Sequestered defensive toxins in tetrapod vertebrates: Principles, patterns, and prospects for future studies

Chemoecology

Volumn 22, Issue 3, 2012, Pages 141-158

  Savitzky, Alan H ^a   Mori, Akira ^b   Hutchinson, Deborah A ^c   Saporito, Ralph A ^d   Burghardt, Gordon M ^e   Lillywhite, Harvey B ^f   Meinwald, Jerrold ^g  

^a UTAH STATE UNIVERSITY   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c Department of Public Health   (United States)

^d JOHN CARROLL UNIVERSITY   (United States)

^e UNIVERSITY OF TENNESSEE   (United States)

^f University of Florida ^*  (United States)

^g Department of Obstetrics Gynecology   (United States)

Author keywords

Amphibians; Antipredator defense; Aposematism; Dietary toxins; Reptiles; Sequestration

Indexed keywords

ACARI; AMPHIBIA; ANIMALIA; ANURA; AVES; DENDROBATIDAE; GASTROPODA; HEXAPODA; INVERTEBRATA; REPTILIA; SERPENTES; TETRAPODA; VERTEBRATA;

EID: 84865521655     PISSN: 09377409     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00049-012-0112-z     Document Type: Review

References (209)

1. Adalsteinsson SA, Branch WR, Trape S, Vitt LJ, Hedges SB (2009) Molecular phylogeny, classification, and biogeography of snakes of the Family Leptotyphlopidae (Reptilia, Squamata). Zootaxa 2244: 1-50.
2. Baker R, Coles HR, Edwards M, Evans DA, Howse PE, Walmsley S (1981) Chemical composition of the frontal gland secretion of Syntermes soldiers (Isoptera, Termitidae). J Chem Ecol 7: 135-145.
3. Baker R, Parton AH, Howse PE (1982) Identification of an acyclic diterpene alcohol in the defense secretion of soldiers of Reticulitermes lucifugus. Experientia 38: 297-298.
4. Baptista de Oliveira R, Di-Bernardo M, Pontes GMF, Maciel AP, Krause L (2000) Dieta e comportamento alimentar da cobra-nariguda, Lystrophis dorbignyi (Duméril, Bibron & Duméril, 1854), no Litoral Norte do Rio Grande do Sul, Brasil. Cuad Herpetol 14: 117-122.
5. Berenbaum MR (1995) The chemistry of defense: theory and practice. In: Eisner T, Meinwald J (eds) Chemical ecology: the chemistry of biotic interaction. National Academy Press, Washington, DC, pp 1-16.
6. Boggs ASP, Botteri NL, Hamlin HJ, Guillette LJ Jr (2011) Endocrine disruption of reproduction in reptiles. In: Norris DO, Lopez KH (eds) Hormones and reproduction of vertebrates. Reptiles, vol 3. Academic Press, New York, pp 373-396.
7. Branch B (1998) Field guide to snakes and other reptiles of Southern Africa. Ralph Curtis Books Publishing, Sanibel Island.
8. Brodie ED Jr (1977a) Hedgehogs use toad venom in their own defence. Nature 268: 627-628.
9. Brodie ED Jr (1977b) Salamander antipredator postures. Copeia 1977: 523-535.
10. Brodie ED Jr, Johnson JA, Dodd CK Jr (1974) Immobility as a defensive behavior in salamanders. Herpetologica 30: 79-85.
11. Brodie ED III, Brodie ED Jr, Motychak JE (2002) Recovery of garter snakes (Thamnophis sirtalis) from the effects of tetrodotoxin. J Herpetol 36: 95-98.
12. Brodie ED III, Feldman CR, Hanifin CT, Motychak JE, Mulcahy DG, Williams BL, Brodie ED Jr (2005) Parallel arms races between garter snakes and newts involving tetrodotoxin as the phenotypic interface of coevolution. J Chem Ecol 31: 343-356.
13. Brucker RM, Baylor CM, Walters RL, Lauer A, Harris RN, Minbiole KPC (2008a) The identification of 2, 4-diacetylphloroglucinal as an antifungal metabolite produced by cutaneous bacteria of the salamander Plethodon cinereus. J Chem Ecol 34: 39-43.
14. Brucker RM, Harris RN, Schwantes CR, Gallaher TN, Flaherty DC, Lam BA, Minbiole KPC (2008b) Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J Chem Ecol 34: 1422-1429.
15. Bruner G, Fernández-Marín H, Touchon JC, Wcislo WT (2012) Eggs of the blind snake, Liotyphlops albirostris, are incubated in a nest of the lower fungus-growing ant, Apterostigma cf. goniodes. Psyche 2012: 1-5.
16. Burghardt GM, Greene HW (1988) Predator simulation and duration of death feigning in neonate hognose snakes. Anim Behav 36: 1842-1844.
17. Cadle JE, Myers CW (2003) Systematics of snakes referred to Dipsas variegata in Panama and western South America, with revalidation of two species and notes on defensive behaviors in the Dipsadini (Colubridae). Am Mus Novitates 3409: 1-47.
18. Central Research Laboratories (1999) Ecology and artificial propagation of the Mamushi. Yomeishu Seizo Co., Ltd., Nagano.
19. Chau R, Kalaitzis JA, Neilan BA (2011) On the origins and biosynthesis of tetrodotoxin. Aquat Toxicol 104: 61-72.
20. Cimino G, Ghiselin MT (2009) Chemical defense and the evolution of opisthobranch gastropods. Proc Calif Acad Sci 60: 175-422.
