Noise in Chemical Communication

  • Volker Nehring
  • Tristram D. Wyatt
  • Patrizia d’Ettorre
Chapter
Part of the Animal Signals and Communication book series (ANISIGCOM, volume 2)

Abstract

Chemical communication is ubiquitous. It is not only employed in inter-individual communication, but also used to transfer information within individuals, from cell to cell and from one organ to another within a body with a complicated network of hormones and neurotransmitters. However, how noise affects chemical communication has been largely neglected. Here, we review possible sources of noise and the effects noise has on the behaviour of receivers. We will also discuss variation in chemical cues and signals that may provide information in some contexts, but obscure messages in others. Finally, we attempt to identify strategies that senders and receivers can follow to either reduce the occurrence or mitigate the effects of noise.

Notes

Acknowledgments

We thank Marc Weissburg for the photograph of the underwater odour plume visualised with dye and Rob Beynon for the Darcin ribbon graphic. We also thank Jan Benda, Henrik Brumm and an anonymous referee for their helpful comments on drafts of this chapter.

References

  1. Alberts A (1990) Chemical properties of femoral gland secretions in the desert iguana, Dipsosaurus dorsalis. J Chem Ecol 16:13–25PubMedGoogle Scholar
  2. Arnold G, Quenet B, Cornuet J-M et al (1996) Kin recognition in honeybees. Nature 379:498Google Scholar
  3. Asahina K, Louis M, Piccinotti S, Vosshall LB (2009) A circuit supporting concentration-invariant odor perception in Drosophila. J Biol 8:9. doi:10.1186/jbiol108 PubMedCentralPubMedGoogle Scholar
  4. Baker TC (2008) Balanced olfactory antagonism as a concept for understanding evolutionary shifts in moth sex pheromone blends. J Chem Ecol 34:971–981. doi:10.1007/s10886-008-9468-5 PubMedGoogle Scholar
  5. Bargmann CI (2006) Comparative chemosensation from receptors to ecology. Nature 444:295–301. doi:10.1038/nature05402 PubMedGoogle Scholar
  6. Barja I, Silván G, Illera JC (2008) Relationships between sex and stress hormone levels in feces and marking behavior in a wild population of Iberian wolves (Canis lupus signatus). J Chem Ecol 6:697–701Google Scholar
  7. Barth MB, Kellner K, Heinze J (2010) The police are not the army: context-dependent aggressiveness in a clonal ant. Biol Lett 6:329–332. doi:10.1098/rsbl.2009.0849 PubMedCentralPubMedGoogle Scholar
  8. Berg BG, Almaas TJ, Bjaalie JG, Mustaparta H (1998) The macroglomerular complex of the antennal lobe in the tobacco budworm moth Heliothis virescens: specified subdivision in four compartments according to information about biologically significant compounds. J Comp Physiol A 183:669–682. doi:10.1007/s003590050290 Google Scholar
  9. Berglund B, Berglund U, Engen T, Lindvall T (1971) The effect of adaptation on odor detection. Percept Psychophys 9:435–438Google Scholar
  10. Bialek W (1987) Physical limits to sensation and perception. Annu Rev Biophys Biophys Chem 16:455–478. doi:10.1146/annurev.bb.16.060187.002323 PubMedGoogle Scholar
  11. Boeckh J, Selsam P (1984) Quantitative investigation of the odour specificity of central olfactory neurones in the American cockroach. Chem Senses 9:369–380Google Scholar
  12. Boeckh J, Tolbert LP (1993) Synaptic organization and development of the antennal lobe in insects. Microsc Res Tech 24:260–280. doi:10.1002/jemt.1070240305 PubMedGoogle Scholar
