Evolutionary Ecology

, Volume 27, Issue 5, pp 863–881 | Cite as

Does chemical defence increase niche space? A phylogenetic comparative analysis of the Musteloidea

  • Kevin ArbuckleEmail author
  • Michael Brockhurst
  • Michael P. Speed
Original Paper


Avoidance of predation can impose opportunity costs on prey species that use behavioural avoidance strategies to evade detection. An animal that spends much time hiding or remaining immobile, for example, may have less time for other important activities such as foraging or finding mates. Here we examine the idea that the evolution of chemical defence may act to release prey from these constraints, freeing defended prey to exploit their habitats more effectively, and increasing their niche space. We tested this hypothesis using comparative methods on a mammal group containing both chemically defended and non-defended species: Musteloidea. We found that defended species had a more omnivorous diet and were more likely to be active during both day and night than non-defended species. We also found that chemically defended species were less likely to be strictly diurnal or to show sexual size dimorphism, and had earlier maturing females and a shorter lifespan than non-defended species. Taken together, our results support the hypothesis that chemical defence increases the niche space available to a species. More generally, this also supports recent suggestions that strategies taken to avoid natural enemies can have important effects on diverse components of life history.


Ecological opportunity Antipredator mechanisms Behavioural constraints Natural enemies 



We thank Ted Garland for kindly providing the Matlab programs used herein. M.P.S. thanks Andrew Higginson (University of Bristol) for preliminary help with comparative methods. We also thank Tim Caro for valuable discussions and two anonymous reviewers for valuable comments on the manuscript. This work was funded by a NERC Doctoral Training Grant to K.A.

Supplementary material

10682_2013_9629_MOESM1_ESM.doc (296 kb)
Supplementary material 1 (DOC 296 kb)