21. Clark VC, Raxworthy CJ, Rakotomalala V, Sierwald P, Fisher BL (2005) Convergent evolution of chemical defense in poison frogs and arthropod prey between Madagascar and the Neotropics. Proc Natl Acad Sci USA 102: 11617-11622.
22. Clucas B, Rowe MP, Owings DH, Arrowood PC (2008) Snake scent application in ground squirrels, Spermophilus spp.: a novel form of antipredator behaviour? Anim Behav 75: 299-307.
23. Cocroft RB, Hambler K (1989) Observations on a commensal relationship of the microhylid frog Chiasmocleis ventrimaculata and the burrowing theraphosid spider Xenesthis immanis in southeastern Peru. Biotropica 21: 2-8.
24. Cogger HG (1992) Reptiles & amphibians of Australia. Reed Books, Chatswood.
25. Collins JP, Crump ML (2009) Extinction in our times: global amphibian decline. Oxford University Press, New York.
26. Cooper WE Jr, Caldwell JP, Vitt LJ (2009) Conspicuousness and vestigial escape behaviour by two dendrobatid frogs, Dendrobates auratus and Oophaga pumilio. Behaviour 146: 325-349.
27. Crump M (2000) In search of the golden frog. University of Chicago Press, Chicago.
28. Daly JW (1995) The chemistry of poisons in amphibian skin. In: Eisner T, Meinwald J (eds) Chemical ecology: the chemistry of biotic interaction. National Academy Press, Washington, DC, pp 17-28.
29. Daly JW (1998) Thirty years of discovering arthropod alkaloids in amphibian skin. J Nat Prod 61: 162-172.
30. Daly JW (2003) Ernest Guenther Award in chemistry of natural products. Amphibian skin: a remarkable source of biologically active arthropod alkaloids. J Med Chem 46: 445-452.
31. Daly JW (2004) Marine toxins and nonmarine toxins: convergence or symbiotic organisms? J Nat Prod 67: 1211-1215.
32. Daly JW, Garraffo HM, Spande TF, Jaramillo C, Rand AS (1994a) Dietary source for skin alkaloids of poison frogs (Dendrobatidae)? J Chem Ecol 20: 943-955.
33. Daly JW, Secunda SI, Garraffo HM, Spande TF, Wisnieski A, Cover JF Jr (1994b) An uptake system for dietary alkaloids in poison frogs (Dendrobatidae). Toxicon 32: 657-663.
34. Daly JW, Garraffo HM, Hall GSE, Cover JF Jr (1997) Absence of skin alkaloids in captive-raised Madagascan mantelline frogs (Mantella) and sequestration of dietary alkaloids. Toxicon 35: 1131-1135.
35. Daly JW, Kaneko T, Wilham J, Garraffo HM, Spande TF, Espinosa A, Donnelly MA (2002) Bioactive alkaloids of frog skin: combinatorial bioprospecting reveals that pumiliotoxins have an arthropod source. Proc Natl Acad Sci USA 99: 13996-14001.
36. Daly JW, Garraffo HM, Spande TF, Clark VC, Ma J, Ziffer H, Cover JF Jr (2003) Evidence for an enantioselective pumiliotoxin 7-hydroxylate in dendrobatid posion frogs of the genus Dendrobates. Proc Natl Acad Sci USA 100: 11092-11097.
37. Daly JW, Wilham JM, Spande TF, Garraffo HM, Gil RR, Silva GL, Vaira M (2007) Alkaloids in bufonid toads (Melanophryniscus): temporal and geographic determinants for two Argentinian species. J Chem Ecol 33: 871-887.
38. Delêtre M, Measey GJ (2004) Sexual selection vs ecological causation in a sexually dimorphic caecilian, Schistometopum thomense (Amphibia Gymnophiona Caeciliidae). Ethol Ecol Evol 16: 243-253.
39. Deligne J, Quennedey A, Blum MS (1981) The enemies and defense mechanisms of termites. In: Hermann HR (ed) Social insects. Academic Press, New York, pp 1-76.
40. Dettner K (1997) Inter- and intraspecific transfer of toxic insect compound cantharidin. In: Dettner K, Bauer G, Völkl W (eds) Vertical food web interactions: evolutionary patterns and driving forces. Springer, Berlin, pp 115-145.
41. Dettner K, Liepert C (1994) Chemical mimicry and camouflage. Annu Rev Entomol 39: 129-154.
42. do Amaral JPS (1999) Lip-curling in redbelly snakes (Storeria occipitomaculata): functional morphology and ecological significance. J Zool 248: 289-293.
43. Duffey SS (1980) Sequestration of plant natural products by insects. Annu Rev Entomol 25: 447-477.
44. Dumbacher JP, Pruett-Jones S (1996) Avian chemical defense. In: Nolan V Jr, Ketterson ED (eds) Current ornithology, vol 13. Plenum Press, New York, pp 137-174.
45. Dumbacher JP, Beehler BM, Spande TF, Garraffo HM, Daly JW (1992) Homobatrachotoxin in the genus Pitohui: chemical defense in birds? Science 258: 799-801.
46. Dumbacher JP, Spande TF, Daly JW (2000) Batrachotoxin alkaloids from passerine birds: a second toxic bird genus (Ifrita kowaldi). Proc Natl Acad Sci USA 97: 12970-12975.
47. Dumbacher JP, Wako A, Derrickson SR, Samuelson A, Spande TF, Daly JW (2004) Melyrid beetles (Choresine): a putative source for the batrachotoxin alkaloids found in poison-dart frogs and toxic passerine birds. Proc Natl Acad Sci USA 101: 15857-15860.
