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Distribution of Microcystins in a Lake Foodweb: No Evidence for Biomagnification

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Abstract

Microcystins, toxins produced by cyanobacteria, may play a role in fish kills, although their specific contribution remains unclear. A better understanding of the eco-toxicological effects of microcystins is hampered by a lack of analyses at different trophic levels in lake foodwebs. We present 3 years of monitoring data, and directly compare the transfer of microcystin in the foodweb starting with the uptake of (toxic) cyanobacteria by two different filter feeders: the cladoceran Daphnia galeata and the zebra mussel Dreissena polymorpha. Furthermore foodwebs are compared in years in which the colonial cyanobacterium Microcystis aeruginosa or the filamentous cyanobacterium Planktothrix agardhii dominated; there are implications in terms of the types and amount of microcystins produced and in the ingestion of cyanobacteria. Microcystin concentrations in the seston commonly reached levels where harmful effects on zooplankton are to be expected. Likewise, concentrations in zooplankton reached levels where intoxication of fish is likely. The food chain starting with Dreissena (consumed by roach and diving ducks) remained relatively free from microcystins. Liver damage, typical for exposure to microcystins, was observed in a large fraction of the populations of different fish species, although no relation with the amount of microcystin could be established. Microcystin levels were especially high in the livers of planktivorous fish, mainly smelt. This puts piscivorous birds at risk. We found no evidence for biomagnification of microcystins. Concentrations in filter feeders were always much below those in the seston, and yet vectorial transport to higher trophic levels took place. Concentrations of microcystin in smelt liver exceeded those in the diet of these fish, but it is incorrect to compare levels in a selected organ to those in a whole organism (zooplankton). The discussion focuses on the implications of detoxication and covalent binding of microcystin for the transfer of the toxin in the foodweb. It seems likely that microcystins are one, but not the sole, factor involved in fish kills during blooms of cyanobacteria.

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References

  1. A Amorim V Vasconcelos (1999) ArticleTitleDynamics of microcystins in the mussel Mytilus galloprovincialis Toxicon 37 1041–1052 Occurrence Handle10.1016/S0041-0101(98)00231-1 Occurrence Handle10484739

    Article  PubMed  Google Scholar 

  2. L Babcock-Jackson WW Carmichael DA Culver (2002) ArticleTitleDreissenid mussels increase exposure of benthic and pelagic organisms to toxic microcystins Verh Internat Verein Limnol 28 1082–1085

    Google Scholar 

  3. D Baganz G Staaks C Steinberg (1998) ArticleTitleImpact of the cyanobacterial toxin, microcystin-LR on behaviour of zebrafish, Danio rerio Wat Res 32 948–952 Occurrence Handle10.1016/S0043-1354(97)00207-8

    Article  Google Scholar 

  4. SM Baker JS Levinton JP Kurdziel SE Shumway (1998) ArticleTitleSelective feeding and biodeposition by zebra mussels and their relation to changes in phytoplankton composition and seston load J Shellfish Res 17 1207–1213

    Google Scholar 

  5. JH Best FB Eddy GA Codd (2003) ArticleTitleEffects of Microcystis cells, cell extracts and lipopolysaccharide on drinking and liver function in rainbow trout Oncorhynchus mykiss walbaum Aquat Toxicol 64 419–426 Occurrence Handle10.1016/S0166-445X(03)00105-X Occurrence Handle12878412

    Article  PubMed  Google Scholar 

  6. CW Burns (1987) ArticleTitleInsights into zooplankton–cyanobacteria interactions New Zealand J Mar Freshwat Res 21 477–483

    Google Scholar 

  7. NR Bury FB Eddy GA Codd (1995) ArticleTitleThe effects of the cyanobacterium Microcystis-aeruginosa, the cyanobacterial hepatotoxin microcystin-LR, and ammonia on growth-rate and ionic regulation of brown trout J Fish Biol 46 1042–1054