  1. Abrahams MV (1995) The interaction between antipredator behaviour and antipredator morphology: experiments with fathead minnows and brook sticklebacks. Can J Zool 73:2209–2215CrossRefGoogle Scholar
  2. Agnarsson I, Kuntner M, May-Collado LJ (2010) Dogs, cats, and kin: a molecular species-level phylogeny of Carnivora. Mol Phylogenet Evol 54:726–745PubMedCrossRefGoogle Scholar
  3. Bendt RR, Auerbach PS (1991) Foreign body reaction following stingray envenomation. J Wilderness Med 2:298–303CrossRefGoogle Scholar
  4. Bininda-Emonds ORP, Gittleman JL, Purvis A (1999) Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biol Rev 74:143–175PubMedCrossRefGoogle Scholar
  5. Blanco MA, Sherman PW (2005) Maximum longevities of chemically protected and non-protected fishes, reptiles, and amphibians support evolutionary hypotheses of aging. Mech Ageing Dev 126:794–803PubMedCrossRefGoogle Scholar
  6. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745PubMedGoogle Scholar
  7. Blount JD, Speed MP, Ruxton GD, Stephens PA (2009) Warning displays may function as honest signals of toxicity. Proc R Soc Lond B Biol Sci 276:871–877CrossRefGoogle Scholar
  8. Bonacci T, Aloise G, Brandmayr P, Brandmayr TZ, Capula M (2008) Testing the predatory behaviour of Podarcis sicula (Reptilia: Lacertidae) towards aposematic and non-aposematic preys. Amphibia Reptilia 29:449–453CrossRefGoogle Scholar
  9. Bosher BT, Newton SH, Fine ML (2006) The spines of the channel catfish, Ictalurus punctatus, as an anti-predator adaptation: an experimental study. Ethology 112:188–195CrossRefGoogle Scholar
  10. Bowers MD (1993) Aposematic caterpillars: life-styles of the warningly colored and unpalatable. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman and Hall, New York, USA, pp 331–371Google Scholar
  11. Burns KJ (1998) A phylogenetic perspective on the evolution of sexual dichromatism in tanagers (Thraupidae): the role of female versus male plumage. Evolution 52:1219–1224CrossRefGoogle Scholar
  12. Burton M (1976) Guide to the mammals of Britain and Europe. Elsevier Phaidon, Oxford, UKGoogle Scholar
  13. Caro T (2005a) Antipredator defenses in birds and mammals. University Chicago Press, Chicago, ILGoogle Scholar
  14. Caro T (2005b) The adaptive significance of coloration in mammals. Bioscience 55:125–136CrossRefGoogle Scholar
  15. Chanin P (1985) The natural history of otters. Croom Helm, LondonGoogle Scholar
  16. Chiari Y, Vences M, Vieites DR, Rabemananjara F, Bora P, Ravoahangimalala OR, Meyer A (2004) New evidence for parallel evolution of colour patterns in Malagasy poison frogs (Mantella). Mol Ecol 13:3763–3774PubMedCrossRefGoogle Scholar
  17. Clark TW, Anderson E, Douglas C, Strickland M (1987) Martes americana. Mamm Species 289:1–8CrossRefGoogle Scholar
  18. Cooper WE, Sherbrooke WC (2010) Crypsis influences escape decisions in the round-tailed horned lizard (Phrynosoma modestum). Can J Zool 88:1003–1010CrossRefGoogle Scholar
  19. Corbet GB, Southern HN (1977) The handbook of British mammals, 2nd edn. Blackwell Scientific Publications, Oxford, UKGoogle Scholar
  20. Darst CR, Menéndez-Guerrero PA, Coloma LA, Cannatella DC (2005) Evolution of dietary specialization and chemical defense in poison frogs (Dendrobatidae): a comparative analysis. Am Nat 165:56–69PubMedCrossRefGoogle Scholar
  21. Del Cerro I, Marmi J, Ferrando A, Chashchin P, Taberlet P, Bosch M (2010) Nuclear and mitochondrial phylogenies provide evidence for four species of Eurasian badgers (Carnivora). Zool Scr 39:415–425CrossRefGoogle Scholar
  22. Dragoo JW, Sheffield SR (2009) Conepatus leuconotus. Mamm Species 827:1–8CrossRefGoogle Scholar
  23. Dunstone W (1993) The mink. T&AD Poyser, London, UKGoogle Scholar
  24. Eizirik E, Murphy WJ, Koepfli KP, Johnson WE, Dragoo JW, Wayne RK, O’Brien SJ (2010) Pattern and timing of diversification of the mammalian order Carnivora inferred from multiple nuclear gene sequences. Mol Phylogenet Evol 56:49–63PubMedCrossRefGoogle Scholar