48. Eisner T (2003a) Chemical ecology: can it survive without natural products chemistry? Proc Natl Acad Sci USA 100: 14517-14518.
49. Eisner T (2003b) For love of insects. Belknap Press of Harvard University Press, Cambridge.
50. Eisner T, Berenbaum M (2002) Chemical ecology: missed opportunities? Science 295: 1973.
51. Eisner T, Kriston I, Aneshansley DJ (1976) Defensive behavior of a termite (Nasutitermes exitiosus). Behav Ecol Sociobiol 1: 83-125.
52. Eisner T, Smedley SR, Young DK, Eisner M, Roach B, Meinwald J (1996a) Chemical basis of courtship in a beetle (Neopyrochroa flabellata): cantharidin as "nuptial gift". Proc Natl Acad Sci USA 93: 6499-6503.
53. Eisner T, Smedley SR, Young DK, Eisner M, Roach B, Meinwald J (1996b) Chemical basis of courtship in a beetle (Neopyrochroa flabellata): cantharidin as precopulatory "enticing" agent. Proc Natl Acad Sci USA 93: 6494-6498.
54. Elgar MA, Allan RA (2004) Predatory spider mimics acquire colony-specific cuticular hydrocarbons from their ant model prey. Naturwissenschaften 91: 143-147.
55. Erspamer V (1994) Bioactive secretions of the amphibian integument. In: Heatwole H, Barthalmus GT (eds) Amphibian biology. The integument, vol 1. Surrey Beatty & Sons Pty. Ltd., Chipping Norton, pp 178-350.
56. Feldman CR, Brodie ED Jr, Brodie ED III, Pfrender ME (2009) The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly prey. Proc Natl Acad Sci USA 106: 13415-13420.
57. Feldman CR, Brodie ED Jr, Brodie ED III, Pfrender ME (2012) Constraint shapes convergence in tetrodotoxin-resistant sodium channels of snakes. Proc Natl Acad Sci USA 109: 4556-4561.
58. Fukada H (1959) Biological studies on the snakes. VI. Growth and maturity of Natrix tigrina tigrina (Boie). Bull Kyoto Gakugei Univ Ser B 15: 25-41.
59. Fukada H (1961) Peculiar habits of the Japanese snake, Natrix t. tigrina (Boie). Bull Kyoto Gakugei Univ Ser B 18: 13-16.
60. Gaborieau O, Measey GJ (2004) Termitivore or detritivore? A quantitative investigation into the diet of the East African caecilian Boulengerula taitanus (Amphibia: Gymnophiona: Caeciliidae). Anim Biol 54: 45-56.
61. Gamble T, Daza JD, Colli GR, Vitt LJ, Bauer AM (2011) A new genus of miniaturized and pug-nosed gecko from South America (Sphaerodactylidae: Gekkota). Zool J Linn Soc 163: 1244-1266.
62. Garg AD, Hippargi RV, Gandhare AN (2008) Toad skin-secretions: potent source of pharmacologically and therapeutically significant compounds. Internet J Pharmacol 5. ISSN 1531-2976. doi: 10. 5580/18b6.
63. Garton JD, Mushinsky HR (1979) Integumentary toxicity and unpalatability as an antipredator mechanism in the narrow mouthed toad, Gastrophryne carolinensis. Can J Zool/Rev Can Zool 57: 1965-1973.
64. Geffeney S, Brodie ED Jr, Ruben PC, Brodie ED III (2002) Mechanisms of adaptation in a predator-prey arms race: TTX-resistant sodium channels. Science 297: 1336-1339.
65. Gehlbach FR (1970) Death-feigning and erratic behavior in leptotyphlopid, colubrid, and elapid snakes. Herpetologica 26: 24-34.
66. Gehlbach FR, Baldridge RS (1987) Live blind snakes (Leptotyphlops dulcis) in eastern screech owl (Otus asio) nests: a novel commensalism. Oecologia 71: 560-563.
67. Gehlbach FR, Watkins JF II, Kroll JC (1971) Pheromone trail-following studies of typhlopid, leptotyphlopid, and colubrid snakes. Behaviour 40: 282-294.
68. Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S, Winne CT (2000) The global decline of reptiles, déjà vu amphibians. BioScience 50: 653-666.
69. González ARC, Eisner M, Eisner T (1999) Sexually transmitted chemical defense in a moth (Utetheisa ornatrix). Proc Nat Acad Sci USA 96: 5570-5574.
70. Grant T, Frost DR, Caldwell JP, Gagliardo R, Haddad CFB, Kok PJR, Means DB, Noonan BP, Schargel WE, Wheeler WC (2006) Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bull Am Mus Nat Hist 299: 1-262.
71. Grant T, Colombo P, Verrastro L, Saporito RA (2012) The occurrence of defensive alkaloids in non-integumentary tissues of the Brazilian red-belly toad Melanophryniscus simplex (Bufonidae). Chemoecology 22. doi: 10. 1007/s00049-012-0107-9.
72. Greene HW (1986) Diet and arboreality in the emerald monitor, Varanus prasinus, with comments on the study of adaptation. Fieldiana Zool (ns) 31: 1-12.
73. Greene HW (1988) Antipredator mechanisms in reptiles. In: Gans C, Huey RB (eds) Biology of the reptilia. Ecology B: defense and life history, vol 16. Alan R. Liss, Inc., New York, pp 1-152.
