First evidence of "paralytic shellfish toxins" and cylindrospermopsin in a Mexican freshwater system, Lago Catemaco, and apparent bioaccumulation of the toxins in "tegogolo" snails (Pomacea patula catemacensis)

Toxicon

Volumn 55, Issue 5, 2010, Pages 930-938

  Berry, John P ^a   Lind, Owen ^b  

^a FLORIDA INTERNATIONAL UNIVERSITY   (United States)

^b BAYLOR UNIVERSITY   (United States)

Author keywords

Bioaccumulation; Cylindrospermopsin; Gastropod; Lago Catemaco; Mexico; Microcystin; Paralytic shellfish poisoning (PSP); Saxitoxin

Indexed keywords

CYLINDROSPERMOPSIN; FRESH WATER; MICROCYSTIN; SHELLFISH TOXIN;

ARTICLE; BIOACCUMULATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYLINDROSPERMOPSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FOOD CONTAMINATION; FOOD WEB; FRESHWATER ENVIRONMENT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LAKE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MEXICO; PHYTOPLANKTON; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SENSITIVITY AND SPECIFICITY; SNAIL; SPECIES ENDEMICITY; TOXICOKINETICS; TOXIN ANALYSIS; ULTRAVIOLET SPECTROSCOPY; WATER CONTAMINATION; WATER SAMPLING;

ALKALOIDS; ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYANOBACTERIA; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; FRESH WATER; HARMFUL ALGAL BLOOM; MASS SPECTROMETRY; MEXICO; MICROCYSTINS; SAXITOXIN; SHELLFISH POISONING; SNAILS; TISSUE EXTRACTS; URACIL; WATER MICROBIOLOGY; WATER POLLUTANTS, CHEMICAL;

ALGAE; CYANOBACTERIA; CYLINDROSPERMOPSIS; CYLINDROSPERMOPSIS CATEMACO; CYLINDROSPERMOPSIS PHILIPPINENSIS; GASTROPODA; POMACEA PATULA;

EID: 77649235214     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2009.07.035     Document Type: Article

References (79)