  13. Bonavita-Cougourdan A, Clement J-L, Lange C (1993) Functional subcaste discrimination (foragers and brood-tenders) in the ant Camponotus vagus Csop: polymorphism of cuticular hydrocarbons. J Chem Ecol 19:1461–1477PubMedGoogle Scholar
  14. Boomsma JJ, Nielsen J, Sundström L et al (2003) Informational constraints on optimal sex allocation in ants. Proc Natl Acad Sci USA 100:8799–8804. doi:10.1073/pnas.1430283100 PubMedCentralPubMedGoogle Scholar
  15. Borroni PF, Atema J (1988) Adaptation in chemoreceptor cells. I. Self-adapting backgrounds determine threshold and cause parallel shift of response function. J Comp Physiol A 164:67–74PubMedGoogle Scholar
  16. Brodmann J, Twele R, Francke W et al (2009) Orchid mimics honey bee alarm pheromone in order to attract hornets for pollination. Curr Biol 19:1368–1372PubMedGoogle Scholar
  17. Brown RE (1985) The rodents II: suborder Myomorpha. In: Brown RE, Macdonald DW (ed) Social odours in mammals. Oxford University Press, Oxford, pp 345–457Google Scholar
  18. de Bruyne M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34:882–897. doi:10.1007/s10886-008-9485-4 PubMedGoogle Scholar
  19. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595PubMedGoogle Scholar
  20. Cardé RT, Haynes KF (2004) Structure of the pheromone communication channel in moths. In: Cardé R, Millar J (eds) Advances in insect chemical ecology. Cambridge University Press, Cambridge, pp 283–332Google Scholar
  21. Charlton RE, Webster FX, Zhang A et al (1993) Sex pheromone for the brown banded cockroach is an unusual dialkyl-substituted alpha-pyrone. Proc Natl Acad Sci USA 90:10202–10205PubMedCentralPubMedGoogle Scholar
  22. Chittka L, Niven J (2009) Are bigger brains better? Curr Biol 19:R995–R1008. doi:10.1016/j.cub.2009.08.023 PubMedGoogle Scholar
  23. Cleland TA, Johnson BA, Leon M, Linster C (2007) Relational representation in the olfactory system. Proc Natl Acad Sci USA 104:1953–1958PubMedCentralPubMedGoogle Scholar
  24. Cleland TA, Narla VAA, Boudadi K (2009) Multiple learning parameters differentially regulate olfactory generalization. Behav Neurosci 123:26. doi:10.1037/a0013991.Multiple PubMedCentralPubMedGoogle Scholar
  25. Conner W, Weller SJ (2004) A quest for alkaloids: the curious relationship of tiger moths and plants containing pyrrolizidine alkaloids. In: Cardé RT, Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, Cambridge, pp 248–282Google Scholar
  26. Dani FR, Foster KR, Zacchi F et al (2004) Can cuticular lipids provide sufficient information for within-colony nepotism in wasps? Proc R Soc Lond B 271:745–753. doi:10.1098/rspb.2003.2646 Google Scholar
  27. Dani FR, Jones GR, Corsi S et al (2005) Nestmate recognition cues in the honey bee: differential importance of cuticular alkanes and alkenes. Chem Senses 30:477–489. doi:10.1093/chemse/bji040 PubMedGoogle Scholar
  28. Dicke M, Agrawal AA, Bruin J (2003) Plants talk, but are they deaf? Trends Plant Sci 8:403–405PubMedGoogle Scholar
  29. Dickson BJ (2008) Wired for sex: the neurobiology of Drosophila mating decisions. Science 322:904–909PubMedGoogle Scholar
  30. Domingue MJ, Haynes KF, Todd JL, Baker TC (2009) Altered olfactory receptor neuron responsiveness is correlated with a shift in behavioral response in an evolved colony of the cabbage looper moth, Trichoplusia ni. J Chem Ecol 35:405–415. doi:10.1007/s10886-009-9621-9 PubMedGoogle Scholar
  31. Dybdahl MF, Storfer A (2003) Parasite local adaptation: red queen versus suicide king. Trend Ecol Evol 18:523–530Google Scholar
