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Marine Biology

, Volume 156, Issue 3, pp 493–504 | Cite as

Presence of Alexandrium catenella and paralytic shellfish toxins in finfish, shellfish and rock crabs in Monterey Bay, California, USA

  • Rozalind J. JesterEmail author
  • Keri A. Baugh
  • Kathi A. Lefebvre
Original Paper

Abstract

The central California coast is a highly productive, biodiverse region that is frequently affected by the toxin-producing dinoflagellate Alexandrium catenella. Despite the consistent presence of A. catenella along our coast, very little is known about the movement of its toxins through local marine food webs. In the present study, we investigated 13 species of commercial finfish and rock crabs harvested in Monterey Bay, California for the presence of paralytic shellfish toxins (PSTs) and compared them to the presence of A. catenella and PSTs in sentinel shellfish over a 3-year period. Between 2003 and 2005, A. catenella was noted in 55% of surface water samples (n = 307) and reached a maximum concentration of 17,387 cells L−1 at our nearshore site in Monterey Bay. Peak cell densities occurred in the month of July and were associated with elevated shellfish toxicity in the summers of 2004 and 2005. When A. catenella was present, particulate PSTs were detected 71% of the time and reached a maximum concentration of 962 ng STXeq L−1. Of the 13 species tested, we frequently detected PSTs in Pacific sardines (Sardinops sagax; maximum 250 μg STXeq 100 g−1), northern anchovies (Engraulis mordax; maximum 23.2 μg STXeq 100 g−1), brown rock crabs (Cancer antennarius; maximum 49.3 μg STXeq 100 g−1) and red rock crabs (C. productus; 23.8 μg STXeq 100 g−1). PSTs were also present in one sample of Pacific herring (Clupea pallas; 13.3 μg STXeq 100 g−1) and one sample of English sole (Pleuronectes vetulus; 4.5 μg STXeq 100 g−1), and not detected in seven other species of flatfish tested. The presence of PSTs in several of these organisms reveals that toxins produced by A. catenella are more prevalent in California food webs than previously thought and also indicates potential routes of toxin transfer to higher trophic levels.

Keywords

Domoic Acid Planktivorous Fish Paralytic Shellfish Poisoning Mouse Bioassay English Sole 

Notes

Acknowledgments

We would like to thank the individuals who assisted in sample collection, especially Kurt Buck, Josh Plant, Capt. Lee Bradford, Chris Reeves, Don Pearson, Itchung Cheung, Veronica Vigilant and the crew of the R/V Pt. Lobos. Special thanks are due to Gregg Langlois of CDPH for information on local HAB conditions and to Vera Trainer for access to lab space and helpful discussions. This material is based on work supported under a National Science Foundation Graduate Research Fellowship and was funded by NOAA Center for Integrated Marine Technology (CIMT) project (NOAA Award #NA16OC2936-3) and a University of California Office of the President Award to M. Silver (03T-CEQI-07-0062). Additional funding was awarded to R. Jester by the Friends of Long Marine Lab, the PADI Foundation and the Meyers Oceanographic and Marine Biology Trust Award.

Open Access

This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.

Supplementary material

227_2008_1103_MOESM1_ESM.doc (66 kb)
Collection dates, number of specimens pooled (n) and total weight of viscera for planktivorous fish and hepatopancreas for crabs (DOC 66 kb)

