Costs of venom production in the common death adder (Acanthophis antarcticus)

Toxicon

Volumn 56, Issue 6, 2010, Pages 1035-1042

  Pintor, Anna F V ^a   Krockenberger, Andrew K ^a   Seymour, Jamie E ^a  

^a JAMES COOK UNIVERSITY   (Australia)

Author keywords

Acanthophis; Elapids; Energetic expenditure; Venom cost

Indexed keywords

SNAKE VENOM;

ARTICLE; CONTROLLED STUDY; DIGESTION; ENERGY EXPENDITURE; FEMALE; MALE; METABOLIC RATE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RESPIROMETER;

ANIMALS; CALORIMETRY, INDIRECT; ELAPID VENOMS; ELAPIDAE; ENERGY METABOLISM; FEMALE; MALE; NEUROTOXINS; OXYGEN CONSUMPTION; RESPIRATORY FUNCTION TESTS; SPIROMETRY;

ACANTHOPHIS; ACANTHOPHIS ANTARCTICUS; ELAPIDAE; SERPENTES;

EID: 77956063242     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2010.07.008     Document Type: Article

References (63)

1. Barlow A., Pook C.E., Harrison R.A., Wüster W. Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution. P. Roy. Soc. B. 2009, 276:2443-2449. 10.1098/rspb.2009.0048.
2. Benabib M., Congdon J.D. Metabolic and water-flux rates of free-ranging tropical lizards Sceloporus variabilis. Physiol. Zool. 1992, 65:788-802.
3. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254. 10.1016/0003-2697(76)90527-3.
4. Brenneke F., Hatz C. Stonefish envenomation-a lucky outcome. Travel Med. Infect. Dis. 2006, 4:281. 10.1016/j.tmaid.2005.09.001.
5. Broad A.J., Sutherland S.K., Coulter A.R. The lethality in mice of dangerous Australian and other snake venoms. Toxicon 1979, 17:661-664. 10.1016/0041-0101(79)90245-9.
6. Brown R.S. Accumulation of some secretory enzymes in venom glands of Vipera palaestinae. Am. J. Physiol. 1975, 229:1675-1679.
7. Castoe T.A., Jiang Z.J., Gu W., Wang Z.O., Pollock D.D. Adaptive evolution and functional redesign of core metabolic proteins in snakes. PLoS ONE 2008, 3:e2201. 10.1371/journal.pone.0002201.
8. Christian K., Webb J.K., Schultz T., Green B. Effects of seasonal variation in prey abundance on field metabolism, water flux, and activity of a tropical ambush foraging snake. Physiol. Biochem. Zool. 2007, 80:522-533. 10.1086/519959.
9. Diller L.V., Wallace R.L. Reproductive biology of the Northern Pacific rattlesnake (Crotalus viridis oreganus) in Northern Idaho. Herpetologica 1984, 40:182-193.
10. Dufton M.J. Venomous mammals. Pharmacol. Therapeut 1992, 53:199-215. 10.1016/0163-7258(92)90009-O.
11. Fitch H.S. Study of snake populations in central California. Am. Midl. Nat. 1949, 41:513-579.
12. Fry B.G., Wickramaratna J.C., Hodgson W.C., Alewood P.F., Kini R.M., Ho H., Wuester W. Electrospray liquid chromatography/mass spectrometry fingerprinting of Acanthophis (death adder) venoms: taxonomic and toxinological implications. Rapid Commun. Mass Sp 2002, 16:600-608. 10.1002/rcm.613.
13. Gessaman J.A., Nagy K.A. Energy metabolism: errors in gas-exchange conversion factors. Physiol. Zool. 1988, 61:507-513.
14. GraphPad Software Inc. 1992-2007 Prism 5 for Windows, Version 5.00 (Trial), 12. March 2007.
15. Hayes W.K. Venom metering by juvenile prairie rattlesnakes, Crotalus v. viridis: effects of prey size and experience. Anim. Behav. 1995, 50:33-40. 10.1006/anbe.1995.0218.
16. Hayes W.K., Lavin-Murcio P., Kardong K.V. Northern Pacific rattlesnakes (Crotalus viridis oreganus) meter venom when feeding on prey of different sizes. Copeia 1995, 1995:337-343.
17. Hayes W.K. The snake venom-metering controversy: levels of analysis, assumptions, and evidence. The Biology of Rattlesnakes 2008, 191-220. Loma Linda University Press, Loma Linda, California. W.K. Hayes, K.R. Beaman, M.D. Cardwell, S.P. Bush (Eds.).
18. Hoser R. Death adders (genus Acanthophis): an overview, including descriptions of five new species and one subspecies. Monitor-Journal Victorian Herpetological Soc. 1998, 9:20-41.
19. Inceoglu B., Lango J., Jing J., Chen L., Doymaz F., Pessah I.N., Hammock B.D. One scorpion, two venoms: prevenom of Parabuthus transvaalicus acts as an alternative type of venom with distinct mechanism of action. P. Natl. Acad. Sci. USA 2003, 100:922-927. 10.1073/pnas.242735499.