  32. d’Ettorre P, Heinze J (2005) Individual recognition in ant queens. Curr Biol 15:1–2. doi:10.1016/j.cub.2005.10.067 Google Scholar
  33. d’Ettorre P, Moore AJ (2008) Chemical communication and the coordination of social interactions in insects. In: d’Ettorre P, Hughes DP (ed) Sociobiology of communication. Oxford Scholarship Online Monographs, pp 81–97Google Scholar
  34. Eizaguirre M, López C, Sans A et al (2009) Response of Mythimna unipuncta males to components of the Sesamia nonagrioides pheromone. J Chem Ecol 35:779–784PubMedGoogle Scholar
  35. Frisch K von (1915) Der Farbensinn und Formensinn der Biene. Zool Jb Physiol 35:1–182Google Scholar
  36. Fouks B, d’Ettorre P, Nehring V (2011) Brood adoption in the leaf-cutting ant Acromyrmex echinatior: adaptation or recognition noise? Insectes Soc 58:479–485. doi: 10.1007/s00040-011-0167-9 Google Scholar
  37. Gemeno C, Schal C (2004) Sex pheromones of cockroaches. In: Cardé R, Millar J (eds) Advances in insect chemical ecology. Cambridge University Press, New York, pp 179–247Google Scholar
  38. Gosling LM (1981) Demarkation in a gerenuk territory: an economic approach. Z Tierpsychol 56:305–322Google Scholar
  39. Greene MJ, Gordon DM (2003) Social insects: cuticular hydrocarbons inform task decisions. Nature 423:32PubMedGoogle Scholar
  40. Greenspan RJ, Ferveur J-F (2000) Courtship in Drosophila. Annu Rev Genet 34:205–232PubMedGoogle Scholar
  41. Hallem EA, Carlson JR (2006) Coding of odors by a receptor repertoire. Cell 125:143–160Google Scholar
  42. Hansson BS, Baker TC (1991) Differential adaptation rates in a male moth’s sex pheromone receptor neurons. Naturwissenschaften 78:517–520Google Scholar
  43. Harris MO, Foster SP (1994) Behavior and integration. In: Carde RT, Bell WJ (ed) Chemical ecology of insects 2. Chapman and Hall, New York, pp 3–46Google Scholar
  44. Havlicek J, Roberts SC (2009) MHC-correlated mate choice in humans: a review. Psychoneuroendocrinology 34:497–512PubMedGoogle Scholar
  45. Haynes KF, Hunt RE (1990) A mutation in pheromonal communication system of cabbage looper moth, Trichoplusia ni. J Chem Ecol 16:1249–1257Google Scholar
  46. Haynes KF, Gemeno C, Yeargan KV et al (2002) Aggressive chemical mimicry of moth pheromones by a bolas spider: how does this specialist predator attract more than one species of prey? Chemoecology 12:99–105Google Scholar
  47. Hebets EA, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57:197–214Google Scholar
  48. Helanterä H, Ratnieks FLW (2008) Two independent mechanisms of egg recognition in worker Formica fusca ants. Behav Ecol Sociobiol 63:573–580. doi:10.1007/s00265-008-0692-3 Google Scholar
  49. Helsper JPFG, Davies JA, Bouwmeester HJ et al. (1998) Circadian rhythmicity in emission of volatile compounds by flowers of Rosa hybrida L. cv. Honesty. Planta 207:88–95. doi: 10.1007/s004250050459 Google Scholar
  50. Holman L, Dreier S, d’Ettorre P (2010) Selfish strategies and honest signalling: reproductive conflicts in ant queen associations. Proc R Soc Lond B 277:2007–2015. doi: 10.1098/rspb.2009.2311
  51. Hurst J, Beynon R (2004) Scent wars: the chemobiology of competitive signalling in mice. BioEssays 26:1288–1298PubMedGoogle Scholar
  52. Ibba I, Angioy AM, Hansson BS, Dekker T (2010) Macroglomeruli for fruit odors change blend preference in Drosophila. Naturwissenschaften 97:1059–1066. doi:10.1007/s00114-010-0727-2 PubMedGoogle Scholar
  53. Johnson RP (1973) Scent marking in mammals. Anim Behav 21:521–535Google Scholar
