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Scaling of work and energy use in social insect colonies

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Abstract

Group size has profound effects on the organization of work. In the social insects, larger colony size is consistently associated with lower mass-specific energy use; similar hypometric relationships between group size and per-gram energy use may extend across other social taxa. The specific mechanisms driving social metabolic scaling vary among species, but evidence suggests that it can be associated with organizational changes in work (task) performance that allow more efficient energy use by larger groups. In social insect colonies, larger group size allows stronger individual specialization, greater diversity in task performance, and likely gives improved resilience to stochastic events. Larger colonies often also allocate a larger proportion of workers to maintenance and reserve rather than to foraging and brood care tasks, potentially reducing costs. For the few species examined, these organizational changes seem to be associated with lower mean but higher variance in movement rates, providing a concrete connection to metabolic use. Interestingly, colony group size is not generally associated with changes in the proportional number of colony workers resting versus doing work, but this may vary across social systems. Colonies with hypometric metabolic scaling tend to show constant or greater efficiency of brood production, consistent with efficiency rather than constraint-based scaling models. These patterns of work and energetics in social groups show distinct parallels with organismal scaling. Investigation into social metabolic scaling could contribute to identifying unifying scaling theories for the disparate fields of animal behavior, physiology, and human sociology.

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References

  • Agutter PS, Tuszynski JA (2011) Analytic theories of allometric scaling. J Exp Biol 214:1055–1062

    Article  PubMed  Google Scholar 

  • Amador-Vargas S, Gronenberg W, Wcislo WT, Mueller U (2015) Specialization and group size: brain and behavioural correlates of colony size in ants lacking morphological castes. Proc Royal Soc London B 282:20142502

    Article  Google Scholar 

  • Anderson C, McShea DW (2001) Individual versus social complexity, with particular reference to ant colonies. Biol Rev 76:211–237

    Article  CAS  PubMed  Google Scholar 

  • Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Ann Rev of Entomol 46:413–440

    Article  CAS  Google Scholar 

  • Blonder B, Dornhaus A (2011) Time-ordered networks reveal limitations to information flow in ant colonies. PLoS ONE 6:e20298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonabeau E, Theraulaz G, Deneubourg JL (1998) Fixed response thresholds and the regulation of division of labor in insect societies. Bull Math Biol 60:753–807

    Article  Google Scholar 

  • Bonner JT (2006) Why size matters: from bacteria to blue whales. Princeton University Press, Princeton, N.J

  • Bouwma AM, Nordheim EV, Jeanne RL (2006) Per-capita productivity in a social wasp: no evidence for a negative effect of colony size. Insectes Soc 53:412–419

    Article  Google Scholar 

  • Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  • Calder WAI (1996) Size, function and life history. Dover Publications, Mineola, NY

    Google Scholar 

  • Cao TT, Dornhaus A (2013) Larger laboratory colonies consume proportionally less energy and have lower per capita brood production in Temnothorax ants. Insectes Soc 60:1–5

    Article  Google Scholar 

  • Cassill DL, Tschinkel WR (1999) Task selection by workers of the fire ant Solenopsis invicta. Behav Ecol Sociobiol 45:301–310

    Article  Google Scholar 

  • Charbonneau D, Dornhaus A (2015a) Workers ‘specialized’ on inactivity: behavioral consistency of inactive workers and their role in task allocation. Behav Ecol Sociobiol 69:1459–1472

  • Charbonneau D, Dornhaus A (2015b) When doing nothing is something. How task allocation strategies compromise between flexibility, efficiency, and inactive agents. J Bioecon 17:217–242

  • Charbonneau D, Hillis N, Dornhaus A (2015) ‘Lazy’ in nature: ant colony time budgets show high ‘inactivity’ in the field as well as in the lab. Insectes Soc 62:31–35

    Article  Google Scholar 

  • Chittka L, Muller H (2009) Learning, specialization, efficiency and task allocation in social insects. Commun Integr Biol 2:151–154

    Article  PubMed  PubMed Central  Google Scholar 

  • Chown SL, Marais E, Terblanche JS, Klok CJ, Lighton JRB, Blackburn TM (2007) Scaling of insect metabolic rate is inconsistent with the nutrient supply network model. Funct Ecol 21:282–290

    Article  Google Scholar 

  • Clark R, Fewell J (2014a) Social dynamics drive selection in cooperative associations of ant queens. Behav Ecol 25:117-123