  25. Endler JA (1986) Defense against predators. In: Feder ME, Lauder GV (eds) Predator-prey relationships: perspectives and approaches from the study of lower vertebrates. University Chicago Press, Chicago, IL, pp 109–134Google Scholar
  26. Estes RD (1991) The behavior guide to African mammals: including hoofed mammals, carnivores, primates. University California Press, Berkeley, CAGoogle Scholar
  27. Faulkner DJ, Ghiselin MT (1983) Chemical defense and evolutionary ecology of dorid nudibranchs and some other opisthobranch gastropods. Mar Ecol Prog Ser 13:295–301CrossRefGoogle Scholar
  28. Ford LS, Hoffmann RS (1988) Potos flavus. Mamm Species 321:1–9CrossRefGoogle Scholar
  29. Gardezi T (1997) A comparative study of species diversity in relation to body size in carnivores (Mammalia: Carnivora). MSc thesis, Laurentian University, Ontario, CanadaGoogle Scholar
  30. Gompper ME (1995) Nasua narica. Mamm Species 487:1–10CrossRefGoogle Scholar
  31. Gompper ME, Decker DM (1998) Nasua nasua. Mamm Species 580:1–9CrossRefGoogle Scholar
  32. Götmark F, Unger U (1994) Are conspicuous birds unprofitable prey? Field experiments with hawks and stuffed prey species. Auk 111:251–262CrossRefGoogle Scholar
  33. Guilford T (1988) The evolution of conspicuous coloration. Am Nat 131:S7–S21CrossRefGoogle Scholar
  34. Haddad V, de Souza RA, Auerbach PS (2008) Marine catfish sting causing fatal heart perforation in a fisherman. Wilderness Environ Med 19:114–118PubMedCrossRefGoogle Scholar
  35. Hanlon RT, Forsythe JW, Joneschild DE (1999) Crypsis, conspicuousness, mimicry and polyphenism as antipredator defences of foraging octopuses on Indo-Pacific coral reefs, with a method of quantifying crypsis from video tapes. Biol J Linn Soc 66:1–22CrossRefGoogle Scholar
  36. Helgen KM, Kays R, Helgen LE, Tsuchiya-Jerep MTN, Pinto CM, Koepfli K-P, Eizirik E, Maldonado JE (2009) Taxonomic boundaries and geographic distributions revealed by an integrative systematic overview of the mountain coatis, Nasuella (Carnivora: Procyonidae). Small Carnivore Conserv 41:65–74Google Scholar
  37. Higginson AD, Delf J, Ruxton GD, Speed MP (2011) Growth and reproductive costs of larval defence in the aposematic lepidopteran Pieris brassicae. J Anim Ecol 80:384–392PubMedCrossRefGoogle Scholar
  38. Hillman CN, Clark TW (1980) Mustela nigripes. Mamm Species 126:1–3CrossRefGoogle Scholar
  39. Hwang YT, Larivière S (2001) Mephitis macroura. Mamm Species 686:1–3CrossRefGoogle Scholar
  40. Hwang YT, Larivière S (2003) Mydaus javanensis. Mamm Species 723:1–3CrossRefGoogle Scholar
  41. Hwang YT, Larivière S (2004) Mydaus marchei. Mamm Species 757:1–3CrossRefGoogle Scholar
  42. Inbar M, Lev-Yadun S (2005) Conspicuous and aposematic spines in the animal kingdom. Naturwissenschaften 92:170–172PubMedCrossRefGoogle Scholar
  43. Ives AR, Garland T (2010) Phylogenetic logistic regression for binary dependent variables. Syst Biol 59:9–26PubMedCrossRefGoogle Scholar
  44. Kingdon J (1977) East African mammals: an atlas of evolution in Africa, vol 3 part A. Academic Press, LondonGoogle Scholar
  45. Lakshmanan P, Roy S, Fairclough JA (2004) Management of crown-of-thorns starfish injury. Foot Ankle Surg 10:155–157CrossRefGoogle Scholar
  46. Larivière S (1998) Lontra felina. Mamm Species 575:1–5Google Scholar
  47. Larivière S (1999a) Mustela vison. Mamm Species 608:1–9Google Scholar
  48. Larivière S (1999b) Lontra longicaudis. Mamm Species 609:1–5Google Scholar
  49. Larivière S (2002a) Ictonyx striatus. Mamm Species 698:1–5CrossRefGoogle Scholar
  50. Larivière S (2002b) Lutra maculicollis. Mamm Species 712:1–6CrossRefGoogle Scholar
  51. Larivière S, Walton LR (1998) Lontra canadensis. Mamm Species 587:1–8Google Scholar
  52. Lavin SR, Karasov WH, Ives AR, Middleton KM, Garland T (2008) Morphometrics of the avian small intestine compared with that of nonflying mammals: a phylogenetic approach. Physiol Biochem Zool 81:526–550PubMedCrossRefGoogle Scholar
  53. Lindstedt C, Lindström L, Mappes J (2008) Hairiness and warning colours as components of antipredator defence: additive or interactive benefits? Anim Behav 75:1703–1713CrossRefGoogle Scholar
