Ants regulate colony spatial organization using multiple chemical road-signs

Yael Heyman; Noam Shental; Alexander Brandis; Abraham Hefetz; Ofer Feinerman

doi:10.1038/ncomms15414

journal article Open Access Jun 01, 2017

Ants regulate colony spatial organization using multiple chemical road-signs

Yael Heyman Noam Shental Alexander Brandis Abraham Hefetz Ofer Feinerman

Nature Communications Vol. 8 No. 1 · Springer Science and Business Media LLC

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Abstract

AbstractCommunication provides the basis for social life. In ant colonies, the prevalence of local, often chemically mediated, interactions introduces strong links between communication networks and the spatial distribution of ants. It is, however, unknown how ants identify and maintain nest chambers with distinct functions. Here, we combine individual tracking, chemical analysis and machine learning to decipher the chemical signatures present on multiple nest surfaces. We present evidence for several distinct chemical ‘road-signs’ that guide the ants’ movements within the dark nest. These chemical signatures can be used to classify nest chambers with different functional roles. Using behavioural manipulations, we demonstrate that at least three of these chemical signatures are functionally meaningful and allow ants from different task groups to identify their specific nest destinations, thus facilitating colony coordination and stabilization. The use of multiple chemicals that assist spatiotemporal guidance, segregation and pattern formation is abundant in multi-cellular organisms. Here, we provide a rare example for the use of these principles in the ant colony.

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References

59

[1]

Wilson, E. O. & Hölldobler, B. Dense heterarchies and mass communication as the basis of organization in ant colonies. Trends Ecol. Evol. 3, 65–68 (1988). 10.1016/0169-5347(88)90018-3

[2]

Sumpter, D. J. The principles of collective animal behaviour. Philos. Trans. R. Soc. Lond. B. Biol. Sci 361, 5–22 (2006). 10.1098/rstb.2005.1733

[3]

Camazine, S. et al. Self-organisation in biological systems. Princet. Stud. Complex 538, 217–376 (2001).

[4]

Sendova-Franks, A. B. & Franks, N. R. Spatial relationships within nests of the antLeptothorax unifasciatus (Latr.) and their implications for the division of labour. Anim. Behav. 50, 121–136 (1995). 10.1006/anbe.1995.0226

[5]

Franks, N. R. & Tofts, C. Foraging for work: how tasks allocate workers. Anim. Behav. 48, 470–472 (1994). 10.1006/anbe.1994.1261

[6]

Pinter-Wollman, N., Wollman, R., Guetz, A., Holmes, S. & Gordon, D. M. The effect of individual variation on the structure and function of interaction networks in harvester ants. J. R. Soc. Interface 8, 1562–1573 (2011). 10.1098/rsif.2011.0059

[7]

Mersch, D. P., Crespi, A. & Keller, L. Tracking individuals shows spatial fidelity is a key regulator of ant social organization. Science 340, 1090–1093 (2013). 10.1126/science.1234316

[8]

Jeanson, R. Long-term dynamics in proximity networks in ants. Anim. Behav. 83, 915–923 (2012). 10.1016/j.anbehav.2012.01.009

[9]

Moreau, M., Arrufat, P., Latil, G. & Jeanson, R. Use of radio-tagging to map spatial organization and social interactions in insects. J. Exp. Biol. 214, 17–21 (2011). 10.1242/jeb.050526

[10]

Gordon, D. M. Ant Encounters: Interaction Networks and Colony Behavior Princeton University Press (2010). 10.1515/9781400835447

[11]

Tschinkel, W. R. The nest architecture of the Florida harvester ant, Pogonomyrmex badius. J. Insect Sci. 4, 21 (2004). 10.1093/jis/4.1.21

[12]

Knaden, M. & Graham, P. The sensory ecology of ant navigation: from natural environments to neural mechanisms. Annu. Rev. Entomol. 61, 63–76 (2016). 10.1146/annurev-ento-010715-023703

[13]

Merkle, T. & Wehner, R. Landmark guidance and vector navigation in outbound desert ants. J. Exp. Biol. 211, 3370–3377 (2008). 10.1242/jeb.022715

[14]

Wehner, R. & Räber, F. Visual spatial memory in desert ants, Cataglyphis bicolor (Hymenoptera: Formicidae). Experientia 35, 1569–1571 (1979). 10.1007/bf01953197

[15]

