Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Multimodal warning signals for a multiple predator world

Abstract

Aposematism is an anti-predator defence, dependent on a predator’s ability to associate unprofitable prey with a prey-borne signal1. Multimodal signals should vary in efficacy according to the sensory systems of different predators; however, until now, the impact of multiple predator classes on the evolution of these signals had not been investigated2,3. Here, using a community-level molecular phylogeny to generate phylogenetically independent contrasts, we show that warning signals of tiger moths vary according to the seasonal and daily activity patterns of birds and bats—predators with divergent sensory capacities. Many tiger moths advertise chemical defence4,5 using conspicuous colouration and/or ultrasonic clicks3,6. During spring, when birds are active and bats less so, we found that tiger moths did not produce ultrasonic clicks. Throughout both spring and summer, tiger moths most active during the day were visually conspicuous. Those species emerging later in the season produced ultrasonic clicks; those that were most nocturnal were visually cryptic. Our results indicate that selective pressures from multiple predator classes have distinct roles in the evolution of multimodal warning displays now effective against a single predator class. We also suggest that the evolution of acoustic warning signals may lack the theoretical difficulties associated with the origination of conspicuous colouration.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Representatives of each visual class.
Figure 2: Representative sonograms.
Figure 3: 50% majority consensus phylogram of the bayesian trees.
Figure 4: Phylogenetically independent contrasts (mean ± s.e.).

Similar content being viewed by others

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

All sequences were submitted to GenBank under accession numbers EU333575EU333652.

References

  1. Cott, H. B. Adaptive Coloration in Animals (Methuen, London, 1940)

    Google Scholar 

  2. Mappes, J., Marples, N. & Endler, J. A. The complex business of survival by aposematism. Trends Ecol. Evol. 20, 598–603 (2005)

    Article  Google Scholar 

  3. Ruxton, G. D., Sherrat, T. N. & Speed, M. Avoiding Attack: the Evolutionary Ecology of Crypsis, Warning Signals and Mimicry (Oxford Univ. Press, Oxford, 2004)

    Book  Google Scholar 

  4. Nishida, R. Sequestration of defensive substances from plants by Lepidoptera. Annu. Rev. Entomol. 47, 57–92 (2002)

    Article  CAS  Google Scholar 

  5. Hristov, N. & Conner, W. E. Effectiveness of tiger moth (Lepidoptera, Arctiidae) chemical defenses against an insectivorous bat (Eptesicus fuscus). Chemoecology 15, 105–113 (2005)

    Article  Google Scholar 

  6. Hristov, I. H. & Conner, W. E. Sound strategy: acoustic aposematism in the bat–tiger moth arms race. Naturwissenschaften 92, 164–169 (2005)

    Article  ADS  CAS  Google Scholar 

  7. Cadman, M. D., Eagles, P. F. J. & Helleiner, F. M. Atlas of the Breeding Birds of Ontario (Univ. Waterloo Press, Waterloo, 1987)

    Google Scholar 

  8. Godfrey, W. E. 1986. The Birds of Canada, rev. ed. (Natl Mus. Nat. Sci. Canada, Ottawa, 1986)

    Google Scholar 

  9. Ward, P. S., Harmsen, R. & Hebert, P. D. N. An annotated checklist of the Macroheterocera of South-eastern Ontario. J. Res. Lepidoptera 13, 23–42 (1974)

    Google Scholar 

  10. Fullard, J. H. Phenology of sound-producing arctiid moths and the activity of insectivorous bats. Nature 267, 42–43 (1977)

    Article  ADS  CAS  Google Scholar 

  11. Fullard, J. H. & Barclay, R. M. R. Audition in spring moths as a possible response to differential levels of insectivorous bat predation. Can. J. Zool. 58, 1745–1750 (1980)

    Article  Google Scholar 

  12. Yack, J. E. Seasonal partitioning of atympanate moths in relation to bat activity. Can. J. Zool. 66, 753–755 (1988)

    Article  Google Scholar 

  13. Bennett, A. T. D. & Cuthill, I. C. Ultraviolet vision in birds: what is its function? Vision Res. 34, 1471–1478 (1994)

    Article  CAS  Google Scholar 

  14. Lyytinen, A., Lindstrom, L. & Mappes, J. Ultraviolet reflection and predation risk in diurnal and nocturnal Lepidoptera. Behav. Ecol. 15, 982–987 (2004)

    Article  Google Scholar 

  15. Ratcliffe, J. M. & Fullard, J. H. The adaptive function of tiger moth clicks against echolocating bats: an experimental and synthetic approach. J. Exp. Biol. 208, 4689–4698 (2005)

    Article  Google Scholar 

  16. Dooling, R. J., Lohr, B. & Dent, M. L. in Comparative Hearing: Birds and Reptiles (eds Dooling, R. J., Popper, A. N. & Fay, R. R.) 308–359 (Springer, New York, 2000)

    Google Scholar 

  17. Nicolaus, L. K., Cassel, J. F., Carlson, R. B. & Gustavson, C. R. Taste-aversion conditioning of crows to control predation on eggs. Science 220, 212–214 (1983)

    Article  ADS  CAS  Google Scholar 

  18. Ratcliffe, J. M., Fenton, M. B. & Galef, B. G. An exception to the rule: common vampire bats do not learn taste aversions. Anim. Behav. 65, 385–389 (2003)

    Article  Google Scholar 

  19. Fullard, J. H. & Fenton, M. B. Acoustic and behavioural analyses of the sounds produced by some species of Nearctic Arctiidae (Lepidoptera). Can. J. Zool. 55, 1213–1224 (1977)