    Google Scholar 

  8. CR Carbis GT Rawlin P Grant GF Mitchell JW Anderson I McCauley (1997) ArticleTitleA study of feral carp, Cyprinus carpio L, exposed to Microcystis aeruginosa at Lake Mokoan, Australia, and possible implications for fish health J Fish Dis 20 81–91 Occurrence Handle10.1046/j.1365-2761.1997.d01-111.x

    Article  Google Scholar 

  9. WW Carmichael (1997) The cyanotoxins J Callow (Eds) Advances in Botanical Research, vol 27 Academic Press London 211–256

    Google Scholar 

  10. PGJ De Maagd AJ Hendriks W Seinen D Sijm (1999) ArticleTitlepH-dependent hydrophobicity of the cyanobacterial toxin microcystin-LR Wat Res 33 677–680 Occurrence Handle10.1016/S0043-1354(98)00258-9

    Article  Google Scholar 

  11. VF De Magalhaes RM Soares S Azevedo (2001) ArticleTitleMicrocystin contamination in fish from the Jacarepagua lagoon (Rio de Janeiro, Brazil): ecological implication and human health risk Toxicon 39 1077–1085 Occurrence Handle10.1016/S0041-0101(00)00251-8 Occurrence Handle11223098

    Article  PubMed  Google Scholar 

  12. WR Demott (1999) ArticleTitleForaging strategies and growth inhibition in five daphnids feeding on mixtures of a toxic cyanobacterium and a green alga Freshwat Biol 42 263–274 Occurrence Handle10.1046/j.1365-2427.1999.444494.x

    Article  Google Scholar 

  13. LM Dionisio Pires KM Karlsson JAO Meriluoto PM Visser K Siewertsen E Van Donk BW Ibelings (2004) ArticleTitleAssimilation and depuration of microcystin-LR by the zebra mussel, Dreissena polymorpha Aquat Toxicol 69 385–396 Occurrence Handle10.1016/j.aquatox.2004.06.004 Occurrence Handle15312721

    Article  PubMed  Google Scholar 

  14. GBJ Dubelaar CS van der Reijden (1995) ArticleTitleSize distributions of Microcystis aeruginosa colonies: a flow cytometric approach Wat Sci Technol 32 171–176 Occurrence Handle10.1016/0273-1223(95)00695-8

    Article  Google Scholar 

  15. J Fastner M Erhard WW Carmichael F Sun KL Rinehart H Ronicke I Chorus (1999) ArticleTitleCharacterization and diversity of microcystins in natural blooms and strains of the genera Microcystis and Planktothrix from German freshwaters Arch Hydrobiol 145 147–163

    Google Scholar 

  16. JK Fawell RE Mitchell DJ Everett RE Hill (1999) ArticleTitleThe toxicity of cyanobacterial toxins in the mouse: I microcystin-LR Hum Exp Toxicol 18 162–167 Occurrence Handle10.1191/096032799678839842 Occurrence Handle10215106

    Article  PubMed  Google Scholar 

  17. A Ghadouani B Pinel-Alloul EE Prepas (2003) ArticleTitleEffects of experimentally induced cyanobacterial blooms on crustacean zooplankton communities Freshwat Biol 48 363–381 Occurrence Handle10.1046/j.1365-2427.2003.01010.x

    Article  Google Scholar 

  18. ZM Gliwicz E Siedlar (1980) ArticleTitleFood size limitation and algae interefering with food collection in Daphnia Arch Hydrobiol 88 155–177

    Google Scholar 

  19. F Gobas JB Wilcockson RW Russell GD Haffner (1999) ArticleTitleMechanism of biomagnification in fish under laboratory and field conditions Environ Sci Technol 33 133–141 Occurrence Handle10.1021/es980681m

    Article  Google Scholar 

  20. JS Gray (2002) ArticleTitleBiomagnification in marine systems: the perspective of an ecologist Mar Pollut Bull 45 46–52 Occurrence Handle12398366