1. Adamovsky O., Kopp R., Hilscherova K., Babica P., Palikova M., Paskova V., et al. Microcystin kinetics (bioaccumulation and elimination) and biochemical responses in common carp (Cyprinus carpio) and silver carp (Hypophtalmichthys molitrix) exposed to toxic cyanobacterial blooms. Environ Toxicol Chem 26 12 (2007) 2687-2693
2. Amorim A., and Vasconcelos V. Dynamics of microcystins in the mussel Mytilus galloprovincialis. Toxicon 37 7 (1999) 1041-1052
3. Baqueiro, E., 1994. Principales recursos malacológicos del Golfo de México. In: Instituto Nacional de Pesca (Ed.), Pesquerías Relevantes de México, Tomo II. Secretaria de Medio Ambiente, Recursos Naturales y Pesca (SEMARNAP), México, pp. 131-142.
4. Bischoff K. The toxicology of microcystin-LR: occurrence, toxicokinetics, toxicodynamics, diagnosis and treatment. Vet Hum Toxicol 43 5 (2001) 294-297
5. Blahova L., Oravec M., Marsalek B., Sejnohova L., Simek Z., and Blaha L. The first occurrence of the cyanobacterial alkaloid toxin cylindrospermopsin in the Czech Republic as determined by immunochemical and LC-MS methods. Toxicon 53 5 (2009) 519-524
6. Burch M.D. Effective doses, guidelines and regulations. Adv Exp Med Biol 619 (2008) 831-853
7. Carmichael W.W., Evans W.R., Yin Q.Q., Bell P., and Moczydlowsky E. Evidence of paralytic shellfish poisons in the freshwater cyanobacterium Lyngbya wollei. Appl Environ Microbiol 63 (1997) 3104-3110
8. Cazenave J., Wunderlin D.A., de Los Angeles Bistoni M., Amé M.V., Krause E., Pflugmacher S., et al. Uptake, tissue distribution and accumulation of microcystin-RR in Corydoras paleatus, Jenynsia multidentata and Odontesthes bonariensis. A field and laboratory study. Aquat Toxicol 75 2 (2005) 178-190
9. Chen J., and Xie P. Seasonal dynamics of the hepatotoxic microcystins in various organs of four freshwater bivalves from the large eutrophic lake Taihu of subtropical China and the risk to human consumption. Environ Toxicol 20 6 (2005) 572-584
10. Chen J., Xie P., Guo L., Zheng L., and Ni L. Tissue distribution and seasonal dynamics of the hepatotoxic microcystins-LR and -RR in a freshwater snail (Bellamya aeruginosa) from a large shallow, eutrophic lake of the subtropical China. Environ Pollut 134 3 (2005) 423-430
11. Chen J., and Xie P. Microcystin accumulation in freshwater bivalves from Lake Taihu, China, and the potential risk to human consumption. Environ Toxicol Chem 26 5 (2007) 1066-1073
12. Chen J., Zhang D., Xie P., Wang Q., Ma Z., 2009. Simultaneous determination of microcystin contaminations in various vertebrates (fish, turtle, duck and water bird) from a large eutrophic Chinese lake, Lake Taihu, with toxic Microcystis blooms. Sci Total Environ 407 (10), 3317-3322.
13. Chong M.W., Wong B.S., Lam P.K., Shaw G.R., and Seawright A.A. Toxicity and uptake mechanism of cylindrospermopsin and lophyrotomin in primary rat hepatocytes. Toxicon 40 2 (2002) 205-211
14. Codd G.A., Ward C.J., Bell, S.G., 1997. Cyanobacterial toxins: occurrence, modes of action, health effects and exposure routes. Arch Toxicol Suppl 19, 399-410.
15. Codd G.A., Morrison L.F., and Metcalf J.S. Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203 3 (2005) 264-272
16. Dawson R.M. The toxicology of microcystins. Toxicon 36 7 (1998) 953-962
17. Deeds J.R., Landsberg J.H., Etheridge S.M., Pitcher G.C., and Longan S.W. Non-traditional vectors for paralytic shellfish poisoning. Mar Drugs 6 2 (2008) 308-348
18. Dörr F.A., Tomaz J.C., Lopes N.P., and Pinto E. Comparative analysis of the gas-phase reactions of cylindrospermopsin and the difference in the alkali metal cation mobility. Rap Commun Mass Spectrom 22 13 (2008) 2015-2020
19. Duy T.N., Lam P.K., Shaw G.R., and Connell D.W. Toxicology and risk assessment of freshwater cyanobacterial (blue-green algal) toxins in water. Rev Environ Contam Toxicol 163 (2000) 113-185
20. Falconer I.R., and Humpage A.R. Cyanobacterial (blue-green algal) toxins in water supplies: cylindrospermopsins. Environ Toxicol 21 4 (2006) 299-304
