Abstract
Fishes represent the most diverse group of vertebrates, having inhabited the Earth for approximately 480 million years during which they evolved many specialised adaptations. One such adaptation is the evolution of a venom system, which has convergently arisen on at least 19 separate occasions across their evolutionary history. Venom evolution across fishes has taken two forms: chemical weaponisation of previously evolved defensive spines and the development of an oral venom system. Fish venoms have been shown to contain a myriad of toxin types, some of which may have pharmacological potential. However, due to the labile nature of many toxins, fish venom has not been extensively investigated compared to other venomous groups such as reptiles and arachnids. This review provides an updated scope of our current knowledge regarding the biology, biochemistry, and evolution of fish venom systems. It also attempts to provide a coherent assessment of the dated literature while seeking to address particular issues in order to drive fish venom research further.
Similar content being viewed by others
References
Abe T, Sumatora M, Hashimoto Y, Yoshihara J, Shimamura Y, Fukami J (1996) Purification and properties of a cardioactive toxin, cardioleputin, from stonefish, Synanceja verrucosa. J Venom Anim Toxins 2(2):135–149
Amesbury E, Snelson FF (1997) Spine replacement in a freshwater population of the Atlantic stingray. Dasyatis Sabina Copeia 1997(1):220–223
Amorim FG, Costa TR, Baiwir D, De Pauw E, Quinton L, Sampaio SV (2018) Proteopeptidomic, functional and immunoreactivity characterization of Bothrops moojeni snake venom: influence of snake gender on venom composition. Toxins 10(5):177
Andersen HH, Elberling J, Arendt-Nielsen L (2015) Human surrogate models of histaminergic and non-histaminergic itch. Acta Derm Venereol 95(7):771–779
Andrich F, Carnielli JBT, Cassoli JS, Lautner RQ, Santos RAS, Pimenta AMC, De Lima ME, Figueiredo SG (2010) A potent vasoactive cytolysin isolated from Scorpaena plumieri scorpionfish venom. Toxicon 56(4):487–496
Andrich F, Richardson M, Naumann G, Cordeiro M, Santos A, Santos D, Oliveira J, de Lima M, Figueiredo S (2015) Identification of C-type isolectins in the venom of the scorpionfish Scorpaena plumieri. Toxicon 95:67–71
Anitescu M (2018) Ischemic pain. In: Cheng J, Rosenquist R (eds) Fundamentals of pain medicine. Springer, Berlin, pp 141–151
Antoniazzi MM, Benvenuti LA, Lira MS, Jared SG, Neto DG, Jared C, Barbaro KC (2011) Histopathological changes induced by extracts from the tissue covering the stingers of Potamotrygon falkneri freshwater stingrays. Toxicon 57(2):297–303
Araújo MML (2019). Evolution of northeast atlantic and mediterranean scorpionfish Scorpaena and their venom protein profiles. ISPA–Instituto Universitário
Arbuckle K (2017) Evolutionary context of venom in animals. In: Gopalakrishnakone P, Malhotra A (eds) Evolution of venomous animals and their toxins. Toxinology, vol 24. Springer, Dordrecht, pp 3–31
Arbuckle K, Harris RJ (2021) Radiating pain: venom has contributed to the diversification of the largest radiations of vertebrate and invertebrate animals. BMC Ecol Evol 21(1):1–12
Atkinson P, Boyle A, Hartin D, McAuley D (2006) Is hot water immersion an effective treatment for marine envenomation? Emerg Med J 23(7):503–508
Auddy B, Muhuri DC, Alam MI, Gomes A (1995) A lethal protein toxin (toxin-PC) from the Indian catfish (Plotosus canius, Hamilton) venom. Nat Toxins 3(5):363–368
Austin L, Gillis R, Youatt G (1965) Stonefish venom: some biochemical and chemical observations. Aust J Exp Biol Med Sci 43(1):79–90
Balasubashini MS, Karthigayan S, Somasundaram S, Balasubramanian T, Viswanathan V, Raveendran P, Menon VP (2006) Fish venom (Pterios volitans) peptide reduces tumor burden and ameliorates oxidative stress in Ehrlich’s ascites carcinoma xenografted mice. Bioorg Med Chem Lett 16(24):6219–6225
Barbaro KC, Lira MS, Malta MB, Soares SL, Neto DG, Cardoso JL, Santoro ML, Junior VH (2007) Comparative study on extracts from the tissue covering the stingers of freshwater (Potamotrygon falkneri) and marine (Dasyatis guttata) stingrays. Toxicon 50(5):676–687
Barber CM, Isbister GK, Hodgson WC (2013) Alpha neurotoxins. Toxicon 66:47–58
Barnett S, Saggiomo S, Smout M, Seymour J (2017) Heat deactivation of the stonefish Synanceia horrida venom-implications for first-aid management. Diving Hyperb Med 47(3):155
Barre A, Bourne Y, Van Damme EJ, Peumans WJ, Rougé P (2001) Mannose-binding plant lectins: different structural scaffolds for a common sugar-recognition process. Biochimie 83(7):645–651
Baxter E (1956) Observations on the buccal glands of lampreys (Petromyzonidae). In: Proceedings of the zoological society of London, 127, p 95–118. Wiley Online Library
Becerra-Amezcua MP, Hernández-Sámano AC, Puch-Hau C, Aguilar MB, Collí-Dulá RC (2020) Effect of Pterois volitans (lionfish) venom on cholinergic and dopaminergic systems. Environ Toxicol Pharmacol 77:103359
Bigelow H, Schroeder W (1953) Fishes of the Western North Atlantic: sawfishes, guitarfishes, skates and rays. Mem Sears Found Mar Res 1:1–514
Borges MH, Andrich F, Lemos PH, Soares TG, Menezes TN, Campos FV, Neves LX, Castro-Borges W, Figueiredo SG (2018) Combined proteomic and functional analysis reveals rich sources of protein diversity in skin mucus and venom from the Scorpaena plumieri fish. J Proteomics 187:200–211
Borondo J, Sanz P, Nogué S, Poncela J, Garrido P, Valverde J (2001) Fatal weeverfish sting. Hum Exp Toxicol 20(2):118–119
Bottard A (1889) Les poissons venimeux, contribution à l'hygiene navale. Impr. du Journal Le Havre
Branco ACCC, Yoshikawa FSY, Pietrobon AJ, Sato MN (2018) Role of histamine in modulating the immune response and inflammation. Mediat Inflamm. https://doi.org/10.1155/2018/9524075
Briars G, Gordon G (1992) Envenomation by the lesser weever fish. Br J Gen Pract 42(358):213
Buchheim JR, Hixon MA (1992) Competition for shelter holes in the coral-reef fish Acanthemblemaria spinosa Metzelaar. J Exp Mar Biol Ecol 164(1):45–54
Cambi A, Figdor C (2009) Necrosis: C-type lectins sense cell death. Curr Biol 19(9):R375–R378
Cameron AM (1976) Toxicity of coral reef fishes. Biol Geol Coral Reefs 3:155–176
Cameron AM, Endean R (1966) The venom apparatus of the scorpion fish Notesthes robusta. Toxicon 4(2):111–114
