Journal of Insect Behavior

, Volume 28, Issue 4, pp 482–498 | Cite as

Substrate-Borne Vibrational Signals in Mating Communication of Macrolophus Bugs

  • César GemenoEmail author
  • Giordana Baldo
  • Rachele Nieri
  • Joan Valls
  • Oscar Alomar
  • Valerio Mazzoni


The mirid bugs Macrolophus pygmaeus and M. costalis use substrate-borne vibrational signals during pair formation and in male-male interactions as determined by laser vibrometry. The vibrational communication of Macrolophus is more complex than in other mirids, with a signal repertoire composed of two elements, only produced by males, while the females are mute. The “yelp” signal consists of one or several consecutive brief pulses with harmonic structure and is commonly produced by stationary males before mating, as a key-element of courtship. “Yelping” is also associated with contacts between males. The “roar” signal differs from “yelps” in that it has a broadband frequency pattern, a longer and more variable duration than “yelping”, and is produced by males in association with walking on the leaf. Playback experiments did not affect male vibration emission, but when “roaring” was used as stimulus, it elicited a significant increase in the time spent walking. We detected significant differences between M. costalis and M. pygmaeus in some spectral parameters of the “roar” and “yelp” signals, so these signals could contain species-specific information. We conclude that “roaring” and “yelping” vibrational signals are used by Macrolophus in social communication, in particular in the context of mating behavior.


Substrate borne communication miridae courtship 



CG was funded by an Erasmus Training Grant. OA was funded by the Spanish Ministry of Economy and Competitiveness (MINECO) (Project AGL2011-24349).

Supplementary material

10905_2015_9518_MOESM1_ESM.docx (475 kb)
ESM 1 (DOCX 475 kb)
10905_2015_9518_MOESM2_ESM.docx (117 kb)
ESM 2 (DOCX 116 kb)
10905_2015_9518_MOESM3_ESM.docx (52 kb)
ESM 3 (DOCX 52 kb)
Video 1

Loading insects on the plant. The insect is sucked into the aspirator which is brought into contact with the plant. If the individual is slow at leaving the aspirator a movable plunge is used to help it to exit. The release process has to be done very slowly because if the individuals are overexcited they may not stay on the plant and will walk or fly away. (MPG 1754 kb)

Video 2

Generic sounds. Vibrations produced by a) a male walking on the leaf and “not roaring” and the same male walking on the same leaf and “roaring”, b) a male-female pair mating, and c) a female inserting an egg in the main vein of the leaf. (MPG 14022 kb)

Video 3

Male “yelp” posture. A male is standing on the edge of the leaf with the legs stretched out. He “yelps” several times. Each time that he “yelps” his legs are slightly flexed. It is a very faint movement and it may need watching it several times to clearly distinguish it. (MPG 528 kb)

Video 4

Two males. Two males are walking on a leaf and producing multiple “roaring” and “yelping”. Occasionally they contact with each other and this elicits “yelping”. Notice the two reflective stickers placed on the leaf. One of them is reflecting the laser beam from the laser vibrometer (red dot). (MPG 10058 kb)

Video 5

Mating. A male (below) contacts a female (above) and “yelps”. The female shakes her body and the male walks away. After a few seconds the male (left) turns around and approaches the female (right) as he “roars”. He contacts her with the antennae, then he “yelps” and immediately mounts her. (MPG 2142 kb)

Video 6

Close-up mating with immobilized female. A female (left) is immobilized by squeezing her head with forceps. A male approaches her (right) and after contacting her with his antennae he starts to “yelp”. There is a second male on the leaf that also “yelps” and approaches the scene (far left) as he “roars”. The “yelps” from each male can be distinguished. The male that is with the female produces a higher pitch “yelp” than the other male. The male that is contacting the female with the antennae turns around, produces 4 “yelps” and mates with the immobilized female. After the couple has formed, the other male “yelps” 3 times. (MPG 1540 kb)