21. Fastener J., Heinze R., Humpage A.R., Mischke U., Eaglesham G.K., and Chorus I. Cylindrospermopsin occurrence in two German lakes and preliminary assessment and toxin production of Cylindrospermopsis raciborskii isolates. Toxicon 42 3 (2003) 313-321
22. Ferrao-Filho A.S., Kozlowsky-Suzuki B., and Azevedo S.M. Accumulation of microcystins by a tropical zooplankton community. Aquat Toxicol 59 3-4 (2002) 201-208
23. Ferreira F.M.B., Soler J.M.F., Fidalgo M.L., and Fernandez-Villa P. PSP toxins from Aphanizomenon flos-aquae (cyanobacteria) collected in the Crestuma-Lever reservoir (Douro River, northern Portugal). Toxicon 39 6 (2001) 757-761
24. Funari E., and Testai E. Human health risk assessment related to cyanotoxins exposure. Crit Rev Toxicol 38 2 (2008) 97-125
25. Gerwick W.H., Tan L.T., and Sitachitta N. Nitrogen-containing metabolites from marine cyanobacteria. Alkaloids Chem Biol 57 (2001) 75-184
26. Griffiths D.J., and Saker M.L. The Palm Island mystery disease 20 years on: a review of research on the cyanotoxin cylindrospermopsin. Environ Toxicol 18 2 (2003) 78-93
27. Harada K.I., Ohtani I., Iwamoto K., Suzuki M., Watanabe M.F., Watanabe M., et al. Isolation of cylindrospermopsin from a cyanobacterium, Umezekia natans, and its screening method. Toxicon 32 1 (1994) 73-84
28. Hawkins P.R., Putt E., Falconer I., and Humpage A. Phenotypical variation in toxic strain of the phytoplankter, Cylindrospermopsis raciborskii, during batch culture. Environ Toxicol 16 6 (2001) 460-467
29. Hitzfield B.C., Höger S.J., and Dietrich D.R. Cyanobacterial toxins: removal during drinking water treatment, and human risk assessment. Environ Health Perspect 108 Suppl. 1 (2000) 113-122
30. Hoeger S.J., Shaw G., Hitzfield B.C., and Dietrich D.R. Occurrence and elimination of cyanobacterial toxins in two Australian drinking water treatment plants. Toxicon 43 6 (2004) 639-649
31. Hoeger S.J., Hitzfield B.C., and Dietrich D.R. Occurrence and elimination of cyanobacterial toxins in drinking water treatment plants. Toxicol Appl Pharmacol 203 3 (2005) 231-242
32. Humpage A.R., Rositano J., Bretag A., Brown R., Baker P., Nicholson B.C., et al. Paralytic shellfish poisons from Australian cyanobacterial blooms. Aust J Mar Freshw Res 45 (1994) 761-771
33. Hungerford J.M. Committee on natural toxins and food allergens. Marine and freshwater toxins. J AOAC Int 88 1 (2005) 299-313
34. Ibelings B.W., Bruning K., de Jonge J., Wolfstein K., Pires L.M., Postma J., et al. Distribution of microcystins in a lake foodweb: no evidence for biomagnification. Microb Ecol 49 4 (2005) 487-500
35. Ibelings B.W., and Chorus I. Accumulation of cyanobacterial toxins in freshwater "seafood" and its consequences for public health: a review. Environ Pollut 150 1 (2007) 177-192
36. Kankaanpää H.T., Holliday J., Schröder H., Goddard T.J., von Fister R., and Carmichael W.W. Cyanobacterial and prawn farming in northern New South Wales, Australia-a case study on cyanobacteria diversity and hepatotoxin bioaccumulation. Toxicol Appl Pharmacol 203 3 (2005) 243-256
37. Kellmann R., Mihali T.K., Jeon Y.J., Pickford R., Pomati F., and Neilan B.A. Biosynthetic intermediate analysis and functional homology reveal a saxitoxin gene cluster in cyanobacteria. Appl Environ Microbiol 74 13 (2008) 4044-4053
38. Komárkova J., and Tavera R. Cyanoprokaryota (Cyanobacteria) in the phytoplankton of the lake Catemaco (Veracruz, Mexico). Archiv Für Hydrobiol Algolog Studies 83 (1996) 403-422
39. Komárková J. Fish stock as a variable modifying trophic pattern of phytoplankton. Hydrobiologia 367/370 (1998) 139-152
40. Komárkova J., and Tavera R. Steady state of phytoplankton assemblage in the tropical Lake Catemaco (Mexico). Hydrobiologia 502 (2003) 187-196
41. Kubo T., Sano T., Hosoya K., Tanaka N., and Kaya K. A new simply and effective fractionation method for cylindrospermopsin analyses. Toxicon 46 (2005) 104-107
42. Lagos N., Onodera H., Zagatto P., Andrinolo D., Azevedo S., and Oshima Y. The first evidence of paralytic shellfish toxins in the freshwater cyanobacterium, Cylindrospermopsis raciborskii, isolated from Brazil. Toxicon 37 (1999) 1359-1373
