Abstract
There has been a recent push for human consumption of the invasive Pacific lionfishes Pterois miles/volitans as a management strategy throughout the greater western tropical Atlantic region, where lionfish have become a significant ecological problem. Recent tests have indicated that invasive lionfishes may be ciguatoxic, threatening the viability of a fishery-based management strategy. However, if innate scorpaenitoxins in the flesh of lionfish are mimicking ciguatoxin, consumption may be safe after all. There have been no confirmed cases of ciguatoxin poisoning from eating lionfish, indicating that false positive tests may be occurring. Based on the high degree of similarity in the biochemical effects of ciguatoxin and scorpaenitoxins, it is possible that bioassays for ciguatoxin are inaccurate in scorpaeniform fishes. Preliminary results suggest that scorpaenitoxins or other venom components are capable of contaminating ciguatoxin assays, and thus we urge caution regarding interpretation of ciguatoxin assays in invasive lionfishes. We recommend that ciguatera tests of lionfish be done after cooking the flesh, which denatures the scorpaenitoxins yet leaves ciguatoxin intact.
References
Albins MA (2013) Effects of invasive Pacific red lionfish Pterois volitans versus a native predator on Bahamian coral-reef fish communities. Biol Invasions 15:29–43
Albins MA, Hixon MA (2008) Invasive Indo-Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Mar Ecol Prog Ser 367:233–238
Albins MA, Hixon MA (2013) Worst-case scenario: potential long-term effects of invasive predatory lionfish (Pterois volitans) on Atlantic and Caribbean coral-reef communities. Environ Biol Fish 96:1151–1157
Allen GR, Eschmeyer WN (1973) Turkeyfishes at Eniwetok. Pac Discov 26:3–11
Andrich F, Carnielli J, Cassoli J, Lautner R, Santos RA, Pimenta AM, de Lima ME, Figueiredo SG (2010) A potent vasoactive cytolysin isolated from Scorpaena plumieri scorpionfish venom. Toxicon 56:487–496
Arena P, Levin B, Fleming L, Friedman M, Blythe D (2004) A pilot study of the cognitive and psychological correlates of chronic ciguatera poisoning. Harmful Algae 3:51–60
Austin L, Gillis R, Youatt G (1965) Stonefish venom: some biochemical and chemical observations. Aust J Exp Biol Med Sci 43:79–90
Balasubashini SR, Karthigayan S, Somasundaram ST, Balasubramanian T, Rukkumani R, Menon VP (2006) FV peptide induces apoptosis in HEp 2 and HeLa cells: an insight into the mechanism of induction. J Carcinog 5:27
Barbour AB, Allen MS, Frazer TK, Sherman KD (2011) Evaluating the potential efficacy of invasive lionfish (Pterois volitans) removals. PLoS ONE 6(5):e19666. doi:10.1371/journal.pone.0019666
Britton JR, Gozlan RE, Copp GH (2010) Managing non-native fish in the environment. Fish Fish 12:256–274
Casewell NR, Wüster W, Vonk FJ, Harrison R, Fry BG (2012) Complex cocktails: the evolutionary novelty of venoms. Trends Ecol Evol 28:219–229
Choromanski J (1985) Chemical stabilization and pharmacological characterization of the venom of the lionfish, Pterois volitans. Dissertation, Oregon State University
Chun, LH (2005) Functional and structural studies of Stonustoxin (SNTX), a lethal factor from Stonefish (Synanceja horrida) venom. Master’s Thesis, National University of Singapore
Church J, Hodgson W (2001) Stonefish (Synanceia spp.) antivenom neutralizes the in vitro and in vivo cardiovascular activity of soldierfish (Gymnapistes marmoratus) venom. Toxicon 39:319–324