  1. Agresti A (2014) Categorical data analysis. John Wiley & Sons, New YorkGoogle Scholar
  2. Alomar Ò, Riudavets J, Castañé C (2006) Macrolophus caliginosus in the biological control of Bemisia tabaci on greenhouse melons. Biol Control 36(2):154–162CrossRefGoogle Scholar
  3. Bro-Jørgensen J (2010) Dynamics of multiple signalling systems: animal communication in a world in flux. Trends Ecol Evol 25(5):292–300CrossRefPubMedGoogle Scholar
  4. Byers JA, Fefer D, Levi-Zada A (2013) Sex pheromone component ratios and mating isolation among three Lygus plant bug species of North America. Naturwissenschaften 100(12):1115–1123CrossRefPubMedGoogle Scholar
  5. Castañé C, Alomar O, Riudavets J, Gemeno C (2007) Reproductive biology of the predator Macrolophus caliginosus: effect of age on sexual maturation and mating. Biol Control 43(3):278–286CrossRefGoogle Scholar
  6. Castañé C, Agustí N, Arnó J, Gabarra R, Riudavets J, Comas J, Alomar O (2013) Taxonomic identification of Macrolophus pygmaeus and Macrolophus melanotoma based on morphometry and molecular markers. Bull Entomol Res 103(2):204–215CrossRefPubMedGoogle Scholar
  7. Cocroft RB, McNett GD (2005) Vibratory communication in treehoppers (Hemiptera: Membracidae). In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication: physiology, behaviour, ecology and evolution. CRC Press, Boca Raton, pp 305–317Google Scholar
  8. Čokl A, Virant-Doberlet M (2003) Communication with substrate- borne signals in small plant-dwelling insects. Annu Rev Entomol 48(1):29–50CrossRefPubMedGoogle Scholar
  9. de Groot M, Derlink M, Pavlovčič P, Prešern J, Čokl A, Virant-Doberlet M (2012) Duetting behaviour in the leafhopper Aphrodes makarovi (Hemiptera: Cicadellidae). J Insect Behav 25(5):419–440CrossRefGoogle Scholar
  10. Elias DO, Mason AC (2010) Signaling in variable environments: substrate-borne signaling mechanisms and communication behavior in spiders. In: O’Connell-Rodwell CE (ed) The use of vibrations in communication: properties, mechanisms and function across taxa, research signpost, Scarborough, Ontario, CanadaGoogle Scholar
  11. Fountain M, Jåstad G, Hall D, Douglas P, Farman D, Cross J (2014) Further studies on sex pheromones of female Lygus and related bugs: development of effective lures and investigation of species-specificity. J Chem Ecol 40(1):71–83CrossRefPubMedGoogle Scholar
  12. Franco K, Jauset A, Castañé C (2011) Monogamy and polygamy in two species of mirid bugs: a functional-based approach. J Insect Physiol 57(2):307–315CrossRefPubMedGoogle Scholar
  13. Gemeno C, Alomar O, Riudavets J, Castañé C (2007) Mating periodicity and post-mating refractory period in the zoophytophagous plant bug Macrolophus caliginosus (Heteroptera: Miridae). Eur J Entomol 104(4):715–720CrossRefGoogle Scholar
  14. Gemeno C, Laserna N, Riba M, Valls J, Castañé C, Alomar Ò (2012) Cuticular hydrocarbons discriminate cryptic Macrolophus species (Hemiptera: Miridae). Bull Entomol Res 102(6):624–631CrossRefPubMedGoogle Scholar
  15. Gerhardt HC (1991) Female mate choice in treefrogs: static and dynamic acoustic criteria. Anim Behav 42(4):615–635CrossRefGoogle Scholar
  16. Gogala M (2005) Vibratory signals produced by Heteroptera – Pentatomorpha and Cimicomorpha. In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication: physiology, behaviour, ecology and evolution. CRC Press, Boca Raton, pp 275–295CrossRefGoogle Scholar
  17. Groot AT, Wall E, Schuurman A, Visser JH, Blommers LH, Beek TA (1998) Copulation behavior of Lygocoris pabulinus under laboratory conditions. Entomol Exp Appl 88(3):219–228CrossRefGoogle Scholar
  18. Koczor S, Čokl A (2014) Percussion signals of Lygus rugulipennis Poppius (Heteroptera: Miridae). Cent Eur J Biol 9(5):543–549Google Scholar
  19. Lakes-Harlan R, Strauß J (2014) Functional morphology and evolutionary diversity of vibration receptors in insects. In: Cocroft RB, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational communication. Springer, London, pp 277–302Google Scholar
  20. Mazzoni V, Prešern J, Lucchi A, Virant-Doberlet M (2009) Reproductive strategy of the Nearctic leafhopper Scaphoideus titanius Ball (Hemiptera: Cicadellidae). Bull Entomol Res 99(4):401–413CrossRefPubMedGoogle Scholar