    PubMed  Google Scholar 

  21. K Hamasaki T Takahashi S Uye (2003) ArticleTitleAccumulation of paralytic shellfish poisoning toxins in planktonic copepods during a bloom of the toxic dinoflagellate Alexandrium tamarense in Hiroshima Bay, western Japan Mar Biol 143 981–988 Occurrence Handle10.1007/s00227-003-1131-7

    Article  Google Scholar 

  22. MJ Horgan EL Mills (1997) ArticleTitleClearance rates and filtering activity of zebra mussel (Dreissena polymorpha): implications for freshwater lakes Can J Fish Aquat Sci 54 249–255 Occurrence Handle10.1139/cjfas-54-2-249

    Article  Google Scholar 

  23. BW Ibelings M Vonk HFJ Los DT Van der Molen WM Mooij (2003) ArticleTitleFuzzy modeling of cyanobacterial surface waterblooms: validation with NOAA-AVHRR satellite images Ecol Appl 13 1456–1472

    Google Scholar 

  24. HT Kankaanpaa VO Sipia JS Kuparinen JL Ott WW Carmichael (2001) ArticleTitleNodularin analyses and toxicity of a Nodularia spumigena (Nostocales, cyanobacteria) water-bloom in the western Gulf of Finland, Baltic Sea, in August 1999 Phycologia 40 268–274

    Google Scholar 

  25. C Keil A Forchert J Fastner U Szewzyk W Retard I Chorus R Kratke (2002) ArticleTitleToxicity and microcystin content of extracts from a Planktothrix bloom and two laboratory strains Wat Res 36 2133–2139 Occurrence Handle10.1016/S0043-1354(01)00417-1

    Article  Google Scholar 

  26. BG Kotak S Semalulu DL Fritz EE Prepas SE Hrudey RW Coppock (1996) ArticleTitleHepatic and renal pathology of intraperitoneally administered microcystin-LR in rainbow trout (Oncorhynchus mykiss) Toxicon 34 517–525 Occurrence Handle10.1016/0041-0101(96)00009-8 Occurrence Handle8783446

    Article  PubMed  Google Scholar 

  27. BG Kotak RW Zurawell EE Prepas CFB Holmes (1996) ArticleTitleMicrocystin-LR concentration in aquatic food web compartments from lakes of varying trophic status Can J Fish Aquat Sci 53 1974–1985 Occurrence Handle10.1139/cjfas-53-9-1974

    Article  Google Scholar 

  28. L Krienitz A Ballot K Kotut C Wiegand S Putz JS Metcalf GA Codd S Pflugmacher (2003) ArticleTitleContribution of hot spring cyanobacteria to the mysterious deaths of lesser flamingos at Lake Bogoria, Kenya FEMS Microbiol Ecol 43 141–148 Occurrence Handle10.1016/S0168-6496(02)00387-2

    Article  Google Scholar 

  29. LA Lawton C Edwards GA Codd (1994) ArticleTitleExtraction and high-performance liquid-chromatographic method for the determination of microcystins in raw and treated waters Analyst 119 1525–1530 Occurrence Handle10.1039/an9941901525 Occurrence Handle7943743

    Article  PubMed  Google Scholar 

  30. M Lurling (2003) ArticleTitleDaphnia growth on microcystin-producing and microcystin-free Microcystis aeruginosa in different mixtures with the green alga Scenedesmus obliquus Limnol Oceanogr 48 2214–2220

    Google Scholar 

  31. M Lurling E van der Grinten (2003) ArticleTitleLife-history characteristics of Daphnia exposed to dissolved microcystin-LR and to the cyanobacterium Microcystis aeruginosa with and without microcystins Environ Toxicol Chem 22 1281–1287 Occurrence Handle10.1897/1551-5028(2003)022<1281:LHCODE>2.0.CO;2 Occurrence Handle12785585

    Article  PubMed  Google Scholar 

  32. D Mackay A Fraser (2000) ArticleTitleBioaccumulation of persistent organic chemicals: mechanisms and models Environ Pollut 110 375–391 Occurrence Handle10.1016/S0269-7491(00)00162-7 Occurrence Handle15092817