    Article  Google Scholar 

  20. Fullard, J. H. & Napoleone, N. Diel flight periodicity and the evolution of auditory defences in the Macrolepidoptera. Anim. Behav. 62, 349–368 (2001)

    Article  Google Scholar 

  21. Purvis, A. & Rambaut, A. Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comp. Appl. Biosci. 11, 247–251 (1995)

    CAS  PubMed  Google Scholar 

  22. Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis Version 2. 0 <http://mesquiteproject.org> (2007)

    MATH  Google Scholar 

  23. Barber, J. R. & Conner, W. E. Acoustic mimicry in a predator–prey interaction. Proc. Natl Acad. Sci. USA 104, 9331–9334 (2007)

    Article  ADS  CAS  Google Scholar 

  24. Acharya, L. & Fenton, M. B. Echolocation behaviour of vespertilionid bats (Lasiurus cinereus and L. borealis) attacking airborne targets including arctiid moths. Can. J. Zool. 70, 1292–1298 (1992)

    Article  Google Scholar 

  25. Barclay, R. M. R. & Brigham, R. M. Constraints on optimal foraging: a field test of prey discrimination by echolocating insectivorous bats. Anim. Behav. 48, 1013–1021 (1994)

    Article  Google Scholar 

  26. Barber, J. R. & Conner, W. E. Tiger moth responses to a simulated bat attack: timing and duty cycle. J. Exp. Biol. 209, 2637–2650 (2006)

    Article  CAS  Google Scholar 

  27. Rowe, C. & Guilford, T. The evolution of multimodal warning displays. Evol. Ecol. 13, 655–671 (1999)

    Article  Google Scholar 

  28. Rowe, C. Sound improves visual discrimination learning in avian predators. Proc. R. Soc. Lond. B 269, 1353–1357 (2002)

    Article  Google Scholar 

  29. Gronquist, M. et al. Attractive and defensive functions of the ultraviolet pigments of a flower (Hypericum calycinum). Proc. Natl Acad. Sci. USA 98, 13745–13750 (2001)

    Article  ADS  CAS  Google Scholar 

  30. Ronquist, F. & Huelsenbeck, J. P. MrBayes3: Bayesian inference under mixed models. Bioinformatics 19, 1572–1574 (2003)

    Article  CAS  Google Scholar 

  31. Stevens, M., Parrage, C. A., Cuthill, I. C., Partridge, J. C. & Troscianko, T. S. Using digital photography to study animal coloration. Biol. J. Linn. Soc. 90, 211–237 (2007)

    Article  Google Scholar 

  32. Simon, C., Frati, F., Beckenbach, A., Liu, H. & Flook, P. Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann. Ent. Soc. Am. 87, 651–701 (1994)

    Article  CAS  Google Scholar 

  33. Cho, S. et al. A highly conserved nuclear gene for low-level phylogenetics: elongation factor 1-α recovers morphology-based tree for heliothine moths. Mol. Biol. Evol. 12, 650–656 (1995)

    CAS  PubMed  Google Scholar 

  34. Monteiro, A. & Pierce, N. Phylogeny of Bicyclus (Lepidoptera: Nymphalidae) inferred from COI, COII, and EF1-α gene sequences. Mol. Phylogenet. Evol. 18, 264–281 (2001)

    Article  CAS  Google Scholar 

  35. Mitchell, A., Mitter, C. & Regier, J. C. Systematics and evolution of the cutworm moths (Lepidoptera: Noctuidae): evidence from two protein-coding nuclear genes. Syst. Ent. 31, 21–46 (2006)

    Article  Google Scholar 

  36. Brower, A. & DeSalle, R. Patterns of mitochondrial versus nuclear DNA sequence divergence among nymphalid butterflies: the utility of wingless as a source of characters for phylogenetic inference. Insect Mol. Biol. 7, 73–82 (1998)

    Article  CAS  Google Scholar 

  37. Jacobson, N. L. & Weller, S. J. A cladistic Study of the Arctiidae (Lepidoptera) by Using Characters of Immatures and Adults (Thomas Say Publications in Entomology, Ent. Soc. Am., Lanham, MD, 2002)

    Google Scholar 

  38. Posada, D. & Crandall, K. A. MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818 (1998)

    Article  CAS  Google Scholar 

  39. Swofford, D. L. PAUP*: Phylogenetic Analysis using Parsimony (* and other Methods) v. 4.0b 10 (Sinauer Associates, Sunderland, 2003)

    Google Scholar 

  40. Dunn, P. O., Whittingham, L. A. & Pitcher, T. E. Mating systems, sperm competition and the evolution of sexual dimorphism in birds. Evolution 55, 161–175 (2001)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank R. Hoebeke for access to the Cornell University Insect Collection, T. Eisner for the loan of ultraviolet photography equipment, and the 15 people who scored the photographs. J.M.R. thanks M. Fitzpatrick for discussion. J. Barber, C. Beatty, I. Cuthill, T. Eisner and J. Fullard provided detailed comments that improved the manuscript. This study was funded by research grants to J. Fullard (NSERC), R. Hoy (NIDCD) and J.M.R. (NSERC and DNSRC). Molecular work was conducted at Cornell in the laboratory of R. Harrison and the Evolutionary Genetics Core Facility.

Author Contributions M.L.N. was responsible for genetic analyses. J.M.R. was responsible for behavioural, comparative and signal analyses. J.M.R. wrote the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to John M. Ratcliffe or Marie L. Nydam.

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ratcliffe, J., Nydam, M. Multimodal warning signals for a multiple predator world. Nature 455, 96–99 (2008). https://doi.org/10.1038/nature07087

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature07087

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing