Chemical defense in pelagic octopus paralarvae: Tetrodotoxin alone does not protect individual paralarvae of the greater blue-ringed octopus (Hapalochlaena lunulata) from common reef predators

Chemoecology

Volumn 21, Issue 3, 2011, Pages 131-141

  Williams, Becky L ^a   Lovenburg, Vanessa ^b   Huffard, Christine L ^c   Caldwell, Roy L ^b  

^a NEW MEXICO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Division of Fisheries and Environmental Conservation   (Indonesia)

Author keywords

Cephalopod blue ringed octopus; Chemical defense; Hapalochlaena lunulata; Palatability; Paralarvae; Pelagic larvae; Tetrodotoxin

Indexed keywords

CEPHALOPODA; HAPALOCHLAENA LUNULATA; HAPTOSQUILLA TRISPINOSA; OCTOPUS; STOMATOPODA;

EID: 79960986808     PISSN: 09377409     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00049-011-0075-5     Document Type: Article

References (54)

1. Brodie ED Jr (1968) Investigations on the skin toxin of the adult rough-skinned newt, Taricha granulosa. Copeia 1968: 307-313.
2. Brodie ED III, Brodie ED Jr (1999) The cost of exploiting poisonous prey: evolutionary tradeoffs in a predator-prey arms race. Evolution 53: 626-631.
3. Bullard SG, Niels L, Hay M (1999) Susceptibility of invertebrate larvae to predators: how common are post-capture larval defenses? Mar Ecol Prog Ser 191: 153-161.
4. Cheng MW, Caldwell RL (2000) Sex identification and mating in the blue-ringed octopus, Hapalochlaena lunulata. Anim Behav 60: 27-33.
5. Daly JW, Garaffo HM, Hall GSE, Cover JF (1997) Absence of skin alkaloids in captive-raised Madagascan mantelline frogs (Mantella) and sequestration of dietary alkaloids. Toxicon 35: 1131-1135.
6. Derby CD (2007) Escape by inking and secreting: marine mollusks avoid predators through a rich array of chemicals and mechanisms. Biol Bull 213: 274-289.
7. Eisner T, Eisner M, Rossini C, Iyengar VK, Roach BL, Benedikt E, Meinwald J (2000) Chemical defense against predation in an insect egg. Proc Natl Acad Sci USA 15: 1634-1639.
8. Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, Oxford.
9. Häikiö E, Makkonen M, Julkunen-Tiitto R, Sitte J, Freiwald V, Silfver T, Pandey V, Beuker E, Holopainen T, Oksanen E (2009) Performance and secondary chemistry of two hybrid aspen (Populus tremula L. × Populus tremuloides Michx.) clones in long-term elevated ozone exposure. J Chem Ecol 35: 664-678.
10. Hanifin CT, Yotsu-Yamashita M, Yasumoto T, Brodie ED III, Brodie ED Jr (1999) Toxicity of dangerous prey: variation of tetrodotoxin levels within and among populations of the newt Taricha granulosa. J Chem Ecol 25: 2161-2175.
11. Hanlon RT, Messenger JB (1996) Cephalopod behaviour. Cambridge University Press, Cambridge.
12. Huffard CL, Caldwell RL (2002) Inking in a blue-ringed octopus, Hapalochlaena lunulata, with a vestigial ink sac. Pac Sci 56: 255-257.
13. Hwang DF, Arakawa O, Saito T, Noguchi T, Simidu U, Tsukamoto K, Shida Y, Hashimoto K (1989) Tetrodotoxin-producing bacteria from the blue-ringed octopus, Octopus maculosus. Mar Biol 100: 327-332.
14. Jereb P, Roper CFE, Vecchione M (2005) Introduction. In: Roper CFE (ed) Jereb P. an Annotated and Illustrated Catalog of Species Known to Date. FAO Rome Italy, Cephalopods of the World.
15. Johnson S (2001) Hidden in plain sight: the ecology and physiology of organismal transparency. Biol Bull 201: 301-318.
16. Jones EC (1963) Tremoctopus violaceus uses Physalia tentacles as weapons. Science 139: 764-766.
17. Kao CY (1966) Tetrodotoxin, saxitoxin, and their significance in the study of excitation phenomena. Pharmacol Rev 18: 997-1049.
18. Lindquist N, Hay ME (1996) Palatability and chemical defense of marine invertebrate larvae. Ecol Monogr 66: 431-450.
19. Lindquist N, Hay ME, Fenical W (1992) Defense of ascidians and their conspicuous larvae: adult versus larval chemical defenses. Ecol Monogr 62: 547-568.
20. Matsui T, Sato H, Hamada S, Shimizu C (1982) Comparison of toxicity of the cultured and wild puffer fish Fugu niphobles. Bull Jpn Soc Sci Fish 48: 253.
21. Matsumura K (1996) Tetrodotoxin concentration in cultured puffer fish, Fugu rubripes. J Agric Food Chem 44: 1-2.
22. McClintock JB, Vernon JD (1990) Chemical defense in the eggs and embryos of Antarctic sea stars (Echinodermata). Mar Biol 105: 491-495.
23. Miyazawa K, Jeon JK, Noguchi T, Ito K, Hashimoto K (1987) Distribution of tetrodotoxin in the tissues of the flatworm Planocera multitentaculata (Platyhelminthes). Toxicon 25: 975-980.
24. Mobley JA, Stidham TA (2000) Great horned owl death from predation of a toxic California newt. Wilson Bull 112: 563-564.
25. Mochida K (2009) A parallel geographical mosaic of morphological and behavioural aposematic traits of the newt, Cynops pyrrhogaster (Urodela: Salamandridae). Biol J Linn Soc 97: 613-622.