  21. Mazzoni V, Lucchi A, Ioriatti C, Virant-Doberlet M, Anfora G (2010) Mating behavior of Hyalesthes obsoletus (Hemiptera: Cixiidae). Ann Entomol Soc Am 103(5):813–822CrossRefGoogle Scholar
  22. Mazzoni V, Eriksson A, Anfora G, Lucchi A, Virant-Doberlet M (2014) Active space and the role of amplitude in plant-borne vibrational communication. In: Cocroft RB, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational communication. Springer, London, pp 125–145Google Scholar
  23. Michelsen A, Fink F, Gogala M, Traue D (1982) Plants as transmission channels for insect vibrational song. Behav Ecol Sociobiol 11(4):269–281CrossRefGoogle Scholar
  24. Millar JG (2005) Pheromones of true bugs. In: Schulz S (ed) The chemistry of pheromones and other semiochemicals II. Springer, Berlin, pp 37–84Google Scholar
  25. Perdikis D, Fantinou A, Lykouressis D (2011) Enhancing pest control in annual crops by conservation of predatory Heteroptera. Biol Control 59(1):13–21CrossRefGoogle Scholar
  26. Pérez-Hedo M, Urbaneja A (2014) Prospects for predatory mirid bugs as biocontrol agents of aphids in sweet peppers. J Pest Sci. doi: 10.1007/s10340-014-0587-1 Google Scholar
  27. Polajnar J, Svenšek D, Čokl A (2012) Resonance in herbaceous plant stems as a factor in vibrational communication of pentatomid bugs (Heteroptera: Pentatomidae). J R Soc Interface 9:1898–1907. doi: 10.1098/rsif.2011.0770 PubMedCentralCrossRefPubMedGoogle Scholar
  28. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  29. Rendall D, Owen MJ, Ryan MJ (2009) What do animal signals mean? Anim Behav 78(2):233–240CrossRefGoogle Scholar
  30. Ringo J (1996) Sexual receptivity in insects. Annu Rev Entomol 41(1):473–494CrossRefPubMedGoogle Scholar
  31. Searcy WA, Nowicki S (2009) Sexual selection and the evolution of animal signals. In: Squire LR (ed) Encyclopedia of neuroscience, vol 8. Academic, Oxford, pp 769–776Google Scholar
  32. Smith JM, Harper D (2003) Animal signals. Oxford University Press, OxfordGoogle Scholar
  33. Virant-Doberlet M, Cokl A (2004) Vibrational communication in insects. Neotrop Entomol 33(2):121–134CrossRefGoogle Scholar
  34. Virant-Doberlet M, Čokl A, Zorović M (2006) Use of substrate vibrations for orientation: from behaviour to physiology. In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication: physiology, behaviour, ecology and evolution. CRC Press, Boca Raton, pp 81–97Google Scholar
  35. Wessel A, Mühlethaler R, Hartung V, Kuštor, Gogala M (2014) The tymbal: evolution of a complex vibration-producing organ in the Tymbalia (Hemiptera excl. Sternorrhyncha). In: Cocroft RB, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational communication. Springer, London, pp 395–444Google Scholar
  36. Wheeler AG Jr (2001) Biology of the plant bugs. Cornell University Press, IthacaGoogle Scholar
  37. Yamane T, Yasuda T (2014) The effects of mating status and time since mating on female sex pheromone levels in the rice leaf bug, Trigonotylus caelestialium. Naturwissenschaften 101(2):153–156PubMedCentralCrossRefPubMedGoogle Scholar
  38. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53(1):205–214CrossRefPubMedGoogle Scholar
  39. Zappalà L, Biondi A, Alma et al (2013) Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies. J Pest Sci 86(4):635–647CrossRefGoogle Scholar
  40. Zhang QH, Aldrich JR (2003) Pheromones of milkweed bugs (Heteroptera: Lygaeidae) attract wayward plant bugs: Phytocoris mirid sex pheromone. J Chem Ecol 29(8):1835–1851CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • César Gemeno
    • 1
    Email author
  • Giordana Baldo
    • 1
  • Rachele Nieri
    • 2
  • Joan Valls
    • 3
  • Oscar Alomar
    • 4
  • Valerio Mazzoni
    • 2
  1. 1.Department of Crop and Forest SciencesUniversity of LleidaLleidaSpain
  2. 2.Research and Innovation CenterFondazione Edmund MachS. Michele all’AdigeItaly
  3. 3.Biostatistics Unit, Institut de Recerca Biomèdica de Lleida (IRBLLEIDA)Hospital Universitari Arnau de Vilanova de Lleida (HUAV)LleidaSpain
  4. 4.IRTA CabrilsCabrilsSpain

Personalised recommendations