Cameron AM, Endean R (1970) Venom glands in scatophagid fish. Toxicon 8(2):171–174
Cameron AM, Endean R (1973) Epidermal secretions and the evolution of venom glands in fishes. Toxicon 11(5):401–410
Campos FV, Fiorotti HB, Coitinho JB, Figueiredo SG (2021) Fish cytolysins in all their complexity. Toxins 13(12):877
Campos FV, Menezes TN, Malacarne PF, Costa FL, Naumann GB, Gomes HL, Figueiredo SG (2017) A review on the Scorpaena plumieri fish venom and its bioactive compounds. J Venom Anim Toxins Incl Trop Dis 22
Cappa G, Barcella B, Pettenazza P (2020) Extraction procedure of a stingray spine. J Travel Med 27(6):137
Carlisle D (1962) On the venom of the lesser weeverfish, Trachinus vipera. J Mar Biol Assoc UK 42(2):155–162
Carvalho TI, Klaczko J, Slobodian V (2021) Pectoral-fin glands and delivery apparatus in the catfish genus Brachyrhamdia Myers, 1927 (Siluriformes: Heptapteridae). Papéis Avulsos de Zoologia 61
Casewell NR, Wüster W, Vonk FJ, Harrison RA, Fry BG (2013) Complex cocktails: the evolutionary novelty of venoms. Trends Ecol Evol 28(4):219–229
Casewell NR, Visser JC, Baumann K, Dobson J, Han H, Kuruppu S, Morgan M, Romilio A, Weisbecker V, Mardon K (2017) The evolution of fangs, venom, and mimicry systems in blenny fishes. Curr Biol 27(8):1184–1191
Casewell NR, Jackson TN, Laustsen AH, Sunagar K (2020) Causes and consequences of snake venom variation. Trends Pharmacol Sci 41(8):570–581
Chakrabarty D, Bhattacharyya D, Sarkar HS, Lahiri SC (1993) Purification and partial characterization of a haemorrhagin (VRH-1) from Vipera russelli russelli venom. Toxicon 31(12):1601–1614
Chen L-L, Xie J, Cao D-D, Jia N, Li Y-J, Sun H, Li W-F, Hu B, Chen Y, Zhou C-Z (2018) The pore-forming protein Aep1 is an innate immune molecule that prevents zebrafish from bacterial infection. Dev Comp Immunol 82:49–54
Chhatwal I, Dreyer F (1992a) Biological properties of a crude venom extract from the greater weever fish Trachinus draco. Toxicon 30(1):77–85
Chhatwal I, Dreyer F (1992b) Isolation and characterization of dracotoxin from the venom of the greater weever fish Trachinus draco. Toxicon 30(1):87–93
Chi S, Xiao R, Li Q, Zhou L, He R, Qi Z (2009) Suppression of neuronal excitability by the secretion of the lamprey (Lampetra japonica) provides a mechanism for its evolutionary stability. Pflügers Archiv-Eur J Physiol 458(3):537–545
Chippaux J-P, Williams V, White J (1991) Snake venom variability: methods of study, results and interpretation. Toxicon 29(11):1279–1303
Chuang P-S, Shiao J-C (2014) Toxin gene determination and evolution in scorpaenoid fish. Toxicon 88:21–33
Church JE, Hodgson WC (2001) Stonefish (Synanceia spp.) antivenom neutralises the in vitro and in vivo cardiovascular activity of soldierfish (Gymnapistes marmoratus) venom. Toxicon 39(2–3):319–324
Church JE, Hodgson WC (2002) The pharmacological activity of fish venoms. Toxicon 40(8):1083–1093
Church JE, Hodgson WC (2003) Stonefish (Synanceia trachynis) antivenom: in vitro efficacy and clinical use. J Toxicol: Toxin Rev 22(1):69–76
Cipriani V, Debono J, Goldenberg J, Jackson TN, Arbuckle K, Dobson J, Koludarov I, Li B, Hay C, Dunstan N (2017) Correlation between ontogenetic dietary shifts and venom variation in Australian brown snakes (Pseudonaja). Comp Biochem Physiol c: Toxicol Pharmacol 197:53–60
Clark RF, Girard RH, Rao D, Ly BT, Davis DP (2007) Stingray envenomation: a retrospective review of clinical presentation and treatment in 119 cases. J Emerg Med 33(1):33–37
Cohen AS, Olek AJ (1989) An extract of lionfish (Pterois volitans) spine tissue contains acetylcholine and a toxin that affects neuromuscular transmission. Toxicon 27(12):1367–1376
Colasante C, Meunier FA, Kreger AS, Molgó J (1996) Selective depletion of clear synaptic vesicles and enhanced quantal transmitter release at frog motor nerve endings produced by trachynilysin, a protein toxin isolated from stonefish (Synanceia trachynis) venom. Eur J Neurosci 8(10):2149–2156
Conceição K, Konno K, Melo RL, Marques EE, Hiruma-Lima CA, Lima C, Richardson M, Pimenta DC, Lopes-Ferreira M (2006) Orpotrin: a novel vasoconstrictor peptide from the venom of the Brazilian stingray Potamotrygon gr. orbignyi. Peptides 27(12):3039–3046
Conceição K, Santos JM, Bruni FM, Klitzke CF, Marques EE, Borges MH, Melo RL, Fernandez JH, Lopes-Ferreira M (2009) Characterization of a new bioactive peptide from Potamotrygon gr. orbignyi freshwater stingray venom. Peptides 30(12):2191–2199
Conway KW, Baldwin C, White MD (2014) Cryptic diversity and venom glands in western Atlantic clingfishes of the genus Acyrtus (Teleostei: Gobiesocidae). PLoS ONE 9(5):e97664
Cook R, Potter I, Hilliard R (1990) Morphology and innervation of the buccal glands of the southern hemisphere lamprey, Geotria australis. J Morphol 206(1):133–145
Couture R, Harrisson M, Vianna RM, Cloutier F (2001) Kinin receptors in pain and inflammation. Eur J Pharmacol 429(1–3):161–176
Davies R, Evans R (1996) Weever fish stings: a report of two cases presenting to an accident and emergency department. J Accid Emerg Med 13(2):139
Davis J, Jones A, Lewis RJ (2009) Remarkable inter-and intra-species complexity of conotoxins revealed by LC/MS. Peptides 30(7):1222–1227
de Oliveira Júnior NG, da Rocha Fernandes G, Cardoso MH, Costa FF, de Souza Cândido E, Neto DG, Mortari MR, Schwartz EF, Franco OL, De Alencar SA (2016) Venom gland transcriptome analyses of two freshwater stingrays (Myliobatiformes: Potamotrygonidae) from Brazil. Sci Rep 6(1):1–14
de Santana Evangelista K, Andrich F, de Rezende FF, Niland S, Cordeiro MN, Horlacher T, Castelli R, Schmidt-Hederich A, Seeberger PH, Sanchez EF (2009) Plumieribetin, a fish lectin homologous to mannose-binding B-type lectins, inhibits the collagen-binding α1β1 integrin. J Biol Chem 284(50):34747–34759
Deakins DE, Saunders PR (1967) Purification of the lethal fraction of the venom of the stonefish Synanceja horrida (Linnaeus). Toxicon 4(4):257–262
Domingos MO, Franzolin MR, dos Anjos MT, Franzolin TM, Albes RCB, de Andrade GR, Lopes RJ, Barbaro KC (2011) The influence of environmental bacteria in freshwater stingray wound-healing. Toxicon 58(2):147–153
Donoghue PC, Forey PL, Aldridge RJ (2000) Conodont affinity and chordate phylogeny. Biol Rev 75(2):191–251