  • Clark R, Fewell J (2014b) Transitioning from unstable to stable colony growth in the desert leafcutter ant Acromyrmex versicolor. Behav Ecol Sociobiol 68:163-171

  • Clark C, Mangel M (1986) The evolutionary advantages of group foraging. Theor Popul Biol 30:45–75

    Article  Google Scholar 

  • Clutton-Brock TH, Russell AF, Sharpe LL, Brotherton PNM, McIlrath GM, White S, Cameron EZ (2001) Effects of helpers on juvenile development and survival in meerkats. Science 293:2446–2449

    Article  CAS  PubMed  Google Scholar 

  • Cole BJ (1986) The social behavior of Leptothorax allardycei (Hymenoptera, Formicidae): time budgets and the evolution of workers reproduction. Behav Ecol Sociobiol 18:165–173

    Article  Google Scholar 

  • Cole BJ (2009) The ecological setting of social evolution: the demography of ant populations. In: Gadau J, Fewell JH (eds) The organization of insect societies. Harvard University Press, Cambridge, MA, pp 74–104

    Google Scholar 

  • Cole BJ, Wiernasz DC (2000) Colony size and reproduction in the western harvester ant, Pogonomyrmex occidentalis. Insect Soc 47:249–255

    Article  Google Scholar 

  • Courchamp F, Rasmussen GSA, Macdonald DW (2002) Small pack size imposes a trade-off between hunting and pup-guarding in the painted hunting dog Lycaon pictus. Behav Ecol 13:20–27

    Article  Google Scholar 

  • Creel S (1997) Cooperative hunting and group size. Anim Behav 54:1319–1324

    Article  PubMed  Google Scholar 

  • Creel S, Creel NM (1995) Communal hunting and pack size in African wild dogs, Lycaon pictus. Anim Behav 50:1325–1339

    Article  Google Scholar 

  • Damuth J (1981) Home range, home range overlap, and species energy use among herbivorous mammals. Biol J Linn Soc 15:185–193

    Article  Google Scholar 

  • Deslippe RJ, Savolainen RA (1994) Role of food supply in structuring a population of Formica ants. J Anim Ecol 63:756–764

    Article  Google Scholar 

  • Dornhaus A (2008) Specialization does not predict individual efficiency in an ant. PLoS Biol 6:2368–2375

    Article  CAS  Google Scholar 

  • Dornhaus A, Holley JA, Pook VG, Worswick G, Franks NR (2008) Why do not all workers work? Colony size and workload during emigrations in the ant Temnothorax albipennis. Behav Ecol Sociobiol 63:43–51

    Article  Google Scholar 

  • Dornhaus A, Holley JA, Franks NR (2009) Larger colonies do not have more specialized workers in the ant Temnothorax albipennis. Behav Ecol 20:922–929

    Article  Google Scholar 

  • Duarte A, Weissing FJ, Pen I, Keller L (2011) An evolutionary perspective on self-organized division of labor in social insects. Ann Rev Ecol, Evol, and Syst 42:91–110

    Article  Google Scholar 

  • Dussutour A, Simpson SJ (2008) Carbohydrate regulation in relation to colony growth in ants. J Exp Biol 211:2224–2232

    Article  CAS  PubMed  Google Scholar 

  • Dussutour A, Simpson SJ (2009) Communal nutrition in ants. Curr Biol 19:740–744

    Article  CAS  PubMed  Google Scholar 

  • Elgar MA (1989) Predator vigilance and group size in mammals and birds: a critical review of the empirical evidence. Biol Rev 64:13–33

    Article  CAS  PubMed  Google Scholar 

  • Fewell JH (1988) Energetic and time costs of foraging in harvester ants, Pogonomyrmex occidentalis. Behav Ecol Sociobiol 22:401–408

    Article  Google Scholar 

  • Fewell JH (2003) Social insect networks. Science 301:1867–1870

    Article  CAS  PubMed  Google Scholar 

  • Fewell JH, Page RE Jr (1993) Genotypic variation in foraging responses to environmental stimuli by honey bees, Apis mellifera. Experientia 49:1106–1112

    Article  Google Scholar 

  • Fewell JH, Page RE Jr (1999) Emergence of division of labour in forced associations of normally solitary ant queens. Evol Ecol Res 1:537–548

    Google Scholar 

  • Fewell J, Harrison J, Lighton JB, Breed M (1996) Foraging energetics of the ant, Paraponera clavata. Oecologia 105:419–427