43. Lance E., Brient L., Bormans M., and Gerard C. Interactions between cyanobacteria and gastropods I. Ingestion of toxic Planktothrix agardhii by Lymnaea stagnalis and the kinetics of microcystin bioaccumulation and detoxification. Aquat Toxicol 79 2 (2006) 140-148
44. Li R., Carmichael W.W., Brittain S., Eaglesham G.K., Shaw G.R., Mahakhant A., et al. Isolation and identification of the cyanotoxin cylindrospermopsin and deoxy-cylindrospermopsin from Thailand strain of Cylindrospermopsis raciborskii (Cyanobacteria). Toxicon 39 7 (2001) 973-980
45. Lind O., Dávalos-Lind L., Lopez C., Lopez M. Rainy and dry season differences of Cylindrospermopsis catemaco (Cyanobacteria) trichome morphotypes, heterocyte size and abundance in tropical Lake Catemaco, México. Hydrobiologia, in press.
46. Magalhaes V.F., Soares R.M., and Azevedo S.M. Microcystin contamination in fish from Jacarepaguá Lagoon (Rio de Janeiro, Brazil): ecological implication and human health risk. Toxicon 39 7 (2001) 1077-1085
47. Magalhaes V.F., Marinho M.M., Domingos P., Oliveira A.C., Costa S.M., Azevedo L.O., et al. Microcystins (cyanobacteria hepatotoxins) bioaccumulation in fish and crustaceans from Sepetiba Bay (Brazil, RJ). Toxicon 42 3 (2003) 289-295
48. Mohamed Z.A. Accumulation of cyanobacterial hepatotoxins by Daphnia in some Egyptian irrigation canals. Ecotoxicol Environ Saf 50 1 (2001) 4-8
49. Negri A.P., and Jones G.J. Bioaccumulation of paralytic shellfish poisoning (PSP) toxins from the cyanobacterium Anabaena circinalis by the freshwater mussel Alathyria Condola. Toxicon 33 5 (1995) 667-678
50. Nelson S., and Gonzalez-Caver E. Geology and K-Ar dating of the Tuxtla volcanic field, Veracruz, Mexico. Bull Volcanology 55 (1992) 85-96
51. Norris R.L., Eaglesham G.K., Shaw G.R., Senogles P., Chiswell R.K., Smith M.J., et al. Extraction and purification of the zwitterions cylindrospermopsin and deoxycylindrospermopsin from Cylindrospermopsis raciborskii. Environ Toxicol 16 5 (2001) 391-396
52. Pereira P., Onodera H., Andrinolo D., Franca S., Araujo F., Lago N., et al. Paralytic shellfish toxins in the freshwater cyanobacterium Aphanizomenon flos-aquae isolated from Montargil reservoir, Portugal. Toxicon 38 12 (2000) 1689-1702
53. Pereira P., Dias E., Franca S., Pereira E., Carolino M., and Vasconcelos V. Accumulation and depuration of cyanobacterial paralytic shellfish toxins by the freshwater mussel Anodonta cygnea. Aquat Toxicol 68 4 (2004) 339-350
54. Pires L.M., Karlsson K.M., Meriluoto J.A., Kardinaal E., Visser P.M., Siewertsen K., et al. Assimilation and depuration of microcystin-LR by the zebra mussel, Dreissena polymorpha. Aquat Toxicol 69 4 (2004) 385-396
55. Pomati F., SacchiRossetti C., Giovannardi S., Onodera H., Oshima Y., and Neilan B.A. The freshwater cyanobacterium Planktothrix sp. FP1: molecular identification and detection of paralytic shellfish poisoning toxins. J Phycol 36 (2000) 553-562
56. Rao P.V., Gupta N., Bhaskar A.S., and Jayaraj R. Toxins and bioactive compounds from cyanobacteria and their implications on human health. J Environ Biol 23 3 (2002) 215-224
57. Rapala J., Robertson A., Negri A.P., Berg K.A., Tuomi P., Lyra C., et al. First report of saxitoxin in Finnish lakes and possible associated effects on human health. Environ Toxicol 20 3 (2005) 331-340
58. Rücker J., Stüken A., Nixdorf B., Fastner J., Chorus I., and Wiedner C. Concentrations of particulate and dissolved cylindrospermopsin in 21 Aphanizomenon-dominated temperate lakes. Toxicon 50 6 (2007) 800-809
59. Ruiz-Ramirez R., Espinosa-Chavez F., and Martinez-Jeronimo F. Growth and reproduction of Pomacea patula catemacensis when fed Calothrix sp. J World Aquacult Soc 36 1 (2005) 87-95
60. Saker M.L., and Eaglesham G.K. The accumulation of cylindrospermopsin from the cyanobacterium Cylindrospermopsis raciborskii in tissues of the Redclaw crayfish, Cherax quadricarinatus. Toxicon 37 7 (1999) 1065-1077
