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Pacific Ciguatoxins in Food Web Components of Coral Reef Systems

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Pacific Ciguatoxins in Food Web Components of Coral Reef Systems Article pubs.acs.org/est Pacific Ciguatoxins in Food Web Components of Coral Reef Systems in the Republic of Kiribati † § † § † ‡ † § † § Yim Ling Mak, , Tak-Cheung Wai, , Margaret B. Murphy, , Wing Hei Chan, , Jia Jun Wu, , † § † § † ‡ § James C. W. Lam, , Leo L. Chan,*, , and Paul K. S. Lam*, , , † ‡ State Key Laboratory in Marine Pollution and Department of Biology and Chemistry, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong Special Administrative Region, China § Research Centre for the Oceans and Human Health, City University of Hong Kong Shenzhen Research Institute, Shenzhen 518057, China *S Supporting Information ABSTRACT: Ciguatera fish poisoning (CFP) is a foodborne illness caused by consumption of coral reef fishes contaminated by ciguatoxins (CTXs); of the known CTX congeners, the Pacific ciguatoxins (P-CTXs) are the most toxic. Little is known about the trophodynamics of P-CTXs in coral reef systems. The present study explores the distribution, transfer, and trophic magnification of P-CTX-1, -2, and -3 in coral reef systems with high (ciguatoxic) and low (reference) ciguatoxicity in a CFP-endemic nation by use of liquid chromatography-tandem mass spectrometry (LC-MS/ MS). In ciguatoxic coral reef systems, P-CTXs were detected in 54% of herbivorous fishes [total P-CTXs <0.500−1670 pg/g wet weight (ww)], 72% of omnivorous fishes (<0.500−1810 pg/g ww), and 76% of carnivorous fishes (<0.500−69 500 pg/g ww), as well as a lobster (Panulirus penicillatus; 2.36 pg/g ww) and an octopus (Octopodidae; 2.56 pg/g ww). The dominant P-CTXs in grazers and piscivorous fishes were P-CTX-2 and -1, respectively. No significant correlation between P-CTX levels and lipid content in three target predatory fishes indicated that accumulation of P-CTXs does not depend on fat content. A weak but significant positive relationship was observed between δ15N and P-CTX-1 levels, but further investigation is required to confirm its biomagnification potential. ■ INTRODUCTION CFP-endemic regions, CTXs now represent a global threat to human health.2 Ciguatoxins (CTXs) are a group of natural marine biotoxins; 6 fi The food web hypothesis was proposed by Randall in 1958 more than 30 congeners or isomers have been identi ed in fi fl fi 1 to explain the sources of CTXs in shes. Epibenthic dino agellates and shes. They are highly oxygenated fl fi − dino agellates such as Gambierdiscus spp. have been identi ed lipophilic cyclic polyethers consisting of 13 14 rings fused as causative agents that produced gambiertoxins (such as P- into a rigid ladderlike structure. On the basis of geographic fi CTX-4A/4B) and a suite of CTX intermediate products (such origins and structural variants, ciguatoxins are classi ed as as P-CTX-2 and -3, also known as 52-epi-54-deoxy-CTX-1B fi 2 Paci c (P-CTXs), Caribbean (C-CTXs), or Indian (I-CTXs). and 54-deoxy-CTX-1B, respectively).7 These dinoflagellates not ff CTXs are of great concern, as exposure may a ect the survival only may be attached to macroalgae and turf algae but also may 3 of invertebrates and marine mammals such as endangered be found in association with sand, coral rubble, and 4 − Hawaiian monk seals (Monachus schauinslandi). In addition, seagrasses.8 10 Herbivorous fishes including surgeonfish and CTXs are present in coral reef fishes on the international parrotfish that graze on macroalgae or other substrates also market, and consumption of fishes containing more than 100 ingest the associated epiphytic dinoflagellates and their toxins, pg of P-CTX-1 equiv/g can cause ciguatera fish poisoning and these fishes are then in turn preyed upon by carnivorous (CFP) in humans.2 Worldwide public health institutions have fishes, which transform CTX precursors and intermediates to ranked CFP as one of the most common food-borne illnesses.1 relatively oxidized CTXs (such as P-CTX-1, also known as P- In the United States, CTXs were viewed as the second most CTX-1B). The lipophilic CTXs accumulate in fishes and then dangerous seafood-borne hazard and were estimated to account 5 for 21% of all seafood-related outbreaks from 1990 to 2006. Received: July 18, 2013 Annually, more than 50 000 people around the world are Revised: November 12, 2013 estimated to be adversely affected by CTXs.2 Because of the Accepted: November 14, 2013 expansion of the international trade of coral reef fishes into Published: November 14, 2013 © 2013 American Chemical Society 14070 dx.doi.org/10.1021/es403175d | Environ. Sci. Technol. 