    Article  PubMed  Google Scholar 

  33. VF de Magalhaes MM Marinho P Domingos AC Oliveira SM Costa LO Azevedo S Azevedo (2003) ArticleTitleMicrocystins (cyanobacteria hepatotoxins) bioaccumulation in fish and crustaceans from Sepetiba Bay (Brasil, RJ) Toxicon 42 289–295 Occurrence Handle10.1016/S0041-0101(03)00144-2 Occurrence Handle14559080

    Article  PubMed  Google Scholar 

  34. C Malbrouck G Trausch P Devos P Kestemont (2003) ArticleTitleHepatic accumulation and effects of microcystin-LR on juvenile goldfish Carassius auratus 1 Comp Biochem Physiol C—Toxicol Pharmacol 135 39–48 Occurrence Handle12781839

    PubMed  Google Scholar 

  35. H Matsunaga KI Harada M Senma Y Ito N Yasuda S Ushida Y Kimura (1999) ArticleTitlePossible cause of unnatural mass death of wild birds in a pond in Nishinomiya, Japan: sudden appearance of toxic cyanobacteria Natural Toxins 7 81–84 Occurrence Handle10.1002/(SICI)1522-7189(199903/04)7:2<81::AID-NT44>3.0.CO;2-O Occurrence Handle10495470

    Article  PubMed  Google Scholar 

  36. JS Metcalf KA Beattie J Ressler S Gerbersdorf S Pflugmacher GA Codd (2002) ArticleTitleCross-reactivity and performance assessment of four microcystin immunoassays with detoxication products of the cyanobacterial toxin, microcystin-LR J Wat Supply Res Technol Aqua 51 145–151

    Google Scholar 

  37. AP Negri GJ Jones (1995) ArticleTitleBioaccumulation of paralytic shellfish poisoning (PSP) toxins from the cyanobacterium Anabaena-circinalis by the fresh-water mussel Alathyria-condola Toxicon 33 667–678 Occurrence Handle10.1016/0041-0101(94)00180-G Occurrence Handle7660371

    Article  PubMed  Google Scholar 

  38. Noordhuis, R (2000) Watersysteemrapportage IJsselmeer en Markermeer. RIZA, Lelystad, 81 pp

  39. HD Park C Iwami MF Watanabe K Harada T Okino H Hayashi (1998) ArticleTitleTemporal variabilities of the concentrations of intra- and extracellular microcystin and toxic Microcystis species in a hypertrophic lake, Lake Suwa, Japan (1991–1994) Environ Toxicol Wat Qual 13 61–72 Occurrence Handle10.1002/(SICI)1098-2256(1998)13:1<61::AID-TOX4>3.0.CO;2-5

    Article  Google Scholar 

  40. S Pflugmacher V Ame C Wiegand C Steinberg (2001) ArticleTitleCyanobacterial toxins and endotoxins — their origin and their ecophysiological effects in aquatic organisms Wasser Boden 53 15–20

    Google Scholar 

  41. C Pietsch C Wiegand MV Ame A Nicklisch D Wunderlin S Pflugmacher (2001) ArticleTitleThe effects of a cyanobacterial crude extract on different aquatic organisms: evidence for cyanobacterial toxin modulating factors Environ Toxicol 16 535–542 Occurrence Handle10.1002/tox.10014 Occurrence Handle11769252

    Article  PubMed  Google Scholar 

  42. EE Prepas BG Kotak LM Campbell JC Evans SE Hrudey CFB Holmes (1997) ArticleTitleAccumulation and elimination of cyanobacterial hepatotoxins by the freshwater clam Anodonta grandis simpsoniana Can J Fish Aquat Sci 54 41–46 Occurrence Handle10.1139/cjfas-54-1-41

    Article  Google Scholar 

  43. GP Quinn MJ Keough (2002) Experimental Design and Data Analysis for Biologists Cambridge University Press Cambridge, UK