26. Morgan SG (1989) Adaptive significance of spination in estuarine crab zoeae. Ecol 70: 462-482.
27. Narahasi T (2001) Pharmacology of tetrodotoxin. J Toxicol Toxin Rev 20: 67-84.
28. Nicolaus LK, Cassel JF, Carlson RB, Gustavson CR (1983) Taste-aversion conditioning of crows to control predation on eggs. Science 220: 212-214.
29. Noguchi T, Arakawa O (2008) Tetrodotoxin-distribution and accumulation in aquatic organisms, and cases of human intoxication. Mar Drugs 6: 220-242.
30. Noguchi T, Ebesu JSM (2001) Puffer poisoning: epidemiology and treatment. J Toxicol Toxin Rev 20: 1-10.
31. Noguchi T, Arakawa O, Takatani T (2006) Toxicity of pufferfish Takifugu rubripes cultured in netcages at sea or aquaria on land. Comp Biochem PhysiolD 1: 153-157.
32. Norman MD (2000) Cephalopods: a world guide. ConchBooks, Hackenheim.
33. Overath H, von Boletzky S (1974) Laboratory observations on spawning and embryonic development of a blue-ringed octopus. Mar Biol 27: 333-337.
34. Prota G, Ortonne JP, Voulot C, Khatchadourian GN, Palumbo A (1981) Occurrence and properties of tyrosinase in the ejected ink of cephalopods. Comp Biochem Physiol68B: 415-419.
35. Ritson-Williams RR, Yotsu-Yamashita M, Paul V (2006) Ecological functions of tetrodotoxin in a deadly polyclad flatworm. Proc Natl Acad Sci USA 103: 3176-3179.
36. Robson GC (1929) A monograph of the recent Cephalopoda based on the collections in the British Museum (Natural History) Part 1 Octopodinae. London, British Museum 1-236.
37. Russo GL, De Nisco E, Fiore G, Di Donato P, d'Ishcia M, Palumbo A (2003) Toxicity of melanin-free ink of Sepia officinalis to transformed cell lines: identification of the active factor as tyrosinase. Biochem Biophys Res Commun 308: 293-299.
38. Saito T, Maruyama J, Kanoh S, Jeon JK, Noguchi T, Harada T, Murata O, Hashimoto K (1984) Toxicity of the cultured pufferfish Fugu rubripes rubripes along with their resistibility against tetrodotoxin. Bull Jpn Soc Sci Fish 50: 1573-1575.
39. Savage IVE, Howden MEH (1977) Hapalotoxin: a second lethal toxin from the octopus Hapalochlaena maculosa. Toxicon 15: 463-466.
40. Sheumack DD, Howden MEH, Spence I (1978) Maculotoxin: a neurotoxin from the glands of the octopus, Hapalochlaena maculosa identified as tetrodotoxin. Science 199: 188-189.
41. Sheumack DD, Howden ME, Spence I (1984) Occurrence of a tetrodotoxin-like compound in the eggs of the venomous blue-ringed octopus (Hapalochlaena maculosa). Toxicon 22: 811-812.
42. Tranter DJ, Augustine O (1973) Observations on the life history of the blue-ringed octopus Hapalochlaena maculosa. Mar Biol (Berl) 18: 115-128.
43. Villanueva R, Norman MD (2008) Biology of the planktonic stages of benthic octopuses. Oceanogr Mar Biol Ann Rev 46: 105-202.
44. Williams BL (2010) Behavioral and chemical ecology of marine organisms with respect to tetrodotoxin. Marine Drugs 8(3): 381-398.
45. Williams BL, Caldwell RL (2009) Intra-organismal distribution of tetrodotoxin in two species of blue-ringed octopuses (Hapalochlaena fasciata and H. lunulata). Toxicon 54(3): 345-353.
46. Williams BL, Brodie ED Jr, Brodie ED III (2003) Coevolution of deadly toxins and predator resistance: self-assessment of resistance by garter snakes leads to behavioral rejection of toxic newt prey. Herpetologica 59: 155-163.
47. Williams BL, Hanifin CT, Brodie ED Jr, Brodie ED III (2010) Tetrodotoxin (TTX) affects survival probability of rough skinned newts (Taricha granulosa) faced with TTX-resistant garter snake predators (Thamnophis sirtalis). Chemoecology 20: 285-290.
48. Williams BL, Hanifin CT, Brodie ED Jr, Caldwell RL (2011) Ontogeny of tetrodotoxin levels in blue-ringed octopuses: maternal investment and apparent independent production in offspring of Hapalochlaena lunulata. J Chem Ecol. doi: 10. 1007/s10886-010-9901-4.
49. Yamamori K, Nakamura M, Hara TJ (1987) Gustatory responses to tetrodotoxin and saxitoxin in rainbow trout (Salmo gairdneri) and arctic char (Salvelinus alpinus): a possible biological defense mechanism. Ann NY Acad Sci 510: 727-729.
50. Yasumoto T, Yotsu-Yamashita M (1996) Chemical and etiological studies on tetrodotoxin and its analogs. J Toxicol Toxin Rev 15: 81-90.
51. Yotsu M, End A, Yasumoto T (1989) An improved tetrodotoxin analyzer. Agric Biol Chem 53: 893-895.
52. Yotsu-Yamashita M, Mebs D, Flachsenberger W (2007) Distribution of tetrodotoxin in the body of the blue-ringed octopus (Hapalochlaena maculosa). Toxicon 49: 410-412.
53. Young CM, Bingham BL (1987) Chemical defense and aposematic coloration in larvae of the ascidian Ecteinascidia turbinata. Mar Biol 96: 539-544.
54. Zangerl AR, Berenbaum MR (1997) Cost of chemically defending seeds: furanocourmarins and Pastinaca sativa. Am Nat 150: 491-504.