Bimodal alarm signals modulate responses to monomodal alarm signals in Camponotus modoc carpenter ants

Abstract

Distressed western carpenter ants,Camponotus modoc, produce alarm pheromone and substrate-borne vibrations. The alarm pheromone attracts nestmates but the effects of vibratory signals, or of bimodal pheromonal and vibratory signals, are not known. Worker ants of two Camponotus congeners reportedly stand still (“freeze”) or run fast in response to engineered drumming vibrations inputted on plastic, but many responses to ant-produced vibratory signals on wood have not yet been investigated. Generally, orientating toward signalers under vertebrate predator attack seems maladaptive and not beneficial to ant colonies. We tested the hypotheses (1) that vibratory alarm signals cause freezing, rapid running but not attraction of nestmates, and (2) that bimodal alarm signals modulate responses to monomodal alarm signals, thereby possibly reducing predation risk. Laser Doppler vibrometry recordings revealed that the ants’ vibratory signals readily propagate through ant nest lamellae, and thus quickly inform nest mates of perceived threats. With a speaker modified to record and deliver vibratory signals, we obtained drumming signals of distressed ants on a Douglas fir veneer, and bioassayed signal effects on ants in an arena with a suspended veneer floor. In response playback of vibratory signals, ants ran rapidly, or froze, but did not approach the vibratory signals. Exposed to alarm pheromone, ants frequently visited the pheromone source. However, concurrently exposed to both alarm pheromone and vibratory signals, ants visited the pheromone source less often but spent more time “frozen.” The ants’ modulated responses to bimodal signals seem adaptive but the reproductive fitness benefits are still to be quantified.

Keywords

alarm pheromone / communication / Formicidae / Hymenoptera / nest defense / vibratory signal

References

[1] Abbot, P. (2022) Defense in social insects: diversity, division of labor, and evolution. Annual Review of Entomology,67,407–436.

[2] Angilletta, M.J.,Roth, T.C.,Wilson, R.S.,Niehaus, A.C. and Ribeiro, P.L. (2008) The fast and the fractalous: speed and tortuosity trade off in running ants. Functional Ecology,22,78–83.

[3] Ayasse, M. and Paxton, R.J. (2002) Brood protection in social insects. In Chemoecology of Insect Eggs and Egg Deposition (eds. M. Hilker & T. Meiners), pp. 117–148. Wiley-Blackwell.

[4] Baracchi, D.,Giurfa, M. and D’Ettorre, P. (2021) Formic acid modulates latency and accuracy of nestmate recognition in carpenter ants. Journal of Experimental Biology,224,jeb242784.

[5] Batchelor, T.P. and Briffa, M. (2011) Fight tactics in wood ants: individuals in smaller groups fight harder but die faster. Proceedings of the Royal Society B: Biological Sciences,278,3243–3250.

[6] Bennett, A.T.D.,Lloyd, M.H. and Cuthill, I.C. (1996) Ant-derived formic acid can be toxic for birds. Chemoecology,7,189–190.

[7] Bota, J.L.,Schöner, M.G.,Schöner, C.R. and Eberhard, M.J.B. (2022) Rustling ants: vibrational communication performed by two Camponotus species in Borneo. Arthropod Structure and Development,70,101172.

[8] Bradshaw, J.W.S.,Baker, R. and Howse, P.E. (1975) Multicomponent alarm pheromones of the weaver ant. Nature,258,230–231.

[9] Bradshaw, J.W.S.,Baker, R. and Howse, P.E. (1979) Multicomponent alarm pheromones in the mandibular glands of major workers of the African weaver ant,Oecophylla longinoda. Physiological Entomology,4,15–25.

[10] Brooks, M.E.,Kristensen, K.,van Benthem, K.J.,Magnusson, A.,Berg, C.W.,Nielsen, A. et al. (2019) GlmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal,9,378–400.