Drickamer K (1993) Evolution of Ca2+-dependent animal lectins. Prog Nucleic Acid Res Mol Biol 45:207–232
Drickamer K (1999) C-type lectin-like domains. Curr Opin Struct Biol 9(5):585–590
Eliahu K, Zlotkin, E (2009) Pathogens, parasites and predators. In: Zaccone G, Perrière C, Mathis A, kapoor BG (eds) Fish defenses, vol. 2. CRC Press, Boca raton
Ellisdon AM, Reboul CF, Panjikar S, Huynh K, Oellig CA, Winter KL, Dunstone MA, Hodgson WC, Seymour J, Dearden PK (2015) Stonefish toxin defines an ancient branch of the perforin-like superfamily. Proc Natl Acad Sci 112(50):15360–15365
Endean R (1961) A study of distribution, habitat, behaviour, venom apparatus, and venom of the stone-fish. Mar Freshw Res 12(2):177–190
Eschmeyer WN, Fricke R, Van der Laan R (2021) Catalog of fishes: genera, species, references
Fenner P (2000) Marine envenomation: an update—a presentation on the current status of marine envenomation first aid and medical treatments. Emerg Med 12(4):295–302
Fenner PJ, Williamson JA, Skinner RA (1989) Fatal and non-fatal stingray envenomation. Med J Aust 151(11–12):621–625
Flach J, Pilet P-E, Jolles P (1992) What’s new in chitinase research? Experientia 48(8):701–716
Fry B (2015) Venomous reptiles and their toxins: evolution, pathophysiology and biodiscovery. Oxford University Press, Oxford
Fry BG, Wüster W, Kini RM, Brusic V, Khan A, Venkataraman D, Rooney A (2003) Molecular evolution and phylogeny of elapid snake venom three-finger toxins. J Mol Evol 57(1):110–129
Fry BG, Roelants K, Champagne DE, Scheib H, Tyndall JD, King GF, Nevalainen TJ, Norman JA, Lewis RJ, Norton RS (2009) The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet 10:483–511
Fry B, Sunagar K, Casewell N, Kochva E, Roelants K, Scheib H, Wüster W, Vidal N, Young B, Burbrink F (2015) The origin and evolution of the Toxicofera reptile venom system. In: Venomous reptiles and their Toxins: evolution, pathophysiology and biodiscovery. (ed B. Fry), p 1–31
Gage SH, Gage-Day M (1927) The anti-coagulating action of the secretion of the buccal glands of the lampreys (Petromyzon, Lampetra and Entosphenus). Science 66(1708):282–284
Gage S, Gage-Day M (1928) Development and structure of the buccal glands of lampreys; anticoagulating action on blood of the gland secretion. Anat Rec 38:11–12
Galloway KA, Porter ME (2019) Mechanical properties of the venomous spines of Pterois volitans and morphology among lionfish species. J Exp Biol 222(6):jeb197905
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(2):143–155
Garnier P, Grosclaude J-M, 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 Sci Appl 685(2):364–369
Garnier P, Ducancel F, Ogawa T, Boulain J-C, Goudey-Perrière F, Perrière C, Ménez A (1997a) Complete amino-acid sequence of the β-subunit of VTX from venom of the stonefish (Synanceia verrucosa) as identified from cDNA cloning experiments. Biochim Biophys Acta (BBA)-Protein Struct Mol Enzymol 1337(1):1–5
Garnier P, Sauviat M-P, Goudey-Perriere F, Perriere C (1997b) Cardiotoxicity of verrucotoxin, a protein isolated from the venom of Synanceia verrucosa. Toxicon 35(1):47–55
Ghadessy FJ, Chen D, Kini RM, Chung MM, Jeyaseelan K, Khoo HE, Yuen R (1996) Stonustoxin is a novel lethal factor from stonefish (Synanceja horrida) venom: cDNA cloning and characterization. J Biol Chem 271(41):25575–25581
Ghanem H, Khan MT, Al-Ghanem S, Al-Qasem G (2019) Stonefish (Synanceiea verrucosa) envenomation in the Kingdom of Bahrain. J Bahrain Med Soc 31:5–9
Gibbs SP (1956) The anatomy and development of the buccal glands of the lake lamprey (Petromyzon marinus Linnaeus) and the histochemistry of their secretion. J Morphol 98(3):429–469
Glasauer SM, Neuhauss SC (2014) Whole-genome duplication in teleost fishes and its evolutionary consequences. Mol Genet Genom 289(6):1045–1060
Gomes HL, Menezes TN, Carnielli JB, Andrich F, Evangelista KS, Chávez-Olórtegui C, Vassallo DV, Figueiredo SG (2011) Stonefish antivenom neutralises the inflammatory and cardiovascular effects induced by scorpionfish Scorpaena plumieri venom. Toxicon 57(7–8):992–999
Gopalakrishnakone P, Gwee M (1993) The structure of the venom gland of stonefish Synanceja horrida. Toxicon 31(8):979–988
Gratzer B, Millesi E, Walzl M, Herler J (2015) Skin toxins in coral-associated Gobiodon species (Teleostei: Gobiidae) affect predator preference and prey survival. Mar Ecol 36(1):67–76
Gross MR, Sargent RC (1985) The evolution of male and female parental care in fishes. Am Zool 25(3):807–822
Gulen M, Sari S (2020) Envenomation by Trachinus draco and pain management. Wilderness Environ Med 31(3):332–336
Haavaldsen R, Fonnum F (1963) Weever venom. Nature 199(4890):286–287
Haddad V Jr, Pardal PPO, Cardoso JLC, Martins IA (2003) The venomous toadfish Thalassophryne nattereri (niquim or miquim): report of 43 injuries provoked in fishermen of Salinópolis (Pará State) and Aracaju (Sergipe State), Brazil. Rev Inst Med Trop Sao Paulo 45:221–223
Haddad V Jr, Neto DG, de Paula Neto JB, de Luna Marques FP, Barbaro KC (2004) Freshwater stingrays: study of epidemiologic, clinic and therapeutic aspects based on 84 envenomings in humans and some enzymatic activities of the venom. Toxicon 43(3):287–294
Haddad V Jr, De Souza RA, Auerbach PS (2008) Marine catfish sting causing fatal heart perforation in a fisherman. Wilderness Environ Med 19(2):114–118
Halstead BW, Chitwood MJ, Modglin FR (1956) Stonefish stings, and the venom apparatus of Synanceja horrida (Linnaeus). Trans Amer Microscop Soc 75(4):381–397
Hahn S, O’connor J (2000) An investigation of the biological activity of bullrout (Notesthes robusta) venom. Toxicon 38(1):79–89
Halstead BW (1959) Dangerous marine animals. Cornell Maritime Press, Cambridge
Halstead BW, Dalgleish AE (1967) The venom apparatus of the European star-gazer Uranoscopus scaber linnaeus. In: Russel FE, Saunders PR (eds) Animal toxins: a collection of papers presented at the first international symoposium of animal toxins. Pergamon Press, Oxford
Halstead BW, Chitwood MJ, Modglin FR (1955a) The anatomy of the venom apparatus of the zebrafish, Pterois volitans (Linnaeus). Anat Rec 122(3):317–333
Halstead BW, Chitwood MJ, Modglin FR (1955b) The venom apparatus of the California scorpionfish, Scorpaena guttata Girard. Trans Am Microsc Soc 74(2):145–158