61. Saker M.L., and Neilan B.A. Varied diazotrophies, morphologies, and toxicities of genetically similar isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from North Australia. Appl Environ Microbiol 67 4 (2001) 1839-1845
62. Saker M.L., Nogueira I.C., Vasconcelos V.M., Neilan B.A., Eaglesham G.K., and Pereira P. First report and toxicological assessment of the cyanobacterium Cylindrospermopsis raciborskii from Portuguese freshwaters. Ecotoxicol Environ Saf 55 2 (2003) 243-250
63. Saker M.L., Metcalf J.S., Codd G.A., and Vasconcelos V.M. Accumulation and depuration of the cyanobacterial toxin cylindrospermopsin in the freshwater mussel Anodonta cygnea. Toxicon 43 2 (2004) 185-194
64. Smith J.L., and Haney J.F. Foodweb transfer, accumulation, and depuration of microcystins, a cyanobacterial toxins, in pumpkinseed sunfish (Lepomis gibbosus. Toxicon 48 5 (2006) 580-589
65. Song L., Chen W., Peng L., Wan N., Gan N., and Zhang X. Distribution and bioaccumulation of microcystins in water columns: a systematic investigation into the environmental fate and the risks associated with microcystins in Meiliang Bay, Lake Taihu. Water Res 41 13 (2007) 2853-2864
66. Streit B. Bioaccumulation of contaminants in fish. In: Braunbeck T., Hinton D.E., and Streit B. (Eds). Fish Ecotoxicology (1998), Birkhauser, Basel, Switzerland 353-388
67. Törökne A., Asztalos M., Bankine M., Bickel H., Borbely G., Carmeli S., et al. Interlaboratory comparison trial on cylindrospermopsin measurement. Anal Biochem 332 2 (2004) 280-284
68. Van Apeldoorn M.E., van Egmond H.P., Speijers G.J., and Bakker G.J. Toxins of cyanobacteria. Mol Nutr Food Res 51 1 (2007) 7-60
69. Watanabe M.F., Park H.D., Kondo F., Harada K., Hayashi H., and Okino T. Identification and estimation of microcystins in freshwater mussels. Nat Toxins 5 1 (1997) 31-35
70. Welker M., Bickel H., and Fastner J. HPLC-PDA detection of cylindrospermopsin-opportunities and limits. Water Res 36 18 (2002) 4659-4663
71. White S.H., Duivenvoorden L.J., Fabbro L.D., and Eaglesham G.K. Influence of intracellular toxin concentrations on cylindrospermopsin bioaccumulation in a freshwater gastropod (Melanoides tuberculata). Toxicon 47 (2006) 497-509
72. Wilson A.E., Gossiaux D.C., Höök T.O., Berry J.P., Landrum P.F., Dyble J., et al. Evaluation of the human health threat associated with the hepatotoxin microcystin in the muscle and liver tissues of yellow perch (Perca flavescens). Can J Fish Aquat Sci 65 (2008) 1487-1497
73. Wood S.A., Briggs L.R., Sprosen J., Ruck J.G., Wear R.G., Holland P.T., et al. Changes in concentration of microcystins in rainbow trout, freshwater mussels, and cyanobacteria in Lake Rotoiti and Rotoehu. Environ Toxicol 21 3 (2006) 205-222
74. Xie L., Xie P., Guo L., Li L., Miyabara Y., and Park H.D. Organ distribution and bioaccumulation of microcystins in freshwater fish at different trophic levels from the eutrophic Lake Chaohu, China. Environ Toxicol 20 3 (2005) 293-300
75. Xie L., Yokoyama A., Nakamura K., and Park H. Accumulation of microcystins in various organs of the freshwater snail Sinotaia histrica and three fishes in a temperate lake, the eutrophic Lake Suwa, Japan. Toxicon 49 5 (2007) 646-652
76. Yilmaz M., Phlips E.J., Szabo N.J., and Badylak S. A comparative study of Florida strains of Cylindrospermopsis and Aphanizomenon for cylindrospermopsin production. Toxicon 51 (2008) 130-139
77. Zhang D., Xie P., Liu Y., Chen J., and Liang G. Bioaccumulation of the hepatotoxic microcystins in various organs of a freshwater snail from a subtropical Chinese lake, Taihu Lake, with dense toxic Microcystis blooms. Environ Toxicol Chem 26 1 (2007) 171-176
78. Zhang D., Xie P., Liu Y., and Qiu T. Transfer, distribution and bioaccumulation of microcystins in the aquatic food web in Lake Taihu, China with potential risks to human health. Sci Total Environ 407 7 (2009) 2191-2199
79. Zurawell R.W., Goldberg J.I., Holmes C.F., and Prepas E.E. Tissue distribution and oral dose effects of microcystin in the freshwater pulmonate snail Lymnaea stagnalis jugularis (Say). J Toxicol Environ Health A 70 7 (2007) 620-626