References

  1. Alaska Department of Environmental Conservation (2007) Seafood processing and inspection 18 AAC 34.122 seafood product standards. Alaska Administrative Code 23 Apr 2008. <https://doi.org/old-www.legis.state.ak.us>
  2. AOAC (2000) AOAC official method 959.08. Paralytic shellfish poison biological method. In: Horwitz W (ed) Official methods of analysis of AOAC international. AOAC, GaithersburgGoogle Scholar
  3. Balech E (1995) The genus Alexandrium Halim (Dinoflagellata). Sherkin Island Marine Station, Sherkin IslandGoogle Scholar
  4. Bargu S, Powell CL, Coale SL, Busman M, Doucette GJ, Silver MW (2002) Krill: a potential vector for domoic acid in marine food webs. Mar Ecol Prog Ser 237:209–216. doi: https://doi.org/10.3354/meps237209 CrossRefGoogle Scholar
  5. Bargu S, Powell CL, Wang Z, Doucette GJ, Silver MW (2008) Note on the occurrence of Pseudo-nitzschia australis and domoic acid in squid from Monterey Bay, CA (USA). Harmful Algae 7:45–51. doi: https://doi.org/10.1016/j.hal.2007.05.008 CrossRefGoogle Scholar
  6. Bretz CK, Manouki TJ, Kvitek RG (2002) Emerita analoga (Stimpson) as an indicator species for paralytic shellfish poisoning toxicity along the California coast. Toxicon 40:1189–1196. doi: https://doi.org/10.1016/S0041-0101(02)00127-7 CrossRefGoogle Scholar
  7. California Department of Fish and Game Marine Region (2007) Final California commercial landings for 2006. Los Alamitos, CaliforniaGoogle Scholar
  8. Carroll JC, Winn RN (1989) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Pacific Southwest)—brown rock crab, red rock crab, and yellow crab. US Fish Wildl Serv Biol Rep 82 (11.117). US Army Corps of Engineers, TR EL-82-4Google Scholar
  9. Desbiens M, Cembella AD (1997) Retention and possible transformation of paralytic shellfish toxins in lobster (Homarus americanus). Bull Aquacult Assoc Can 97(2):75–77Google Scholar
  10. Doucette GJ, Turner JT, Powell CL, Keafer BA, Anderson DM (2005) Trophic accumulation of PSP toxins in zooplankton during Alexandrium fundyense blooms in Casco Bay, Gulf of Maine, April–June 1998. I. Toxin levels in A. fundyense and zooplankton size fractions. Deep Sea Res Part II Top Stud Oceanogr 52:2764–2783. doi: https://doi.org/10.1016/j.dsr2.2005.06.031 CrossRefGoogle Scholar
  11. Durbin E, Teegarden G, Campbell R, Cembella A, Baumgartner MF, Mated BR (2002) North Atlantic right whales, Eubalaena glacialis, exposed to paralytic shellfish poisoning (PSP) toxins via a zooplankton vector, Calanus finmarchicus. Harmful Algae 1:243–251. doi: https://doi.org/10.1016/S1568-9883(02)00046-X CrossRefGoogle Scholar
  12. Estes JA, Riedman ML, Staedler MM, Tinker MT, Lyon BE (2003) Individual variation in prey selection by sea otters: patterns, causes and implications. J Anim Ecol 72:144–155. doi: https://doi.org/10.1046/j.1365-2656.2003.00690.x CrossRefGoogle Scholar
  13. Fire SE, Silver MW (2005) Domoic acid in the Santa Cruz wharf fishery. Calif Fish Game 91:179–192Google Scholar
  14. Fritz L, Quilliam M, Wright J, Beale A, Work T (1992) An outbreak of domoic acid poisoning attributed to the pennate diatom Pseudonitzschia australis. J Phycol 28:439–442. doi: https://doi.org/10.1111/j.0022-3646.1992.00439.x CrossRefGoogle Scholar
  15. Garrido S, Marcalo A, Zwolinski J, van der Lingen CD (2007) Laboratory investigations on the effect of prey size and concentration on the feeding behaviour of Sardina pilchardus. Mar Ecol Prog Ser 330:189–199. doi: https://doi.org/10.3354/meps330189 CrossRefGoogle Scholar
  16. Geraci JR, Anderson DM, Timperi RJ, St. Aubin DJ, Early GA, Prescott JH, Mayo C (1989) Humpback whales (Megaptera novaeangliae) fatally poisoned by dinoflagellate toxin. Can J Fish Aquat Sci 46:1895–1898. doi: https://doi.org/10.1139/f89-238 CrossRefGoogle Scholar
  17. Goldberg J (2003) Domoic acid in the benthic foodweb of Monterey Bay, California. Marine Science MS Thesis, California State University of Monterey Bay, Moss Landing, CaliforniaGoogle Scholar