  54. Johnston RE (2008) Individual odors and social communication: individual recognition, kin recognition, and scent over-marking. In: Brockmann H, Roper T, Naguib M et al. (eds) Advances in the study of behavior. Academic Press, New York, pp 439–505Google Scholar
  55. Karlson P, Lüscher M (1959) “Pheromones”, a new term for a class of biologically active substances. Nature 183:55–56. doi:10.1038/183055a0 PubMedGoogle Scholar
  56. Kaupp UB (2010) Olfactory signalling in vertebrates and insects: differences and commonalities. Nat Rev Neurosci 11:188–200PubMedGoogle Scholar
  57. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241Google Scholar
  58. Kay LM, Stopfer M (2006) Information processing in the olfactory systems of insects and vertebrates. Semin Cell Dev Biol 17:433–442. doi:10.1016/j.semcdb.2006.04.012 PubMedGoogle Scholar
  59. Kelly DR (1996) When is a butterfly like an elephant? Chem Biol 3:595–602PubMedGoogle Scholar
  60. Kleene SJ (1997) High-gain, low-noise amplification in olfactory transduction. Biophys J 73:1110–1117PubMedCentralPubMedGoogle Scholar
  61. Kleineidam CJ, Obermayer M, Halbich W, Rössler W (2005) A macroglomerulus in the antennal lobe of leaf-cutting ant workers and its possible functional significance. Chem Senses 30:383–392. doi:10.1093/chemse/bji033 PubMedGoogle Scholar
  62. Lacaille F, Hiroi M, Twele R et al (2007) An inhibitory sex pheromone tastes bitter for Drosophila males. Plos One 2:e661. doi:10.1371/journal.pone.0000661 PubMedCentralPubMedGoogle Scholar
  63. Lanier GN, Classon ALF, Piston JJ et al (1980) Ips pini: the basis for interpopulational differences in pheromone biology. J Chem Ecol 6:677–687Google Scholar
  64. Lassance J-M (2010) Journey in the Ostrinia world: from pest to model in chemical ecology. J Chem Ecol 36:1155–1169. doi:10.1007/s10886-010-9856-5 PubMedGoogle Scholar
  65. Lassance J-M, Groot AT, Liénard MA et al. (2010) Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones. Nature 466:486–489. doi: 10.1038/nature09058 Google Scholar
  66. Lenoir A, d’Ettorre P, Errard C, Hefetz A (2001) Chemical ecology and social parasitism in ants. Ann Rev Entomol 46:573–599Google Scholar
  67. Lenoir A, Fresneau D, Errard C, Hefetz A (1999) Individuality and colonial identity in ants. In: Detrain C, Deneubourg JL, Pasteels JM (ed) Information processing in social insects. Birkhäuser Verlag, Basel, pp 219–237Google Scholar
  68. Leon M, Johnson BA (2003) Olfactory coding in the mammalian olfactory bulb. Brain Res Rev 42:23–32. doi: 10.1016/S0165-0173(03)00142-5 Google Scholar
  69. Liang D, Blomquist GJ, Silverman J (2001) Hydrocarbon-released nestmate aggression in the Argentine ant, Linepithema humile, following encounters with insect prey. Comp Biochem Physiol B 129:871–882PubMedGoogle Scholar
  70. Linn CE, Campbell MG, Roelofs WL (1987) Pheromone components and active spaces: what do moths smell and where do they smell it? Science 237:650–652PubMedGoogle Scholar
  71. Linn CEJ, Bjostad LB, Du JW, Roelofs WL (1984) Redundancy in a chemical signal; behavioral responses of male Trichoplusia ni to a 6-component sex pheromone blend. J Chem Ecol 10:1635–1658PubMedGoogle Scholar
  72. Linster C, Johnson Morse et al (2001) Perceptual correlates of neural representations evoked by odorant enantiomers. J Neurosci 21:9837–9843PubMedGoogle Scholar
  73. Linster C, Johnson Morse et al (2002) Spontaneous versus reinforced olfactory discriminations. J Neurosci 22:6842–6845PubMedGoogle Scholar
