Abstract
Taking bad decisions to solve problems can negatively affect organism fitness, hence, the costs accrued by them should modulate decisions about when and how problems should be solved. We studied the problem of trail maintenance in leaf-cutting ants. We evaluated whether colonies have individuals exclusively dedicated to trail maintenance, and how obstacle size and ant forager flux influence the decision of removing obstacles, and the number of trail-clearing ants. We placed obstacles of different sizes, in low and high ant fluxes in different trails of Atta sexdens, and measured ant flux without and with obstacles, if ants removed obstacles, the number of trail-clearing ants and removal time. Obstacle cost was estimated as the proportion of ants that were blocked by the obstacle. We found that colonies lack exclusive trail-clearing ants, i.e., clearing ants also foraged and vice versa. The obstacle cost increased with obstacle size and ant flux. Removal probability increased with this cost. The number of trail-clearing ants increased with obstacle size but did not vary with ant flux, suggesting that the number of trail-clearing ants depends on intrinsic problem characteristics (i.e., higher resistance to traction in bigger obstacles), but does not depend on social context (i.e., interference with foragers). Regardless of the obstacle size, the removal time increased with the number of trail-clearing ants suggesting that interference among individuals is higher in larger working groups than in smaller ones. Our results suggest that individual capabilities as well as the coordination level among individuals influence the solving of a problem and the number of individuals involved in it. We discuss possible mechanisms behind results and propose a conceptual model about the costs and benefits of the removal task.
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References
Amé J-M, Halloy J, Rivault C et al (2006) Collegial decision making based on social amplification leads to optimal group formation. Proc Natl Acad Sci 103:5835–5840. https://doi.org/10.1073/pnas.0507877103
Amor F, Ortega P, Cerdá X, Boulay R (2010) Cooperative prey-retrieving in the ant Cataglyphis floricola: an unusual short-distance recruitment. Insectes Soc 57:91–94. https://doi.org/10.1007/s00040-009-0053-x
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.2307/2533043%3E
Beckers R, Deneubourg J, Goss S (1992) Trails and u-turns in the selection of a path by the ant Lasius niger. J Theor Biol 159:397–415
Bochynek T, Meyer B, Burd M (2017) Energetics of trail clearing in the leaf-cutter ant Atta. Behav Ecol Sociobiol 71:1–10
Bollazzi M, Roces F (2011) Information needs at the beginning of foraging: grass-cutting ants trade off load size for a faster return to the nest. PLoS One 6:1–9. https://doi.org/10.1371/journal.pone.0017667
Bray RM, Kerr NL, Atkin RS (1978) Effects of group size, problem difficulty, and sex on group performance and member reactions. J Pers Soc Psychol 36:1224–1240. https://doi.org/10.1037//0022-3514.36.11.1224
Bruce AI (2016) Regulation of building behaviour relating to nest space and transport in leaf-cutting ants
Bruce AI, Burd M (2012) Allometric scaling of foraging rate with trail dimensions in leaf-cutting ants. Proc Biol Sci 279:2442–2447. https://doi.org/10.1098/rspb.2011.2583
Bruce AI, Czaczkes TJ, Burd M (2017) Tall trails: ants resolve an asymmetry of information and capacity in collective maintenance of infrastructure. Anim Behav 127:179–185. https://doi.org/10.1016/j.anbehav.2017.03.018
Burd M (2000) Foraging behaviour of Atta cephalotes (leaf-cutting ants): an examination of two predictions for load selection. Anim Behav 60:781–788. https://doi.org/10.1006/anbe.2000.1537
Burd M, Archer D, Aranwela N, Stradling DJ (2002) Traffic dynamics of the leaf-cutting ant, Atta cephalotes. Am Nat 159:283–293. https://doi.org/10.1086/338541
Caldato N, Forti LC, da Silva Camargo R et al (2016) Dynamics of the restoration of physical trails in the grass-cutting ant Atta capiguara (Hymenoptera, Formicidae). Rev Bras Entomol 60:63–67. https://doi.org/10.1016/j.rbe.2015.10.001
Cevallos Dupuis E, Harrison JF (2016) Trunk trail maintenance in leafcutter ants: caste involvement and effects of obstacle type and size on path clearing in Atta cephalotes. Insectes Soc 64:1–8. https://doi.org/10.1007/s00040-016-0530-y