    Article  Google Scholar 

  • Fewell JH, Schmidt SK, Taylor T (2009) Division of labor in the context of complexity. In: Gadau J, Fewell JH (eds) Organization of insect societies. Harvard University Press, Cambridge, MA, pp 483–502

    Google Scholar 

  • Fonck C, Jaffé K (1996) On the energetic cost of sociality. Physiol Behav 59:713–719

    Article  CAS  PubMed  Google Scholar 

  • Gautrais J, Theraulaz G, Deneubourg J-L, Anderson C (2002) Emergent polyethism as a consequence of increased colony size in insect societies. J Theor Biol 215:363–373

    Article  PubMed  Google Scholar 

  • Glazier D (2009) Activity affects intraspecific body-size scaling of metabolic rate in ectothermic animals. J Comp Physiol B 179:821–828

    Article  PubMed  Google Scholar 

  • Glazier DS (2010) A unifying explanation for diverse metabolic scaling in animals and plants. Biol Rev 85:111–138

    Article  PubMed  Google Scholar 

  • Glazier DS (2014) Metabolic scaling in complex living systems. Systems 2:451–540

    Article  Google Scholar 

  • Gordon DM (1986) The dynamics of the daily round of the harvester ant colony (Pogonomyrmex barbatus). Anim Behav 34:1402–1419

    Article  Google Scholar 

  • Gordon DM (1987) Group level dynamics in harvester ants: young colonies and the role of patrolling. Anim Behav 35:833–843

    Article  Google Scholar 

  • Gordon DM (1996) The organization of work in social insect colonies. Nature 380:121–124

    Article  CAS  Google Scholar 

  • Gordon DM (1999) Interaction patterns and task allocation in ant colonies. In: Detrain C, Deneubourg JL, Pasteels JM (eds) Information processing in social insects. Birkhauser Verlag, Basel, Switzerland, pp 51–67

    Chapter  Google Scholar 

  • Gordon DM, Mehdiabadi NJ (1999) Encounter rate and task allocation in harvester ants. Behav Ecol Sociobiol 45:370–3777

    Article  Google Scholar 

  • Gorelick R, Bertram SM, Killeen PR, Fewell JH (2004) Normalized mutual entropy in biology: quantifying division of labor. Am Nat 164:677–682

    Article  PubMed  Google Scholar 

  • Gould SJ (1966) Allometry and size in ontogeny and phylogeny. Biol Rev 41:587–640

    Article  CAS  PubMed  Google Scholar 

  • Greene MJ, Gordon DM (2007) Interaction rate informs harvester ant task decisions. Behav Ecol 18:451–455

    Article  Google Scholar 

  • Gusset M, Macdonald DW (2010) Group size effects in cooperatively breeding African wild dogs. Anim Behav 79:425–428

    Article  Google Scholar 

  • Hamann H, Karsai I, Schmickl T (2013) Time delay implies cost on task switching: a model to investigate the efficiency of task partitioning. Bull Math Biol 75:1181–1206

    Article  PubMed  Google Scholar 

  • Hansen PJ, Bjornsen PK, Hansen BW (1997) Zooplankton grazing and growth: scaling in the 2–2,000 micron body size range. Limnol Oceanogr 42:687–704

    Article  Google Scholar 

  • Harrison JF, Woods HA, Roberts SP (2012) Ecological and environmental physiology of insects. Oxford University Press, New York

    Book  Google Scholar 

  • Harrison JF, Klok CJ, Waters JS (2014) Critical PO2 is size-independent in insects: implications for the metabolic theory of ecology. Current Opinion Ins Sci 4:54–59

    Article  Google Scholar 

  • Hee JJ, Holway DA, Suarez AV, Case TJ (2000) Role of propagule size in the success of incipient colonies of the invasive Argentine ant. Conserv Biol 14:559–563

  • Herbers JM (1981) Time resources and laziness in animals. Oecologia 49:252–262

    Article  Google Scholar 

  • Holbrook C, Clark R, Jeanson R, Bertram S, Kukuk P, Fewell J (2009) Emergence and consequences of division of labor in associations of normally solitary sweat bees. Ethology 115:301–310

    Article  Google Scholar 

  • Holbrook CT, Barden PM, Fewell JH (2011) Division of labor increases with colony size in the harvester ant Pogonomyrmex californicus. Behav Ecol 22:960–966

    Article  Google Scholar 

  • Holbrook CT, Eriksson TH, Overson RP, Gadau J, Fewell JH (2013a) Colony-size effects on task organization in the harvester ant Pogonomyrmex californicus. Insectes Soc 60:191-201