Halstead BW, Ocampo RR, Modglin FR (1955c) A study on the comparative anatomy of the venom apparatus of certain North American stingrays. J Morphol 97(1):1–21
Halstead B (1971) Venomous fish. In: Venomous animals and their venom II, p 588–626. Academic Press, Washington
Halstead BW (1988). Poisonous and venomous marine animals of the world
Harris RJ, Arbuckle K (2016) Tempo and mode of the evolution of venom and poison in tetrapods. Toxins 8(7):193
Harris RJ, Jenner RA (2019) Evolutionary ecology of fish venom: adaptations and consequences of evolving a venom system. Toxins 11(2):60
Harris RJ, Youngman NJ, Chan W, Bosmans F, Cheney KL, Fry BG (2021) Getting stoned: characterisation of the coagulotoxic and neurotoxic effects of reef stonefish (Synanceia verrucosa) venom. Toxicol Lett 346:16–22
Hawkins BS (2006) Toxicological review of cyanobacterial toxins: anatoxin-A (ed. U. S. E. P. Agency), p 1–29. United States Environmental Protection Agency, Washington, DC, USA
Helfman G, Collette BB, Facey DE, Bowen BW (2009) The diversity of fishes: biology, evolution, and ecology. Wiley, Hoboken
Herzig V, Ward RJ, dos Santos WF (2002) Intersexual variations in the venom of the Brazilian ‘armed’ spider Phoneutria nigriventer (Keyserling, 1891). Toxicon 40(10):1399–1406
Hoffman SG, Robertson DR (1983) Foraging and reproduction of two Caribbean reef toadfishes (Batrachoididae). Bull Mar Sci 33(4):919–927
Hopkins BJ, Hodgson WC, Sutherland SK (1997) An in vitro pharmacological examination of venom from the soldierfish Gymnapistes marmoratus. Toxicon 35(7):1101–1111
Hughes R, Pedersen K, Huskey S (2018) The kinematics of envenomation by the yellow stingray. Urobatis Jamaicensis Zoomorphology 137(3):409–418
Iannicelli M (2017) Solving the mystery of endless life between conodonts and lampreys, plus a reason for final extinction of the conodonts. J Oceanogr Mar Res 1:2
Isbister GK (2001) Venomous fish stings in tropical northern Australia. Am J Emerg Med 19(7):561–565
Ito N, Mita M, Takahashi Y, Matsushima A, Watanabe YG, Hirano S, Odani S (2007) Novel cysteine-rich secretory protein in the buccal gland secretion of the parasitic lamprey, Lethenteron japonicum. Biochem Biophys Res Commun 358(1):35–40
IUCN (2022) Summary statistics
Jia N, Liu N, Cheng W, Jiang YL, Sun H, Chen LL, Peng J, Zhang Y, Ding YH, Zhang ZH (2016) Structural basis for receptor recognition and pore formation of a zebrafish aerolysin-like protein. EMBO Rep 17(2):235–248
Jonnakuty C, Gragnoli C (2008) What do we know about serotonin? J Cell Physiol 217(2):301–306
Jung H (2020) Hyaluronidase: an overview of its properties, applications, and side effects. Arch Plast Surg 47(4):297
Kakigi R, Watanabe S (1996) Pain relief by various kinds of interference stimulation applied to the peripheral skin in humans: pain-related brain potentials following CO2 laser stimulation. J Peripher Nerv Syst 1(3):189–198
Karmakar S, Muhuri D, Dasgupta S, Nagchaudhuri A, Gomes A (2004) Isolation of a haemorrhagic protein toxin (SA-HT) from the Indian venomous butterfish (Scatophagus argus, Linn) sting extract. Indian J Exp Biol 42(5):452–460
Kato K, Nakagawa H, Shinohara M, Ohura K (2016) Purification of a novel lectin from the dorsal spines of the stonefish, Synanceia verrucosa. J Osaka Dent Univ 50(2):55–61
Khoo HE (2002) Bioactive proteins from stonefish venom. Clin Exp Pharmacol Physiol 29(9):802–806
Khoo H, Yuen R, Poh C, Tan C (1992) Biological activities of Synanceja horrida (stonefish) venom. Nat Toxins 1(1):54–60
Khoo HE, Chen D, Yuen R (1998) The role of cationic amino acid residues in the lethal activity of stonustoxin from stonefish (Synanceja horrida) venom. IUBMB Life 44(3):643–646
Kiehl E, Rieger C, Greven H (2006) Axillary gland secretions contribute to the stress-induced discharge of a bactericidal substance in Corydoras sterbai (Callichthyidae, Siluriformes). Verhandlungen Der Gesellschaft Für Ichthyologie 5:111–115
Kimura LF, Prezotto-Neto JP, Távora BC, Faquim-Mauro EL, Pereira NA, Antoniazzi MM, Jared SG, Teixeira CF, Santoro ML, Barbaro KC (2015) Mast cells and histamine play an important role in edema and leukocyte recruitment induced by Potamotrygon motoro stingray venom in mice. Toxicon 103:65–73
Kimura LF, Santos-Neto M, Barbaro KC, Picolo G (2018) Potamotrygon motoro stingray venom induces both neurogenic and inflammatory pain behavior in rodents. Toxicon 150:168–174
King GF, Gentz MC, Escoubas P, Nicholson GM (2008) A rational nomenclature for naming peptide toxins from spiders and other venomous animals. Toxicon 52(2):264–276
Kini RM (2004) Platelet aggregation and exogenous factors from animal sources. Curr Drug Targets-Cardiovasc Hematol Disord 4(4):301–325
Kini RM, Chow G (2001) Exogenous inhibitors of platelet aggregation from animal sources. Thromb Haemost 85(01):179–181
Kirchhoff KN, Klingelhöfer I, Dahse H-M, Morlock G, Wilke T (2014) Maturity-related changes in venom toxicity of the freshwater stingray Potamotrygon leopoldi. Toxicon 92:97–101
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(6–7):494–501
Kiriake A, Suzuki Y, Nagashima Y, Shiomi K (2013) Proteinaceous toxins from three species of scorpaeniform fish (lionfish Pterois lunulata, devil stinger Inimicus japonicus and waspfish Hypodytes rubripinnis): close similarity in properties and primary structures to stonefish toxins. Toxicon 70:184–193
Kiriake A, Madokoro M, Shiomi K (2014) Enzymatic properties and primary structures of hyaluronidases from two species of lionfish (Pterois antennata and Pterois volitans). Fish Physiol Biochem 40(4):1043–1053
Kiriake A, Ishizaki S, Nagashima Y, Shiomi K (2017) Occurrence of a stonefish toxin-like toxin in the venom of the rabbitfish Siganus fuscescens. Toxicon 140:139–146
Kochva E (1987) The origin of snakes and evolution of the venom apparatus. Toxicon 25(1):65–106
Komegae EN, Ramos AD, Oliveira AK, de Toledo Serrano SM, Lopes-Ferreira M, Lima C (2011) Insights into the local pathogenesis induced by fish toxins: Role of natterins and nattectin in the disruption of cell–cell and cell–extracellular matrix interactions and modulation of cell migration. Toxicon 58(6–7):509–517
Komegae EN, Souza TAM, Grund LZ, Lima C, Lopes-Ferreira M (2017) Multiple functional therapeutic effects of TnP: a small stable synthetic peptide derived from fish venom in a mouse model of multiple sclerosis. PLoS ONE 12(2):e0171796