Church J, Hodgson W (2002) Adrenergic and cholinergic activity contributes to the cardiovascular effects of lionfish (Pterois volitans) venom. Toxicon 40:787–796
Church J, Hodgson W (2003) Stonefish (Synanceia trachynis) antivenom: in vitro efficacy and clinical use. Toxin Rev 22:69–76
Cohen AS, Olek AJ (1989) An extract of lionfish (Pterois volitans) spine tissue contains acetylcholine and a toxin that affects neuromuscular transmission. Toxicon 27:1367–1376
Côté IM, Green SJ, Hixon MA (2013) Predatory fish invaders: Insights from Indo-Pacific lionfish in the western Atlantic and Caribbean. Biol Conserv 164:50–61. doi:10.1016/j.biocon.2013.04.014
Ehrenfield JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80
Erickson MC (1993) Lipid extraction from channel catfish muscle: comparison of solvent systems. J Food Sci 58:84–89
Ferguson T, Akins L (2010) The lionfish cookbook. REEF Environmental Education Foundation, Key Largo
Fleming LE, Baden DG, Bean JA, Weisman R, Blythe DG (1998) Marine seafood toxin diseases: Issues in epidemiology and community outreach. In: Reguera B, Blanco J, Fernandez ML, Wyatt T (eds) Harmal Algae. Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, Vigo and Paris, pp 245–248
Fry BG, Roelants K, Champagne DE, Scheib H, Tyndall JD, King GF, Nevalainen TJ, Norman JA, Lewis RJ, Norton RS, Renjifo C, de la Vega RC (2009) The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet 10:483–511
Garnier P, Goudey-Perriere F, Breton P, Dewulf C, Petek F, Perriere C (1995) Enzymatic properties of the stonefish (Synanceia verrucosa Bloch and Schneider, 1801) venom and purification of a lethal, hypotensive and cytolytic factor. Toxicon 33:143–155
Garnier P, Grosclaude JM, Goudey-Perrière F, Gervat V, Gayral P, Jacquot C, Perrière C (1996) Presence of norepinephrine and other biogenic amines in stonefish venom. J Chromatogr B Biomed Appl 685:364–369
Garnier P, Ducancel F, Ogawa T, Boulain J, Goudey-Perrière F, Perrière C, Ménez A (1997) Complete amino-acid sequence of the [beta]-subunit of VTX from venom of the stonefish (Synanceia verrucosa) as identified from cDNA cloning experiments. Biochim Biophys Acta 1337:1–5
Ghadessy F, Chen D, Kini R, Chung M, Jeyaseelan K, Khoo H, Yuen R (1996) Stonustoxin is a novel lethal factor from stonefish (Synanceja horrida) venom. J Biol Chem 271:25575–22581
Gill E (2012) Florida Sea Grant says not to eat lionfish. TCPalm. http://www.tcpalm.com/news/2012/jul/02/florida-sea-grant-says-not-to-eat-lionfish-23815/. Accessed 02 July 2012
Glaziou P, Legrand A-M (1994) The epidemiology of ciguatera fish poisoning. Toxicon 32:863–873
Green SJ, Akins JL, Maljković A, Côté IM (2012) Invasive lionfish drive Atlantic coral reef fish declines. PLoS ONE 7:e32596. doi:10.1371/journal.pone.0032596
Hackerott S, Valdivia A, Green SJ, Côté IM, Cox CE, Akins L, Layman CA, Precht WF, Bruno JF (2013) Native predators do not influence invasion success of Pacific lionfish on Caribbean reefs. PLoS ONE 8(7):e68259. doi:10.1371/journal.pone.0068259
Halstead B (1988) Poisonous and venomous marine animals of the world. Darwin Press, Princeton
Hokama Y (2004) Ciguatera fish poisoning: Features tissue and body effects. In: Watson RR, Preedy VR (eds) Reviews in food and nutrition toxicity. CRC Press, Boca Raton, pp 43–83
Hopkins BJ, Hodgson WC, Sutherland SK (1996) Evidence for adrenergic and tachykinin activity in venom of the stonefish (Synanceja trachynis). Toxicon 34:541–554