  74. Loftfield RB, Vanderjagt D (1963) The frequency of errors in protein biosynthesis. Biochem J 89:82–92PubMedCentralPubMedGoogle Scholar
  75. Lowe G, Gold GH (1995) Olfactory transduction is intrinsically noisy. Proc Natl Acad Sci USA 92:7864–7868PubMedCentralPubMedGoogle Scholar
  76. Löfstedt C (1990) Population variation and genetic control of pheromone communication systems in moths. Entomol Exp Appl 54:199–218Google Scholar
  77. Löfstedt C, Herrebout WM, Menken SBJ (1991) Sex pheromones and their potential role in the evolution of reproductive isolation in small ermine moths (Yponomeutidae). Chemoecology 2:20–28. doi:10.1007/BF01240662 Google Scholar
  78. Macdonald DW (1985) The carnivores: order Carnivora. In: Brown RE, Macdonald DW (ed) Social odours in mammals. Oxford University Press, Oxford, pp 619–722Google Scholar
  79. Martin SJ, Drijfhout FP (2009) A review of ant cuticular hydrocarbons. J Chem Ecol 35:1151–1161. doi:10.1007/s10886-009-9695-4 PubMedGoogle Scholar
  80. Martin SJ, Helanterä H, Drijfhout FP (2011) Is parasite pressure a driver of chemical cue diversity in ants? Proc R Soc Lond B 278:496–503. doi:10.1098/rspb.2010.1047 Google Scholar
  81. Martin SJ, Helanterä H, Kiss K et al (2009) Polygyny reduces rather than increases nestmate discrimination cue diversity in Formica exsecta ants. Insectes Soc 56:375–383. doi:10.1007/s00040-009-0035-z Google Scholar
  82. Maynard Smith J, Harper D (2003) Animal signals. Oxford University Press, OxfordGoogle Scholar
  83. Miklas N, Renou M, Malosse I, Malosse C (2000) Repeatability of pheromone blend composition in individual males of the southern green stink bug, Nezara viridula. J Chem Ecol 26:2473–2485Google Scholar
  84. Miller JR, McGhee PS, Siegert PY et al (2010) General principles of attraction and competitive attraction as revealed by large-cage studies of moths responding to sex pheromone. Proc Natl Acad Sci USA 107:22–27. doi:10.1073/pnas.0908453107 PubMedCentralPubMedGoogle Scholar
  85. Minks AK, Cardé RT (1988) Disruption of pheromone communication in moths—is the natural blend really most efficacious. Entomol Exp Appl 49:25–36Google Scholar
  86. Monnin T, Peeters C (1999) Dominance hierarchy and reproductive conflicts among subordinates in a monogynous queenless ant. Behav Ecol 10:323–332. doi:10.1093/beheco/10.3.323 Google Scholar
  87. Moore D, Liebig J (2010) Mixed messages: fertility signaling interferes with nestmate recognition in the monogynous ant Camponotus floridanus. Behav Ecol Sociobiol 64:1011–1018. doi:10.1007/s00265-010-0916-1 Google Scholar
  88. Murlis J, Elkinton JS, Cardé RT (1992) Odor plumes and how insects use them. Annu Rev Entomol 37:505–532. doi:10.1146/annurev.ento.37.1.505 Google Scholar
  89. Mustaparta H (1997) Olfactory coding mechanisms for pheromone and interspecific signal information in related moth species. In: Carde RT, Minks AK (eds) Insect Pheromone Research: New Directions, SpringerGoogle Scholar
  90. Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments? Behav Ecol Sociobiol 32:167–176. doi:10.1007/BF00173774 Google Scholar
  91. Müller-Schwarze D (2006) Chemical ecology of vertebrates. Cambridge University Press, CambridgeGoogle Scholar
  92. Nehring V, Evison SEF, Santorelli LA, d’Ettorre P, Hughes WOH (2011) Kin-informative recognition cues in ants. Proc R Soc Lond B 278:1942–1948. doi:10.1098/rspb.2010.2295 Google Scholar
  93. Novotny M, Harvey S, Jemiolo B, Alberts J (1985) Synthetic pheromones that promote inter-male aggression in mice. Proc Natl Acad Sci USA 82:2059–2061PubMedCentralPubMedGoogle Scholar
