Evolutionary Ecology

, Volume 30, Issue 3, pp 567–581 | Cite as

Hoverflies are imperfect mimics of wasp colouration

  • Christopher H. Taylor
  • Tom Reader
  • Francis Gilbert
Evolutionary Ecology Natural History

Abstract

Many Batesian mimics are considered to be inaccurate copies of their models, including a number of hoverfly species which appear to be poor mimics of bees and wasps. This inaccuracy is surprising since more similar mimics are expected to deceive predators more frequently and therefore have greater survival. One suggested explanation is that mimics which appear inaccurate to human eyes may be perceived differently by birds, the probable agents of selection. For example, if patterns contain an ultra-violet (UV) component, this would be visible to birds but overlooked by humans. So far, indirect comparisons have been made using human and bird responses to mimetic stimuli, but direct colour measurements of mimetic hoverflies are lacking. We took spectral readings from a wide range of hoverfly and wasp patterns. They show very low reflectance in the UV range, and do not display any human-invisible colour boundaries. We modelled how the recorded spectra would be perceived by both birds and humans. While colour differences between wasps and hoverflies are slightly more distinct according to human visual abilities, bird vision is capable of discriminating the two taxa in almost all cases. We discuss a number of factors that might make the discrimination task more challenging for a predator in the field, which could explain the apparent lack of selection for accurate colour mimicry.

Keywords

Spectrophotometry Colour analysis Visual model Just Noticeable Difference Batesian mimicry Syrphidae 

Notes

Acknowledgments

We would like to thank John Endler for advice on spectrophotometry methods, Mark Strickland for manufacture of our custom probe-cover, and two anonymous reviewers for invaluable comments on our manuscript. This research was partly funded by a small equipment grant from the University of Nottingham.

Supplementary material

10682_2016_9824_MOESM1_ESM.docx (380 kb)
Supplementary material 1 (DOCX 379 kb)