74. Greene HW (1997) Snakes: the evolution of mystery in nature. University of California Press, Berkeley.
75. Greene HW (2005) Organisms in nature as a central focus for biology. Trends Ecol Evol 20: 23-27.
76. Greenwood PG, Mariscal RN (1984) The utilization of cnidarian nematocysts by aeolid nudibranchs: nematocyst maintenance and release in Spurilla. Tissue Cell 16: 719-730.
77. Greenwood PG, Garry K, Hunter A, Jennings M (2004) Adaptable defense: a nudibranch mucus inhibits nematocyst discharge and changes with prey type. Biol Bull Mar Biol Lab Woods Hole 206: 113-120.
78. Gregory PT (2008) Bluffing and waiting: handling effects and post-release immobility in a death-feigning snake (Natrix natrix). Ethology 114: 768-774.
79. Gregory PT, Isaac LA, Griffiths RA (2007) Death feigning by grass snakes (Natrix natrix) in response to human "predators". J Comp Psychol 121: 123-129.
80. Haber M, Cerfeda S, Carbone M, Calado G, Gaspar H, Neves R, Maharajan V, Cimino G, Gavagnin M, Ghiselin MT, Mollo E (2010) Coloration and defense in the nudibranch gastropod Hypselodoris fontandraui. Biol Bull Mar Biol Lab Woods Hole 218: 181-188.
81. Hanifin CT (2010) The chemical and evolutionary ecology of tetrodotoxin (TTX) toxicity in terrestrial vertebrates. Mar Drugs 8: 577-593.
82. Hanifin C, Brodie ED III, Brodie ED Jr (2002) Tetrodotoxin levels of the rough-skin newt, Taricha granulosa, increase in long-term captivity. Toxicon 40: 1149-1153.
83. Hanken J (1985) Morphological novelty in the limb skeleton accompanies miniaturization in salamanders. Science 229: 871-874.
84. Hartmann T, Theuring C, Witte L, Schulz S, Pasteels JM (2003) Biochemical processing of plant acquired pyrrolizidine alkaloids by the neotropical leaf-beetle Platyphora boucardi. Insect Biochem Mol Biol 33: 515-523.
85. Hartmann T, Theuring C, Beuerle T, Bernays EA, Singer MS (2005a) Acquisition, transformation and maintenance of plant pyrrolizidine alkaloids by the polyphagous arctiid Grammia geneura. Insect Biochem Mol Biol 35: 1083-1099.
86. Hartmann T, Theuring C, Beuerle T, Klewer N, Schulz S, Singer MS, Bernays EA (2005b) Specific recognition, detoxification and metabolism of pyrrolizidine alkaloids by the polyphagous arctiid Estigmene acrea. Insect Biochem Mol Biol 35: 391-411.
87. Hermann HR, Blum MS (1981) Defensive mechanisms in the social Hymenoptera. In: Hermann HR (ed) Social insects. Academic Press, New York, pp 77-197.
88. Hess ZJ, Harris RN (2000) Eggs of Hemidactylium scutatum (Caudata: Plethodontidae) are unpalatable to insect predators. Copeia 2000: 597-600.
89. Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Cambridge.
90. Hoso M, Asami T, Hori M (2007) Right-handed snakes: convergent evolution of asymmetry for functional specialization. Biol Lett 3: 169-173.
91. How RA, Dell J, Wellington BD (1986) Comparative biology of eight species of Diplodactylus gecko in Western Australia. Herpetologica 42: 471-482.
92. Hunt RH (1980) Toad sanctuary in a tarantula burrow. Nat Hist 89: 48-53.
93. Hutchinson DA, Mori A, Savitzky AH, Burghardt GM, Wu X, Meinwald J, Schroeder FC (2007) Dietary sequestration of defensive steroids in nuchal glands of the Asian snake Rhabdophis tigrinus. Proc Natl Acad Sci USA 104: 2265-2270.
94. Hutchinson DA, Savitzky AH, Mori A, Meinwald J, Schroeder FC (2008) Maternal provisioning of sequestered defensive steroids by the Asian snake Rhabdophis tigrinus. Chemoecology 18: 181-190.
95. Hutchinson DA, Savitzky AH, Mori A, Burghardt GM, Meinwald J, Schroeder FC (2012) Chemical investigations of defensive steroid sequestration by the Asian snake Rhabdophis tigrinus. Chemoecology 22. doi: 10. 1007/s00049-011-0078-2.
96. Jaksic FM, Fuentes ER, Yáñez JL (1979) Two types of adaptation of vertebrate predators toward their prey. Arch Biol Med Exp 12: 143-152.
97. Jared C, Navas CA, Toledo RC (1999) An appreciation of the physiology and morphology of the caecilians (Amphibia: Gymnophiona). Comp Biochem Physiol A Mol Integr Physiol 123A: 313-328.
98. Jones TH, Blum MS, Robertson HG (1990) Novel dialkylpiperidine in the venom of the ant Monomorium delagoense. J Nat Prod 53: 429-435.
99. Jones TH, Torres JA, Spande TF, Garraffo HM, Blum MS, Snelling RR (1996) Chemistry of venom alkaloids in some Solenopsis (Diplorhoptrum) species from Puerto Rico. J Chem Ecol 22: 1221-1236.
100. Jones TH, Flournoy RC, Torres JA, Snelling RR, Spande TF, Garraffo HM (1999a) 3-Methyl-4-phenylpyrrole from the ants Anochetus kempfi and Anochetus mayri. J Nat Prod 62: 1343-1345.