Juranovic LR, Park DL (1991) Foodborne toxins of marine origin: ciguatera. Rev Environ Contam T 117:51–94
Juzans P, Colasante C, Kreger AS, Molgo J (1995) Increase in spontaneous quantal ACh release and alterations of motor nerve terminals induced by an isolated peptide of stonefish (Synanceia trachinis) venom. Toxicon 33:1125
Kasdan ML, Kasdan AS, Hamilton DL (1987) Lionfish envenomation. Plast Reconstr Surg 80:613–614
Khoo H (2002) Bioactive proteins from stonefish venom. Clin Exp Pharmacol Physiol 29:802–806
Khoo H, Yuen R, Poh C, Tan C (1992) Biological activities of Synanceja horrida (stonefish) venom. Nat Toxins 1:54–60
Kimball ME, Miller JM, Whitfield PE, Hare JA (2004) Thermal tolerance and potential distribution of invasive lionfish (Pterois volitans/miles complex) on the east coast of the United States. Mar Ecol Prog Ser 283:269–278
Kiriake A, Shiomi K (2011) Some properties and cDNA cloning of proteinaceous toxins from two species of lionfish (Pterois antennata and Pterois volitans). Toxicon 58:494–501
Kizer KW, McKinney HE, Auerbach PS (1985) Scorpaenidae envenomation: a 5-year poison center experience. JAMA 8:807–810
Kreger A (1991) Detection of a cytolytic toxin in the venom of the stonefish (Synanceia trachynis). Toxicon 29:733–743
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lesser MP, Slattery M (2011) Phase shift to algal dominated communities at mesophotic depths associated with lionfish (Pterois volitans) invasion on a Bahamian coral reef. Biol Invasions 13:1855–1868
Lewis ND (1986) Epidemiology and impact of ciguatera in the Pacific: a review. Mar Fish Rev 48:6–13
Lewis R (1988) Negative inotropic and arrhythmic effects of high doses of ciguatoxin on guinea-pig atria and papillary muscle. Toxicon 26:639–649
Lovell SJ, Stone SF (2005) The economic impacts of aquatic invasive species: a review of the literature. US Environmental Protection Agency Working Paper #05-02, 64
Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492
Moore AM (2012) The aquatic invaders: marine management figuring fishermen, fisheries, and lionfish in the Bahamas. Cult Anthropol 27:667–688
Morris JA (2012) Invasive lionfish: a guide to control and management, vol 1. Gulf and Caribbean Fisheries Institute Special Publication, Marathon
Morris JA, Whitfield PE (2009) Biology, ecology, control and management of the invasive Indo-Pacific lionfish: an updated integrated assessment. NOAA Technical Memorandum NOS NCCOS 99
Morris JA, Thomas A, Rhyne AL, Breen N, Akins L, Nash B (2011) Nutritional properties of the invasive lionfish: a delicious and nutritious approach for controlling the invasion. AACL Bioflux 4:21–26
Mumby PJ, Harborne AR, Brumbaugh DR (2011) Grouper as a natural biocontrol of invasive lionfish. PLoS ONE 6:e21510. doi:10.1371/journal.pone.0021510
Nair MSR, Cheung P, Leong I, Ruggieri GD (1985) Short communications: a non-proteinaceous toxin from the venomous spines of the lionfish Pterois volitans (Linnaeus). Toxicon 23:525–527
Patel MR, Wells S (1993) Lionfish envenomation of the hand. J Hand Surg [Am] 18:523–525
Pimental D, McNair S, Janecka J, Wightman J, Simmonds C, O’Connell C, Wong E, Russel L, Zern J, Aquino T, Tsomondo T (2001) Economic and environmental threats of alien plant, animal and microbe invasions. Agric Ecosyst Environ 84:1–20
Poh C, Yuen R, Khoo H, Chung M, Gwee M, Gopalakrishnakone P (1991) Purification and partial characterization of stonustoxin (lethal factor) from Synanceja horrida venom. Comp Biochem Physiol B 99:793–798
Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632
Saunders PR (1960) Pharmacological and chemical studies of the venom of the stonefish (genus Synanceja) and other scorpion fishes. Ann N Y Acad Sci 90:798–804
Saunders P, Taylor P (1959) Venom of the lionfish Pterois volitans. Am J Physiol 197:437
Semmens BX, Buhle ER, Salomon AK, Pattengill-Semmens CV (2004) A hotspot of non-native marine fishes: evidence for the aquarium trade as an invasion pathway. Mar Ecol Prog Ser 266:239–244
Shimojo RY, Iwaoka WT (2000) A rapid hemolysis assay for the detection of sodium channel-specific marine toxins. Toxicol 154:1–7
Shiomi K, Hosaka M, Fujita S, Yamanaka H, Kikuchi T (1989) Venoms from six species of marine fish: lethal and hemolytic activities and their neutralization by commercial stonefish antivenom. Mar Biol 103:285–289
Silk R (2012) FDA wavers on ciguatera warning. Florida Keys News. http://keysnews.com/node/40782. Accessed 30 June 2012
Sutherland WJ, Clout M, Côté IM, Daszak P, Depledge MH, Fellman L, Fleishman E, Garthwaite R, Gibbons DW, De Lurio J, Impey AJ, Lickorish F, Lindenmayer D, Madgwick J, Margerison C, Maynard T, Peck LS, Pretty J, Prior S, Redford KH, Scharlemann JPW, Spalding M, Watkinson AR (2010) A horizon scan of global conservation issues for 2010. Trends Ecol Evol 25:1–7
Ting JY, Brown AF (2001) Ciguatera poisoning: a global issue with common management problems. Eur J Emerg Med 8:295–300
Trestrail JH, Al-Mahasneh QM (1989) Lionfish sting experiences of an inland poison center: a retrospective study of 23 cases. Vet Hum Toxicol 31:173–175
Ueda A, Suzuki M, Honma T, Nagai H, Nagashima Y, Shiomi K (2006) Purification, properties and cDNA cloning of neoverrucotoxin (neoVTX), a hemolytic lethal factor from the stonefish Synanceia verrucosa venom. Biochim Biophys Acta 1760:1713–1722
Wilcove DS, Rothstein D, Dubow J, Phillips J, Losos E (1998) Quantifying threats to imperiled species in the United States. Biosci 48:607–615
Acknowledgments
We gratefully acknowledge the four anonymous reviewers for helpful comments that much improved the manuscript. CLW thanks Sigma Xi’s Grants-In-Aid of Research and Achievement Rewards for College Scientists Honolulu Chapter for their support. CLW also thanks K. Winkel and B. Fry for their contributions of SFAV, M. Gerschenson and D. Libutti for their advice and generous assistance in the laboratory, Discovery Diving in Beaufort, NC for their help in specimen collection, and Stumpy for his personal donations to this work. MAH thanks the National Science Foundation for supporting his lab’s research on the ecological effects of the lionfish invasion (08–51162 and 12–33027). This is contribution no. 1594 from the Hawai’i Institute of Marine Biology, no. 9174 from the School of Ocean and Earth Science and Technology, and no. 2014-13 from the Department of Biology at the University of Hawaii at Manoa. This study complied with current laws in the United States and was conducted in accordance with the regulations of the University of Hawai’i Institutional Animal Care and Use Committee (IACUC).
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Wilcox, C.L., Hixon, M.A. False positive tests for ciguatera may derail efforts to control invasive lionfish. Environ Biol Fish 98, 961–969 (2015). https://doi.org/10.1007/s10641-014-0313-0
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DOI: https://doi.org/10.1007/s10641-014-0313-0