[11] Chapman, B.B.,Thain, H.,Coughlin, J. and Hughes, W.O.H. (2011) Behavioural syndromes at multiple scales in Myrmica ants. Animal Behaviour,82,391–397.

[12] Chen, J.,Rashid, T. and Feng, G. (2012) Toxicity of formic acid to red imported fire ants,Solenopsis invicta Buren. Pest Management Science,68,1393–1399.

[13] Dornhaus, A. and Powell, S. (2010) Foraging and defence strategies. In Ant Ecology (eds. L. Lach & C. L. Parr), pp. 210–230. Oxford University Press.

[14] Dudley, R.,Byrnes, G.,Yanoviak, S.P.,Borrell, B.,Brown, R.M. and McGuire, J.A. (2007) Gliding and the functional origins of flight: biomechanical novelty or necessity? Annual Review of Ecology. Evolution, and Systematics,38,179–201.

[15] Ershov, D.,Phan, M.S.,Pylvänäinen, J.W.,Rigaud, S.U.,Le Blanc, L.,Charles-Orszag, A. et al. (2022) TrackMate 7: integrating state-of-the-art segmentation algorithms into tracking pipelines. Nature Methods,19,829–832.

[16] Feldhaar, H. (2011) Predators as prey: top-down effects on predatory Hymenoptera. In Predation in the Hymenoptera: An Evolutionary Perspective (ed. C. Polidori), pp. 217–245. Transworld Research Network.

[17] Fuchs, S. (1976) The response to vibrations of the substrate and reactions to the specific drumming in colonies of carpenter ants (Camponotus, Formicidae, Hymenoptera). Behavioral Ecology and Sociobiology,1,155–184.

[18] Golden, T.M.J. and Hill, P.S.M. (2016) The evolution of stridulatory communication in ants, revisited. Insectes Sociaux,63,309–319.

[19] Grasso, D.A.,Giannetti, D.,Castracani, C. and Spotti, F.A. (2020) Rolling away: a novel context-dependent escape behaviour discovered in ants. Scientific Reports,10,3874.

[20] Gyug, L.W.,Higgins, R.J.,Todd, M.A.,Meggs, J.M. and Lindgren, B.S. (2014) Dietary dependence of Williamson’s Sapsucker nestlings on ants associated with dead and decaying wood in British Columbia. Canadian Journal of Forest Research,44,628–637.

[21] Hager, F.A.,Kirchner, L. and Kirchner, W.H. (2017) Directional vibration sensing in the leafcutter ant Atta sexdens. Biology Open,6,1949–1952.

[22] Hansen, L.D. and Akre, R.D. (1985) Biology of Carpenter Ants in Washington State (Hymenoptera: Formicidae: Camponotus), pp. 1–65. Washington State University.

[23] Hansen, L.D. and Klotz, J.H. (2005) Carpenter Ants of the United States and Canada. Cornell University Press.

[24] Hartig, F. (2022) DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models (0.4.6). https://cran.r-project.org/package=DHARMa.

[25] Hölldobler, B. (1999) Multimodal signals in ant communication. Journal of Comparative Physiology A,184,129–141.

[26] Hölldobler, B. and Roces, F. (2001) The behavioral ecology of stridulatory communication in leaf-cutting ants. In Model Systems in Behavioral Ecology -Integrating Conceptual, Theoretical, and Empirical Approaches (ed. A.L Dugatkin), pp. 92–109. Princeton University Press.

[27] Hölldobler, B. and Wilson, E.O. (1990) The Ants. Harvard University Press.

[28] Huang, M.H. (2010) Multi-phase defense by the big-headed ant,Pheidole obtusospinosa, against raiding army ants. Journal of Insect Science,10,1.

[29] Hunt, J.H. and Richard, F.J. (2013) Intracolony vibroacoustic communication in social insects. Insectes Sociaux,60,403–417.

