton RS (1998) Intraspecific phylogeography across the point conception biogeographic boundary. Evolution 52:734–735CrossRefGoogle Scholar
  10. Calado R, Vitorino A, Dinis MT (2006) Bopyrid isopods do not castrate the simultaneously hermaphroditic shrimp Lysmata amboinensis. Dis Aquat Org 73:73–76PubMedCrossRefGoogle Scholar
  11. California Department of Fish and Game (2007) Commercial Fish Business License Information Guide (accessed 22 Nov 2007 at http://www.dfg.ca.gov/licensing/commfishbus/commfishbusinfo.html)
  12. Carlton JT, Kuris AM (1975) Keys to decapod crustacea. In: Smith RI, Carlton JT (eds) Light’s manual: intertidal invertebrates of the central California coast, 3rd edn. University of California Press, BerkeleyGoogle Scholar
  13. Carlton JT (2001) Introduced species in US coastal waters: environmental impacts and management priorities. Pew Oceans Commission, Arlington, VAGoogle Scholar
  14. Cash CE, Bauer RT (1993) Adaptations of the branchial ectoparasite Probopyrus pandalicola for survival and reproduction related to ecdysis of the host, Palaemonetes pugio. J Crust Biol 13:111–124CrossRefGoogle Scholar
  15. Cassone BJ, Boulding EG (2006) Genetic structure and phylogeography of the lined shore crab, Pachygrapsus crassipes, along the northeastern and western Pacific coasts. Mar Biol 149:213–226CrossRefGoogle Scholar
  16. Chapman J, Dumbauld BR, McCoy L, Smith A, Markham JC, Itani G (2006) How mud shrimp Upogebia pugettensis got big new bumps. Pacific Estuarine Research Soc. Ann. Mtg. abstract (accessed 16 Aug 2007 at http://www.pers-erf.org/PERS_2006_Abstracts.pdf)
  17. Cohen AN, Weinstein A, Emmett MA, Lau W, Carlton JT (2001) Investigations into the introduction of non-indigenous marine organisms via the cross- continental trade in marine baitworms. Report for US Fish and Wildlife Service, San Francisco Bay ProgramGoogle Scholar
  18. Cunningham CW (1997) Can three incongruence tests predict when data should be combined? Mol Biol Evol 14:733–740PubMedGoogle Scholar
  19. Dawson MN (2001) Phylogeography in coastal marine animals: a solution from California? J Biogeogr 28:723–736CrossRefGoogle Scholar
  20. Drake JM, Lodge DM (2006) Allee effects, propagule pressure, and the probability of establishment: risk analysis for biological invasions. Biol Inv 8:365–375CrossRefGoogle Scholar
  21. Ellingson RA, Krug PJ (2006) Evolution of poecilogony from planktotrophy: cryptic speciation, phylogeography, and larval development in the gastropod genus Alderia. Evolution 60:2293–2310PubMedGoogle Scholar
  22. Emmett R, Llanso R, Newton J, Thom R, Hornberger M, Morgan C, Levings C, Copping A, Fishman P (2000) Geographic signatures of North American west coast estuaries. Estuaries 23:765–792CrossRefGoogle Scholar
  23. Espinosa-Perez MC, Hendrickx ME (2006) A comparative analysis of biodiversity and distribution of shallow-water marine isopods (Crustacea: Isopoda) from polar and temperate water in the East Pacific. Belg J Zool 136:219–247Google Scholar
  24. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedGoogle Scholar
  25. Farley RD, Case JF (1968) Perception of external oxygen by the burrowing shrimp, Callianassa californiensis and C. affinis. Biol Bull 134:261–265PubMedCrossRefGoogle Scholar
  26. Folmer OM, Black R, Hoeh R, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cyctochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  27. Griffis RB, Chavez FL (1988) Effects of sediment type on burrows of Callianassa californiensis and C. gigas. J Exp Mar Biol Ecol 117:239–253CrossRefGoogle Scholar
  28. Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27CrossRefGoogle Scholar
  29. Gruenthal KM, Acheson LK, Burton RS (2007) Genetic structure of natural populations of California red abalone (Haliotis rufescens) using multiple genetic markers. Mar Biol. doi: 10.1007/s00227-007-0771-4
  30. Jacobs DK, Haney TA, Louie KD (2004) Genes, diversity, and geologic process on the Pacific coast. Ann Rev Earth Planet Sci 32:601–652CrossRefGoogle Scholar
  31. Jensen GC (1995) Pacific coast crabs and shrimps. Sea Challengers Press, MontereyGoogle Scholar
  32. Johnson G, Gonor J (1982) The tidal exchange of Callianassa californiensis larvae between the ocean and the Salmon River estuary, Oregon. Est Coast Shelf Sci 14:501–516CrossRefGoogle Scholar
  33. Kelly DW, MacIsaac HJ, Heath DD (2006) Vicariance and dispersal effects on phylogeographic structure in a widespread estuarine invertebrate. Evolution 60:257–267PubMedGoogle Scholar
  34. Knowlton N, Weight LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc R Soc B 265:2257–2263CrossRefGoogle Scholar
  35. Koike I, Mukai H (1983) Oxygen and inorganic nitrogen contents and fluxes in burrows of the shrimps Callianassa japonica and Upogebia major. Mar Ecol Preg Ser 12:185–190CrossRefGoogle Scholar
  36. Kozloff EN (1987) Marine invertebrates of the Pacific Northwest. University of Washington Press, SeattleGoogle Scholar