Clement TS, Feltus JR, Kaiser DH, Zentall TR (2000) “Work ethic” in pigeons: reward value is directly related to the effort or time required to obtain the reward. Psychon Bull Rev 7:100–106. https://doi.org/10.3758/BF03210727
Codling AEA, Pitchford JW, Simpson SD (2007) Group navigation and the " many-wrongs principle " in models of animal movement. Ecology 88:1864–1870
Conradt L, List C (2009) Group decisions in humans and animals: a survey. Philos Trans R Soc B Biol Sci 364:719–742. https://doi.org/10.1098/rstb.2008.0276
Czaczkes TJ, Grüter C, Ratnieks FLW (2013) Negative feedback in ants: crowding results in less trail pheromone deposition. J R Soc Interface 10:1–6. https://doi.org/10.1098/rsif.2012.1009
Czaczkes TJ, Nouvellet P, Ratnieks FLW (2011) Cooperative food transport in the Neotropical ant, Pheidole oxyops. Insectes Soc 58:153–161. https://doi.org/10.1007/s00040-010-0130-1
Czaczkes TJ, Ratnieks FLW (2011) Simple rules result in the adaptive turning of food items to reduce drag during cooperative food transport in the ant Pheidole oxyops. Insectes Soc 58:91–96. https://doi.org/10.1007/s00040-010-0121-2
Czaczkes TJ, Ratnieks FLW (2012) Pheromone trails in the Brazilian ant Pheidole oxyops: extreme properties and dual recruitment action. Behav Ecol Sociobiol 66:1149–1156. https://doi.org/10.1007/s00265-012-1367-7
Czaczkes TJC, Ratnieks FLWR (2013) Cooperative transport in ants (Hymenoptera: Formicidae) and elsewhere. Mymercological News 18:1–11
Deneubourg JL, Lioni A, Detrain C (2002) Dynamics of aggregation and emergence of cooperation. Biol Bull 202:262–267
Denny AJ, Wright J, Grief B (2001) Foraging efficiency in the wood ant, Formica rufa: is time of the essence in trail following? Anim Behav 62:139–146. https://doi.org/10.1006/anbe.2001.1718
Depickère S, Fresneau D, Deneubourg JL (2004) A basis for spatial and social patterns in ant species: dynamics and mechanisms of aggregation. J Insect Behav 17:81–97. https://doi.org/10.1023/B:JOIR.0000025134.06111.be
Depickère S, Fresneau D, Deneubourg JL (2008) Effect of social and environmental factors on ant aggregation: a general response? J Insect Physiol 54:1349–1355. https://doi.org/10.1016/j.jinsphys.2008.07.013
Detrain C, Deneubourg J (1997) Scavenging by Pheidole pallidula: a key for understanding decision-making systems in ants. Anim Behav 53:537–547
Dorigo M, Maria L (1997) Ant colonies for the travelling salesman problem. BioSystems 43:73–81
Dussutour A, Deneubourg J-L, Beshers S, Fourcassié V (2009) Individual and collective problem-solving in a foraging context in the leaf-cutting ant Atta colombica. Anim Cogn 12:21–30. https://doi.org/10.1007/s10071-008-0165-0
Faria JJ, Codling EA, Dyer JRG et al (2009) Navigation in human crowds; testing the many-wrongs principle. Anim Behav 78:587–591. https://doi.org/10.1016/j.anbehav.2009.05.019
Farji-Brener A, Chinchilla F, Umaña MN et al (2015) Branching angles reflect a tradeoff between reducing trail maintenance cost or travel distance in leaf-cutting ants. Ecology 96:510–517
Farji-Brener AG, Amador-Vargas S, Chinchilla F et al (2010) Information transfer in head-on encounters between leaf-cutting ant workers: food, trail condition or orientation cues? Anim Behav 79:343–349. https://doi.org/10.1016/j.anbehav.2009.11.009
Farji-Brener AG, Barrantes G, Laverde O et al (2007) Fallen branches as part of leaf-cutting ats trails: their role in resource discovery and leaf transport rates in Atta cephalotes. Biotropica 39:211–215
Fehr E, Fischbacher U (2003) The nature of human altruism. Nature 425:785–791. https://doi.org/10.1038/nature02043
Fewell JH (1988) Energetic and time costs of foraging in harvester ants, Pogonomyrmex occidentalis. Behav Ecol Sociobiol 22:401–408
Fowler HG, Robinson S (1979) Foraging by Atta sexdens (Fornicidae: Attini): seasonal patterns, caste and efficiency. Ecol Entomol 4:239–247
Ganskopp D, Cruz R, Johnson DE (2000) Least-effort pathways?: a GIS analysis of livestock trails in rugged terrain. Appl Anim Behav Sci 68:179–190
Gelblum A, Pinkoviezky I, Fonio E et al (2015) Ant groups optimally amplify the effect of transiently informed individuals. Nat Commun 6:1–9. https://doi.org/10.1038/ncomms8729
Gordon DM (2018) The Ecology of Collective Behavior in Ants. Annu Rev Entomol 13:1–16
Gordon DM, Paul RE, Thorpe K (1993) What is the function of encounter patterns in ant colonies? Anim Behav 45:1083–1100