  94. Olsson SB, Kesevan S, Groot AT et al (2010) Ostrinia revisited: evidence for sex linkage in European Corn Borer Ostrinia nubilalis (Hubner) pheromone reception. BMC Evol Biol 10:285. doi:10.1186/1471-2148-10-285 PubMedCentralPubMedGoogle Scholar
  95. Peeters C, Monnin T, Malosse C (1999) Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc R Soc Lond B 266:1323–1327. doi:10.1098/rspb.1999.0782 Google Scholar
  96. Phelan MM, Mclean L, Beynon RJ, Hurst JL, Lian L (2012) Structural insights into the specificity of darcin, an atypical major urinary protein. PDB 2L9C, doi:10.2210/pdb2l9c/pdb
  97. Penn DJ (2002) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1–21Google Scholar
  98. Porter RH, Winberg J (1999) Unique salience of maternal breast odors for newborn infants. Neurosci Biobehav Rev 23:439–449PubMedGoogle Scholar
  99. Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236Google Scholar
  100. Roberts SA, Simpson DM, Armstrong SD, Davidson AJ, Robertson DH, McLean L, Beynon RJ, Hurst JL (2010) Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male’s odour. BMC Biol 8:75PubMedCentralPubMedGoogle Scholar
  101. Roelofs WL (1995) Chemistry of sex attraction. Proc Natl Acad Sci USA 92:44–49PubMedCentralPubMedGoogle Scholar
  102. Ryne C, Svensson GP, Löfstedt C (2001) Mating disruption of Plodia interpunctella in small-scale plots: effects of pheromone blend, emission rates, and population density. J Chem Ecol 27:2109–2124PubMedGoogle Scholar
  103. Schiestl FP (2005) On the success of a swindle: pollination by deception in orchids. Naturwissenschaften 92:255–264PubMedGoogle Scholar
  104. Schiestl FP, Peakall R, Mant JG et al (2003) The chemistry of sexual deception in an orchid-wasp pollination system. Science 302:437–438. doi:10.1126/science.1087835 PubMedGoogle Scholar
  105. Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee (Apis mellifera L). J Chem Ecol 31:2731–2745PubMedGoogle Scholar
  106. Smadja C, Butlin RK (2009) On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102:77–97. doi:10.1038/hdy.2008.55 PubMedGoogle Scholar
  107. Smith AA, Hölldobler B, Liebig J (2009) Cuticular hydrocarbons reliably identify cheaters and allow enforcement of altruism in a social insect. Curr Biol 19:78–81. doi:10.1016/j.cub.2008.11.059 PubMedGoogle Scholar
  108. Sorensen PW, Scott AP, Kihslinger RL (2000) How common hormonal metabolites function as relatively specific pheromonal signals in the goldfish. In: Norberg B, Kjesbu OS, Taranger GL et al. (eds) Proceedings of the sixth international symposium on the reproductive physiology of fish. Institute of Marine Research and University of Bergen, Bergen, pp 125–128Google Scholar
  109. Soroker V, Vienne C, Hefetz A (1995) Hydrocarbon dynamics within and between nestmates in Cataglyphis niger (Hymenoptera: Formicidae). J Chem Ecol 21:365–378PubMedGoogle Scholar
  110. Spors H, Wachowiak M, Cohen LB, Friedrich RW (2006) Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. J Neurosci 26:1247–1259. doi:10.1523/JNEUROSCI.3100-05.2006 PubMedGoogle Scholar
  111. Steiger S, Schmitt T, Schaefer HM (2011) The origin and dynamic evolution of chemical information transfer. Proc R Soc Lond B 278:970–979. doi:10.1098/rspb.2010.2285 Google Scholar
  112. Stensmyr MC, Urru I, Collu I et al (2002) Pollination: rotting smell of dead-horse arum florets. Nature 420:625–626PubMedGoogle Scholar
  113. Stowe MK, Tumlinson JH, Heath RR (1987) Chemical mimicry: bolas spiders emit components of moth prey species sex pheromones. Science (80-) 236:964–967Google Scholar