Anderson, J. B. & Meer, R. K. Magnetic orientation in the fire ant, Solenopsis invicta. Naturwissenschaften 80, 568–570 (1993). 10.1007/bf01149274

[16]

Steck, K., Hansson, B. S. & Knaden, M. Smells like home: desert ants, Cataglyphis fortis, use olfactory landmarks to pinpoint the nest. Front. Zool. 6, 5 (2009). 10.1186/1742-9994-6-5

[17]

Attygalle, A. B. & Morgan, E. D. Ant trail pheromones. Adv. Insect Phys. 18, 1–30 (1985). 10.1016/s0065-2806(08)60038-7

[18]

Czaczkes, T. J., Grüter, C. & Ratnieks, F. L. W. Trail pheromones, an integrative view of their role in social insect colony organization. Annu. Rev. Entomol. 60, 581–599 (2015). 10.1146/annurev-ento-010814-020627

[19]

Tschinkel, W. R. Florida harvester ant nest architecture, nest relocation and soil carbon dioxide gradients. PLoS ONE 8, 1–13 (2013).

[20]

Theraulaz, G. & Bonabeau, E. A brief history of stigmergy. Cell 161, 181–183 (2015). 10.1016/j.cell.2015.03.044

[21]

Hölldobler, B. & Wilson, E. O. The Ants Harvard University Press (1990). 10.1007/978-3-662-10306-7

[22]

Khuong, A. et al. Stigmergic construction and topochemical information shape ant nest architecture. Proc. Natl Acad. Sci. USA 113, 1303–1308 (2015). 10.1073/pnas.1509829113

[23]

Reid, C. R., Sumpter, D. J. T. & Beekman, M. Optimisation in a natural system: argentine ants solve the Towers of Hanoi. J. Exp. Biol. 214, 50–58 (2011). 10.1242/jeb.048173

[24]

Sturgis, S. J., Greene, M. J. & Gordon, D. M. Hydrocarbons on harvester ant (Pogonomyrmex barbatus) middens guide foragers to the nest. J. Chem. Ecol. 37, 514–524 (2011). 10.1007/s10886-011-9947-y

[25]

Lenoir, A., Depickère, S., Devers, S., Christidès, J. P. & Detrain, C. Hydrocarbons in the ant Lasius niger: from the cuticle to the nest and home range marking. J. Chem. Ecol. 35, 913–921 (2009). 10.1007/s10886-009-9669-6

[26]

Robinson, E. J. H., Jackson, D. E., Holcombe, M. & Ratnieks, F. L. W. Insect communication: ‘no entry’ signal in ant foraging. Nature 438, 442 (2005). 10.1038/438442a

[27]

Hangartner, W., Reichson, J. M. & Wilson, E. O. Orientation to nest material by the ant, Pogonomyrmex badius (Latreille). Anim. Behav. 18, 331–334 (1970). 10.1016/s0003-3472(70)80045-8

[28]

Bos, N., Grinsted, L. & Holman, L. Wax on, wax off: nest soil facilitates indirect transfer of recognition cues between ant nestmates. PLoS ONE 6, 2–7 (2011). 10.1371/journal.pone.0019435

[29]

Greenwald, E., Segre, E. & Feinerman, O. Ant trophallactic networks: simultaneous measurement of interaction patterns and food dissemination. Sci. Rep. 5, 12496 (2015). 10.1038/srep12496

[30]

Blomquist, G. J. & Anne-Geneviève, B. (eds). in Insect hydrocarbons: Biology, Biochemistry, and Chemical Ecology 222–253Cambridge University Press (2010). 10.1017/cbo9780511711909

[31]

Boulay, R., Hefetz, A., Soroker, V. & Lenoir, A. Camponotus fellah colony integration: worker individuality necessitates frequent hydrocarbon exchanges. Anim. Behav. 59, 1127–1133 (2000). 10.1006/anbe.2000.1408

[32]

Cristianini, N. & Shawe-Taylor, J. An Introduction to Support Vector Machines and Other Kernel Based Learning Methods. Ai Magazine 22, Cambridge University Press (2000). 10.1017/cbo9780511801389

[33]

Suykens, J. A. K., Van Gestel, T., De Brabanter, J., De Moor, B. & Vandewalle, J. Least Squares Support Vector Machines World Scientific (2002). 10.1142/5089

[34]

Kecman, V. Learning and Soft Computing. The MIT Press The MIT Press (2001) At http://scholar.google.com/scholar?hl=en&btnG=Search&q=intitle:Learning+and+Soft+Computing#4.