2013, 47, 14070−14079 Environmental Science & Technology Article Table 1. List of Fishes and Invertebrates Collected from Two Ciguatoxic Sites (T1 and T2) and a Reference Site (R) in Coral Reef System of Marakei in the Republic of Kiribati genus and species common name family type sampling site n Herbivorous Fishes Acanthurus glaucopareius whitecheek surgeonfish Acanthuridae surgeonfishes T1, T2 2 Acanthurus lineatus lined surgeonfish Acanthuridae surgeonfishes T1, T2 4 Acanthurus maculiceps white-freckled surgeonfish Acanthuridae surgeonfishes T1, R 3 Calotomus carolinus Carolines parrotfish Scaridae parrotfishes T1 1 Ctenochaetus marginatus striped-fin surgeonfish Scaridae parrotfishes R 1 Kyphosus cinerascens blue sea chub Kyphosidae sea chubs T1 1 Naso lituratus orange-spine unicornfish Acanthuridae surgeonfishes T1 1 Scarus ghobban blue-barred parrotfish Scaridae parrotfishes T1, R 5 Scarus globiceps Scaridae parrotfishes R 1 Scarus rubroviolaceus ember parrotfish Scaridae parrotfishes T2 1 Scarus russelii eclipse parrotfish Scaridae parrotfishes T2 1 Scarus schlegeli yellowband parrotfish Scaridae parrotfishes T1 1 Scarus tricolor three-color parrotfish Scaridae parrotfishes T1 1 Scarus forsteni Forsten’s parrotfish Scaridae parrotfishes T2 1 Siganus argenteus streamlined spinefoot Siganidae rabbitfishes T1, R 3 Omnivorous Fishes Acanthurus gahhm black surgeonfish Acanthuridae surgeonfishes T1 4 Acanthurus mata elongate surgeonfish Acanthuridae surgeonfishes T1 1 Acanthurus xanthopterus yellowfin surgeonfish Acanthuridae surgeonfishes T1 3 Aluterus scriptus scribbled leatherjacket filefish Monacanthidae filefishes T1 1 Arothron nigropunctatus black-spotted puffer Tetraodontidae pufferfishes T1 1 Balistapus undulatus orange-lined triggerfish Balistidae triggerfishes T2 1 Bolbometopon muricatum green humphead parrotfish Scaridae parrotfishes T1 1 Chaetodon ulietensis Pacific double-saddle butterflyfish Chaetodontidae butterflyfishes R 1 Chaetodon auriga threadfin butterflyfish Chaetodontidae butterflyfishes T1 1 Cheilopogon atrisignis glider flyingfish Exocoetidae flyingfishes T1, R 3 Ctenochaetus striatus striated surgeonfish Acanthuridae surgeonfishes T1, R 4 Hipposcarus longiceps Pacific longnose parrotfish Scaridae parrotfishes T1 1 Melichthys niger black triggerfish Balistidae triggerfishes R 1 Myripristis murdjan pinecone soldierfish Holocentridae soldierfishes R 1 Carnivorous Fishes Caesio lunaris lunar fusilier Caesionidae fusiliers R 1 Caesio xanthonotus yellow-back fusilier Caesionidae fusiliers R 1 Cantherhines paradalis honeycomb filefish Monacanthidae filefishes R 1 Cephalopholis argus blue-spotted grouper Serranidae groupers T1, T2, R 24 Cephalopholis urodeta darkfin hind Serranidae groupers T1, R 3 Cephalopholis sexmaculata sixblotch hind Serranidae groupers T2 1 Chaetodon lunula raccoon butterflyfish Chaetodontidae butterflyfishes T1 1 Chaetodon meyeri scrawled butterflyfish Chaetodontidae butterflyfishes T1, R 7 Chaetodon reticulatus mailed butterflyfish Chaetodontidae butterflyfishes T2, R 2 Cheilopogon antoncich Exocoetidae flyingfishes T1 10 Coris aygula clown coris Labridae wrasses T1 1 Diodon hystrix spot-fin porcupinefish Diodontidae ballonfishes T2 1 Diodon liturosus black-blotched porcupinefish Diodontidae ballonfishes T1 1 Epibulus insidiator slingjaw wrasse Labridae wrasses T1 1 Epinephelus coeruleopunctatus white-spotted grouper Serranidae groupers T1 1 Epinephelus fuscoguattus brown-marbled grouper Serranidae groupers T1 2 Epinephelus merra honeycomb grouper Serranidae groupers T1 2 Epinephelus multinotatus white-blotched grouper Serranidae groupers T1 1 Epinephelus polyphekadion camouflage grouper Serranidae groupers T1 3 Epinephelus spilotoceps foursaddle grouper Serranidae groupers T1 4 Epinephelus tauvina greasy grouper Serranidae groupers T1 3 Forcipiger longirostris longnose butterflyfish Chaetodontidae butterflyfishes T1, T2 2 Gomphosus varius bird wrasse Labridae wrasses T1 1 Gracila albomarginata masked grouper Serranidae groupers T1 1 Gymnothorax flavimarginatus yellow-edged moray Muraenidae moray eels T1, T2, R 26 Gymnothorax javanicus giant moray Muraenidae moray eels T1, T2, R 22 Halichoeres hortulanus checkerboard wrasse Labridae wrasses T1 1 Lutjanus bohar blacktail snapper Lutjanidae snappers T1 3 14071 dx.doi.org/10.1021/es403175d | Environ. Sci. Technol. 2013, 47, 14070−14079 Environmental Science & Technology Article Table 1. continued genus and species common name family type sampling site n Carnivorous Fishes Lutjanus fulvus blacktail snapper Lutjanidae snappers T1 1 Macolor niger black and white snapper Lutjanidae snappers T1 1 Monotaxis grandoculis humpnose big-eye bream Lethrinidae emperors T1, R 4 Myripristis berndti blotcheye soldierfish Holocentridae soldierfishes T1 1 Paracirrhites hemistictus whitespot hawkfish Cirrhitidae hawkfishes T2, R 3 Pomacanthus imperator emperor angelfish Pomacanthidae angelfishes T2, R 2 Parupeneus bifasciatus doublebar goatfish Mullidae goatfishes T1 1 Pygoplites diacanthus royal angelfish Pomacanthidae angelfishes T1, R 4 Sargocentron tiere
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