  114. Tanaka N, Awasaki T, Shimada T (2004) Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr Biol 14:449–457. doi:10.1016/j PubMedGoogle Scholar
  115. Todd JL, Baker TC (1999) Function of peripheral olfactory organs. In: Hansson BS (ed) Insect olfaction. Springer, Berlin, pp 67–96Google Scholar
  116. Touhara K (2008) Sexual communication via peptide and protein pheromones. Curr Opin Pharmacol 8:759–764PubMedGoogle Scholar
  117. Toyoda F, Yamamoto K, Iwata T et al (2004) Peptide pheromones in newts. Peptides 25:1531–1536PubMedGoogle Scholar
  118. van Zweden JS, Fürst MA, Heinze J, D’Ettorre P (2007) Specialization in policing behaviour among workers of the ant Pachycondyla inversa. Proc R Soc Lond B 274:1421–1428. doi:10.1098/rspb.2007.0113 Google Scholar
  119. van Zweden JS, Dreier S, d’Ettorre P (2009) Disentangling environmental and heritable nestmate recognition cues in a carpenter ant. J Insect Physiol 55:159–164. doi: DOI: 10.1016/j.jinsphys.2008.11.001 Google Scholar
  120. van Zweden JS, d’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ, Bagneres AG (eds) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge, pp 222–243Google Scholar
  121. van Zweden JS, Brask JB, Christensen JH et al (2010) Blending of heritable recognition cues among ant nestmates creates distinct colony gestalt odours but prevents within-colony nepotism. J Evol Biol 23:1498–1508. doi:10.1111/j.1420-9101.2010.02020.x PubMedGoogle Scholar
  122. Vickers NJ, Baker TC (1994) Reiterative responses to single strands of odor promote sustained upwind flight and odor source location by moths. Proc Natl Acad Sci USA 91:5756–5760PubMedCentralPubMedGoogle Scholar
  123. Wark B, Lundstrom BN, Fairhall A (2007) Sensory adaptation. Curr Opin Neurobiol 17:423–429PubMedCentralPubMedGoogle Scholar
  124. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–46. doi: 10.1146/annurev.cellbio.21.012704.131001 Google Scholar
  125. Webster DR, Weissburg MJ (2009) The hydrodynamics of chemical cues among aquatic organisms. Annu Rev Fluid Mech 41:73–90Google Scholar
  126. Witzgall P, Frerot B (1989) Pheromone emission by individual females of carnation tortrix, Cacoecimorpha pronubana. J Chem Ecol 15:707–717PubMedGoogle Scholar
  127. Wright GA, Kottcamp SM, Thomson MGA (2008) Generalization mediates sensitivity to complex odor features in the honeybee. Plos One 3:e1704PubMedCentralPubMedGoogle Scholar
  128. Wyatt TD (2009) Fifty years of pheromones. Nature 457:262–263PubMedGoogle Scholar
  129. Wyatt TD (2010) Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J Comp Physiol A 196:685–700. doi:10.1007/s00359-010-0564-y Google Scholar
  130. Wyatt TD (2011) Pheromones and behavior. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, New York, pp 23–38Google Scholar
  131. Wyatt TD (2014) Pheromones and animal behavior: chemical signals and signature mixtures, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  132. Zaher HS, Green R (2009) Quality control by the ribosome following peptide bond formation. Nature 457:161–166. doi:10.1038/nature07582 PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Volker Nehring
    • 1
  • Tristram D. Wyatt
    • 2
  • Patrizia d’Ettorre
    • 3
  1. 1.University Freiburg, Biology I, Hauptstrasse 1FreiburgGermany
  2. 2.Department of ZoologyUniversity of OxfordOxfordUK
  3. 3.Laboratory of Experimental and Comparative EthologySorbonne Paris CitéFrance

Personalised recommendations