Abstract
Sociality is widespread in caterpillars, but the communication mechanisms used for group formation and cohesion are poorly understood. Here, we present the first evidence that caterpillars produce complex vibratory signals to advertise food and shelter sites to conspecifics. We first tested the hypothesis that early instars of the masked birch caterpillar (Drepana arcuata) actively form groups. Larvae placed alone on different leaves of a birch twig began assembling within minutes and forming groups of 2–6 at a median time of 2 h. In Y-choice experiments, larvae joined arms occupied by conspecifics significantly more frequently than unoccupied arms. To test the hypothesis that group formation is vibration-mediated, signals were monitored in solitary residents of silk leaf shelters before and during natural recruitment events. Four distinct signal types were recorded: anal scraping, mandible drumming, mandible scraping, and buzz scraping. Anal scraping and buzz scraping were the most common in residents prior to being approached, and these signals were strongly correlated to feeding and laying silk. Signaling occurred in 100% of residents, and higher signal rates resulted in significantly faster recruitment times. As a recruit approached a resident, complex signaling interactions occurred, which may communicate information about resource quality or location. We conclude that caterpillars, similar to other social animals, use acoustic communication to advertise resources. The vibratory signaling repertoire of these tiny caterpillars exhibits a complexity rivaling that of eusocial insects. Further investigations of vibroacoustic communication are essential to fully appreciate the intricacies of social interactions in caterpillars and other juvenile insects.
Significance statement
Group living provides many survival benefits to juvenile insects such as caterpillars, but little is known about the communication signals mediating social interactions such as group formation. Our study shows that caterpillars use vibration signals to “invite” conspecifics to social gatherings. Pinhead-sized early-instar caterpillars (Drepana arcuata) are capable of locating conspecifics on birch leaves to form small groups. But how do they accomplish this? We report that individual resident caterpillars established in a silk shelter produced complex vibrations by dragging their anal segments, scraping and drumming their mouthparts, and tremulating their bodies to advertise a feeding spot and shelter. These results provide the first evidence that caterpillars use vibratory signaling to form social groups, providing insight into the poorly understood role of vibratory communication in juvenile insects.
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References
Blumstein DT, Daniel JC, Evans CS (2010) JWatcher V1.0. University of California, Los Angeles and Macquarie University, Sydney
Bradbury JW, Vehrencamp SL (2011) Principles of animal communication, 2nd edn. Sinauer Associates, Sunderland
Bryner R (1999) Drepanidae - Drépanidés. In Les Papillons et leur Biotopes: Espèces; Danger qui les menacent; Protection. Suisse et regions limitrophe, vol. 2 (ed. L. S. p. l. P. d. l. Nature), pp. 447–476 Switzerland: Pro Natura
Caine NG, Addington RL, Windfelder TL (1995) Factors affecting the rates of food calls given by red-bellied tamarins. Anim Behav 50:53–60
Clay Z, Smith CL, Blumstein DT (2012) Food-associated vocalizations in mammals and birds: what do these calls really mean? Anim Behav 83:323–330
Cocroft RB (1996) Insect vibrational defence signals. Nature 382:679–680
Cocroft RB (2005) Vibrational communication facilitates cooperative foraging in a phloem-feeding insect. P Roy Soc Lond B Bio 272:1023–1029
Cocroft RB, Hamel JA (2010) Vibrational communication in the “other insect societies”: a diversity of ecology signals, and signal functions. In: O’Connell-Rodwell CE (ed) The use of vibrations in communication: properties, mechanism and function across taxa. Transworld Research Network, Kerala, India, pp 47–68
Cocroft RB, Rodríguez RL (2005) The behavioral ecology of insect vibrational communication. Bioscience 55:323–334
Costa JT (2006) The other insect societies. The Belknap Press of Harvard University Press, Cambridge
Costa JT, Pierce NE (1997) Social evolution in the Lepidoptera: ecological context and communication in larval societies. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 407–422
Di Bitetti MS (2003) Food-associated calls of tufted capuchin monkeys (Cebus apella nigritus) are functionally referential signals. Behaviour 140:565–592
Di Bitetti MS (2005) Food-associated calls and audience effects in tufted capuchin monkeys, Cebus apella nigritus. Anim Behav 69:911–919
