Behavioral Ecology and Sociobiology

, Volume 69, Issue 4, pp 583–591 | Cite as

Social isolation causes mortality by disrupting energy homeostasis in ants

  • Akiko KotoEmail author
  • Danielle Mersch
  • Brian Hollis
  • Laurent KellerEmail author
Original Paper


Social deprivation can have negative effects on the lives of social animals, including humans, yet little is known about the mechanisms by which social withdrawal affects animal health. Here we show that in the carpenter ant Camponotus fellah, socially isolated workers have a greatly reduced life span relative to ants kept in groups of ten individuals. By using a new tracking system, we found that social isolation resulted in important behavioral changes and greatly increased locomotor activity. The higher activity of single ants and their increased propensity to leave the nest to move along the walls suggested that the increased mortality of isolated ants might stem from an imbalance of energy income and expenditure. This view was supported by the finding that while isolated ants ingested the same amount of food as grouped ants, they retained food in the crop, hence preventing its use as an energy source. Moreover, the difference in life span between single and grouped individuals vanished when ants were not fed. This study thus underlines the role of social interactions as key regulators of energy balance, which ultimately affects aging and health in a highly social organism.


Social insect Behavior tracking Social isolation Energy homeostasis 



We thank A. Hefetz for collecting queens, A. Crespi for the technical support for the tracking system, and the Swiss Institute of Bioinformatics for the data storage. We are grateful to M. Miura for the helpful discussion and O. Rueppel and two reviewers for useful comments. This work was funded by several grants from the Swiss National Science Foundation, the Japan Society for the Promotion of Science, and an advanced ERC grant. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflict of interest

We declare no conflict of interest.

Supplementary material

265_2014_1869_MOESM1_ESM.pdf (1.8 mb)
Figure S1 Single ants died younger than grouped ants in each age class. Average life span (± S.E.) of single (light grey) and grouped (dark grey) treatment are shown in each age class, ranging from 2 to 7 month old workers. The effect of social treatment (single versus grouped) on each age class was tested using Wald sandwich test and shown in each column. ns; p > 0.05; *p < 0.05; ** p < 0.01; *** p < 0.001 (PDF 1.77 MB)