20. Johnson R.G. The origin and evolution of the venomous snakes. Evolution 1956, 10:56-65.
21. Kardong K.V. Predatory strike behavior of the rattlesnake, Crotalus viridis oreganus. J. Comp. Psychol. 1986, 100:304-314.
22. Kerchove C.M., Carneiro S.M., Markus R.P., Yamanouye N. Stimulation of the α-adrenoreceptor triggers the venom production cycle in the venom gland of Bothrops jararaca. J. Exp. Biol. 2004, 207:411-416. 10.1242/jeb.00778.
23. Kerchove C.M., Luna M.S.A., Zablith M.B., Lazari M.F.M., Smaili S.S., Yamanouye N. α1-adrenoreceptors trigger the snake venom production cycle in secretory cells by activating phosphatidylinositol 4,5-bisphosphate hydrolysis and ERK signaling pathway. Comp. Biochem. Phys. A 2008, 150:431-437. 10.1016/j.cbpa.2008.04.607.
24. Kintner A.H., Seymour J.E., Edwards S.L. Variation in lethality and effects of two Australian chirodropid jellyfish venoms in fish. Toxicon 2005, 46:699-708. 10.1016/j.toxicon.2005.07.015.
25. Kochva E., Oron U., Bdolah A., Allon N. Regulation of venom secretion and injection in viperid snakes. Toxicon 1975, 13:104. 10.1016/0041-0101(75)90052-5.
26. Kochva E., Tönsing L., Louw A.I., Liebenberg N.V., Visser L. Biosynthesis, secretion and in vivo isotopic labelling of venom of the Egyptian cobra, Naja haje annulifera. Toxicon 1982, 20:615.
27. Krane S., Itagaki Y., Nakanishi K., Weldon P.J. " Venom" of the slow loris: sequence similarity of prosimian skin gland protein and Fel d 1 cat allergen. Naturwissenschaften 2003, 90:60-62. 10.1007/s00114-002-0394-z.
28. Li M., Fry B.G., Kini R.M. Eggs-only diet: its implications for the toxin profile changes and ecology of the marbled sea snake (Aipysurus eydouxii). J. Mol. Evol. 2005, 60:81-89. 10.1007/s00239-004-0138-0.
29. Li M., Fry B.G., Kini R.M. Putting the brakes on snake venom evolution: the unique molecular evolutionary patterns of Aipysurus eydouxii (marbled sea snake) phospholipase A2 toxins. Mol. Biol. Evol. 2005, 22:934-941. 10.1093/molbev/msi077.
30. Lillywhite H.B. Behavioral thermoregulation in Australian elapid snakes. Copeia 1980, 3:452-458.
31. Luna M.S.A., Hortencio T.M.A., Ferreira Z.S., Yamanouye N. Sympathetic outflow activates the venom gland of the snake Bothrops jararaca by regulating the activation of transcription factors and the synthesis of venom gland proteins. J. Exp. Biol. 2009, 212:1535-1543. 10.1242/jeb.030197.
32. Mackessy S.P. The field of reptile toxinology: snakes, lizards and their venoms. Handbook of Venoms and Toxins of Reptiles 2009, 3-23. Taylor & Francis/CRC Press, Boca Raton, FL. S.P. Mackessy (Ed.).
33. Mackessy S.P., Baxter L.M. Bioweapons synthesis and storage: the venom gland of front-fanged snakes. Zool. Anzeiger 2006, 245:147-159. 10.1016/j.jcz.2006.01.003.
34. Maderson P.F.A., Chiu K.W., Phillips J.G. Changes in the epidermal histology during the sloughing cycle in the rat snake Ptyas korros Schlegel, with correlated observations on the thyroid gland. Biol. Bull. 1970, 139:304-312.
35. Magalhães K.W., Lima C., Piran-Soares A.A., Marques E.E., Hiruma-Lima C.A., Lopes-Ferreira M. Biological and biochemical properties of the Brazilian Potamotrygon stingrays: Potamotrygon cf. scobina and Potamotrygon gr. orbignyi. Toxicon 2006, 47:575-583. 10.1016/j.toxicon.2006.01.028.
36. Malli H. Effects of size, motility and paralysation time of prey on the quantity of venom injected by the hunting spider Cupiennius salei. J. Exp. Biol. 1999, 202:2083-2089.
37. Malli H., Imboden H., Kuhn-Nentwig L. Quantifying the venom dose of the spider Cupiennius salei using monoclonal antibodies. Toxicon 1998, 36:1959-1969. 10.1016/S0041-0101(98)00120-2.
38. Mebs D. Toxicity in animals. Trends in evolution?. Toxicon 2001, 39:87-96. 10.1016/S0041-0101(00)00155-0.
39. McCue M.D. Enzyme activities and biological functions of snake venoms. Appl. Herpetol 2005, 2:109-123. 10.1163/1570754043492135.
40. McCue M.D. Cost of producing venom in three North American pitviper species. Copeia 2006, 2006:818-825. (2006)6[818:COPVIT]2.0.CO;2). 10.1643/0045-8511.