101. Jones TH, Gorman JST, Snelling RR, Delabie JHC, Blum MS, Garraffo HM, Jain P, Daly JW, Spande TF (1999b) Further alkaloids common to ants and frogs: Decahydroquinolines and a quinolizidine. J Chem Ecol 25: 1179-1193.
102. Jordan R Jr (1970) Death-feigning in a captive red-bellied snake, Storeria occipitomaculata (Storer). Herpetologica 26: 466-468.
103. Karasov WH, Martínez del Rio C (2007) Physiological ecology: how animals process energy, nutrients, and toxins. Princeton University Press, Princeton.
104. Karunarathna DMSS, Amarasinghe AAT (2009) Mutualism in Ramanella nagaoi Manamendra-Arachchi & Pethiyagoda, 2001 (Amphibia: Microhylidae) and Poecilotheria species (Aracnida [sic]: Thereposidae [sic]) from Sri Lanka. Taprobanica 1: 16-18.
105. Kingdon J, Agwanda B, Kinnaird M, O'Brien T, Holland C, Gheysens T, Boulet-Audet M, Vollrath F (2011) A poisonous surprise under the coat of the African crested rat. Proc R Soc Lond Ser B Biol Sci 279: 675-680.
106. Kley NJ (2001) Prey transport mechanisms in blindsnakes and the evolution of unilateral feeding systems in snakes. Am Zool 41: 1321-1337.
107. La Marca E, Lips KR, Lötters S, Puschendorf R, Ibáñez R, Rueda-Almonacid JV, Schulte R, Marty C, Castro F, Manzanilla-Puppo J, García-Pérez JE, Bolaños F, Chaves G, Pounds JA, Toral E, Young BE (2005) Catastrophic population declines and extinctions in Neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica 37: 190-201.
108. Larson A, Losos JB (1996) Phylogenetic systematics of adaptation. In: Rose MR, Lauder GV (eds) Adaptation. Academic Press, San Diego, pp 187-220.
109. Lee JC (1996) The amphibians and reptiles of the Yucatán Peninsula. Comstock Publ. Assoc., Cornell Univ. Press, Ithaca.
110. Lehman EM, Brodie ED Jr, Brodie ED III (2004) No evidence for an endosymbiotic bacterial origin of tetrodotoxin in the newt Taricha granulosa. Toxicon 44: 243-249.
111. Lenoir A, D'Ettorre P, Errard C, Hefetz A (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46: 573-599.
112. Leonard WP, Stebbins RC (1999) Observations of antipredator tactics of the sharp-tailed snake (Contia tenuis). Northwest Nat 80: 74-77.
113. Licht LE, Low B (1968) Cardiac response of snakes after ingestion of toad parotoid venom. Copeia 1968: 547-551.
114. Lindstedt C, Huttunen H, Kakko M, Mappes J (2011) Disentangling the evolution of weak warning signals: high detection risk and low production costs of chemical defences in gregarious pine sawfly larvae. Evol Ecol 25: 1029-1046.
115. Lydeard C, Cowie RH, Ponder WF, Bogan AE, Bouchet P, Clark SA, Cummings KS, Frest TJ, Gargominy O, Herbert DG, Hersheler R, Peres KE, Roth B, Seddon M, Strong EE, Thompson FG (2004) The global decline of nonmarine mollusks. BioScience 54: 321-330.
116. Marks MJ, Laverty DS, Whiteaker P, Salminen O, Grady SR, McIntosh JM, Collins AC (2010) John Daly's compound, epibatidine, facilitates identification of nicotinic receptor subtypes. J Mol Neurosci 40: 96-104.
117. McClintock JB, Baker BJ (2001) Marine chemical ecology. CRC Press, Boca Raton.
118. McDowell SB (1974) A catalogue of the snakes of New Guinea and the Solomons, with special reference to those in the Bernice P. Bishop Museum, Part I. Scolecophidia. J Herpetol 8: 1-57.
119. McPhail KL, Davies-Coleman MT, Starmer J (2001) Sequestered chemistry of the arminacean nudibranch Leminda millecra in Algoa Bay, South Africa. J Nat Prod 64: 1183-1190.
120. Measey GJ, Gower DJ, Oommen OV, Wilkinson M (2004) A subterranean generalist predator: diet of the soil-dwelling caecilian Gegeneophis ramaswamii (Amphibia; Gymnophiona; Caeciliidae) in southern India. C R Biol 327: 65-76.
121. Mebs D (2001) Toxicity in animals. Trends in evolution? Toxicon 39: 87-96.
122. Meinwald J, Eisner T (1995) The chemistry of phyletic dominance. In: Eisner T, Meinwald J (eds) Chemical ecology: the chemistry of biotic interaction. National Academy Press, Washington, DC, pp 29-40.
123. Meinwald J, Eisner T (2003) Natural products chemistry: new opportunities, uncertain future. Helv Chim Acta 86: 3633-3637.
124. Meinwald J, Prestwich GD, Nakanishi K, Kubo I (1978) Chemical ecology: studies from East Africa. Science 199: 1167-1173.
125. Melville J, Schulte JA II, Larson A (2004) A molecular study of phylogenetic relationships and evolution of antipredator strategies in Australian Diplodactylus geckos, subgenus Strophurus. Biol J Linn Soc 82: 123-138.
126. Miyatake T, Katayama K, Takeda Y, Nakashima A, Sugita A, Mizumoto M (2004) Is death-feigning adaptive? Heritable variation in fitness difference of death-feigning behavior. Proc R Soc Lond Ser B Biol Sci 271: 2293-2296.