References

  1. Andersson MB (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  2. Andersson S, Örnborg J, Andersson M (1998) Ultraviolet sexual dimorphism and assortative mating in blue tits. Proc R Soc Lond B 265(1395):445–450CrossRefGoogle Scholar
  3. Aronsson M, Gamberale-Stille G (2012) Colour and pattern similarity in mimicry: evidence for a hierarchical discriminative learning of different components. Anim Behav 84(4):881–887CrossRefGoogle Scholar
  4. Aronsson M, Gamberale-Stille G (2013) Evidence of signaling benefits to contrasting internal color boundaries in warning coloration. Behav Ecol 24(2):349–354CrossRefGoogle Scholar
  5. Azmeh S, Owen J, Sørensen K, Grewcock D, Gilbert F (1998) Mimicry profiles are affected by human-induced habitat changes. Proc R Soc Lond B 265(1412):2285–2290CrossRefGoogle Scholar
  6. Bain RS, Rashed A, Cowper VJ, Gilbert FS, Sherratt TN (2007) The key mimetic features of hoverflies through avian eyes. Proc R Soc Lond B 274(1621):1949–1954CrossRefGoogle Scholar
  7. Bates HW (1862) XXXII. Contributions to an insect fauna of the amazon valley. Lepidoptera: Heliconidæ. Trans Linn Soc Lond 23(3):495–566CrossRefGoogle Scholar
  8. Birkhead TR (1974) Predation by birds on social wasps. Br Birds 67(6):221–229Google Scholar
  9. Burr D (1980) Motion smear. Nature 284(5752):164–165CrossRefPubMedGoogle Scholar
  10. Chen DM, Goldsmith TH (1986) Four spectral classes of cone in the retinas of birds. J Comp Physiol A 159(4):473–479CrossRefPubMedGoogle Scholar
  11. Cheney KL, Marshall NJ (2009) Mimicry in coral reef fish: how accurate is this deception in terms of color and luminance? Behav Ecol 20(3):459–468CrossRefGoogle Scholar
  12. Cuthill IC, Bennett ATD (1993) Mimicry and the eye of the beholder. Proc R Soc Lond B 253(1337):203–204CrossRefGoogle Scholar
  13. Dittrich W, Gilbert F, Green P, Mcgregor P, Grewcock D (1993) Imperfect mimicry: a pigeon’s perspective. Proc R Soc Lond B 251(1332):195–200CrossRefGoogle Scholar
  14. Dlusski G (1984) Are dipteran insects protected by their similarity to stinging Hymenoptera? Byull Mosk O-Va Ispyt Prir Otd Biol 89:25–40Google Scholar
  15. Donner KO (1951) The visual acuity of some passerine birds. Acta Zool Fenn 66:1–40Google Scholar
  16. Dyer AG, Neumeyer C (2005) Simultaneous and successive colour discrimination in the honeybee (Apis mellifera). J Comp Physiol A 191(6):547–557CrossRefGoogle Scholar
  17. Edmunds M (2000) Why are there good and poor mimics? Biol J Linn Soc 70(3):459–466CrossRefGoogle Scholar
  18. Endler JA (1990) On the measurement and classification of colour in studies of animal colour patterns. Biol J Linn Soc 41(4):315–352CrossRefGoogle Scholar
  19. Endler JA (1993) The color of light in forests and its implications. Ecol Monogr 63(1):2–27CrossRefGoogle Scholar
  20. Endler JA, Mielke PWJ (2005) Comparing entire colour patterns as birds see them. Biol J Linn Soc 86:405–431CrossRefGoogle Scholar
  21. Feeney WE, Stoddard MC, Kilner RM, Langmore NE (2014) “Jack-of-all-trades” egg mimicry in the brood parasitic Horsfield’s bronze-cuckoo? Behav Ecol 25(6):1365–1373CrossRefGoogle Scholar
  22. Getty T (1985) Discriminability and the sigmoid functional response: how optimal foragers could stabilize model-mimic complexes. Am Nat 125(2):239–256CrossRefGoogle Scholar
  23. Ghim MM, Hodos W (2006) Spatial contrast sensitivity of birds. J Comp Physiol A 192(5):523–534CrossRefGoogle Scholar
  24. Gilbert F (2005) The evolution of imperfect mimicry. In: Fellowes M, Holloway G, Rolff J (eds) Insect evolutionary ecology. CABI, Wallingford, pp 231–288Google Scholar
  25. Giurfa M, Vorobyev M, Brandt R, Posner B, Menzel R (1997) Discrimination of coloured stimuli by honeybees: alternative use of achromatic and chromatic signals. J Comp Physiol A 180(3):235–243CrossRefGoogle Scholar
  26. Golding YC, Edmunds M, Ennos AR (2005) Flight behaviour during foraging of the social wasp Vespula vulgaris (Hymenoptera: Vespidae) and four mimetic hoverflies (Diptera: Syrphidae) Sericomyia silentis, Myathropa florea, Helophilus sp. and Syrphus sp. J Exp Biol 208(23):4523–4527CrossRefPubMedGoogle Scholar
  27. Green PR, Gentle L, Peake TM, Scudamore RE, McGregor PK, Gilbert F, Dittrich WH (1999) Conditioning pigeons to discriminate naturally lit insect specimens. Behav Processes 46(1):97–102CrossRefPubMedGoogle Scholar
  28. Holloway G, Gilbert F, Brandt A (2002) The relationship between mimetic imperfection and phenotypic variation in insect colour patterns. Proc R Soc Lond B 269(1489):411–416CrossRefGoogle Scholar
  29. Jones RT, Poul YL, Whibley AC, Mérot C, ffrench-Constant RH, Joron M (2013) Wing shape variation associated with mimicry in butterflies. Evolution 67(8):2323–2334CrossRefPubMedGoogle Scholar