  • Holbrook CT, Kukuk PF, Fewell JH (2013b) Increased group size promotes task specialization in a normally solitary halictine bee. Behavior 150:1449-1466

  • Holldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Holldobler B, Wilson EO (2009) The superorganism: the beauty, elegance, and strangeness of insect societies. W.H. Norton, New York

    Google Scholar 

  • Hou C, Kaspari M, Vander Zanden HB, Gillooly JF (2010) Energetic basis of colonial living in social insects. PNAS 107:3634–3638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ingram KK, Pilko A, Heer J, Gordon DM (2013) Colony life history and lifetime reproductive success of red harvester ant colonies. J Anim Ecol 82:540–550

    Article  PubMed  Google Scholar 

  • Jaffe K (2010) Quantifying social synergy in insects and human societies. Behav Ecol Sociobiol 64:1721–1724

    Article  Google Scholar 

  • Jeanne RL (1986) The organization of work in Polybia occidentalis: costs and benefits of specialization in a social wasp. Behav Ecol Sociobiol 19:333–341

    Article  Google Scholar 

  • Jeanne RL (2003) Social complexity in the Hymenoptera, with special attention to the wasps. In: Kikuchi T, Azuma N, Higashi S (eds) Genes, behaviors and evolution of social insects. Hokkaido University Press, Sapporo, Japan, pp 81–130

    Google Scholar 

  • Jeanne RL, Nordheim EV (1996) Productivity in a social wasp: per capita output increases with swarm size. Behav Ecol 7:43–48

    Article  Google Scholar 

  • Jeanson R, Fewell JH (2008) Influence of the social context on division of labor in ant foundress associations. Behav Ecol 19:567–574

    Article  Google Scholar 

  • Jeanson R, Lachaud J-P (2015) Influence of task switching costs on colony homeostasis. Naturwissenschaften 102:1–4

    Article  CAS  Google Scholar 

  • Jeanson R, Weidenmüller A (2014) Interindividual variability in social insects—proximate causes and ultimate consequences. Biol Rev 89:671–687

    Article  PubMed  Google Scholar 

  • Jeanson R, Fewell JH, Gorelick R, Bertram SM (2007) Emergence of increased division of labor as a function of group size. Behav Ecol Sociobiol 62:289–298

    Article  Google Scholar 

  • Jeanson R, Clark RM, Holbrook CT, Bertram SM, Fewell JH, Kukuk PF (2008) Division of labour and socially induced changes in response thresholds in associations of solitary halictine bees. Anim Behav 76:593–602

    Article  Google Scholar 

  • Johnson R (2002) Semi-claustral colony founding in the seed-harvester ant Pogonomyrmex californicus: a comparative analysis of colony founding strategies. Oecologia 132:60–67

    Article  Google Scholar 

  • Johnson RA (2004) Colony founding by pleometrosis in the semiclaustral seed-harvester ant Pogonomyrmex californicus (Hymenoptera: Formicidae). Anim Behav 68:1189–1200

    Article  Google Scholar 

  • Jones JC, Myerscough MR, Graham S, Oldroyd BP (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305:402–404

    Article  CAS  PubMed  Google Scholar 

  • Julian GE, Cahan S (1999) Undertaking specialization in the desert leaf-cutter ant Acromyrmex versicolor. Anim Behav 58:437–452

    Article  PubMed  Google Scholar 

  • Kang Y, Clark R, Makiyama M, Fewell J (2011) Mathematical modeling on obligate mutualism: interactions between leaf-cutter ants and their fungus garden. J Theor Biol 289:116–127

    Article  PubMed  Google Scholar 

  • Karsai I, Schmickl T (2011) Regulation of task partitioning by a “common stomach”: a model of nest construction in social wasps. Behav Ecol 22:819–830

    Article  Google Scholar 

  • Karsai I, Wenzel JW (1998) Productivity, individual-level and colony-level flexibility, and organization of work as consequences of colony size. PNAS 95:665–8669

    Article  Google Scholar 

  • Kaspari M, Weiser MD (2012) Energy, taxonomic aggregation, and the geography of ant abundance. Ecography 35:65–72

    Article  Google Scholar 

  • Kerhoas D, Perwitasari-Farajallah D, Agil M, Widdig A, Engelhardt A (2014) Social and ecological factors influencing offspring survival in wild macaques. Behav Ecol 25:1164–1172

    Article  PubMed  PubMed Central  Google Scholar 

  • Kooijman SALM (2010) Dynamic energy budget theory for metabolic organisation. Cambridge University Press, Cambridge