127. Mori A (2004) Another "poisonous" gland in snakes: function, ultrastructure, and physiology of the nuchal glands of Rhabdophis tigrinus (in Japanese). Bull Herp Soc Jpn 2004: 29-33.
128. Mori A, Moriguchi H (1988) Food habits of snakes in Japan: a critical review. Snake 20: 98-113.
129. Mori A, Burghardt GM, Savitzky AH, Roberts KA, Hutchinson DA, Goris RC (2012) Nuchal glands: a novel defensive system in snakes. Chemoecology 22. doi: 10. 1007/s00049-011-0086-2.
130. Morin PJ (1999) Community ecology. Blackwell Science, Inc., Malden.
131. Mutoh A (1983) Death-feigning behavior of the Japanese colubrid snake Rhabdophis tigrinus. Herpetologica 39: 78-80.
132. Myers CW, Daly JW, Malkin B (1978) A dangerously toxic new frog (Phyllobates) used by Emberá Indians of western Colombia, with discussion of blowgun fabrication and dart poisoning. Bull Am Mus Nat Hist 161: 307-365.
133. Nagnan P, Clement JL (1990) Terpenes from the maritime pine Pinus pinaster: toxins for subterranean termites of the genus Reticulitermes (Isoptera: Rhinotermitidae)? Biochem Syst Ecol 18: 13-16.
134. Nishikawa KC, Kier WM, Smith KK (1999) Morphology and mechanics of tongue movement in the African pig-nosed frog Hemisus marmoratum: a muscular hydrostatic model. J Exp Biol 202: 771-780.
135. Nussbaum RA, Wilkinson M (1989) On the classification and phylogeny of the caecilians (Amphibia: Gymnophiona), a critical review. Herpetol Monogr 3: 1-42.
136. Opitz SEW, Müller C (2009) Plant chemistry and insect sequestration. Chemoecology 19: 117-154.
137. Ovaska K, Engelstoft C (1999) Contia tenuis (sharp-tailed snake). Defensive behavior. Herpetol Rev 30: 168.
138. Pasteels JM, Grégoire J-C, Rowell-Rahier M (1983) The chemical ecology of defense in arthropods. Annu Rev Entomol 28: 263-289.
139. Paul VJ, Cruz-Rivera E, Thacker RW (2001) Chemical mediation of macroalgal-herbivore interactions: ecological and evolutionary perspectives. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 227-265.
140. Pearce MJ (1997) Termites: biology and pest management. CAB International, Oxon.
141. Phillips BL, Brown GP, Shine R (2003) Assessing the potential impact of cane toads on Australian snakes. Conserv Biol 17: 1738-1747.
142. Pianka ER, Parker WS (1975) Ecology of horned lizards: a review with special reference to Phrynosoma platyrhinos. Copeia 1975: 141-162.
143. Pianka ER, Pianka HD (1976) Comparative ecology of twelve species of nocturnal lizards (Gekkonidae) in the Western Australian desert. Copeia 1976: 125-142.
144. Pianka ER, Pianka HD (2000) The ecology of Moloch horridus (Lacertilia: Agamidae) in Western Australia. Copeia 1970: 90-103.
145. Pianka ER, Vitt LJ (2003) Lizards: windows to the evolution of diversity. University of California Press, Berkeley.
146. Piek T (1986) Venoms of the Hymenoptera: biochemical, pharmacological and behavioural aspects. Academic Press, London.
147. Platt DR (1969) Natural history of the hognose snakes Heterodon platyrhinos and Heterodon nasicus. Univ Kansas Publ, Mus Nat Hist 18: 253-420.
148. Polis GA, Winemiller KO (1996) Food webs: integration of patterns & dynamics. Chapman & Hall, New York.
149. Pough FH, Taigen T (1990) Metabolic correlates of the foraging and social behaviour of dart-poison frogs. Anim Behav 39: 145-155.
150. Prestwich GD (1979) Chemical defense by termite soldiers. J Chem Ecol 5: 459-480.
151. Prestwich GD (1988) The chemicals of termite societies (Isoptera). Sociobiology 14: 175-191.
152. Pyron RA, Burbrink FT, Colli GR, Montes de Oca AN, Vitt LJ, Kuczynski CA, Wiens JJ (2011) The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Mol Phylogenet Evol 58: 329-342.
153. Quintana A, Reinhard J, Faure R, Uva P, Bagnères A-G, Massiot G, Clément J-L (2003) Interspecific variation in terpenoid composition of defensive secretions of European Reticulitermes termites. J Chem Ecol 29: 639-652.
154. Radhakrishnan C, Gopi KC, Palot MJ (2007) Extension of range of distribution of Nasikabatrachus sahyadrensis Biju & Bossuyt (Amphibia: Anura: Nasikabatrachidae) along Western Ghats, with some insights into its bionomics. Curr Sci 92: 213-216.
155. Rasmussen S, Young B, Krimm H (2009) On the "spitting" behaviour in cobras (Serpentes: Elapidae). J Zool 237: 27-35.
156. Raspotnig G, Norton RA, Heethoff M (2011) Oribatid mites and skin alkaloids in poison frogs. Biol Lett 7: 555-556.
157. Richardson KC, Hinchliffe PM (1983) Caudal glands and their secretions in the western spiny-tailed gecko, Diplodactylus spinigerus. Copeia 1983: 161-169.