[35]

Hefetz, A. & Orion, T. Pheromones of ants of Israel. I. The alarm-defense system of some larger Formicinae. Isr. J. Entomol. 16, 87–97 (1982).

[36]

Blatrix, R., Schulz, C., Jaisson, P., Francke, W. & Hefetz, A. Trail pheromone of ponerine ant Gnamptogenys striatula: 4-Methylgeranyl esters from Dufour’s gland. J. Chem. Ecol. 28, 2557–2567 (2002). 10.1023/a:1021444321238

[37]

Lenoir, A. et al. Trail-following behaviour in two Aphaenogaster ants. Chemoecology 21, 83–88 (2011). 10.1007/s00049-011-0071-9

[38]

Vander Meer, R. K., Alvarez, F. & Lofgren, C. S. Isolation of the trail recruitment pheromone of Solenopsis invicta. J. Chem. Ecol. 14, 825–838 (1988). 10.1007/bf01018776

[39]

Witte, V., Abrell, L., Attygalle, A. B., Wu, X. & Meinwald, J. Structure and function of Dufour gland pheromones from the crazy ant Paratrechina longicornis. Chemoecology 17, 63–69 (2007). 10.1007/s00049-006-0365-5

[40]

Katzav-Gozansky, T., Boulay, R., Ionescu-Hirsh, A. & Hefetz, A. Nest volatiles as modulators of nestmate recognition in the ant Camponotus fellah. J. Insect Physiol. 54, 378–385 (2008). 10.1016/j.jinsphys.2007.10.008

[41]

Lalzar, I., Simon, T., Meer, R. K. & Hefetz, A. Alteration of cuticular hydrocarbon composition affects heterospecific nestmate recognition in the carpenter ant Camponotus fellah. Chemoecology 20, 19–24 (2009). 10.1007/s00049-009-0030-x

[42]

Greene, M. J. & Gordon, D. M. Social insects: cuticular hydrocarbons inform task decisions. Nature 423, 32 (2003). 10.1038/423032a

[43]

Wagner, D. et al. Task-related differences in the cuticular hydrocarbon composition of harvester ants, Pogonomyrmex barbatus. J. Chem. Ecol. 24, 2021–2037 (1998). 10.1023/a:1020781508889

[44]

Helanterä, H., Aehle, O., Roux, M., Heinze, J. & D’Ettorre, P. Family-based guilds in the ant Pachycondyla inversa. Biol. Lett. 9, 20130125 (2013). 10.1098/rsbl.2013.0125

[45]

Dietemann, V., Peeters, C., Liebig, J., Thivet, V. & Hölldobler, B. Cuticular hydrocarbons mediate discrimination of reproductives and nonreproductives in the ant Myrmecia gulosa. Proc. Natl Acad. Sci. USA 100, 10341–10346 (2003). 10.1073/pnas.1834281100

[46]

D’Ettorre, P., Heinze, J., Schulz, C., Francke, W. & Ayasse, M. Does she smell like a queen? Chemoreception of a cuticular hydrocarbon signal in the ant Pachycondyla inversa. J. Exp. Biol. 207, 1085–1091 (2004). 10.1242/jeb.00865

[47]

Wyatt, T. D. Proteins and peptides as pheromone signals and chemical signatures. Anim. Behav. 97, 273–280 (2014). 10.1016/j.anbehav.2014.07.025

[48]

Strassmann, J. E. & Queller, D. C. The social organism: congresses, parties, and committees. Evolution 64, 605–616 (2010). 10.1111/j.1558-5646.2009.00929.x

[49]

Hölldobler, B. & Wilson, E. O. The superorganism: the beauty, elegance, and strangeness of insect societies. Nature 456, 544 (2009).

[50]

Cyster, J. G. Chemokines and cell migration in secondary lymphoid organs. Science 286, 2098–2102 (1999). 10.1126/science.286.5447.2098

Showing 50 of 59 references

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Published: Jun 01, 2017
Vol/Issue: 8(1)
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Cite This Article

Yael Heyman, Noam Shental, Alexander Brandis, et al. (2017). Ants regulate colony spatial organization using multiple chemical road-signs. Nature Communications, 8(1). https://doi.org/10.1038/ncomms15414

Ants regulate colony spatial organization using multiple chemical road-signs

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