  37. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  38. Kuris AM, Sadeghian PS, Carlton JT, Campos E (2007) Decapoda. In: Carlton JT (ed) The light and smith manual: intertidal invertebrates from central California to oregon. University of California Press, Berkeley, pp 632–656Google Scholar
  39. Lande R (1998) Anthropogenic, ecological, and genetic factors in extinction and conservation. Res Popul Ecol 40:259–269CrossRefGoogle Scholar
  40. Lockwood JL Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228CrossRefGoogle Scholar
  41. Lodge DM, Taylor CA, Holdich DM, Skurdal J (2000) Reducing impacts of exotic crayfish introductions. Fisheries 25(8):21–23CrossRefGoogle Scholar
  42. Ludwig HR, Leitch JA (1996) Interbasin transfer of aquatic biota via angler’s bait buckets. Fisheries 21(7):14–18CrossRefGoogle Scholar
  43. MacGinitie G (1934) The natural history of Callianassa californiensis. Am Midl Nat 15:166–177CrossRefGoogle Scholar
  44. Markham JC (1992) The Isopoda Bopyridae of the Eastern Pacific—missing or just hiding? San Diego Soc Nat Hist 17:1–4Google Scholar
  45. McCrow LT (1972) The ghost shrimp, Callianassa californiensis in Yaquina Bay, Oregon. M.S. Thesis, Oregon State University, p 56Google Scholar
  46. McDermott JJ (1991) Incidence and host-parasite relationship of Leidya bimini in the brachyuran crab Pachygrapsus transversus from Bermuda. Ophelia 33:71–95Google Scholar
  47. Merritt TJS, Shi L, Chase MC, Rex MA, Etter RJ, Quattro JM (1998) Universal cytochrome b primers facilitate intraspecific studies in molluscan taxa. Mol Mar Biol Biotech 7:7–11Google Scholar
  48. Miller M (1984) Bioturbation of intertidal quartz-rich sands: a modern example and its sedimentologic and paleoecologic implications. J Geol 92:201–216CrossRefGoogle Scholar
  49. Morris RH, Abbott DT, Haderlie EC (1980) Intertidal invertebrates of California. Stanford University Press, StanfordGoogle Scholar
  50. Murphy RC (1985) Factors affecting the distribution of the introduced bivalve, Mercenaria mercenaria, in a California lagoon—the importance of bioturbation. J Mar Res 43:673–692CrossRefGoogle Scholar
  51. O’Brien J, Van Wyk P (1985) Effects of crustacean parasitic castrators on growth of crustacean hosts. In: Wenner A (ed) Crustacean issues 3. Factors in Adult Growth, A.A. Balkema, Rotterdam, pp 191–218Google Scholar
  52. Petersen CH (2007) Historical demography and contemporary spatial genetic structure of an estuarine crab in the northeast Pacific (Hemigrapsus oregonensis). Mar Biol. doi: 10.1007/s00227-006-0442-x
  53. Peterson C (1977) Competitive organization of the soft-bottom macrobenthic communities of southern California lagoons. Mar Biol 43:343–359CrossRefGoogle Scholar
  54. Posey M (1986) Changes in a benthic community associated with dense beds of a burrowing deposit feeder, Callianassa californiensis. Mar Ecol Prog Ser 31:15–22CrossRefGoogle Scholar
  55. Ruesink JL, Parker IM, Groom MJ, Kareiva PM (1995) Reducing the risks of nonindigenous species introductions. Bioscience 45:465–477CrossRefGoogle Scholar
  56. Schubart CD, Diesel R, Hedges SB (1998) Rapid evolution to terrestrial life in Jamaican crabs. Nature 393:363–365CrossRefGoogle Scholar
  57. Sotka EE, Wares JP, Barth JA, Grosberg RK, Palumbi SR (2004) Strong genetic clines and geographical variation in gene flow in the rocky intertidal barnacle Balanus glandula. Mol Ecol 13:2143–2156PubMedCrossRefGoogle Scholar
  58. Stevens BA (1928) Callianassidae from the West Coast of North America. Publ Puget Sound Biol Stn 6:315–369Google Scholar
  59. Suchanek T (1983) Control of seagrass communities and sediment distribution by Callianassa bioturbation. J Mar Res 41:281–298Google Scholar
  60. Swofford DL (2001) PAUP*: phylogenetic analysis using parsimony (*and other methods). Ver. 4.0b10. Sinauer Associates, Sunderland, MAGoogle Scholar
  61. Torchin ME, Lafferty KD, Kuris AM (2002) Parasites and marine invasions. Parasitology 124:S137–S151CrossRefGoogle Scholar
  62. Van Wyk PM (1982) Inhibition of the growth and reproduction of the porcellanid crab Pachycheles rudis by the bopyrid isopod, Aporobopyrus muguensis. Parasitology 85:459–473Google Scholar
  63. Weigle SM, Smith LD, Carlton JT, Pederson J (2005) Assessing the risk of introducing exotic species via the live marine species trade. Conserv Biol 19:213–223CrossRefGoogle Scholar
  64. Zedler J, Callaway J, Sullivan G (2001) Declining biodiversity: why species matter and how their functions might be restored in Californian tidal marshes. Bioscience 51:1005–1017CrossRefGoogle Scholar
  65. Ziebis W, Forster S, Huettel M, Jorgensen B (1996) Complex burrows of the mud shrimp Callianassa truncata and their geochemical impact in the sea bed. Nature 382:619CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Bruno Pernet
    • 1
    Email author
  • Aimee Deconinck
    • 1
  • Angela Llaban
    • 1
  • James W. Archie
    • 1
  1. 1.Department of Biological SciencesCalifornia State University, Long BeachLong BeachUSA

Personalised recommendations