    Google Scholar 

  • Kozlowski J, Konarzewski M, Gawelczyk AT (2003) Cell size as a link between noncoding DNA and metabolic rate scaling. PNAS 100:14080–14085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwapich C, Tschinkel W (2013) Demography, demand, death, and the seasonal allocation of labor in the Florida harvester ant (Pogonomyrmex badius). Behav Ecol Sociobiol 67:2011–2027

    Article  Google Scholar 

  • LaBarbera M (1986) The evolution and ecology of body size. In: Raup DM, Jablonski D (eds) Patterns and processes in the history of life. Springer Verlag, Berlin, pp 69–98

    Chapter  Google Scholar 

  • Lighton JRB, Feener DH Jr (1989) A comparison of energetics and ventilation of desert ants during voluntary and forced locomotion. Nature 342:174–175

    Article  Google Scholar 

  • Lighton JRB, Bartholomew GA, Feener DH (1987) Energetics of locomotion and load carriage and a model of the energy cost of foraging in the leaf-cutting ant, Atta colombica Guer. Physiol Zool 60:524–537

    Article  Google Scholar 

  • Lighton JRB, Weier JA, Feener DH (1993) The energetics of locomotion and load carriage in the desert harvester ant Pogogonomyrmex rugosus. J Exp Biol 181:49–61

    Google Scholar 

  • MacNulty DR, Smith DW, Mech LD, Vucetich JA, Packer C (2011) Nonlinear effects of group size on the success of wolves hunting elk. Behav Ecol 23:75–82

    Article  Google Scholar 

  • Maino JL, Kearney MR (2014) Ontogenetic and interspecific metabolic scaling in insects. Amer Nat 184:695–701

    Article  Google Scholar 

  • Maino JL, Kearney MR, Nisbet RM, Kooijman SALM (2014) Reconciling theories for metabolic scaling. J Anim Ecol 83:20–29

    Article  PubMed  Google Scholar 

  • Mason KS, Kwapich CL, Tschinkel WR (2015) Respiration, worker body size, tempo and activity in whole colonies of ants. Physiol Entomol 40:149–165

  • Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362–364

    Article  CAS  PubMed  Google Scholar 

  • McGlynn TP (2006) Ants on the move: resource limitation of a litter-nesting ant community in Costa Rica. Biotropica 38:419–427

    Article  Google Scholar 

  • Mesterton-Gibbons M, Dugatkin LA (1992) Cooperation among unrelated individuals: evolutionary factors. Quart Rev Biol 67:267–281

    Article  Google Scholar 

  • Michener C (1964) Reproductive efficiency in relation to colony size in hymenopterous societies. Insectes Soc 11:317–342

    Article  Google Scholar 

  • Michener C (1974) The social behavior of the bees: a comparative study. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Mirenda JT, Vinson SB (1981) Division of labour and specification of castes in the red imported fire ant Solenopsis invicta Buren. Anim Behav 29:410–420

    Article  Google Scholar 

  • Modlmeier AP, Liebmann JE, Foitzik S (2012) Diverse societies are more productive: a lesson from ants. Proc Royal Society B 279:2142–2150

    Article  Google Scholar 

  • Muradian R, Issa S, Jaffe K (1999) Energy consumption of termite colonies of Nasutitermes ephratae (Isoptera: Termitidae). Physiol Behav 66:731–735

    Article  CAS  PubMed  Google Scholar 

  • Muscedere ML, Willey TA, Traniello JFA (2009) Age and task efficiency in the ant Pheidole dentata: young minor workers are not specialist nurses. Anim Behav 77:911–918

    Article  Google Scholar 

  • Myerscough MR, Oldroyd BP (2004) Simulation models of the role of genetic variability in social insect task allocation. Insectes Soc 51:146–152

    Article  Google Scholar 

  • Nagy KA (1987) Field metabolic rate and food requirement scaling in mammals and birds. Ecological Mongraphs 57:111–128

    Article  Google Scholar 

  • Nagy KA (2005) Field metabolic rate and body size. J Exp Biol 208:1621–1625

    Article  PubMed  Google Scholar 

  • Naug D, Wenzel J (2006) Constraints on foraging success due to resource ecology limit colony productivity in social insects. Behav Ecol Sociobiol 60:62–68

  • O’Donnell S (2001) Worker biting interactions and task performance in a swarm-founding eusocial wasp (Polybia occidentalis, Hymenoptera: Vespidae). Behav Ecol 12:353–359