  54. Long CA (1973) Taxidea taxus. Mamm Species 26:1–4CrossRefGoogle Scholar
  55. Lotze J-H, Anderson S (1979) Procyon lotor. Mamm Species 119:1–8CrossRefGoogle Scholar
  56. Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis, version 2.75.
  57. Marmi J, López-Giráldez JF, Domingo-Roura X (2004) Phylogeny, evolutionary history and taxonomy of the Mustelidae based on sequences of the cytochrome b gene and a complex repetitive flanking region. Zool Scr 33:481–499CrossRefGoogle Scholar
  58. Merilaita S, Tullberg BS (2005) Constrained camouflage facilitates the evolution of conspicuous warning coloration. Evolution 59:38–45PubMedGoogle Scholar
  59. Moors PJ (1980) Sexual dimorphism in the body size of mustelids (Carnivora): the roles of food habits and breeding systems. Oikos 34:147–158CrossRefGoogle Scholar
  60. Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405CrossRefGoogle Scholar
  61. Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045CrossRefGoogle Scholar
  62. Neal E, Cheeseman C (1996) Badgers. T&AD Poyser, LondonGoogle Scholar
  63. Nilsson M, Forsman A (2003) Evolution of conspicuous coloration, body size and gregariousness: a comparative analysis of lepidopteran larvae. Evol Ecol 17:51–66CrossRefGoogle Scholar
  64. Nyakatura K, Bininda-Emonds ORP (2012) Updating the evolutionary history of Carnivora (Mammalia): a new species-level supertree complete with divergence time estimates. BMC Biol 10:12PubMedCrossRefGoogle Scholar
  65. Ortolani A (1999) Spots, stripes, tail tips and dark eyes: predicting the function of carnivore colour patterns using the comparative method. Biol J Linn Soc 67:433–476CrossRefGoogle Scholar
  66. Pagel M (1994) Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc R Soc Lond B Biol Sci 255:37–45CrossRefGoogle Scholar
  67. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884PubMedCrossRefGoogle Scholar
  68. Pagel M, Meade A (2006) Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am Nat 167:808–825PubMedCrossRefGoogle Scholar
  69. Pasitschniak-Arts M, Larivière S (1995) Gulo gulo. Mamm Species 499:1–10Google Scholar
  70. Pearson DL (1985) The function of multiple anti-predator mechanisms in adult tiger beetles (Coleoptera: Cicindelidae). Ecol Entomol 10:65–72CrossRefGoogle Scholar
  71. Perneger TV (1998) What’s wrong with Bonferroni adjustments. Br Med J 316:1236–1238CrossRefGoogle Scholar
  72. Poglayen-Neuwall I, Toweill DE (1988) Bassariscus astutus. Mamm Species 327:1–8CrossRefGoogle Scholar
  73. Pomini AM, Machado G, Pinto-da-Rocha R, Macías-Ordóñez R, Marsaioli AJ (2010) Lines of defense in the harvestman Hoplobunus mexicanus (Arachnida: Opiliones): aposematism, stridulation, thanatosis, and irritant chemicals. Biochem Syst Ecol 38:300–308CrossRefGoogle Scholar
  74. Powell RA (1981) Martes pennanti. Mamm Species 156:1–6Google Scholar
  75. Prange S, Prange TJ (2009) Bassaricyon gabbii. Mamm Species 826:1–7CrossRefGoogle Scholar
  76. Przeczek K, Mueller C, Vamosi SM (2008) The evolution of aposematism is accompanied by increased diversification. Integr Zool 3:149–156PubMedCrossRefGoogle Scholar
  77. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  78. Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223CrossRefGoogle Scholar
  79. Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, OxfordCrossRefGoogle Scholar
  80. Sagegami-Oba R, Takahashi N, Oba Y (2007) The evolutionary process of bioluminescence and aposematism in cantharoid beetles (Coleoptera: Elateroidea) inferred by the analysis of 18S ribosomal DNA. Gene 400:104–113PubMedCrossRefGoogle Scholar
  81. Santos JC, Cannatella DC (2011) Phenotypic integration emerges from aposematism and scale in poison frogs. Proc Natl Acad Sci USA 108:6175–6180PubMedCrossRefGoogle Scholar
  82. Santos JC, Coloma LA, Cannatella DC (2003) Multiple, recurring origins of aposematism and diet specialization in poison frogs. Proc Natl Acad Sci USA 100:12792–12797PubMedCrossRefGoogle Scholar
  83. Schaefer H-C, Vences M, Veith M (2002) Molecular phylogeny of Malagasy poison frogs, genus Mantella (Anura: Mantellidae): homoplastic evolution of colour pattern in aposematic amphibians. Org Divers Evol 2:97–105CrossRefGoogle Scholar