158. Rodríguez A, Poth D, Schulz S, Vences M (2011) Discovery of skin alkaloids in a miniaturized eleutherodactylid frog from Cuba. Biol Lett 7: 414-418.
159. Roitberg BD, Isman MB (eds) (1992) Insect chemical ecology: an evolutionary approach. Chapman & Hall, New York.
160. Rosenberg HI, Russell AP (1980) Structural and functional aspects of tail squirting: a unique defense mechanism of Diplodactylus (Reptilia: Gekkonidae). Can J Zool/Rev Can Zool 58: 865-881.
161. Rosenthal GA, Berenbaum MR (eds) (1991) Herbivores: their interactions with secondary plant metabolites. Academic Press, New York.
162. Sabelis MW, van Baalen M, Bakker FM, Bruin J, Drukker B, Egas M, Janssen ARM, Lesna IK, Pels B, van Rijn PCJ, Scutareanu P (1999) The evolution of direct and indirect defence against herbivorous arthropods. In: Olff H, Brown VK, Drent RH (eds) Herbivores: between plants and predators. Blackwell Science, Malden, pp 109-166.
163. Santos R, Grant T (2011) Diel pattern of migration in a poisonous toad from Brazil and the evolution of chemical defenses in diurnal amphibians. Evol Ecol 25: 249-258.
164. Saporito RA, Donnelly MA, Hoffman RL, Garraffo HM, Daly JW (2003) A siphonotid millipede (Rhinotus) as the source of spiropyrrolizidine oximes of dendrobatid frogs. J Chem Ecol 29: 2781-2786.
165. Saporito RA, Garraffo HM, Donnelly MA, Edwards AL, Longino JT, Daly JW (2004) Formicine ants: an arthropod source for the pumiliotoxin alkaloids of dendrobatid poison frogs. Proc Natl Acad Sci USA 101: 8045-8050.
166. Saporito RA, Donnelly MA, Garraffo HM, Spande TF, Daly JW (2006) Geographic and seasonal variation in alkaloid-based chemical defenses of Dendrobates pumilio from Bocas del Toro, Panama. J Chem Ecol 32: 795-814.
167. Saporito RA, Donnelly MA, Norton RA, Garraffo HM, Spande TF, Daly JW (2007a) Oribatid mites as a major dietary source for alkaloids in poison frogs. Proc Natl Acad Sci USA 104: 8885-8890.
168. Saporito RA, Zuercher R, Roberts M, Gerow KG, Donnelly MA (2007b) Experimental evidence for aposematism in the dendrobatid poison frog Oophaga pumilio. Copeia 2007: 1006-1011.
169. Saporito RA, Isola M, Maccachero VC, Condon K, Donnelly MA (2010) Ontogenetic scaling of poison glands in a dendrobatid poison frog. J Zool 282: 238-245.
170. Saporito RA, Donnelly MA, Spande TF, Garraffo HM (2012) A review of chemical ecology in poison frogs. Chemoecology 22. doi: 10. 1007/s00049-011-0088-0.
171. Savage JM (2002) The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. University of Chicago Press, Chicago.
172. Savitzky AH (1983) Coadapted character complexes among snakes: fossoriality, piscivory, and durophagy. Am Zool 23: 397-409.
173. Schmidly DJ (2005) What it means to be a naturalist and the future of natural history at American universities. J Mammal 86: 449-456.
174. Schneider D, Boppré M, Zweig J, Horsley SB, Bell TW, Meinwald J, Hansen K, Diehl EW (1982) Scent organ development in Creatonotos moths: regulation by pyrrolizidine alkaloids. Science 215: 1264-1265.
175. Schroeder FC, Gonzàlez A, Eisner T, Meinwald J (1999) Miriamin, a defensive diterpene from the eggs of a land slug (Arion sp.). Proc Natl Acad Sci USA 96: 13620-13625.
176. Schwartz ENF, Schwartz CA, Sebben A, Largura SWR, Mendes EG (1999) Indirect cardiotoxic activity of the caecilian Siphonops paulensis (Gymnophiona, Amphibia) skin secretion. Toxicon 37: 47-54.
177. Schwenk K, Padilla DK, Bakken GS, Full RJ (2009) Grand challenges in organismal biology. Integr Comp Biol 49: 7-14.
178. Sherbrooke WC, Middendorf GA III (2001) Blood-squirting variability in horned lizards (Phrynosoma). Copeia 2001: 1114-1122.
179. Sherbrooke WC, Middendorf GA III (2004) Responses of kit foxes (Vulpes macrotis) to antipredator blood-squirting and blood of Texas horned lizards (Phrynosoma cornutum). Copeia 2004: 652-658.
180. Shine R, Webb JK (1990) Natural history of Australian typhlopid snakes. J Herpetol 24: 357-363.
181. Siliwal M, Ravichandran B (2008) Commensalism in microhylid frogs and mygalomorph spiders. Zoos' Print 23: 13.
182. Smith BP, Tyler MJ, Kaneko T, Garraffo HM, Spande TF, Daly JW (2002) Evidence for biosynthesis of pseudophrynamine alkaloids by an Australian myobatrachid frog (Pseudophryne) and for sequestration of dietary pumiliotoxins. J Nat Prod 65: 439-447.
183. 13C NMR in their conformational analysis. J Nat Prod 62: 5-21.
184. Stuble KL, Kirkman LK, Carroll CR (2009) Patterns of abundance of fire ants and native ants in a native ecosystem. Ecol Entomol 34: 520-526.