Goss S, Deneubourg J, Pasteels J (1989) Self-organized shortcuts in the argentine ant. Naturwissenschaften 79:579–581
Haines B, Foster R (1977) Energy flow through litter in a panamanian forest. J Ecol 65:147–155
Helbing D, Keltsch J, Molnár P (1997) Modelling the evolution of human trail systems. Nature 388:47–50. https://doi.org/10.1038/40353
Heylighen F (2015a) Stigmergy as a universal coordination mechanism I: definition and sciencedirect stigmergy as a universal coordination mechanism I: definition and components. Cogn Syst Res 38:4–13. https://doi.org/10.1016/j.cogsys.2015.12.002
Heylighen F (2015b) Stigmergy as a universal coordination mechanism II: varieties and evolution sciencedirect stigmergy as a universal coordination mechanism II: varieties and evolution. Cogn Syst Res 38:50–59. https://doi.org/10.1016/j.cogsys.2015.12.007
Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge
Holm S (1979) A simple sequeantilly rejective multiple test procedure. Scand J Stat 6:65–70. https://doi.org/10.2307/4615733
Howard JJ (2001) Costs of trail construction and maintenance in the leaf-cutting ant Atta columbica. Behav Ecol Sociobiol 49:348–356. https://doi.org/10.1007/s002650000314
Jaffe K, Howse PE (1979) The mass recruitment system of leaf cutting ant, Atta cephalotes. Anim Behav 27:930–939
King AJ, Myatt JP, Fürtbauer I et al (2015) Social density processes regulate the functioning and performance of foraging human teams. Sci Rep 5:1–8. https://doi.org/10.1038/srep18260
Lerman K, Galstyan A (2002) Mathematical model of foraging in a group of robots: effect of interference. Auton Robots 13:127–141. https://doi.org/10.1023/A:1019633424543
Lewis T, Pollard GV, Dibley GC (1974) Micro-environmental factors affecting diel patterns of foraging in the leaf-cutting ant Atta cephalotes (L.) (Formicidae: Attini). J Anim Ecol 43:143–153
Lugo AE, Farnworth EG, Pool D, Jerez P (1973) The impact of the leaf cutter ant Atta colombica on the energy flow of a tropical west forest. Ecology 54:1292–1301
McCreery HF, Breed MD (2013) Cooperative transport in ants: a review of proximate mechanisms. Insectes Soc 61:99–110. https://doi.org/10.1007/s00040-013-0333-3
Moreira A, Forti LC, Andrade AP et al (2004) Nest architecture of Atta laevigata (F. Smith, 1858) (Hymenoptera: Formicidae). Stud Neotrop Fauna Environ 39:109–116. https://doi.org/10.1080/01650520412331333756
Naug D (2009) Structure and resilience of the social network in an insect colony as a function of colony size. Behav Ecol Sociobiol 63:1023–1028. https://doi.org/10.1007/s00265-009-0721-x
Nielsen MG, Baroni-Urbani C (1990) Energetics and foraging behaviour of the European seed harvesting ant Messor capitatus I. Respiratory metabolism and energy consumption of unloaded and loaded workers during locomotion. Physiol Entomol 15:441–448
Pinheiro J, Bates D, DebRoy S et al (2017) nlme: linear and nonlinear mixed effects models. R Packag 3rd edn 1–336
Powell S, Clark E (2004) Combat between large derived societies: a subterranean army ant established as a predator of mature leaf-cutting ant colonies. Insectes Soc 51:342–351. https://doi.org/10.1007/s00040-004-0752-2
R Development Core Team (2010) R: a language and environment for statistical computing
Rockwood LL, Hubbell SP (1987) Host-plant selection, diet diversity, and optimal foraging in a tropical leafcutting ant. Oecologia 74:55–61
Röschard J, Roces F (2003) Cutters, carriers and transport chains: distance-dependent foraging strategies in the grass-cutting ant Atta vollenweideri. Insectes Soc 50:237–244. https://doi.org/10.1007/s00040-003-0663-7
Röschard J, Roces F (2011) Sequential load transport in grass-cutting ants (Atta vollenweideri): maximization of plant delivery rate or improved information transfer? Psyche A J Entomol 1–10. https://doi.org/10.1155/2011/643127
Sampaio E, Dall’olio A, Nunes K, De Lemos E (1993) A model of litterfall, litter layer losses and mass transfer in a humid tropical forest at Pernambuco, Brazil. J Trop Ecol 9:291–301. https://doi.org/10.1017/S026646740000732X
Sasaki T, Granovskiy B, Mann RP et al (2013) Ant colonies outperform individuals when a sensory discrimination task is difficult but not when it is easy. Proc Natl Acad Sci 110:13769–13773. https://doi.org/10.1073/pnas.1304917110