41. McCue M.D. Specific dynamic action: a century of investigation. Comp. Biochem. Phys. A 2006, 144:381-394. 10.1016/j.cbpa.2006.03.011.
42. Mirtschin P.J., Shine R., Nias T.J., Dunstan N.L., Hough B.J., Mirtschin M. Influences on venom yield in Australian tigersnakes (Notechis scutatus) and brownsnakes (Pseudonaja textilis: Elapidae, Serpentes). Toxicon 2002, 40:1581-1592. 10.1016/S0041-0101(02)00175-7.
43. Nisani Z., Dunbar S.G., Hayes W.K. Cost of venom regeneration in Parabuthus transvaalicus (Arachnida: Buthidae). Comp. Biochem. Phys. A 2007, 147:509-513. 10.1016/j.cbpa.2007.01.027.
44. Oron U., Bdolah A. Regulation of protein synthesis in the venom gland of viperid snakes. J. Cell Biol. 1973, 56:177-190.
45. R Development Core Team R: a Language and Environment for Statistical Computing 2008, R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org.
46. Rotenberg D., Bamberger E.S., Kochva E. Studies on ribonucleic acid synthesis in the venom glands of Vipera palaestinae (Ophidia, Reptilia). Biochem. J. 1971, 121:609-612.
47. Russell F.E. Injuries by venomous animals. Am. J. Nurs. 1966, 66:1322-1326.
48. Saunders P.K. Pharmacological and Chemical studies of the venom of the Stonefish (Genus Synanceja) and other Scorpionfishes. Ann. NY Acad. Sci. 1960, 90:798-804.
49. Secor S.M., Stein E.D., Diamond J. Rapid upregulation of snake intestine in response to feeding: a new model of intestinal adaptation. Am. J. Physiol. Gastr. L. 1994, 266:695-705.
50. Secor S.M., Diamond J.M. Evolution of regulatory responses to feeding in Snakes. Physiol. Biochem. Zool. 2000, 73:123-141. 10.1086/316734.
51. Secor S.M. Specific dynamic action: a review of the postprandial metabolic response. J. Comp. Physiol. B. 2009, 179:1-56. 10.1007/s00360-008-0283-7.
52. Shine R. Ecology of the Australian death adder Acanthophis antarcticus (Elapidae): evidence for convergence with the Viperidae. Herpetologica 1980, 36:281-289.
53. Silva W.P., Silva C.M.D.P.S. LAB fit Curve Fitting software (Nonlinear regression and treatment of data program) V 7.2.44 (1999-2009) Available online at:, (accessed 03.10.09.). http://zeus.df.ufcg.edu.br/labfit/download.htm.
54. SPSS Inc., Sep. 2005. SPSS 14.0.0 for Windows Evaluation Version, Rel. 14.0.0. 5. Chicago.
55. Starck J.M., Moser P., Werner R.A., Linke P. Pythons metabolize prey to fuel the response to feeding. P.R. Soc. B 2004, 271:903-908.
56. Thompson G.G., Withers P.C. Effect of sloughing and digestion on metabolic rate in the Australian carpet python, Morelia spilota impricata. Aust. J. Zool. 1999, 47:605-610. 10.1071/ZO99012.
57. Veiga A.B.G., Ribeiro J.M.C., Guimaraes J.A., Francischetti I.M.B. A catalog for the transcripts from the venomous structures of the caterpillar Lonomia obliqua: identification of the proteins potentially involved in the coagulation disorder and hemorrhagic syndrome. Gene 2005, 355:11-27. 10.1016/j.gene.2005.05.002.
58. Vidal N., Rage J.-C., Couloux A., Hedges S.B. Snakes (Serpentes). The Timetree of Life 2009, 390-397. Oxford University Press, New York. S.B. Hedges, S. Kumar (Eds.).
59. Wilde H. Anaphylactic shock following bite by a 'slow loris', Nycticebus coucang. Am. J. Trop. Med. Hyg. 1972, 21:592.
60. 2, and evaporative water loss with a flow-through mask. J. Appl. Physiol. 1977, 42:120-123.
61. Wüster W., Dumbrell A.J., Hay C., Pook C.E., Williams D.J., Fry B.G. Snakes across the strait: trans-Torresian phylogeographic relationships in three genera of Australasian snakes (Serpentes: Elapidae: Acanthophis, Oxyuranus, and Pseudechis). Mol. Phylogenet. Evol. 2005, 34:1-14. 10.1016/j.ympev.2004.08.018.
62. Yamanouye N., Britto L.R.G., Carneiro S.M., Markus R.P. Control of venom production and secretion by sympathetic outflow in the snake Bothrops jararaca. J. Exp. Biol. 1997, 200:2547-2556.
63. Yamanouye N., Carneiro S.M., Scrivano C.N., Markus R.P. Characterization of β-adrenoreceptors responsible for venom production in the venom gland of the snake Bothrops jararaca. Life Sci. 2000, 67:217-226. 10.1016/S0024-3205(00)00626-3.