185. Takeuchi H, Ota H, Oh H-S, Hikida T (2012) Extensive genetic divergence in the East Asian natricine snake, Rhabdophis tigrinus (Serpentes: Colubridae), with special reference to prominent geographical differentiation of the mitochondrial cytochrome b gene in Japanese populations. Biol J Linn Soc 105: 395-408.
186. Thompson JN (1982) Interaction and coevolution. Wiley-Interscience, New York.
187. Tokuyama T, Daly JW (1983) Steroidal alkaloids (batrachotoxins and 4β-hydroxybatrachotoxins), "indole alkaloids" (calycanthine and chimonanthine) and a piperidinyldipyridine alkaloid (noranabasamine) in skin extracts from the Colombian poison-dart frog Phyllobates terribilis (Dendrobatidae). Tetrahedron 39: 41-47.
188. Tsuneoka Y, Akino T (2012) Chemical camouflage of the slave-making ant Polyergus samurai queen in the process of host colony usurpation (Hymenoptera: Formicidae). Chemoecology 22: 89-99.
189. Vences M, Glaw F, Böhme W (1998) Evolutionary correlates of microphagy in alkaloid-containing frogs (Amphibia: Anura). Zool Anz 236: 217-230.
190. Vences M, Schulz S, Poth D, Rodriguez A (2011) Defining frontiers in mite and frog alkaloid research. Biol Lett 7: 557.
191. Vidal N, Marin J, Morini M, Donnellan S, Branch WR, Thomas R, Vences M, Wynn A, Cruaud C, Hedges SB (2010) Blindsnake evolutionary tree reveals long history on Gondwana. Biol Lett 6: 558-561.
192. Walker CH, Hopkin SP, Sibly RM, Peakall DB (2001) Principles of ecotoxicology. Taylor & Francis, New York.
193. Watkins JF II, Gehlbach FR, Kroll JC (1969) Attractant-repellent secretions of blind snakes (Leptotyphlops dulcis) and their army ant prey (Neivamyrmex nigrescens). Ecology 50: 1098-1102.
194. Webb JK, Shine R (1992) To find an ant: trail-following in Australian blindsnakes (Typhlopidae). Anim Behav 43: 941-948.
195. Webb JK, Shine R, Branch WR, Harlow PS (2000) Life-history strategies in basal snakes: reproduction and dietary habits of the African thread snake Leptotyphlops scutifrons (Serpentes: Leptotyphlopidae). J Zool 250: 321-327.
196. Webb JK, Branch WR, Shine R (2001) Dietary habits and reproductive biology of typhlopid snakes from southern Africa. J Herpetol 35: 558-567.
197. Weldon PJ, Carroll JF (2007) Vertebrate chemical defense: secreted and topically acquired deterrents of arthropods. In: Debbou M, Frences SP, Strickman D (eds) Insect repellents: principles, methods, and uses. CRC Press, Boca Raton.
198. Weldon PJ, Rappole JH (1997) A survey of birds odorous or unpalatable to humans: possible indications of chemical defense. J Chem Ecol 23: 2609-2633.
199. Weldon PJ, Flachsbarth B, Schulz S (2008) Natural products from the integument of nonavian reptiles. Nat Prod Rep 25: 738-756.
200. Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, Chicago.
201. Whiles MR, Lips KR, Pringle CM, Kilham SS, Bixby RJ, Brenes R, Connelly S, Colon-Gaud JC, Hinte-Brown M, Huryn AD, Montgomery C, Peterson S (2006) The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems. Front Ecol Environ 4: 27-34.
202. Whitman DW, Blum MS, Jones CG (1985) Chemical defense in Taeniopoda eques (Orthoptera: Acrididae): role of the metathoracic secretion. Ann Entomol Soc Am 78: 451-455.
203. Wiggins PJ, Smith JM, Harris RN, Minbiole KPC (2011) Gut of red-backed salamanders (Plethodon cinereus) may serve as a reservoir for an antifungal cutaneous bacterium. J Herpetol 45: 329-332.
204. Williams BL (2010) Behavioral and chemical ecology of marine organisms with respect to tetrodotoxin. Mar Drugs 8: 381-398.
205. Williams BL, Brodie ED Jr, Brodie ED III (2004) A resistant predator and its toxic prey: persistence of newt toxin leads to poisonous (not venomous) snakes. J Chem Ecol 30: 1901-1919.
206. Williams BL, Hanifin CT, Brodie ED Jr, Brodie ED III (2012) Predators usurp prey defenses? Toxicokinetics of tetrodotoxin in common garter snakes after consumption of rough-skinned newts. Chemoecology 22. doi: 10. 1007/s00049-011-0093-3.
207. Yanosky AA, Chani JM (1988) Possible dual mimicry of Bothrops and Micrurus by the colubrid, Lystrophis dorbignyi. J Herpetol 22: 222-224.
208. Zaher H, Grazziotin FG, Cadle JE, Murphy RW, de Moura-Leite JC, Bonatto SL (2009) Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American xenodontines: a revised classification and descriptions of new taxa. Pap Avuls Zool 49: 115-153.
209. Zhu F, Qin C, Tao L, Liu X, Shi Z, Ma X, Jia J, Tan Y, Cui C, Lin J, Tan C, Jiang Y, Chen Y (2011) Clustered patterns of species origins of nature-derived drugs and clues for future bioprospecting. Proc Natl Acad Sci USA 108: 12943-12948.