Sasaki T, Pratt SC (2012) Groups have a larger cognitive capacity than individuals. Curr Biol 22:R827–R829. https://doi.org/10.1016/j.cub.2012.07.058
Schaerf TM, Makinson JC, Myerscough MR, Beekman M (2013) Do small swarms have an advantage when house hunting? The effect of swarm size on nest-site selection by Apis mellifera. J R Soc Interface 10:20130533. https://doi.org/10.1098/rsif.2013.0533
Shepherd J (1982) Trunk trails and the searching strategy of a leaf-cutter ant, Atta colombica. Behav Ecol Sociobiol 11:77–84. https://doi.org/10.1007/BF00300095
Starcke K, Brand M (2012) Decision making under stress: A selective review. Neurosci Biobehav Rev 36:1228–1248. https://doi.org/10.1016/j.neubiorev.2012.02.003
Sumpter DJT, Zabzina N, Nicolis SC (2012) Six prediction about the decision making of animal and human groups. Manag Decis Econ 33:295–309. https://doi.org/10.1002/mde
Walton ME, Kennerley SW, Bannerman DM et al (2006) Weighing up the benefits of work: behavioral and neural analyses of effort-related decision making. Neural Networks 19:1302–1314. https://doi.org/10.1016/j.neunet.2006.03.005
Wilson E (1980) Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta): I. The overall pattern in A. sexdens. Behav Ecol Sociobiol 7:143–156
Witte V, Schliessmann D, Hashim R (2010) Attack or call for help? Rapid individual decisions in a group-hunting ant. Behav Ecol 21:1040–1047. https://doi.org/10.1093/beheco/arq100
Yang C, Belawat P, Hafen E et al (2008) Drosophila egg-laying site selection as a system to study simple decision-making processes. Science 319:1679–1683. https://doi.org/10.1126/science.1151842
Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects model and extensions in ecology with R
Acknowledgements
We thank R. Josens, M. Lozada and J. Corley for helpful comments on an earlier version of this article. We thank J. Queiroz, Corina Barrera, Eder Cleyton Barbosa de França and Marina for help during fieldwork. This work was supported by the Fondo para la Investigación Científica y Tecnológica (FONCYT; PICT 2015-1319) and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET; PIP 2014–2016, 11220130100665-CO).
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Supplementary Movie S1: Collective removal of an obstacle by cooperative transport. Leaf-cutting ant (Atta sexdens) cooperatively removing an obstacle of 10 cm2. The ant flux was 118 ants per min. At the end of the video, two workers cooperatively transport the obstacle away from the trail. During the collective removal, both individuals change the directions of pulling or pushing or the place where they picked up the obstacle (MP4 65544 KB)
Supplementary Movie S2: Partitioned collective removal of an obstacle. Leaf-cutting ant (Atta sexdens) collectively removing an obstacle of 20 cm2. The ant flux was 70 ants per min. First the removal is made by one worker and then by another, until the first worker finishes the removal (MP4 344810 KB)
Supplementary Movie S3: Collective removal of an obstacle. Leaf-cutting ant (Atta sexdens) collectively removing an obstacle of 20 cm2. The ant flux was 108 ants per min. First the removal is made by one worker but then two workers cooperatively transport the obstacle away from the trail. During the collective removal, both individuals change the directions of pulling or pushing or the place where they picked up the obstacle (MP4 341926 KB)
Supplementary Movie S4: Individual removal of an obstacle. Leaf-cutting ant (Atta sexdens) individually removing an obstacle of 10 cm2. The ant flux was 54 ants per min. One worker drags the obstacle and never picks it up with the mandible carrying it over its head. Foraging ants walk along the edge of the obstacles and, even some ants cross over it (MP4 39731 KB)
Supplementary Movie S5: Individual removal of an obstacle. Leaf-cutting ant (Atta sexdens) individually removing an obstacle of 30 cm2. The ant flux was 65 ants per min. One worker drags the obstacle and never picks it up with the mandible carrying it over its head (MP4 75832 KB)
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Alma, A.M., Farji-Brener, A.G. & Elizalde, L. When and how obstacle size and the number of foragers affect clearing a foraging trail in leaf-cutting ants. Insect. Soc. 66, 305–316 (2019). https://doi.org/10.1007/s00040-018-00680-x
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DOI: https://doi.org/10.1007/s00040-018-00680-x