Abstract
The collective behavior of ants and the emergence of self-organizing patterns in ant colonies have been explained with various theoretical approaches based on models of trail following behavior elicited by pheromones. Although existing models can explain collective behavior of ants, there is little empirical evidence on how ants precisely respond to various pheromone concentrations. Thus, important knowledge is lacking about how much realistic description of ant behavior can be provided by the models and their underlying mathematical functions. To fill in this gap, we conducted experiments with three different ant species to explore their responses to varying concentrations of pheromones that elicit ants’ trail following behavior. We found that ants’ decision making processes in trail following are best explained by psychophysical theory (PT), which describes the relationship between physical stimuli, sensory perception and decision making in humans, other primates, birds and insects. Furthermore, the theory provides clear definitions of biological parameters, such as detection- and discrimination thresholds. The species studied were distinctively different in the shape and parameters of their psychometric functions, which we attribute to specific adaptions to their environment. The observed differences are discussed in relation to their natural trail following behaviors. Our study opens a new perspective of understanding and explaining important aspects of collective ant behavior using a well-established theory of perception.
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References
Akre KL, Johnsen S (2014) Psychophysics and the evolution of behavior. Trends Ecol Evol 29:291–300
Aron S, Beckers R, Deneubourg JL, Pasteels JM (1993) Memory and chemical communication in the orientation of two mass-recruiting ant species. Insect Soc 40:369–380
Bausenhart KM, Dyjas O, Vorberg D, Ulrich R (2012) Estimating discrimination performance in two-alternative forced choice tasks: routines for MATLAB and R. Behav Res Methods 44:1157–1174
Beckers R, Deneubourg J, Goss S (1992) Trail laying behaviour during food recruitment in the ant Lasius niger (L.). Insect Soc 39:59–72
Beckers R, Deneubourg JL, Goss S (1993) Modulation of trail laying in the ant Lasius niger (Hymenoptera: Formicidae) and its role in the collective selection of a food source. J Insect Behav 6:751–759
Bestmann HJ, Kern F, Schafer D, Witschel MC (1992) 3,4-Dihydroisocoumarins, a new class of ant trail pheromones. Angew Chem Int Ed 6:795–796
Bonabeau E, Theraulaz G, Deneubourg JL (1996) Quantitative study of the fixed threshold model for the regulation of division of labour in insect societies. Proc R Soc Lond B Biol 263:1565–1569
Britten KH, Shadlen MN, Newsome WT, Movshon JA (1992) The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci 12:4745–4765
Byrd RH, Lu P, Nocedal J, Zhu C (1995) A limited memory algorithm for bound constrained optimization. SIAM J Sci Comput 16:1190–1208
Cavill GWK, Robertson PL, Davies NW (1979) An Argentine ant aggregation factor. Experientia (Basel) 35:989–990
Cavill GWK, Davies NW, McDonald JF (1980) Characterization of aggregation factors and associated compounds from the Argentine ant, Iridomyrmex humilis. J Chem Ecol 6:371–384
Chittka L, Skorupski P, Raine NE (2009) Speed–accuracy tradeoffs in animal decision making. Trends Ecol Evol 24:400–407
Choe D-H, Villafuerte DB, Tsutsui ND (2012) Trail pheromone of the Argentine ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae). PLoS One 7(9):e45016
Czaczkes TJ, Grüter C, Jones SM, Ratnieks FLW (2011) Synergy between social and private information increases foraging efficiency in ants. Biol Lett 7:521–524
Deneubourg JL, Aron S, Goss S, Pasteels JM (1990) The self-organizing exploratory pattern of the Argentine ant. J Insect Behav 3:159–168
Detrain C, Pasteels JM (1991) Caste differences in behavioral thresholds as a basis for polyethism during food recruitment in the ant, Pheidole pallidula (Nyl.) Hymenoptera: Myrmicinae). J Insect Behav 4:157–176
Diwold K, Merkle D, Middendorf M (2009) Adapting to dynamic environments: polyethism in response threshold models for social insects. Adv Complex Syst 12:327–346
Dorai-Raj S (2009) Binomial confidence intervals for several parameterizations. In: R package version 1.0-6/r2
Dyer AG, Spaethe J, Prack S (2008) Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. J Comp Physiol A 194:617–627
Efron B, Tibshirani R (1986) Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Stat Sci 1:54–77
Evison SEF, Petchey OL, Beckerman AP, Ratnieks FLW (2008) Combined use of pheromone trails and visual landmarks by the common garden ant Lasius niger. Behav Ecol Sociobiol 63:261–267
Fechner G (1860) Elemente der Psychophysik. Breitkopf und Härtel, Leipzig
Gautrais J, Theraulaz G, Deneubourg JL, Anderson C (2002) Emergent polyethism as a consequence of increased colony size in insect societies. J Theor Biol 215:363–373
Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci U S A 99:6075–6079
Gold JI, Shadlen MN (2007) The neural basis of decision making. Annu Rev Neurosci 30:535–574
Goss S, Aron S, Deneubourg JL, Pasteels JM (1989) Self-organized shortcuts in the Argentine ant. Naturwissenschaften 76:579–581
Grassé PP (1959) La reconstruction du nid et les coordinations interindividuelles chez Bellicositermes natalensis et Cubitermes sp. La théorie de la stigmergie: Essai d'interpretation du comportement des termites constructeurs. Insect Soc 6:41–80