Koppel VH (1988) Habitat selection and space partitioning among two Mediterranean blenniid species. Mar Ecol 9(4):329–346
Kumar MNR (2000) A review of chitin and chitosan applications. React Funct Polym 46(1):1–27
Kumar KR, Vennila R, Kanchana S, Arumugam M, Balasubramaniam T (2011) Fibrinogenolytic and anticoagulant activities in the tissue covering the stingers of marine stingrays Dasyatis sephen and Aetobatis narinari. J Thromb Thrombolysis 31(4):464–471
Kumar S, Stecher G, Suleski M, Hedges SB (2017) TimeTree: a resource for timelines, timetrees, and divergence times. Mol Biol Evol 34(7):1812–1819
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547
Kumari S, Rath PK (2014) Extraction and characterization of chitin and chitosan from (Labeo rohit) fish scales. Proc Mater Sci 6:482–489
Lameiras JLV, da Costa OTF, Moroni FT, de Ribamar Araújo J, Caranhas SME, Marques CMA, Dos-Santos MC, Duncan WLP (2014) Systemic rhabdomyolysis induced by venom of freshwater stingrays Plesiotrygon iwamae and Potamotrygon motoro (Chondrichthyes–Potamotrygonidae) from the Amazon Basin. Toxicon 77:105–113
Lameiras JLV, Moura VMD, Dias LC, Santos IGCD, Costa OTFD, Dos-Santos MC (2019) Cross-reactivity between Potamotrygon motoro antivenoms and dorsal and stinger extracts of others stingrays (Chondrichthyes: Potamotrygonidae) from the Amazon basin. Toxin Rev 38(1):61–70
Le Bars D, Dickenson AH, Besson J-M (1979a) Diffuse noxious inhibitory controls (DNIC). I. Effects on dorsal horn convergent neurones in the rat. Pain 6(3):283–304
Le Bars D, Dickenson AH, Besson J-M (1979b) Diffuse noxious inhibitory controls (DNIC). II. Lack of effect on non-convergent neurones, supraspinal involvement and theoretical implications. Pain 6(3):305–327
Lecointre G, Le Guyader H (2006) The tree of life: a phylogenetic classification. Harvard University Press, Cambridge
Lee J, Teoh L, Leo S (2004) Stonefish envenomations of the hand-a local marine hazard: a series of 8 cases and review of the literature. Ann-Acad Med 33(4):515–520
Lehmann DF, Hardy JC (1993) Stonefish envenomation. N Engl J Med 329(7):510–511
Lennon RE (1954) Feeding mechanism of the sea lamprey and its effect on host fishes. Fish Bull US Fish Wildl Serv 56(98):247–293
Lennox-Bulow D, Smout M, Wilson D, Seymour J (2022) Inter-species variation in stonefish (Synanceia Spp.) ichthyocrinotoxins; an ecological perspective. Toxicon 221:106977
Leprêtre M, Almunia C, Armengaud J, Le Guernic A, Salvador A, Geffard A, Palos-Ladeiro M (2020) Identification of immune-related proteins of Dreissena polymorpha hemocytes and plasma involved in host-microbe interactions by differential proteomics. Sci Rep 10(1):1–18
Lima C, Disner GR, Falcão MAP, Seni-Silva AC, Maleski ALA, Souza MM, Reis Tonello MC, Lopes-Ferreira M (2021) The natterin proteins diversity: a review on phylogeny, structure, and immune function. Toxins 13(8):538
Lima C, Falcão MAP, Pinto FJ, Bernardo JTG, Lopes-Ferreira M (2023) The anti-inflammatory peptide TnP is a candidate molecule for asthma treatment. Cells 12(6):924
Lin K-T, Wang W-X, Ruan H-T, Dai J-G, Sun J-J, Liu L, Huang X-D (2019) Transcriptome analysis of differentially expressed genes in the fore-and hind-intestine of ovate pompano Trachinotus ovatus. Aquaculture 508:76–82
Ling SK, Cheng S, Yen C (2009) Stonefish envenomation with acute carpal tunnel syndrome. Hong Kong Med J 15(6):471–473
Liu X, Li-Ling J, Hou L, Li Q, Ma F (2009) Identification and characterization of a chitinase-coding gene from Lamprey (Lampetra japonica) with a role in gonadal development and innate immunity. Dev Comp Immunol 33(2):257–263
Liu S-YV, Frederich B, Lavoué S, Chang J, Erdmann MV, Mahardika GN, Barber PH (2018) Buccal venom gland associates with increased of diversification rate in the fang blenny fish Meiacanthus (Blenniidae; Teleostei). Mol Phylogenet Evol 125:138–146
Lopes-Ferreira M, Moura-da-Silva AM, Mota I, Takehara H (2000) Neutralization of Thalassophryne nattereri (niquim) fish venom by an experimental antivenom. Toxicon 38(8):1149–1156
Lopes-Ferreira M, da Silva Emim JA, Oliveira V, Puzer L, Cezari MH, da Silva Araújo M, Juliano L, Lapa AJ, Souccar C, Moura-da-Silva AM (2004) Kininogenase activity of Thalassophryne nattereri fish venom. Biochem Pharmacol 68(11):2151–2157
Lopes-Ferreira M, Magalhães GS, Fernandez JH, Inácio de Loiola M, Le Ho P, Lima C, Valente RH, Moura-da-Silva AM (2011) Structural and biological characterization of Nattectin, a new C-type lectin from the venomous fish Thalassophryne nattereri. Biochimie 93(6):971–980
Lopes-Ferreira M, Grund LZ, Lima C (2014) Thalassophryne nattereri fish venom: from the envenoming to the understanding of the immune system. J Venom Anim Toxins Incl Trop Dis 20:1–12
Lopes-Ferreira M, Sosa-Rosales I, Bruni FM, Ramos AD, Portaro FCV, Conceição K, Lima C (2016) Analysis of the intersexual variation in Thalassophryne maculosa fish venoms. Toxicon 115:70–80
Lopes-Ferreira M, Sosa-Rosales I, Silva Junior PI, Conceicao K, Maleski ALA, Balan-Lima L, Disner GR, Lima C (2021) Molecular characterization and functional analysis of the nattectin-like toxin from the venomous fish Thalassophryne maculosa. Toxins 14(1):2
Lord JA, Waterfield AA, Hughes J, Kosterlitz HW (1977) Endogenous opioid peptides: multiple agonists and receptors. Nature 267(5611):495–499
Mackessy SP, Williams K, Ashton KG (2003) Ontogenetic variation in venom composition and diet of Crotalus oreganus concolor: a case of venom paedomorphosis? Copeia 2003(4):769–782
Madokoro M, Ueda A, Kiriake A, Shiomi K (2011) Properties and cDNA cloning of a hyaluronidase from the stonefish Synanceia verrucosa venom. Toxicon 58(4):285–292
Magalhães GS, Lopes-Ferreira M, Junqueira-de-Azevedo IL, Spencer PJ, Araújo M, Portaro F, Ma L, Valente R, Juliano L, Fox J (2005) Natterins, a new class of proteins with kininogenase activity characterized from Thalassophryne nattereri fish venom. Biochimie 87(8):687–699
Magalhães G, Junqueira-de-Azevedo I, Lopes-Ferreira M, Lorenzini D, Ho P, Moura-da-Silva A (2006) Transcriptome analysis of expressed sequence tags from the venom glands of the fish Thalassophryne nattereri. Biochimie 88(6):693–699
Magalhães MR, da Silva Jr NJ, Ulhoa CJ (2008) A hyaluronidase from Potamotrygon motoro (freshwater stingrays) venom: isolation and characterization. Toxicon 51(6):1060–1067
