Abstract
Social insect colonies distribute their workforce with amazing flexibility across a large array of diverse tasks under fluctuating external conditions and internal demands. Deciphering the individual rules of task selection and task performance is at the heart of understanding how colonies can achieve this collective feature. Models play an important role in this endeavor, as they allow us to investigate how the rules of individual behavior give rise to emergent patterns at the colony level. Modulation of individual behavior occurs at many different timescales and to successfully use a model we need to ensure that it applies on the timescale under observation. Here, we focus on short timescales and ask the question whether the most commonly used class of models (response threshold models) adequately describes behavioral modulation on this timescale. We study the fanning behavior of bumblebees on temperature-controlled brood dummies and investigate the effect of (i) stimulus intensity, (ii) repeated task performance, and (iii) task performance feedback. We analyze the timing patterns (rates of task engagement and task disengagement) using survival analysis. Our results show that stimulus intensity does not significantly influence individual task investment at these comparably short timescales. In contrast, repeated task performance and task performance feedback affect individual task investment. We propose an explicitly time-resolved individual-based model and simulate this model to study how patterns of individual task engagement influence task involvement at the group level, finding support for the hypothesis that regulation mechanisms at different timescales can improve performance at the group level in dynamic environments.
Significance statement
Social insect colonies distribute their workforce flexibly across a wide range of tasks. In the absence of a central command structure, it is crucial for our understanding of collective task allocation that we decipher the rules according to which individuals regulate their task engagement. Here, we explore bumblebee thermoregulation. Using temperature-controlled brood dummies. we analyze how temperature, repeated task performance, and performance feedback modulate the timing of individual fanning behavior. We show behavioral modulation in response to task performance. Contrary to common expectation, our results show that in some cases the inability to experience success in performing a task (here cooling the brood when fanning) can result in increased individual task engagement. Based on our analysis, we construct and simulate a detailed model for individual task response to show how this individual-level behavior can impact on group-level performance.
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References
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723
Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440
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 263:1565–1569
Charbonneau D, Dornhaus A (2015) When doing nothing is something. How task allocation strategies compromise between flexibility, efficiency, and inactive agents. J Bioecon 17:217–242
Cook CN, Breed MD (2013) Social context influences the initiation and threshold of thermoregulatory behaviour in honeybees. Anim Behav 86:323–329
Cox DR (1972) Regression models and life-tables. J R Stat Soc B Methodol 34:187–220
Dornhaus A (2008) Specialization does not predict individual efficiency in an ant. PLoS Biol 6:e285
Duarte A, Weissing FJ, Pen I, Keller L (2011) An evolutionary perspective on self-organized division of labor in social insects. Annu Rev Ecol Evol Syst 42:91–110
Dukas R, Visscher PK (1994) Lifetime learning by foraging honey bees. Anim Behav 48:1007–1012
Duong N, Dornhaus A (2012) Ventilation response thresholds do not change with age or self-reinforcement in workers of the bumble bee Bombus impatiens. Insect Soc 59:25–32
Fewell JH, Harrison JF (2016) Scaling of work and energy use in social insect colonies. Behav Ecol Sociobiol 70:1047–1061
Gardner KE, Foster RL, O’Donnell S (2007) Experimental analysis of worker division of labor in bumblebee nest thermoregulation (Bombus huntii, Hymenoptera: Apidae). Behav Ecol Sociobiol 61:783–792
Garrison LK, Kleineidam CJ, Weidenmüller A (2018) Behavioral flexibility promotes collective consistency in a social insect. Sci Rep 8:15836
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
Gillespie DT (1976) A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. J Comput Phys 22:403–434
Gillespie DT (1977) Exact stochastic simulation of coupled chemical reactions. J Phys Chem 81:2340–2361
Gordon DM (1996) The organization of work in social insect colonies. Nature 380:121–124
Gordon DM (2016) From division of labor to the collective behavior of social insects. Behav Ecol Sociobiol 70:1101–1108
Goulson D (2010) Bumblebees: behaviour, ecology, and conservation, 2nd edn. Oxford University Press, New York City
Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, New York City
Heinrich B (1979) Bumblebee economics. Harvard University Press, Cambridge
Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Cambridge
Hölldobler B, Wilson EO (2009) The superorganism: the beauty, elegance, and strageness of insect societies. W. W. Norton & Company, New York City
Jeanne RL (2016) Division of labor is not a process or a misleading concept. Behav Ecol Sociobiol 70:1109–1112
Jeanson R, Weidenmüller A (2014) Interindividual variability in social insects—proximate causes and ultimate consequences. Biol Rev 89:671–687
Johnson BR (2009) A self-organizing model for task allocation via frequent task quitting and random walks in the honeybee. Am Nat 174:537–547
Kleinbaum DG, Klein M (2012) Survival analysis: a self-learning text, 3rd edn. Springer, New York City
Leighton GM, Charbonneau D, Dornhaus A (2017) Task switching is associated with temporal delays in Temnothorax rugatulus ants. Behav Ecol 28:319–327
Liu X (2012) Survival analysis: models and applications. Wiley, West Sussex
Mattila HR, Seeley TD (2010) Promiscuous honeybee queens generate colonies with a critical minority of waggle-dancing foragers. Behav Ecol Sociobiol 64:875–889
Meyer B, Weidenmüller A, Chen R, García J (2015) Collective homeostasis and time-resolved models of self-organised task allocation. In: BICT. ACM, New York City, pp 469–478
Myerscough MR, Oldroyd BP (2004) Simulation models of the role of genetic variability in social insect task allocation. Insect Soc 51:146–152
Naug D (2016) From division of labor to collective behavior: behavioral analyses at different levels. Behav Ecol Sociobiol 70:1113–1115
O’Donnell S, Foster RL (2001) Thresholds of response in nest thermoregulation by worker bumble bees, Bombus bifarius nearcticus (Hymenoptera: Apidae). Ethology 107:387–399
O’Donnell S, Jeanne RL (1992) Forager success increases with experience in Polybia occidentalis (Hymenoptera: Vespidae). Insectes Sociaux 39:451–454
Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton
Page RE, Mitchell SD (1990) Self organization and adaptation in insect societies. PSA 2:289–298
Page RE, Mitchell SD (1998) Self-organization and the evolution of division of labor. Apidologie 29:171–190
Plowright RC, Plowright CMS (1988) Elitism in social insects: a positive feedback model. In: Jeanne R L (ed) Interindividual behavioral variability in social insects. Westview Press, Boulder, pp 419–431
Ravary F, Lecoutey E, Kaminski G, Châline N, Jaisson P (2007) Individual experience alone can generate lasting division of labor in ants. Curr Biol 17:1308–1312
Robinson GE (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37:637–665
Robson SKA, Traniello JFA (2016) Division of labor in complex societies: a new age of conceptual expansion and integrative analysis. Behav Ecol Sociobiol 70:995–998
Schoenfeld D (1982) Partial residuals for the proportional hazards regression model. Biometrika 69:239–241
Schultze-Motel P (1991) Heat loss and thermoregulation in a nest of the bumblebee Bombus lapidarius (hymenoptera, apidae). Thermochim Acta 193:57–66
Schwander T, Rosset H, Chapuisat M (2005) Division of labour and worker size polymorphism in ant colonies: the impact of social and genetic factors. Behav Ecol Sociobiol 59:215–221
Theraulaz G, Bonabeau E, Deneubourg JL (1998) Response threshold reinforcements and division of labour in insect societies. Proc R Soc Lond B 265:327–332
Tripet F, Nonacs P (2004) Foraging for work and age-based polyethism: the roles of age and previous experience on task choice in ants. Ethology 110:863–877
Trumbo ST, Robinson G E (1997) Learning and task interference by corpse-removal specialists in honey bee colonies. Ethology 103:966–975
Weidenmüller A (2004) The control of nest climate in bumblebee (Bombus terrestris) colonies: interindividual variability and self reinforcement in fanning response. Behav Ecol 15:120– 128
Weidenmüller A, Kleineidam C, Tautz J (2002) Collective control of nest climate parameters in bumblebee colonies. Anim Behav 63:1065–1071
Westhus C, Kleineidam C J, Roces F, Weidenmüller A (2013) Behavioural plasticity in the fanning response of bumblebee workers: impact of experience and rate of temperature change. Anim Behav 85:27–34
Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, Cambridge
Wilson EO (1985) The sociogenesis of insect colonies. Science 228:1489–1495
Acknowledgments
We thank Linda Garrison and Christoph Kleineidam for comments on an early version of the manuscript.
Funding
This work was supported by a DAAD grant (Division of Labour and Collective Homeostasis in Dynamic Environments, DAAD PPP Australia, joint project C.K. and B.M.) and by the German Research Foundation (DFG, WE 4252/2-1 to A.W.; and the Centre of Excellence 2117 “Centre for the Advanced Study of Collective Behaviour” (ID: 422037984)).
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Weidenmüller, A., Chen, R. & Meyer, B. Reconsidering response threshold models—short-term response patterns in thermoregulating bumblebees. Behav Ecol Sociobiol 73, 112 (2019). https://doi.org/10.1007/s00265-019-2709-5
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DOI: https://doi.org/10.1007/s00265-019-2709-5