    Google Scholar 

  44. DF Raikow O Sarnelle AE Wilson SK Hamilton (2004) ArticleTitleDominance of the noxious cyanobacterium Microcystis aeruginosa in low-nutrient lakes is associated with exotic zebra mussels Limnol Oceanogr 49 482–487

    Google Scholar 

  45. M Reinikainen F Lindvall JAO Meriluoto S Repka K Sivonen L Spoof M Wahlsten (2002) ArticleTitleEffects of dissolved cyanobacterial toxins on the survival and egg hatching of estuarine calanoid copepods Mar Biol 140 577–583 Occurrence Handle10.1007/s00227-001-0720-6

    Article  Google Scholar 

  46. HD Rodger T Turnbull C Edwards GA Codd (1994) ArticleTitleCyanobacterial (blue-green-algal) bloom associated pathology in brown trout, Salmo-trutta L, in Loch Leven, Scotland J Fish Dis 17 177–181

    Google Scholar 

  47. T Rohrlack M Henning JG Kohl (1999) ArticleTitleMechanisms of the inhibitory effect of the cyanobacterium Microcystis aeruginosa on Daphnia galeata’s ingestion rate J Plankton Res 21 1489–1500 Occurrence Handle10.1093/plankt/21.8.1489

    Article  Google Scholar 

  48. T Rohrlack E Dittmann T Borner K Christoffersen (2001) ArticleTitleEffects of cell-bound microcystins on survival and feeding of Daphnia spp Appl Environ Microbiol 67 3523–3529 Occurrence Handle10.1128/AEM.67.8.3523-3529.2001 Occurrence Handle11472928

    Article  PubMed  Google Scholar 

  49. ML Saker JS Metcalf GA Codd VM Vasconcelos (2004) ArticleTitleAccumulation and depuration of the cyanobacterial toxin cylindrospermopsin in the freshwater mussel Anodonta cygnea Toxicon 43 185–194 Occurrence Handle10.1016/j.toxicon.2003.11.022 Occurrence Handle15019478

    Article  PubMed  Google Scholar 

  50. T Sano K Nohara F Shiraishi K Kaya (1992) ArticleTitleA method for microdetermination of total microcystin content in waterblooms of cyanobacteria (blue-green-algae) Int J Environ Anal Chem 49 163–170

    Google Scholar 

  51. K Sivonen G Jones (1999) Cyanobacterial toxins I Chorus J Bertram (Eds) Toxic Cyanobacteria in Water E&FN Spon London 416

    Google Scholar 

  52. L Spoof P Vesterkvist T Lindholm J Meriluoto (2003) ArticleTitleScreening for cyanobacterial hepatotoxins, microcystins and nodularin in environmental water samples by reversed-phase liquid chromatography–electrospray ionisation mass spectrometry J Chromatogr A 1020 105–119 Occurrence Handle10.1016/S0021-9673(03)00428-X Occurrence Handle14661762

    Article  PubMed  Google Scholar 

  53. F Tencalla D Dietrich (1997) ArticleTitleBiochemical characterization of microcystin toxicity in rainbow trout (Oncorhynchus mykiss) Toxicon 35 583–595 Occurrence Handle10.1016/S0041-0101(96)00153-5 Occurrence Handle9133713

    Article  PubMed  Google Scholar 

  54. FG Tencalla DR Dietrich C Schlatter (1994) ArticleTitleToxicity of Microcystis-aeruginosa peptide toxin to yearling rainbow-trout (Oncorhynchus-mykiss) Aquat Toxicol 30 215–224 Occurrence Handle10.1016/0166-445X(94)90059-0

    Article  Google Scholar 

  55. L Thostrup K Christoffersen (1999) ArticleTitleAccumulation of microcystin in Daphnia magna feeding on toxic Microcystis Arch Hydrobiol 145 447–467