Maillaud C, Sebat C, Pouradier F, Paladini L, Peres O, Durand F (2009) Acute circulatory failure following a stonefish envenomation in New caledonia: case report. Medecine Tropicale: Revue Du Corps De Sante Colonial 69(6):591–594
Maillaud C, Hoang-Oppermann T, Hoang-Oppermann V, Rigot H, Girardot S, Nour M (2020) Is stonefish Synanceia verrucosa envenomation potentially lethal? Toxicon 184:78–82
Maina J, Wood C, Hogstrand C, Hopkins T, Luo Y-H, Gibbs P, Walsh P (1998) Structure and function of the axillary organ of the gulf toadfish, Opsanus beta (Goode and Bean). Comp Biochem Physiol a: Mol Integr Physiol 119(1):17–26
Malacarne PF, Menezes TN, Martins CW, Naumann GB, Gomes HL, Pires RG, Figueiredo SG, Campos FV (2018) Advances in the characterization of the Scorpaena plumieri cytolytic toxin (Sp-CTx). Toxicon 150:220–227
Mandojana RM, Sims JK (1987) 19 Miscellaneous dermatoses associated with the aquatic environment. Clin Dermatol 5(3):134–145
Mans BJ, Louw AI, Neitz AW (2002) Savignygrin, a platelet aggregation inhibitor from the soft tick Ornithodoros savignyi, presents the RGD integrin recognition motif on the Kunitz-BPTI fold. J Biol Chem 277(24):21371–21378
Mazur P, Henzel WJ, Seymour JL, Lazarus RA (1991) Ornatins: potent glycoprotein IIb-IIIa antagonists and platelet aggregation inhibitors from the leech Placobdella ornata. Eur J Biochem 202(3):1073–1082
McClounan S, Seymour J (2012) Venom and cnidome ontogeny of the cubomedusae Chironex fleckeri. Toxicon 60(8):1335–1341
McCue MD (2006) Cost of producing venom in three North American pitviper species. Copeia 2006(4):818–825
Meyer PK (1997) Stingray injuries. Wilderness Environ Med 8(1):24–28
Moayedi M, Davis KD (2013) Theories of pain: from specificity to gate control. J Neurophysiol 109(1):5–12
Monteiro-dos-Santos J, Conceição K, Seibert CS, Marques EE, Silva PI Jr, Soares AB, Lima C, Lopes-Ferreira M (2011) Studies on pharmacological properties of mucus and sting venom of Potamotrygon cf. henlei. Int Immunopharmacol 11(9):1368–1377
Moore RH III, Dowling DA (1980) Effects of intravenously administered Leu-or Met-enkephalin on arterial blood pressure. Regul Pept 1(2):77–87
Muhuri D, Karrnakar S, Dasgupta S, Nagchaudhuri K, Gomes A (2004) Pharmacological studies on the venomous spotted butterfish (Scatophagus argus Linn) sting extract on experimental animals. Indian J Exp Biol 42:461–467
Muhuri D, Dasgupta S, Gomes A (2005) Lethal, oedema, haemorrhagic activity of spotted butterfish (Scatophagus argus, Linn) sting extract and its neutralization by antiserum and pharmacological antagonists. Indian J Exp Biol 43(6):493–497
Muirhead D (2002) Applying pain theory in fish spine envenomation. SPUMS J 32(3):150–152
Nagaraju S, Kemparaju K, Girish K (2009) Hyaluronidases, a neglected class of glycosidases from snake venom: beyond a spreading factor. In: Mackessy SP (ed) Handbook of venoms and toxins of reptiles. CRC Press Inc., London, pp 237–258
Nagasaka K, Nakagawa H, Satoh F, Hosotani T, Yokoigawa K, Sakai H, Sakuraba H, Ohshima T, Shinohara M, Ohura K (2009) A novel cytotoxic protein, Karatoxin, from the dorsal spines of the redfin velvetfish. Hypodytes Rubripinnis Toxin Rev 28(4):260–265
Nair M, Cheung P, Leong I, Ruggieri GD (1985) A non-proteinaceous toxin from the venomous spines of the lionfish Pterois volitans (Linnaeus). Toxicon 23(3):525–527
Nakagawa H, Nagasaka K, Sakai H, Edo K, Shinohara M, Ohura K (2015) Isolation of a novel lectin from the dorsal spines of the devil stinger. Inimicus Japonicus International Aquatic Research 7(2):143–150
Ng HC, Ranganathan S, Chua KL, Khoo HE (2005) Cloning and molecular characterization of the first aquatic hyaluronidase, SFHYA1, from the venom of stonefish (Synanceja horrida). Gene 346:71–81
Nisani Z, Dunbar SG, Hayes WK (2007) Cost of venom regeneration in Parabuthus transvaalicus (Arachnida: Buthidae). Comp Biochem Physiol a: Mol Integr Physiol 147(2):509–513
Ohno S (2013) Evolution by gene duplication. Springer, New York
Ouanounou G, Malo M, Stinnakre J, Kreger AS, Molgó J (2002) Trachynilysin, a neurosecretory protein isolated from stonefish (Synanceia trachynis) venom, forms nonselective pores in the membrane of NG108-15 cells. J Biol Chem 277(42):39119–39127
Pacy H (1966) Australian catfish injuries with report of a typical case. Med J Aust 2(2):63–65
Patel DM, Brinchmann MF (2017) Skin mucus proteins of lumpsucker (Cyclopterus lumpus). Biochem Biophys Rep 9:217–225
Poh C, Yuen R, Chung M, Khoo H (1992) Purification and partial characterization of hyaluronidase from stonefish (Synanceja horrida) venom. Comp Biochem Physiol b, Comp Biochem 101(1–2):159–163
Potter I, Thomson G, Cook R, Cox J, Macey D (1995) Buccal glands of adults of the lamprey Mordacia mordax, including comparisons with other species. J Morphol 226(3):339–349
Rajan B, Patel DM, Kitani Y, Viswanath K, Brinchmann MF (2017) Novel mannose binding natterin-like protein in the skin mucus of Atlantic cod (Gadus morhua). Fish Shellfish Immunol 68:452–457
Ramos AD, Conceição K, Silva PI Jr, Richardson M, Lima C, Lopes-Ferreira M (2012) Specialization of the sting venom and skin mucus of Cathorops spixii reveals functional diversification of the toxins. Toxicon 59(6):651–665
Randall JE (1961) Contribution to the biology of the convict surgeonfish of the Hawaiian Islands, Acanthurus triostegus sandvicensis. Pac Sci 15:215–272
Randall JE, Aida K, Hibiya T, Mitsuura N, Kamiya H, Hashimoto Y (1971) Grammistin, the skin toxin of soapfishes, and its significance in the classification of the Grammistidae. Publ Seto Mar Biol Lab 19(2–3):157–190
Rathjen WF, Halstead BW (1969) Report on two fatalities due to stingrays. Toxicon 6:301–302
Reese AM (1902) Structure and development of the thyroid gland in Petromyzon. In: Proceedings of the academy of natural sciences of Philadelphia, 85–112
Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3(2):217–223
Reyes-Velasco J, Card DC, Andrew AL, Shaney KJ, Adams RH, Schield DR, Casewell NR, Mackessy SP, Castoe TA (2015) Expression of venom gene homologs in diverse python tissues suggests a new model for the evolution of snake venom. Mol Biol Evol 32(1):173–183