[30] Jelley, C. and Moreau, C.S. (2023) Aggressive behavior across ant lineages: importance, quantification, and associations with trait evolution. Insectes Sociaux,70,393–403.

[31] Leclercq, S.,Braekman, J.C.,Daloze, D. and Pasteels, J.M. (2000) The defensive chemistry of ants. Fortschritte der Chemie Organischer Naturstoffe. Progress in the Chemistry of Organic Natural Products,79,115–229.

[32] Lenth, R. (2023) Estimated Marginal Means, Aka Least-squares Means (R package version 1.8.4-1). https://cran.r-project.org/package=emmeans.

[33] Markl, H. (1965) Stridulation in leaf-cutting ants. Science,149,1392–1393.

[34] Markl, H. and Fuchs, S. (1972) Alarm by rapping in carpenter ants (Camponotus, Formicidae, Hymenoptera). Zeitschrift für vergleichende Physiologie,76,204–225.

[35] Morgan, E. (2008) Chemical sorcery for sociality: exocrine secretions of ants (Hymenoptera: Formicidae). Myrmecological News,11,79–90.

[36] Norman, V.C.,Hoppé M. and Hughes, W.O.H. (2014) Old and wise but not size: Factors affecting threat response behaviour and nestmate recognition in Acromyrmex echinatior leaf-cutting ants. Insectes Sociaux,61,289–296.

[37] Nouvian, M. and Breed, M.D. (2020) Colony defense, survival and reproduction. In Encyclopedia of Social Insects (ed. C. Starr), pp. 1–11. Springer,Cham.

[38] Nowbahari, E.,Fénéron, R. and Malherbe, M.C. (1999) Effect of body size on aggression in the ant,Cataglyphis niger (Hymenoptera; Formicidae). Aggressive Behavior,25,369–379.

[39] Noyce, K.V.,Kannowski, P.B. and Riggs, M.R. (1997) Black bears as ant-eaters: Seasonal associations between bear myrmecophagy and ant ecology in north-central Minnesota. Canadian Journal of Zoology,75,1671–1686.

[40] Parmentier, T.,Dekoninck, W. and Wenseleers, T. (2015) Context-dependent specialization in colony defence in the red wood ant Formica rufa. Animal Behaviour,103,161–167.

[41] Pedersen, T. (2023) patchwork: The Composer of Plots. R package version 1.1.3. https://cran.r-project.org/package=patchwork.

[42] Pokorny, T.,Sieber, L.M.,Hofferberth, J.E.,Bernadou, A. and Ruther, J. (2020) Age-dependent release of and response to alarm pheromone in a ponerine ant. Journal of Experimental Biology,223,jeb218040.

[43] Powell, S. (2008) Ecological specialization and the evolution of a specialized caste in Cephalotes ants. Functional Ecology,22,902–911.

[44] Powell, S. and Clark, E. (2004) Combat between large derived societies: a subterranean army ant established as a predator of mature leaf-cutting ant colonies. Insectes Sociaux,51,342–351.

[45] R Core Team. (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing,Vienna, Austria.

[46] Raley, C.M. and Aubry, K.B. (2006) Foraging ecology of pileated woodpeckers in coastal forests of Washington. Journal of Wildlife Management,70,1266–1275.

[47] Renyard, A.,Alamsetti, S.K.,Gries, R.,Munoz, A. and Gries, G. (2019) Identification of the trail pheromone of the carpenter ant Camponotus modoc. Journal of Chemical Ecology,45,901–913.

[48] Renyard, A. and Gries, G. (2024) R-code and data from: Bi-modal alarm signals modulate responses to mono-modal alarm signals in Camponotus modoc carpenter ants V1. Mendeley Data,

[49] Renyard, A.,Gries, R. and Gries, G. (2020) A blend of formic acid, benzoic acid, and aliphatic alkanes mediates alarm recruitment responses in western carpenter ants,Camponotus modoc. Entomologia Experimentalis et Applicata,168,311–321.