    Google Scholar 

  56. HA Vanderploeg JR Liebig WW Carmichael MA Agy TH Johengen GL Fahnenstiel TF Nalepa (2001) ArticleTitleZebra mussel (Dreissena polymorpha) selective filtration promoted toxic Microcystis blooms in Saginaw Bay (Lake Huron) and Lake Erie Can J Fish Aquat Sci 58 1208–1221 Occurrence Handle10.1139/cjfas-58-6-1208

    Article  Google Scholar 

  57. VM Vasconcelos (1999) ArticleTitleCyanobacterial toxins in Portugal: effects on aquatic animals and risk for human health Brazilian J Med Biol Res 32 249–254

    Google Scholar 

  58. RJ Vos JHM Hakvoort RWJ Jordans BW Ibelings (2003) ArticleTitleMultiplatform optical monitoring of eutrophication in temporally and spatially variable lakes Sci Total Environ 312 221–243 Occurrence Handle10.1016/S0048-9697(03)00225-0 Occurrence Handle12873412

    Article  PubMed  Google Scholar 

  59. MM Watanabe K Kaya N Takamura (1992) ArticleTitleFate of toxic cyclic hetapeptides, the microcystin, from blooms of Microcystis (cyanobacteria) in a hypertrophic lake J Phycol 28 761–767 Occurrence Handle10.1111/j.0022-3646.1992.00761.x

    Article  Google Scholar 

  60. DE Williams M Craig SC Dawe ML Kent CFB Holmes RJ Andersen (1997) ArticleTitleEvidence for a covalently bound form of microcystin-LR in salmon liver and Dungeness crab larvae Chem Res Toxicol 10 463–469 Occurrence Handle10.1021/tx9601519 Occurrence Handle9114985

    Article  PubMed  Google Scholar 

  61. DE Williams SC Dawe ML Kent RJ Andersen M Craig CFB Holmes (1997) ArticleTitleBioaccumulation and clearance of microcystins from salt water, mussels, Mytilus edulis, and in vivo evidence for covalently bound microcystins in mussel tissues Toxicon 35 1617–1625 Occurrence Handle10.1016/S0041-0101(97)00039-1 Occurrence Handle9428108

    Article  PubMed  Google Scholar 

  62. LQ Xie P Xie K Ozawa T Honma A Yokoyama HD Park (2004) ArticleTitleDynamics of microcystins-LR and -RR in the phytoplanktivorous silver carp in a sub-chronic toxicity experiment Environ Pollut 127 431–439 Occurrence Handle10.1016/j.envpol.2003.08.011 Occurrence Handle14638304

    Article  PubMed  Google Scholar 

  63. A Yokoyama HD Park (2003) ArticleTitleDepuration kinetics and persistence of the cyanobacterial toxin microcystin-LR in the freshwater bivalve Unio douglasiae Environ Toxicol 18 61–67 Occurrence Handle10.1002/tox.10102 Occurrence Handle12539145

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was funded by Rijkswaterstaat (Hoofdkantoor and Regionale Directie IJsselmeergebied - RDIJ). Harro Reeders and later Winfried Laane made funding available for the study at RDIJ and participated in supervising the study that was carried out by AquaSense. Several employees at AquaSense including Ad van Mullem were involved in the study reported here. Staff from the Ecology Department of the Institute for Inland Water Management and Waste Water Treatment—RIZA contributed to the study via many valuable discussions. N. Stockhofe-Zurwieden from ID-Lelystad performed the histological studies. Analysis of microcystin using the MMPB method was kindly carried out by Krister Karlsson at the laboratory of Dr. Jussi Meriluoto from the Åbo Akademi University in Turku, Finland. We also acknowledge the advice of Dr. Lisette De Senerpont Domis on statistics.

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Ibelings, B., Bruning, K., de Jonge, J. et al. Distribution of Microcystins in a Lake Foodweb: No Evidence for Biomagnification. Microb Ecol 49, 487–500 (2005). https://doi.org/10.1007/s00248-004-0014-x

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