  84. Sheffield SR, King CM (1994) Mustela nivalis. Mamm Species 454:1–10CrossRefGoogle Scholar
  85. Sheffield SR, Thomas HH (1997) Mustela frenata. Mamm Species 570:1–9CrossRefGoogle Scholar
  86. Sillén-Tullberg B (1988) Evolution of gregariousness in aposematic butterfly larvae: a phylogenetic analysis. Evolution 42:293–305CrossRefGoogle Scholar
  87. Speed MP (2000) Warning signals, receiver psychology and predator memory. Anim Behav 60:269–278PubMedCrossRefGoogle Scholar
  88. Speed MP, Ruxton GD (2005) Aposematism: what should our starting point be? Proc R Soc Lond B Biol Sci 272:431–438CrossRefGoogle Scholar
  89. Speed MP, Brockhurst MA, Ruxton GD (2010) The dual benefits of aposematism: predator avoidance and enhanced resource collection. Evolution 64:1622–1633PubMedCrossRefGoogle Scholar
  90. Stamp NE, Wilkens RT (1993) On the cryptic side of life: being unapparent to enemies and the consequences for foraging and growth of caterpillars. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman and Hall, New York, USA, pp 283–330Google Scholar
  91. Stankowich T (2011) Armed and dangerous: predicting the presence and function of defensive weaponry in mammals. Adapt Behav 20:32–43CrossRefGoogle Scholar
  92. Stankowich T, Caro T, Cox M (2011) Bold coloration and the evolution of aposematism in terrestrial carnivores. Evolution 65:3090–3099PubMedCrossRefGoogle Scholar
  93. Stankowich T, Haverkamp P, Caro T (in review) Ecological drivers of antipredator defenses in mammalsGoogle Scholar
  94. Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268CrossRefGoogle Scholar
  95. Stewart TW, Gafford JC, Miner JG, Lowe RL (1999) Dreissena-shell habitat and antipredator behavior: combined effects on survivorship of snails co-occurring with molluscivorous fish. J North Am Benthol Soc 18:274–283CrossRefGoogle Scholar
  96. Tullberg BS, Hunter AF (1996) Evolution of larval gregariousness in relation to repellent defences and warning coloration in tree-feeding Macrolepidoptera: a phylogenetic analysis based on independent contrasts. Biol J Linn Soc 57:253–276CrossRefGoogle Scholar
  97. Vamosi SM (2005) On the role of enemies in divergence and diversification of prey: a review and synthesis. Can J Zool 83:894–910CrossRefGoogle Scholar
  98. Vences M, Kosuch J, Boistel R, Haddad CFB, La Marca E, Lötters S, Veith M (2003) Convergent evolution of aposematic coloration in Neotropical poison frogs: a molecular phylogenetic perspective. Org Divers Evol 3:215–226CrossRefGoogle Scholar
  99. Verts BJ, Carraway LN, Kinlaw A (2001) Spilogale gracilis. Mamm Species 674:1–10CrossRefGoogle Scholar
  100. Wade-Smith J, Verts BJ (1982) Mephitis mephitis. Mamm Species 173:1–7CrossRefGoogle Scholar
  101. Walker EP (1964) Mammals of the world, vol 2. John Hopkins Press, Baltimore, MDGoogle Scholar
  102. Wallace AR (1889) Darwinism: an exposition of the theory of natural selection with some of its applications. MacMillan and Co, LondonGoogle Scholar
  103. Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and character evolution. Bioinformatics 24:2098–2100PubMedCrossRefGoogle Scholar
  104. Wilkinson M, Pisani D, Cotton JA, Corfe I (2005) Measuring support and finding unsupported relationships in supertrees. Syst Biol 54:823–831PubMedCrossRefGoogle Scholar
  105. Wilson DE, Reeder DM (2005) Mammal species of the world: a taxonomic and geographic reference, 3rd edn. John Hopkins University Press, Baltimore, MDGoogle Scholar
  106. Witz BW (1990) Antipredator mechanisms in arthropods: a twenty year literature survey. Fla Entomol 73:71–99CrossRefGoogle Scholar
  107. Youngman PM (1990) Mustela lutreola. Mamm Species 362:1–3CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Kevin Arbuckle
    • 1
    Email author
  • Michael Brockhurst
    • 2
  • Michael P. Speed
    • 1
  1. 1.Institute of Integrative Biology, Biosciences BuildingUniversity of LiverpoolLiverpool, MerseysideUK
  2. 2.Department of BiologyUniversity of YorkYork, YorkshireUK

Personalised recommendations