    Article  Google Scholar 

  • Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis in insect colonies. Trends Ecol Evol 22:408–413

    Article  PubMed  Google Scholar 

  • Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton, N.J

  • Overson R, Gadau J, Clark R, Pratt S, Fewell JH (2014) Behavioral transitions with the evolution of cooperative nest founding by harvester ant queens. Behav Ecol Sociobiol 68:21–30

    Article  Google Scholar 

  • Pacala SW, Gordon DM, Godfray H (1996) Effects of social group size on information transfer and task allocation. Evol Ecol 10:127–165

    Article  Google Scholar 

  • Page RE, Mitchell SD (1998) Self-organization and the evolution of division of labor. Apidologie 29:171–190

    Article  Google Scholar 

  • Page RE, Robinson GE, Fondrk MK, Nasr ME (1995) Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.). Behav Ecol Sociobiol 36:387–396

    Article  Google Scholar 

  • Pinter-Wollman N, Wollman R, Guetz A, Holmes S, Gordon DM (2011) The effect of individual variation on the structure and function of interaction networks in harvester ants. J Royal Soc Interface 8:1562–1573

    Article  Google Scholar 

  • Pinter-Wollman N, Hubler J, Holley J-A, Franks NR, Dornhaus A (2012) How is activity distributed among and within tasks in Temnothorax ants? Behav Ecol Sociobiol 66:1407–1420

    Article  Google Scholar 

  • Porter SD, Tschinkel WR (1985) Fire ant polymorphism: the ergonomics of brood production. Behav Ecol Sociobiol 16:323–336

  • Powell S, Tschinkel WR (1999) Ritualized conflict in Odontomachus brunneus and the generation of interaction-based task allocation: a new organizational mechanism in ants. Anim Behav 58:965–972

    Article  PubMed  Google Scholar 

  • Pruitt JN, Riechert SE (2011) How within-group behavioural variation and task efficiency enhance fitness in a social group. Proc Royal Soc London 278:1209–1215

    Article  Google Scholar 

  • Reid J, Monaghan P, Ruxton G (2002) Males matter: the occurrence and consequences of male incubation in starlings (Sturnus vulgaris). Behav Ecol Sociobiol 51:255–261

    Article  Google Scholar 

  • Reiss MJ (1989) The allometry of growth and reproduction. Cambridge University Press, New York

    Book  Google Scholar 

  • Rheindt FE, Strehl CP, Gadau J (2005) A genetic component in the determination of worker polymorphism in the Florida harvester ant Pogonomyrmex badius. Insectes Soc 52:163–168

    Article  Google Scholar 

  • Ritz DA (2000) Is social aggregation in aquatic crustaceans a strategy to conserve energy? Can J Fish Aquat Sci 57:59–67

    Article  Google Scholar 

  • Robinson GE, Page RE (1989) Genetic basis for division of labor in an insect society. In: Breed MD, Page RE (eds) The genetics of social evolution. Westview, Boulder, CO, pp 61–80

    Google Scholar 

  • Robinson EJ, Feinerman O, Franks NR (2009) Flexible task allocation and the organization of work in ants. Proc Royal Soci B 276:4373–4380

    Article  Google Scholar 

  • Rocha FH, Lachaud J-P, Valle-Mora J, Pérez-Lachaud G (2014) Fine individual specialization and elitism among workers of the ant Ectatomma tuberculatum for a highly specific task: intruder removal. Ethology 120:1185–1198

    Article  Google Scholar 

  • Sakagami SF, Maeta Y (1984) Multifemale nests and rudimentary castes in the normally solitary bee Ceratina japonica (Hymenoptera: Xylocopinae). J Kans Entomol Soc 57:639–656

    Google Scholar 

  • Scantlebury M, Bennett NC, Speakman JR, Pillay N, Schradin C (2006) Huddling in groups leads to daily energy savings in free-living African four-striped grass mice, Rhabdomys pumilio. Funct Ecol 20:166–173

    Article  Google Scholar 

  • Schmid-Hempel P (1990) Reproductive competition and the evolution of work load in social insects. Amer Nat 501:501–526

    Article  Google Scholar 

  • Schoombie RE, Boardman L, Groenewald B, Glazier DS, van Daalen CE, Clusella-Trullas S, Terblanche JS (2013) High metabolic and water-loss rates in caterpillar aggregations: evidence against the resource-conservation hypothesis. J Exper Biol 216:4321–4325