Rifkin J, Williamson J (1996) Venomous fish. In: Venomous and poisonous marine animals: a medical and biological handbook, 354–395
Rumengan I, Suptijah P, Wullur S, Talumepa A (2017) Characterization of chitin extracted from fish scales of marine fish species purchased from local markets in North Sulawesi, Indonesia. In: IOP conference series: earth and environmental science, vol. 89, p 012028. IOP Publishing
Russell FE, Emery JA (1960) Venom of the weevers Trachinus Draco and Trachinus Vipera. Ann N Y Acad Sci 90(3):805–819
Russell FE, Van Harreveld A (1954) Cardiovascular effects of the venom of the round stingray, Urobatis halleri. Arch Int Physiol Biochim 62(3):322–333
Russell FE (1972) Some chemical and zootoxicological properties of stingray venom. Professional Staff Association of LAC/USC Medical Center Los Angeles CA
Sáenz A, Ortiz N, Lomonte B, Rucavado A, Díaz C (2017) Comparison of biochemical and cytotoxic activities of extracts obtained from dorsal spines and caudal fin of adult and juvenile non-native Caribbean lionfish (Pterois volitans/miles). Toxicon 137:158–167
Saggiomo SL, Zelenka C, Seymour J (2017) Relationship between food and venom production in the estuarine stonefish Synanceia horrida. Toxicon 125:19–23
Saggiomo SL, Firth C, Wilson DT, Seymour J, Miles JJ, Wong Y (2021) The geographic distribution, venom components, pathology and treatments of stonefish (Synanceia spp.) venom. Mar Drugs 19(6):302
Santana RC, Perez D, Dobson J, Panagides N, Raven RJ, Nouwens A, Jones A, King GF, Fry BG (2017) Venom profiling of a population of the theraphosid spider Phlogius crassipes reveals continuous ontogenetic changes from juveniles through adulthood. Toxins 9(4):116
Saraiva TC, Grund LZ, Komegae EN, Ramos AD, Conceição K, Orii NM, Lopes-Ferreira M, Lima C (2011) Nattectin a fish C-type lectin drives Th1 responses in vivo: licenses macrophages to differentiate into cells exhibiting typical DC function. Int Immunopharmacol 11(10):1546–1556
Sarropoulou E, Fernandes JM, Mitter K, Magoulas A, Mulero V, Sepulcre MP, Figueras A, Novoa B, Kotoulas G (2010) Evolution of a multifunctional gene: the warm temperature acclimation protein Wap65 in the European seabass Dicentrarchus labrax. Mol Phylogenet Evol 55(2):640–649
Saunders PR, Taylor PB (1959) Venom of the lionfish Pterois volitans. Am J Physiol-Leg Content 197(2):437–440
Sauviat M-P, Garnier P, Goudey-Perriere F, Perriere C (1995) Does crude venom of the stonefish (Synanceia verrucosa) activate β-adrenoceptors in the frog heart muscle? Toxicon 33(9):1207–1213
Sauviat M-P, Meunier FA, Kreger A, Molgó J (2000) Effects of trachynilysin, a protein isolated from stonefish (Synanceia trachynis) venom, on frog atrial heart muscle. Toxicon 38(7):945–959
Seqirus (2019) Australian product information-stonefish antivenom solution for injection, Commonwealth Serum Laboratories (CSL Ltd), Australia, p 1–7
Sha Z, Xu P, Takano T, Liu H, Terhune J, Liu Z (2008) The warm temperature acclimation protein Wap65 as an immune response gene: its duplicates are differentially regulated by temperature and bacterial infections. Mol Immunol 45(5):1458–1469
Sharon N, Lis H (2004) History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 14(11):53R-62R
Shinohara M, Nagasaka K, Nakagawa H, Edo K, Sakai H, Kato K, Iwaki F, Ohura K, Sakuraba H (2010) A novel chemoattractant lectin, karatoxin, from the dorsal spines of the small scorpionfish Hypodytes rubripinnis. J Pharmacol Sci 113(4):414–417
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(3):285–289
Silva F, Huang Y, Yang V, Mu X, Shi Q, Antunes A (2018) Transcriptomic characterization of the south American freshwater stingray Potamotrygon motoro venom apparatus. Toxins 10(12):544
Skeie E (1962) Toxin of the weeverfish (Trachinus draco) experimental studies on animals. Acta Pharmacol Toxicol 19(2):107–120
Smith J (1957) Two rapid fatalities from stonefish stabs. Copeia 3:249
Smith WL, Wheeler WC (2006) Venom evolution widespread in fishes: a phylogenetic road map for the bioprospecting of piscine venoms. J Hered 97(3):206–217
Smith WL, Stern JH, Girard MG, Davis MP (2016) Evolution of venomous cartilaginous and ray-finned fishes. Oxford University Press, Oxford
Sodre JG, Colaco-Fernandes TR, Py-daniel LH, Birindelli JL, Zuanon J (2021) Putative poison gland in the thorny catfish Acanthodoras spinosissimus (Siluriformes: Doradidae). Acta Amazon 51:250–254
Sommeng AN, Eka AK, Ginting MJ, Pebriani S, Sahlan M, Hermansyah H, Wijanarko A (2019) The effect of ammonium sulfate concentration in protein isolation of lionfish (Pterois volitans) spines venom extract for antitumor test. In: AIP conference proceedings, vol. 2193, p 030009. AIP Publishing LLC
Sosa-Rosales J, D’suze G, Salazar V, Fox J, Sevcik C (2005a) Purification of a myotoxin from the toadfish Thalassophryne maculosa (Günter) venom. Toxicon 45(2):147–153
Sosa-Rosales JI, Piran-Soares AA, Farsky SH, Takehara HA, Lima C, Lopes-Ferreira M (2005b) Important biological activities induced by Thalassophryne maculosa fish venom. Toxicon 45(2):155–161
Stephens JS Jr, Johnson RK, Key GS, McCosker JE (1970) The comparative ecology of three sympatric species of California blennies of the genus Hypsoblennius gill (Teleostomi, Blenniidae). Ecol Monogr 40(2):213–233
Sugahara K, Yamada S, Sugiura M, Takeda K, Yuen R, Khoo H, Poh C (1992) Identification of the reaction products of the purified hyaluronidase from stonefish (Synanceja horrida) venom. Biochem J 283(1):99–104
Sugiyama N, Araki M, Ishida M, Nagashima Y, Shiomi K (2005) Further isolation and characterization of grammistins from the skin secretion of the soapfish Grammistes sexlineatus. Toxicon 45(5):595–601
Sun J, Yu S, Xue Z, Liu C, Wu Y, Liu X, Li Q (2010) Lamprey buccal gland secretory protein-2 (BGSP-2) inhibits human T lymphocyte proliferation. Curr Zool 56(2):252–258
Sunagar K, Moran Y (2015) The rise and fall of an evolutionary innovation: contrasting strategies of venom evolution in ancient and young animals. PLoS Genet 11(10):e1005596
Szaniawski H (2009) The earliest known venomous animals recognized among conodonts. Acta Palaeontol Pol 54(4):669–676
Szczesny P, Iacovache I, Muszewska A, Ginalski K, Van Der Goot FG, Grynberg M (2011) Extending the aerolysin family: from bacteria to vertebrates. PLoS ONE 6(6):e20349