[50] Robinson, E.J. and Stockdan, J.A. (2021) Wood Ants (Formica rufa Species Group). In Encyclopedia of Social Insects (ed. C.K. Starr), pp. 1028–1036. Springer International Publishing.

[51] Roces, F. and Hölldobler, B. (1996) Use of stridulation in foraging leaf-cutting ants: mechanical support during cutting or short-range recruitment signal? Behavioral Ecology and Sociobiology,39,293–299.

[52] Roces, F.,Tautz, J. and Hölldobler, B. (1993a) Stridulation in leaf-cutting ants: short-range recruitment through plant-borne vibrations. Naturwissenschaften,80,521–524.

[53] Roces, F.,Tautz, J. and Hölldobler, B. (1993b) Stridulation in leaf-cutting ants. Naturwissenschaften,80,521–524.

[54] Rossi, N.,Baracchi, D.,Giurfa, M. and d’Ettorre, P. (2019) Pheromone-induced accuracy of nestmate recognition in carpenter ants: simultaneous decrease in type I and type II errors. American Naturalist,193,267–278.

[55] Sakai, M. (2021) Death-Feigning in Insects: Mechanism and Function of Tonic Immobility (Sakai, Mas). Springer,Singapore.

[56] Sakata, H. and Katayama, N. (2001) Ant defence system: a mechanism organizing individual responses into efficient collective behavior. Ecological Research,16,395–403.

[57] Sasaki, T.,Hölldobler, B.,Millar, J.G. and Pratt, S.C. (2014) A context-dependent alarm signal in the ant Temnothorax rugatulus. Journal of Experimental Biology,217,3229–3236.

[58] Scharf, I.,Pamminger, T. and Foitzik, S. (2011) Differential response of ant colonies to intruders: attack strategies correlate with potential threat. Ethology,117,731–739.

[59] Smith, A.A. and Haight, K.L. (2008) Army ants as research and collection tools. Journal of Insect Science,8,71.

[60] Stuart, R.J. and Bell, P.D. (1980) Stridulation by workers of the ant,Leptothorax muscorum (Nylander) (Hymenoptera: Formicidae). Psyche: A Journal of Entomology,87,199–210.

[61] Swenson, J.E.,Jansson, A.,Riig, R. and Sandegren, F. (1999) Bears and ants: myrmecophagy by brown bears in central Scandinavia. Canadian Journal of Zoology,77,551–561.

[62] Thompson, S.K. (2012) Sampling (3rd ed.). John Wiley & Sons, Inc.,Hoboken, New Jersey.

[63] Touchard, A.,Aili, S.R.,Fox, E.G.P.,Escoubas, P.,Orivel, J.,Nicholson, G.M. et al. (2016) The biochemical toxin arsenal from ant venoms. Toxins,8,30.

[64] Van Wilgenburg, E.,Clémencet, J. and Tsutsui, N.D. (2010) Experience influences aggressive behaviour in the Argentine ant. Biology Letters,6,152–155.

[65] Verheggen, F.J.,Haubruge, E. and Mescher, M.C. (2010) Alarm pheromones-chemical signaling in response to danger. In Vitamins and Hormones (ed. G. Litwack), pp. 215–239. Elsevier.

[66] Weber, N.A. (1957) The nest of an anomalous colony of the arboreal ant Cephalotes atratus. Psyche,64,60–69.

[67] Wickham, H. (2011) The split-apply-combine strategy for data analysis. Journal of Statistical Software,40,1–29.

[68] Wickham, H. (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag.

[69] Wickham, H.,Averick, M.,Bryan, J.,Chang, W.,McGowan, L.,François, R. et al. (2019) Welcome to the tidyverse. Journal of Open Source Software,4,1686.

[70] Yanoviak, S.P.,Dudley, R. and Kaspari, M. (2005) Directed aerial descent in canopy ants. Nature,433,621–624.

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