    Article  Google Scholar 

  • Seal JN, Tschinkel WR (2008) Food limitation in the fungus-gardening ant, Trachymyrmex septentrionalis. Ecol Entomol 33:597–607

    Article  Google Scholar 

  • Seid MA, Traniello JFA (2006) Age-related repertoire expansion and division of labor in Pheidole dentata (Hymenoptera: Formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants. Behav Ecol Sociobiol 60:631–644

    Article  Google Scholar 

  • Sendova-Franks AB, Hayward RK, Wulf B, Klimek T, James R, Planqué R, Britton NF, Franks NR (2010) Emergency networking: famine relief in ant colonies. Anim Behav 79:473–485

    Article  Google Scholar 

  • Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Champagne, IL

    Google Scholar 

  • Shik JZ (2008) Ant colony size and the scaling of reproductive effort. Funct Ecol 22:674–681

  • Shik JZ (2010) The metabolic costs of building ant colonies from variably sized subunits. Behav Ecol Sociobiol 64:1981–1990

    Article  Google Scholar 

  • Shik JZ, Santos JC, Seal JN, Kay A, Mueller UG, Kaspari M (2014) Metabolism and the rise of fungus cultivation by ants. Am Nat 184:364–373

    Article  PubMed  Google Scholar 

  • Sibly RM, Brown JH, Kodric-Brown A (2012) Metabolic ecology: a scaling approach. Wiley-Blackwell, Hoboken, NJ

    Book  Google Scholar 

  • Smith CR, Tschinkel WR (2006) The sociometry and sociogenesis of reproduction in the Florida harvester ant. Pogonomyrmex badius 6:32

    Google Scholar 

  • Southwick EE (1985) Allometric relations, metabolism and heat conductance in clusters of honeybees at cool temperatures. J Comp Physiol 156:143–149

    Article  Google Scholar 

  • Thomas M, Elgar M (2003) Colony size affects division of labour in the ponerine ant Rhytidoponera metallica. Naturwissenschaften 90:88–92

    CAS  PubMed  Google Scholar 

  • Tofts C, Franks NR (1992) Doing the right thing: ants, honeybees and naked mole-rats. Trends Ecol Evol 7:346–349

    Article  CAS  PubMed  Google Scholar 

  • Trumbo ST, Robinson GE (1997) Learning and task interference by corpse-removal specialists in honey bee colonies. Ethology 103:966–975

    Article  Google Scholar 

  • Tschinkel WR (1988) Colony growth and the ontogeny of worker polymorphism in the fire ant, Solenopsis invicta. Behav Ecol Sociobiol 22:103–115

    Article  Google Scholar 

  • Tschinkel WR (1993) Sociometry and sociogenesis of colonies of the fire ant Solenopsis invicta during one annual cycle. Ecol Monogr 63:425–427

    Article  Google Scholar 

  • Tschinkel WR (1998a) The reproductive biology of fire ant societies. Bioscience 48:593-605

  • Tschinkel WR (1998b) Sociometry and sociogenesis of colonies of the harvester ant, Pogonomyrmex badius: worker characteristics in relation to colony size and season. Insectes Soc 45:385-410

  • Tschinkel WR (1999a) Sociometry and sociogenesis of colonies of the harvester ant, Pogonomyrmex badius: distribution of workers, brood and seeds within the nest in relation to colony size and season. Ecol Entomol 24:222-237

  • Tschinkel WR (1999b) Sociometry and sociogenesis of colony-level attributes of the Florida harvester ant (Hymenoptera: Formicidae). Ann Entomol Soc Am 92:80-89

  • Tschinkel WR (2004) The nest architecture of the Florida harvester ant, Pogonomyrmex badius. J Ins Sci 4:21

    Article  Google Scholar 

  • Tschinkel WR (2006) The fire ants. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Tschinkel WR (2011) The organization of foraging in the fire ant, Solenopsis invicta. J Ins Sci 11:26

    Google Scholar 

  • Tschinkel W (2015) The architecture of subterranean ant nests: beauty and mystery underfoot. J Bioecon 17:271–291

    Article  Google Scholar 

  • Waters JS (2014) Theoretical and empirical perspectives on the scaling of supply and demand in social insect colonies. Entomol Exp Appl 150:99–112

    Article  Google Scholar 

  • Waters JS, Holbrook CT, Fewell JH, Harrison JF (2010) Allometric scaling of metabolism, growth, and activity in whole colonies of the seed-harvester ant Pogonomyrmex californicus. Amer Nat 176:501–510