Tachibana K (1984) Shark-repelling ichthyotoxins from the defensive secretion of the sole Pardachirus pavoninus. In: Bolis L, Zadunaisky 1, Gilles R (eds) Toxins, drugs, and pollutants in marine animals. Springer, Berlin, pp 2–12
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526
Tamura S, Yamakawa M, Shiomi K (2011) Purification, characterization and cDNA cloning of two natterin-like toxins from the skin secretion of oriental catfish Plotosus lineatus. Toxicon 58(5):430–438
Tang WJ, Fernandez JG, Sohn JJ, Amemiya CT (2015) Chitin is endogenously produced in vertebrates. Curr Biol 25(7):897–900
Tang T, Huang Y, Peng C, Liao Y, Lv Y, Shi Q, Gao B (2023) A Chromosome-level genome assembly of the Reef Stonefish (Synanceia verrucosa) provides novel insights into stonustoxin (sntx) genes. Mol Biol Evol. https://doi.org/10.1093/molbev/msad215
Tatemoto K (2004) Neuropeptide Y: history and overview. In: Michel MC (ed) Neuropeptide Y and related peptides. Springer, Berlin, pp 1–21
Tay TKW, Chan HZ, Ahmad TST, Teh KK, Low TH, Ab Wahab N (2016) Stonefish envenomation of hand with impending compartment syndrome. J Occup Med Toxicol 11(1):1–4
Taylor MI (2017) Evolution: fangtastic venoms underpin parasitic mimicry. Curr Biol 27(8):R295–R298
Theakston R, Warrell D (1991) Antivenoms: a list of hyperimmune sera currently available for the treatment of envenoming by bites and stings. Toxicon 29(12):1419–1470
Thorson TB, Langhammer JK, Oetinger MI (1988) Periodic shedding and replacement of venomous caudal spines, with special reference to South American freshwater stingrays, Potamotrygon Spp. Environ Biol Fishes 23(4):299–314
Torrez PP, Quiroga MM, Said R, Abati PA, França FO (2015) Tetanus after envenomations caused by freshwater stingrays. Toxicon 97:32–35
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. Biochimica Et Biophysica Acta (BBA)-General Subjects 1760(11):1713–1722
Ueno A, Oh-ishi S (2003) Roles for the kallikrein-kinin system in inflammatory exudation and pain: lessons from studies on kininogen-deficient rats. J Pharmacol Sci 93(1):1–20
Vetrano SJ, Lebowitz JB, Marcus S (2002) Lionfish envenomation. J Emerg Med 23(4):379–382
Wallace J (1967) The batoid fishes of the east coast of southern Africa, Part. II: Manta, eagle, duckbill, cownose, butterfly and sting rays. Invest Rep Oceanogr Res Inst 16:1–56
Wang J, Han X, Yang H, Lu L, Wu Y, Liu X, Guo R, Zhang Y, Zhang Y, Li Q (2010) A novel RGD-toxin protein, Lj-RGD3, from the buccal gland secretion of Lampetra japonica impacts diverse biological activities. Biochimie 92(10):1387–1396
Ward MJ, Ellsworth SA, Hogan MP, Nystrom GS, Martinez P, Budhdeo A, Zelaya R, Perez A, Powell B, He H (2018) Female-biased population divergence in the venom of the Hentz striped scorpion (Centruroides hentzi). Toxicon 152:137–149
Watters MR, Stommel EW (2004) Marine neurotoxins: envenomations and contact toxins. Curr Treat Options Neurol 6(2):115
Wiener S (1959a) Observations on the venom of the stone fish (Synanceja trachynis). Med J Aust 1(19):620–627
Wiener S (1959b) The production and assay of stone-fish antivenene. Med J Aust 2(20):715–719
Williamson JAH, Fenner PJ, Burnett JW, Rifkin J (1996) Venomous and poisonous marine animals: a medical and biological handbook. University of New South Wales Press
Wong ES, Belov K (2012) Venom evolution through gene duplications. Gene 496(1):1–7
Wright JJ (2009) Diversity, phylogenetic distribution, and origins of venomous catfishes. BMC Evol Biol 9(1):282
Wright JJ (2012) The evolutionary ecology of venomous catfishes, with a focus on members of the North American family Ictaluridae (Teleostei: Siluriformes), University of Michigan
Wright JJ (2015) Evolutionary history of venom glands in the siluriformes. In: Evolution of venomous animals and their toxins. Springer, Dordrecht, p 1–19
Wu F, Feng B, Ren Y, Wu D, Chen Y, Huang S, Chen S, Xu A (2017) A pore-forming protein implements VLR-activated complement cytotoxicity in lamprey. Cell Discov 3(1):1–12
Xiao R, Li Q-W, Perrett S, He R-Q (2007) Characterisation of the fibrinogenolytic properties of the buccal gland secretion from Lampetra japonica. Biochimie 89(3):383–392
Xiao R, Pang Y, Li QW (2012) The buccal gland of Lampetra japonica is a source of diverse bioactive proteins. Biochimie 94(5):1075–1079
Xue Z, Liu X, Pang Y, Yu T, Xiao R, Jin M, Han Y, Su P, Wang J, Lv L (2012) Characterization, phylogenetic analysis and cDNA cloning of natterin-like gene from the blood of lamprey, Lampetra japonica. Immunol Lett 148(1):1–10
Yokota H, Nagashima Y, Shiomi K (2001) Interaction of grammistins with lipids and their antibacterial activity. Fish Sci 67(5):928–933
Yoshinaga-Kiriake A, Nagashima Y, Ishizaki S, Shiomi K (2020) Primary structures and conformations of stonefish toxin-like toxins from three species of rabbitfish, Siganus puellus, Siganus unimaculatus, and Siganus virgatus. Fish Sci 86(5):889–901
Zhang Y, Xu J, Wang Z, Zhang X, Liang X, Civelli O (2012) BmK-YA, an enkephalin-like peptide in scorpion venom. PLoS ONE 7(7):e40417
Ziegman R, Alewood P (2015) Bioactive components in fish venoms. Toxins 7(5):1497–1531
Ziegman R, Undheim EA, Baillie G, Jones A, Alewood PF (2019) Investigation of the estuarine stonefish (Synanceia horrida) venom composition. J Proteom 201:12–26
Zobel-Thropp PA, Bulger EA, Cordes MH, Binford GJ, Gillespie RG, Brewer MS (2018) Sexually dimorphic venom proteins in long-jawed orb-weaving spiders (Tetragnatha) comprise novel gene families. PeerJ 6:e4691
Acknowledgements
I would like to thank the reviewers for making the time to review such a large manuscript and to help improve all aspects of it. I want to also thank Nicholas Youngman, Silvia Saggiomo and Lorenzo Seneci for their comments on some aspects of the manuscript.
Funding
No funding was received to assist with the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
RJH designed, researched, and produced the review material. RJH wrote the first draft and subsequent drafts afterward.
Corresponding author
Ethics declarations
Conflict of interest
There are no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Harris, R.J. The piscine arsenal: an updated review of venomous fishes. Rev Fish Biol Fisheries (2023). https://doi.org/10.1007/s11160-023-09828-w
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11160-023-09828-w