  18. Halstead BW, Schantz EJ (1984) Paralytic shellfish poisoning. WHO Offset Publ, vol 76. World Health Organization, Geneva, pp 1–60Google Scholar
  19. Haya K, Oshima Y, Young-Lai WW (1994) Profile of paralytic shellfish poisoning toxins in lobsters during uptake and depuration. In: Forbes JR (ed) Proceedings of the 4th Canadian workshop on harmful marine algae. Can Tech Rep Fish Aquat Sci 2016, p 17Google Scholar
  20. Horner RA, Garrison DL, Plumley FG (1997) Harmful algal blooms and red tide problems on the U.S. west coast. Limnol Oceanogr 42:1076–1088CrossRefGoogle Scholar
  21. Hortsman DA (1981) Reported red-water outbreaks and their effects on fauna of the west and south coasts of South Africa, 1959–1980. Fish Bull S Afr 15:71–88Google Scholar
  22. Jester RJ, Silver M, Langlois G, Vigilant V, Lefebvre KA, Baugh KA (2008a) A shift in the dominant toxin-producing algal species in central California alters phycotoxins in food webs. Harmful Algae. doi: https://doi.org/10.1016/j.hal.2008.07.001 CrossRefGoogle Scholar
  23. Jester RJ, Rhodes L, Beuzenberg V (2008b) Uptake of paralytic shellfish poisoning and spirolide toxins by paddle crabs (Ovalipes catharus) via a bivalve vector. Harmful Algae. doi: https://doi.org/10.1016/j.hal.2008.08.002 CrossRefGoogle Scholar
  24. Jonas-Davies J, Liston J (1985) The occurrence of PSP toxins in intertidal organisms. In: Anderson DM, White AW, Baden DG (eds) Toxic dinoflagellates. Elsevier, New York, pp 467–472Google Scholar
  25. Kao CY (1993) Paralytic shellfish poisoning. In: Falconer IR (ed) Algal toxins in seafood and drinking water. Academic Press, London, pp 75–86CrossRefGoogle Scholar
  26. Koslow J (1981) Feeding selectivity of schools of northern anchovy, Engraulis mordax, in the southern California bight. Fish Bull (Wash D C) 79:131–142Google Scholar
  27. Langlois GW, Kizer KW, Hansgen KH, Howell R, Loscutoff SM (1993) A note on domoic acid in California coastal mollusks and crabs. J Shellfish Res 12:467–468Google Scholar
  28. Lansberg JH (2002) The effects of harmful algal blooms on aquatic organisms. Rev Fish Sci 10:113–390. doi: https://doi.org/10.1080/20026491051695 CrossRefGoogle Scholar
  29. Lefebvre KA, Powell CL, Busman M, Doucette GJ, Moeller PDR, Silver JB, Miller PE, Hughes MP, Singaram S, Silver MW, Tjeerdema RS (1999) Detection of domoic acid in northern anchovies and California sea lions associated with an unusual mortality event. Nat Toxins 7:85–92. doi:10.1002/(SICI)1522-7189(199905/06)7:3<85::AID-NT39>3.0.CO;2-QCrossRefGoogle Scholar
  30. Lefebvre KA, Bargu S, Kieckhefer T, Silver MW (2002a) From sanddabs to blue whales: the pervasiveness of domoic acid. Toxicon 40:971–977. doi: https://doi.org/10.1016/S0041-0101(02)00093-4 CrossRefGoogle Scholar
  31. Lefebvre KA, Silver MW, Coale SL, Tjeerdema RS (2002b) Domoic acid in planktivorous fish in relation to toxic Pseudo-nitzschia cell densities. Mar Biol (Berl) 140:625–631. doi: https://doi.org/10.1007/s00227-001-0713-5 CrossRefGoogle Scholar
  32. MacLean JL (1979) Indo-Pacific red tides. In: Taylor DL, Seliger HH (eds) Toxic dinoflagellate blooms. Proceedings of the 2nd international conference on toxic dinoflagellate blooms. Elsevier, North Holland, pp 173–178Google Scholar
  33. McKernan DL, Scheffer VB (1942) Unusual numbers of dead birds on the Washington coast. Condor 44:264–266. doi: https://doi.org/10.2307/1364402 CrossRefGoogle Scholar
  34. Meyer KF, Sommer H, Schoenholz P (1928) Mussel poisoning. Am J Prev Med 2:365–394Google Scholar
  35. Mianzan HW, Pajaro M, Machinandiarena L, Cremonte F (1997) Salps: possible vectors of toxic dinoflagellates? Fish Res 29:193–197. doi: https://doi.org/10.1016/S0165-7836(96)00526-7 CrossRefGoogle Scholar