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Weier JA, Feener DH Jr, Lighton JRB (1995) Inter-individual variation in energy cost of running and loading in the seed-harvester ant, Pogonomyrmex maricopa. J Insect Physiol 41:321–327

    Article  CAS  Google Scholar 

  • West GB (1999) The origin of universal scaling laws in biology. Physica 263:104–113

    Article  Google Scholar 

  • West GB, Brown JH (2005) The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization. J Exp Biol 208:1575–1592

    Article  PubMed  Google Scholar 

  • West GB, Kurz H, Sandau K, Brown JH (1998) Allometric scaling in biology. Science 281:751

    Article  Google Scholar 

  • West GB, Brown JH, Enquist BJ (1999) A general model for the structure and allometry of plant vascular systems. Nature 400:664–667

    Article  CAS  Google Scholar 

  • West GB, Brown JH, Enquist BJ (2000) The origin of universal scaling laws in biology. In: Brown JH, West GB (eds). Oxford University Press, pp 87-112

  • West GB, Brown JH, Enquist BJ (2001) A general model for ontogenetic growth. Nature 413:628–631

    Article  CAS  PubMed  Google Scholar 

  • West GB, Woodruff WH, Brown JH (2002) Allometric scaling of metabolic rate from molecules and mitochondria to cells and mammals. PNAS 99:2473-2478

  • West GB, Savage VM, Gillooly J, Enquist BJ, Woodruff WH, Brown JH (2003) Why does metabolic rate scale with body size? Nature 421:713–714

    Article  CAS  PubMed  Google Scholar 

  • Westhus C, Kleineidam CJ, Roces F, Weidenmuller A (2013) Behavioural plasticity in the fanning response of bumblebee workers: impact of experience and rate of temperature change. Anim Behav 85:27–34

    Article  Google Scholar 

  • White CR, Seymour RS (2005) Allometric scaling of mammalian metabolism. J Exp Biol 208:1611–1619

    Article  CAS  PubMed  Google Scholar 

  • White CR, Kearney MR, Matthews PG, Kooijman SALM, Marshall DJ (2011) A manipulative test of competing theories for metabolic scaling. Amer Nat 178:746–754

    Article  Google Scholar 

  • Whiteside GM, Grzybowski B (2002) Self-assembly at all scales. Science 295:2418–2421

    Article  Google Scholar 

  • Wilson EO (1968) The ergonomics of caste in the social insects. Amer Nat 102:41–66

    Article  Google Scholar 

  • Wilson EO (1976) Behavioral discretization and the number of castes in an ant species. Behav Ecol Sociobiol 1:143–154

    Google Scholar 

  • Wilson EO (1980) Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta) II. The ergonomics optimization of leaf-cutting. Behav Ecol Sociobiol 7:157–165

    Article  Google Scholar 

  • Wilson EO (1985) The sociogenesis of insect colonies. Science 228:1489–1495

    Article  CAS  PubMed  Google Scholar 

  • Wilson EO (1986) Caste and division of labor in Erebomyrma, a genus of dimorphic ants (Hymenoptera: Formicidae: Myrmicinae). Insect Soc 33:59–69

    Article  Google Scholar 

  • Wolf TJ, Schmid-Hempel P (1990) On the integration of individual foraging strategies with colony ergonomics in social insects: nectar-collection in honeybees. Behav Ecol Sociobiol 27:103–111

    Article  Google Scholar 

  • Wright CM, Holbrook CT, Pruitt JN (2014) Animal personality aligns task specialization and task proficiency in a spider society. PNAS 111:9533–9537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This research was partially supported by the National Science Foundation Division of Mathematical Sciences, Grant 1313115 to JHF, and the National Science Foundation Division of Integrative and Organismal Systems, Grants 1122157 and 1110796 to JFH. The authors thank Simon Robson and James Traniello for organizing the division of labor symposium and special issue, and James Waters, Tate Holbrook, Rebecca Clark, Raphael Jeanson, Sue Bertram, Root Gorelick, Yun Kang, and the members of ASU’s Social Insect Research Group for many useful discussions on this topic.

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Correspondence to Jennifer H. Fewell.

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Communicated by W. Hughes

This manuscript is a contribution to the special issue Integrative Analysis of Division of Labor—Guest Editors: Simon K. Robson, James F.A. Traniello.

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Fewell, J.H., Harrison, J.F. Scaling of work and energy use in social insect colonies. Behav Ecol Sociobiol 70, 1047–1061 (2016). https://doi.org/10.1007/s00265-016-2097-z

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