  30. Kazemi B, Gamberale-Stille G, Tullberg Birgitta S, Leimar O (2014) Stimulus salience as an explanation for imperfect mimicry. Curr Biol 24(9):965–969CrossRefPubMedGoogle Scholar
  31. Kikuchi DW, Pfennig DW (2013) Imperfect mimicry and the limits of natural selection. Q Rev Biol 88(4):297–315CrossRefPubMedGoogle Scholar
  32. Kikuchi DW, Sherratt TN (2015) Costs of learning and the evolution of mimetic signals. Am Nat 186(3):321–332CrossRefPubMedGoogle Scholar
  33. Kraemer AC, Adams DC (2014) Predator perception of Batesian mimicry and conspicuousness in a salamander. Evolution 68(4):1197–1206CrossRefPubMedGoogle Scholar
  34. Limeri LB, Morehouse NI (2014) Sensory limitations and the maintenance of colour polymorphisms: viewing the ‘alba’ female polymorphism through the visual system of male Colias butterflies. Funct Ecol 28(5):1197–1207CrossRefGoogle Scholar
  35. Lindström L, Alatalo RV, Mappes J (1997) Imperfect Batesian mimicry—the effects of the frequency and the distastefulness of the model. Proc R Soc Lond B 264(1379):149–153CrossRefGoogle Scholar
  36. Llaurens V, Joron M, Théry M (2014) Cryptic differences in colour among Müllerian mimics: how can the visual capacities of predators and prey shape the evolution of wing colours? J Evol Biol 27(3):531–540CrossRefPubMedGoogle Scholar
  37. Maia R, Eliason CM, Bitton P-P, Doucet SM, Shawkey MD (2013) pavo: an R package for the analysis, visualization and organization of spectral data. Methods Ecol Evol 4(10):906–913Google Scholar
  38. Marples NM, van Veelen W, Brakefield PM (1994) The relative importance of colour, taste and smell in the protection of an aposematic insect Coccinella septempunctata. Anim Behav 48(4):967–974CrossRefGoogle Scholar
  39. Morrell GM, Turner JRG (1970) Experiments on mimicry: I. The response of wild birds to artificial prey. Behaviour 36(1/2):116–130CrossRefGoogle Scholar
  40. Mostler G (1935) Beobachtungen zur frage der wespenmimikry (Observations on the question of wasp mimicry). Zoomorphology 29(3):381–454Google Scholar
  41. Ödeen A, Håstad O (2003) Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Mol Biol Evol 20(6):855–861CrossRefPubMedGoogle Scholar
  42. Olsson P, Lind O, Kelber A (2015) Bird colour vision: behavioural thresholds reveal receptor noise. J Exp Biol 218(2):184–193CrossRefPubMedGoogle Scholar
  43. Osorio D, Miklósi A, Gonda Z (1999) Visual ecology and perception of coloration patterns by domestic chicks. Evol Ecol 13(7–8):673–689CrossRefGoogle Scholar
  44. Penney HD, Hassall C, Skevington JH, Abbott KR, Sherratt TN (2012) A comparative analysis of the evolution of imperfect mimicry. Nature 483(7390):461–464CrossRefPubMedGoogle Scholar
  45. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  46. Richards OW (1980) Scolioidea, vespoidea and sphecoidea; hymenoptera, aculeata. Royal Entomological Society of London, LondonGoogle Scholar
  47. Richards-Zawacki CL, Yeager J, Bart HPS (2013) No evidence for differential survival or predation between sympatric color morphs of an aposematic poison frog. Evol Ecol 27(4):783–795CrossRefGoogle Scholar
  48. Rotheray GF, Gilbert F (2011) The natural history of hoverflies. Forrest Text, CardiganGoogle Scholar
  49. Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals, and mimicry. Oxford University Press, OxfordCrossRefGoogle Scholar
  50. Siddiqi A, Cronin TW, Loew ER, Vorobyev M, Summers K (2004) Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. J Exp Biol 207(14):2471–2485CrossRefPubMedGoogle Scholar
  51. Stockman A, Sharpe LT (2000) The spectral sensitivities of the middle- and long-wavelength-sensitive cones derived from measurements in observers of known genotype. Vision Res 40(13):1711–1737CrossRefPubMedGoogle Scholar
  52. Stubbs AE, Falk SJ (2002) British hoverflies: an illustrated identification guide. British Entomological and Natural History Society, ReadingGoogle Scholar
  53. Svádová K, Exnerová A, Štys P, Landová E, Valenta J, Fučíková A, Socha R (2009) Role of different colours of aposematic insects in learning, memory and generalization of naïve bird predators. Anim Behav 77(2):327–336CrossRefGoogle Scholar
  54. Veselý P, Luhanová D, Prášková M, Fuchs R (2013) Generalization of mimics imperfect in colour patterns: the point of view of wild avian predators. Ethology 119(2):138–145CrossRefGoogle Scholar
  55. Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B 265(1394):351–358CrossRefGoogle Scholar
  56. Waldbauer G (1988) Asynchrony between Batesian mimics and their models. Am Nat 131:S103–S121CrossRefGoogle Scholar
  57. Wyszecki G, Stiles WS (2000) Color science: concepts and methods, quantitative data and formulae. Wiley, New YorkGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.School of Life SciencesUniversity of NottinghamNottinghamUK

Personalised recommendations