  36. Miller PE, Scholin CA (1998) Identification and enumeration of cultured and wild Pseudo-nitzschia (Bacillariophyceae) using species-specific LSU rRNA-targeted fluorescent probes and filter-based whole cell hybridization. J Phycol 34:371–382. doi: https://doi.org/10.1046/j.1529-8817.1998.340371.x CrossRefGoogle Scholar
  37. Miller PE, Scholin CA (2000) On detection of Pseudo-nitzschia species using rRNA-targeted probes: sample fixation and stability. J Phycol 36:238–250. doi: https://doi.org/10.1046/j.1529-8817.2000.99041.x CrossRefGoogle Scholar
  38. Montoya NG, Akselman R, Franco J, Carreto JI (1996) Paralytic shellfish toxins and mackerel (Scomber japonicus) mortality in the Argentine sea. In: Yasumoto T, Oshima Y, Fukuyo Y (eds) Harmful and toxic algal blooms. IOC UNESCO, Paris, pp 417–420Google Scholar
  39. Oikawa H, Fujita T, Satomi M, Suzuki T, Kotani Y, Yano Y (2002) Accumulation of paralytic shellfish poisoning toxins in the edible shore crab Telmessus acutidens. Toxicon 40:1593–1599. doi: https://doi.org/10.1016/S0041-0101(02)00176-9 CrossRefGoogle Scholar
  40. Oikawa H, Satomi M, Watabe S, Yano Y (2005) Accumulation and depuration rates of paralytic shellfish poisoning toxins in the shore crab Telmessus acutidens by feeding toxic mussels under laboratory controlled conditions. Toxicon 45:163–169. doi: https://doi.org/10.1016/j.toxicon.2004.10.004 CrossRefGoogle Scholar
  41. Oikawa H, Fujita T, Saito K, Satomi M, Yano Y (2007) Difference in the level of paralytic shellfish poisoning toxin accumulation between the crabs Telmessus acutidens and Charybdis japonica collected in Onahama, Fukushima Prefecture. Fish Sci 73:395–403. doi: https://doi.org/10.1111/j.1444-2906.2007.01347.x CrossRefGoogle Scholar
  42. Oshima Y, Kotaki Y, Harada T, Yasumoto T (1984) Paralytic shellfish toxins in tropical waters. In: Ragelis EP (ed) Seafood toxins. ACS symposium series 262, American Chemical Society, Washington DC, pp 161–170Google Scholar
  43. Pitcher GC, Calder D (2000) Harmful algal blooms of the southern Benguela Current: a review and appraisal of monitoring from 1989 to 1997. S Afr J Mar Sci 22:255–271CrossRefGoogle Scholar
  44. Price DW, Kizer KW, Hansgen KH (1991) California’s paralytic shellfish poisoning prevention program, 1927–89. J Shellfish Res 10:119–145Google Scholar
  45. Reyero M, Cacho E, Martinez A, Vazquez Js, Marina A, Fraga S, Franco JM (1999) Evidence of saxitoxin derivatives as causitive agents in the 1997 mass mortality of monk seals in the Cape Blanc peninsula. Nat Toxins 7:311–315. doi:10.1002/1522-7189(199911/12)7:6<311::AID-NT75>3.0.CO;2-ICrossRefGoogle Scholar
  46. Scholin CA (1994) Identification of group- and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the LSU rRNA gene. J Phycol 30:999–1011. doi: https://doi.org/10.1111/j.0022-3646.1994.00999.x CrossRefGoogle Scholar
  47. Scholin CA, Villac MC, Buck KR, Krupp JM, Powers DA, Fryxell GA, Chavez FP (1994) Ribosomal DNA sequences discriminate among toxic and non-toxic Pseudonitzschia species. Nat Toxins 2:152–165. doi: https://doi.org/10.1002/nt.2620020403 CrossRefGoogle Scholar
  48. Scholin CA, Gulland F, Doucette GJ, Benson S, Busman M, Chavez FP, Cordaro J, De Long R, De Vogelaere A, Harvey J, Haulena M, Lefebvre K, Lipscomb T, Loscutoff S, Lowenstine LJ, Marin R, Miller PE, McLellan WA, Moeller PDR, Powell CL, Rowles T, Silvagni P, Silver M, Spraker T, Trainer V, Van Dolah FM (2000) Mortality of sea lions along the central California coast linked to a toxic diatom bloom. Nature 403:80–84. doi: https://doi.org/10.1038/47481 CrossRefGoogle Scholar
  49. Sephton DH, Haya K, Martin JL, Le Gresley MM, Page FH (2007) Paralytic shellfish toxins in zooplankton, mussels, lobsters and caged Atlantic salmon, Salmo salar, during a bloom of Alexandrium fundyense off Grand Manan Island, in the Bay of Fundy. Harmful Algae 6:745–758. doi: https://doi.org/10.1016/j.hal.2007.03.002 CrossRefGoogle Scholar
  50. Shumway SE (1995) Phycotoxin-related shellfish poisoning: bivalve molluscs are not the only vectors. Rev Fish Sci 3:1–31CrossRefGoogle Scholar
  51. Sommer H (1932) The occurrence of the paralytic shellfish poison in the common sand crab. Science 76:574–575. doi: https://doi.org/10.1126/science.76.1981.574 CrossRefGoogle Scholar
  52. Sommer H, Meyer KF (1937) Paralytic shellfish poisoning. Arch Pathol (Chic) 24:560–598Google Scholar
  53. Teegarden G, Cembella A (1996) Grazing of toxic dinoflagellates, Alexandrium spp., by adult copepods of coastal Maine: implications for the fate of paralytic shellfish toxins in marine food webs. J Exp Mar Biol Ecol 196:145–176. doi: https://doi.org/10.1016/0022-0981(95)00128-X CrossRefGoogle Scholar
  54. Torgersen T, Aasen J, Aune T (2005) Diarrhetic shellfish poisoning by okadaic acid esters from Brown crabs (Cancer pagurus) in Norway. Toxicon 46:572–578. doi: https://doi.org/10.1016/j.toxicon.2005.06.024 CrossRefGoogle Scholar
  55. Trainer VL, Poli MA (2000) Assays for dinoflagellate toxins, specifically brevetoxin, ciguatoxin, and saxitoxin. In: Rochat H, Martin-Eauclaire MF (eds) Methods and tools in biosciences and medicine. Birkhauser, Basel, pp 1–19Google Scholar
  56. Turner JT, Doucette GJ, Powell CL, Kulis DM, Keafer BA, Anderson DM (2000) Accumulation of red tide toxins in larger size fractions of zooplankton assemblages from Massachusetts Bay, USA. Mar Ecol Prog Ser 203:95–107. doi: https://doi.org/10.3354/meps203095 CrossRefGoogle Scholar
  57. van der Lingen CD (1994) Effect of particle-size and concentration on the feeding-behavior of adult pilchard Sardinops sagax. Mar Ecol Prog Ser 109:1–13. doi: https://doi.org/10.3354/meps109001 CrossRefGoogle Scholar
  58. van der Lingen CD (2002) Diet of sardine Sardinops sagax in the southern Benguela upwelling ecosystem. S Afr J Mar Sci 24:301–316CrossRefGoogle Scholar
  59. van der Lingen CD, Hutchings L, Field JG (2006) Comparative trophodynamics of anchovy Engraulis encrasicolus and sardine Sardinops sagax in the southern Benguela: are species alternations between small pelagic fish trophodynamically mediated? Afr J Mar Sci 28:465–477CrossRefGoogle Scholar
  60. Vigilant V, Silver M (2007) Domoic acid in benthic flatfish on the continental shelf of Monterey Bay, California, USA. Mar Biol (Berl) 151:2053–2062. doi: https://doi.org/10.1007/s00227-007-0634-z CrossRefGoogle Scholar
  61. Wekell JC, Hurst J, Lefebvre KA (2004) The origin of the regulatory limits for PSP and ASP toxins in shellfish. J Shellfish Res 23:927–930Google Scholar
  62. White AW (1977) Dinoflagellate toxins as probable cause of an Atlantic herring (Clupea harengus harengus) kill, and pteropods as apparent vector. J Fish Res Board Can 34:2421–2424CrossRefGoogle Scholar
  63. White AW (1980) Recurrence of kills of Atlantic herring (Clupea harengus harengus) caused by dinoflagellate toxins transferred through herbivorous zooplankton. Can J Fish Aquat Sci 37:2262–2265. doi: https://doi.org/10.1139/f80-083 CrossRefGoogle Scholar
  64. Work TM, Barr B, Beale AM, Fritz L, Quilliam MA, Wright JLC (1993) Epidemiology of domoic acid poisoning in brown pelicans (Pelecanus Occidentalis) and brandt cormorants (Phalacrocorax Penicillatus) in California. J Zoo Wildl Med 24:54–62Google Scholar

Copyright information

© The Author(s) 2009

Open AccessThis is an open access article distributed under the terms of the Creative Commons Attribution Noncommercial License (https://doi.org/creativecommons.org/licenses/by-nc/2.0), which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.

Authors and Affiliations

  • Rozalind J. Jester
    • 1
    Email author
  • Keri A. Baugh
    • 2
  • Kathi A. Lefebvre
    • 2
  1. 1.Ocean Science DepartmentUniversity of California, Santa CruzSanta CruzUSA
  2. 2.Marine Biotoxins Program, Environmental Conservation DivisionNorthwest Fisheries Science Center, NOAA-FisheriesSeattleUSA

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