Dussutour A, Nicolis SC, Despland E, Simpson SJ (2008) Individual differences influence collective behaviour in social caterpillars. Anim Behav 76:5–16
Elgar MA (1986) House sparrows establish flocks by giving chirrup calls if the resources are divisible. Anim Behav 34:169–174
Fitzgerald TD, Peterson SC (1988) Cooperative foraging and communication in social caterpillars. Bioscience 38:20–25
Gilbert C (1994) Form and function of stemmata in larvae of holometabolous insects. Annu Rev Entomol 39:323–349
Gros-Louis J (2004) Responses of white-faced capuchins (Cebus capucinus) to naturalistic and experimentally presented food-associated calls. J Comp Psychol 118(4):396–402
Guedes RNC, Matheson SM, Frei B, Smith ML, Yack JE (2012) Vibration detection and discrimination in the masked birch caterpillar (Drepana arcuata). J Comp Physiol A 198:325–335
Hill PSM (2008) Vibration communication in animals. Harvard University Press, London
Hograefe T (1984) Subtrat-stridulation bei den koloniebildended Blattwespenlarven von Hemichroa crocea (Geoff.) (Hymenoptera:Tenthredinidae). Zool Anz 213:234–241
Hrncir M, Barth FG (2014) Vibrational communication in stingless bees (Meliponini): the challenge of interpreting the signals. In: Cocroft RB, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational communication. Springer, New York, pp 349–374
Hunt JH, Richard FJ (2013) Intracolony vibroacoustic communication in social insects. Insect Soc 60:403–417
Mahurin EJ, Freeberg TM (2009) Chick-a-dee call variation in Carolina chickadees and recruiting flockmates to food. Behav Ecol 20:111–116
Matheson SM (2011) Vibratory mediated spacing in groups of insect larvae (Drepana arcuata, Lepidoptera; Scolytus multistriatus, Coleoptera). M.Sc. Dissertation, Carleton University
Prokopy RJ, Roitberg BD (2001) Joining and avoidance behavior in nonsocial insects. Annu Rev Entomol 46:631–635
Rose AH, Lindquist OH (1997) Insects of eastern hardwood trees. Canadian Forestry Service, Ottawa, Forestry Technical Report 29
Scott JL, Kawahara AY, Skevington JH, Yen SH, Sami A, Smith ML, Yack JE (2010) The evolutionary origins of ritualized acoustic signals in caterpillars. Nat Commun 1:1–9
Slocombe KE, Kaller T, Turman L, Townsend SW, Papworth S, Squibbs P, Zuberbühler K (2010) Production of food-associated calls in wild chimpanzees is dependent on the composition of the audience. Behav Ecol Sociobiol 64:1959–1966
Suzuki TN (2012) Long-distance calling by the willow tit, Poecile montanus, facilitates formation of mixed-species foraging flocks. Ethology 118:10–16
Szipl G, Boeckle M, Wascher CAF, Spreafico M (2015) With whom to dine? Ravens’ responses to food-associated calls depend on individual characteristics of the caller. Anim Behav 99:33–42
Tautz J, Roces F, Hölldobler B (1995) Use of a sound-based vibratome by leaf-cutting ants. Science 267:84–87
Travassos MA, Pierce NE (2000) Acoustics, context and function of vibrational signaling in a lycaenid butterfly-ant mutualism. Anim Behav 60:13–26
Virant-Doberlet M, Čokl A (2004) Vibrational communication in insects. Neotrop Entomol 33:121–134
Warrant EJ, Kelber A, Kristensen NP (2003) Eyes and vision. In: Kristensen NP (ed) Handbook of zoology, Part 36, Lepidoptera, moths and butterflies, vol 2: morphology, physiology and development, vol IV. Walter de Gruyter, Berlin/New York, pp 325–359
Yack JE (2016) Vibrational signaling. In: Pollack GS, Mason AC, Fay RR, Popper AN (eds) Springer handbook of auditory research: insect hearing. Springer, New York, pp 99–123
Yack JE, Gill S, Drummond-Main D, Sherratt TN (2013) Residency duration and shelter quality influence vibratory signaling displays in a territorial caterpillar. Ethology 120:354–364
Yack JE, Smith ML, Weatherhead PJ (2001) Caterpillar talk: acoustically mediated territoriality in larval Lepidoptera. P Natl Acad Sci USA 98:11371–11375
Zalucki MP, Clarke AR, Malcolm SB (2002) Ecology and behavior of first instar larval Lepidoptera. Annu Rev Entomol 47:361–393
Acknowledgements
We are grateful to Jake Miall for help with insect collection. This research was funded by the Natural Science and Engineering Council of Canada (2014-05947), the Canadian Foundation for Innovation (9555) and an Early Researcher Award (ERO7-04-1-44) to JEY, and the Brazilian National Council of Scientific and Technological Development of Brazil (301847/2015-0) to RNG.
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Communicated by W. Hughes
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Yadav, C., Guedes, R.N.C., Matheson, S.M. et al. Invitation by vibration: recruitment to feeding shelters in social caterpillars. Behav Ecol Sociobiol 71, 51 (2017). https://doi.org/10.1007/s00265-017-2280-x
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DOI: https://doi.org/10.1007/s00265-017-2280-x