Grüter C, Czaczkes TJ, Ratnieks FL (2011) Decision making in ant foragers (Lasius niger) facing conflicting private and social information. Behav Ecol Sociobiol 65:141–148
Hangartner W (1969) Orientierung von Lasius fuliginosus Latr. an einer Gabelung der Geruchspur. Insect Soc 16:55–60
Hilborn R, Mangel M (1997) The ecological detective: confronting models with data. Princeton University Press, Princeton
Hölldobler B (1995) The chemistry of social regulation: multicomponent signals in ant societies. Proc Natl Acad Sci U S A 92:19–22
Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge
Holway DA, Case TJ (2000) Mechanisms of dispersed central-place foraging in polydomous colonies of the Argentine ant. Anim Behav 59:433–441
Kacelnik A, Brito e Abreu F (1998) Risky choice and Weber's law. J Theor Biol 194:289–298
Kingdom FAA, Prins N (2010) Psychophysics, 1st edn. Elsevier, London
Klein A (2001) Measuring, estimating, and understanding the psychometric function: a commentary. Percept Psychophys 63(8):1421–1455
Mailleux A-C, Buffin A, Detrain C, Deneubourg JL (2011) Recruitment in starved nests: the role of direct and indirect interactions between scouts and nestmates in the ant Lasius niger. Insect Soc 58:559–567
Mallis A (1942) Half a century with the successful Argentine ant. Sci Mon 55:536–545
Perna A, Granovskiy B, Garnier S, Nicolis SC, Labedan M, Theraulaz G, Fourcassie V, Sumpter DJ (2012) Individual rules for trail pattern formation in Argentine ants (Linepithema humile). PLoS Comput Biol 8:e1002592
R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Robertson PL, Dudzinski ML, Orton CJ (1980) Excocrine gland involvement in trailing behaviour in the argentine ant (Formicidae: Dolichoderinae). Anim Behav 28:1255–1273
Sarris V (2006) Relational psychophysics in humans and animals. Psychology Press, New York
Sasaki T, Granovskiy B, Mann RP, Sumpter DJT, Pratt SC (2013) Ant colonies outperform individuals when a sensory discrimination task is difficult but not when it is easy. Proc Natl Acad Sci U S A 110:13769–13773
Seifert B (2007) Die Ameisen Mittel- und Nordeuropas. Lutra Verlags- und Vertriebsgesellschaft, Tauer
Stevens SS (1957) On the psychophysical law. Psychol Rev 64(3):153
Suarez AV, Bolger DT, Case TJ (1998) Effects of fragmentation and invasion on native ant communities in coastal southern California. Ecology 79:2041–2056
Theraulaz G, Bonabeau E, Deneubourg JL (1998) Response threshold reinforcement and division of labour in insect societies. Proc R Soc Lond B Biol 265:327–332
Turing AM (1952) The chemical basis for morphogenesis. Philos Trans R Soc B 237:37–72
Van Vorhis Key SE, Baker TC (1982) Trail-following responses of the Argentine ant, Iridomyrmex humilis (Mayr) to a synthetic trail pheromone component and analogs. J Chem Ecol 8:3–14
Vela-Pérez M, Fontelos MA, Velásquez JJL (2013) Ant foraging and geodesic paths in labyrinths: analytical and computational results. J Theor Biol 320:100–112
von Beeren C, Lizon à l’Allemand S, Hashim R, Witte V (2014) Collective exploitation of a temporally unpredictable food source: mushroom harvesting by the ant Euprenolepis procera. Anim Behav 89:71–77
Weber EH (1834) De Pulsu, resorptione, auditu et tactu. Annotationes anatomicae et physiologicae. In: Koehler (ed) Leipzig
Wetterer JK, Wild AL, Suarez AV, Roura-Pascual N, Espadaler X (2009) Worldwide spread of the Argentine ant, Linepithema humile (Hymenoptera: Formicidae). Myrmecol News 12:187–194
Wichmann FA, Hill NJ (2001) The psychometric function: I. Fitting, sampling, and goodness of fit. Percept Psychophys 63(8):1293–1313
Wilson EB (1927) Probable inference, the law of succession, and statistical inference. J Am Stat Assoc 22:209–212
Wilson EO (1958) A chemical releaser of alarm and digging behavior in the ant Pogonomyrmex badius (Latreille). Psyche 65:41–51
Wilson EO (1962) Chemical communication among workers of the fire ant Solenopsis saevissima (Fr. Smith). Anim Behav 10:134–164
Wilson EO, Pavan M (1959) Glandular sources and specifity of some chemical releasers of social behavior in dolichoderine ants. Psyche 66:70–76
Witte V, Maschwitz U (2008) Mushroom harvesting ants in the tropical rainforest. Naturwissenschaften 95:1049–1054
Acknowledgments
We thank Rolf Ulrich and Karin Bausenhart from the Universität Tübingen for valuable advice on psychophysical theory. We thank C. v. Beeren, T. Czaczkes, Hannah Fried-Petersen, Magdalena Mair, Angelika Pohl and Deborah Schweinfest for reading the manuscript and giving valuable advice. We thank Sandra Franz and Kai von Szadkowski for help with the experimental work.
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The authors declare that the experiments comply with the current law of the country in which they were performed.
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The authors declare that they have no conflict of interest.
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Communicated by W. O. H. Hughes
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von Thienen, W., Metzler, D., Choe, DH. et al. Pheromone communication in ants: a detailed analysis of concentration-dependent decisions in three species. Behav Ecol Sociobiol 68, 1611–1627 (2014). https://doi.org/10.1007/s00265-014-1770-3
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DOI: https://doi.org/10.1007/s00265-014-1770-3