  1. Arnold G (1976) Mechanisms in the group effect of honeybees. C R Acad Sci Hebd Seances Acad Sci D 283:1433–1435PubMedGoogle Scholar
  2. Boulay R, Quagebeur M, Godzinska E, Lenoir A (1999) Social isolation in ants: evidence of its impact on survivorship and behavior in Camponotus fellah (Hymenoptera: Formicidae). Sociobiology 33:111–124Google Scholar
  3. Buffin A, Denis D, Van Simaeys G, Goldman S, Deneubourg JL (2009) Feeding and stocking up: radio-labelled food reveals exchange patterns in ants. PLoS One 4:e5919. doi: 10.1371/journal.pone.0005919 CrossRefPubMedCentralPubMedGoogle Scholar
  4. Buie T et al (2010) Evaluation, diagnosis, and treatment of gastrointestinal disorders in individuals with ASDs: a consensus report. Pediatrics 125(Suppl 1):S1–S18. doi: 10.1542/peds. 2009-1878C CrossRefPubMedGoogle Scholar
  5. Cacioppo JT, Hawkley LC (2009) Perceived social isolation and cognition. Trends Cogn Sci 13:447–454. doi: 10.1016/j.tics.2009.06.005 CrossRefPubMedCentralPubMedGoogle Scholar
  6. Cognigni P, Bailey AP, Miguel-Aliaga I (2011) Enteric neurons and systemic signals couple nutritional and reproductive status with intestinal homeostasis. Cell Metab 13:92–104. doi: 10.1016/j.cmet.2010.12.010 CrossRefPubMedCentralPubMedGoogle Scholar
  7. Coury DL et al (2012) Gastrointestinal conditions in children with autism spectrum disorder: developing a research agenda. Pediatrics 130(Suppl 2):S160–S168. doi: 10.1542/peds. 2012-0900N CrossRefPubMedGoogle Scholar
  8. Eisner T, Happ G (1962) The infrabuccal pocket of a formicine ant: a social filtration device. Psyche 69:107–116CrossRefGoogle Scholar
  9. Grassé P, Chauvin R (1944) L'effet de group et de la survie des neutres dans les sociétées d'insectes. Rev Sci 82:261–264Google Scholar
  10. Hansen L, Klotz J (2005) Carpenter Ants of the United States and Canada. Comstock Pub AssocGoogle Scholar
  11. Heinze J, Walter B (2010) Moribund ants leave their nests to die in social isolation. Curr Biol 20:249–252. doi: 10.1016/j.cub.2009.12.031 CrossRefPubMedGoogle Scholar
  12. Holt-Lunstad J, Smith TB, Layton JB (2010) Social relationships and mortality risk: a meta-analytic review. PLoS Med 7:e1000316. doi: 10.1371/journal.pmed.1000316 CrossRefPubMedCentralPubMedGoogle Scholar
  13. House JS, Landis KR, Umberson D (1988) Social relationships and health. Science 241:540–545CrossRefPubMedGoogle Scholar
  14. Howard D, Tschinkel W (1981) The flow of food in colonies of the fire ant, Solenopsis invicta: a multifactorial study. Physiol Entomol 6:297–306CrossRefGoogle Scholar
  15. Hsiao EY et al (2013) Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155:1451–1463. doi: 10.1016/j.cell.2013.11.024 CrossRefPubMedCentralPubMedGoogle Scholar
  16. Huang ZY, Robinson GE (1992) Honeybee colony integration: worker-worker interactions mediate hormonally regulated plasticity in division of labor. PNAS 89:11726–11729CrossRefPubMedCentralPubMedGoogle Scholar
  17. Ja WW et al (2007) Prandiology of Drosophila and the CAFE assay. PNAS 104:8253–8256. doi: 10.1073/pnas.0702726104 CrossRefPubMedCentralPubMedGoogle Scholar
  18. Karelina K, Norman GJ, Zhang N, Morris JS, Peng H, DeVries AC (2009) Social isolation alters neuroinflammatory response to stroke. PNAS 106:5895–5900. doi: 10.1073/pnas.0810737106 CrossRefPubMedCentralPubMedGoogle Scholar
  19. Keller L, Passera L (1990) Fecundity of ant queens in relation to their age and the mode of colony founding. Insect Soc 37:116–130CrossRefGoogle Scholar
  20. Markin G (1970) Food distribution within laboratory colonies of the argentine ant, Tridomyrmex humilis (Mayr). Insect Soc 17:127–157CrossRefGoogle Scholar
  21. Matsumoto K, Pinna G, Puia G, Guidotti A, Costa E (2005) Social isolation stress-induced aggression in mice: a model to study the pharmacology of neurosteroidogenesis. Stress 8:85–93. doi: 10.1080/10253890500159022 CrossRefPubMedGoogle Scholar
  22. Mersch DP, Crespi A, Keller L (2013) Tracking individuals shows spatial fidelity is a key regulator of ant social organization. Science 340:1090–1093. doi: 10.1126/science.1234316 CrossRefPubMedGoogle Scholar
  23. Modlmeier AP, Foitzik S, Scharf I (2013) Starvation endurance in the ant Temnothorax nylanderi depends on group size, body size and access to larvae. Physiol Entomol 38:89–94. doi: 10.1111/Phen.12007 CrossRefGoogle Scholar
  24. Nonogaki K, Nozue K, Oka Y (2007) Social isolation affects the development of obesity and type 2 diabetes in mice. Endocrinology 148:4658–4666. doi: 10.1210/en.2007-0296 CrossRefPubMedGoogle Scholar
  25. Robinson GE, Page RE Jr, Strambi C, Strambi A (1989) Hormonal and genetic control of behavioral integration in honey bee colonies. Science 246:109–112. doi: 10.1126/science.246.4926.109 CrossRefPubMedGoogle Scholar
  26. Roger G, Pain J (1966) L'influence de la reine d'abeille (Apis mellifica L.) sur le taux de mortalité des ouvrières accompagnatrices. Ann Abeille 9:5–36CrossRefGoogle Scholar
  27. Rozanski A, Blumenthal JA, Kaplan J (1999) Impact of psychological factors on the pathogenesis of cardiovascular disease and implications for therapy. Circulation 99:2192–2217CrossRefPubMedGoogle Scholar
  28. Ruan H, Wu CF (2008) Social interaction-mediated lifespan extension of Drosophila Cu/Zn superoxide dismutase mutants. PNAS 105:7506–7510. doi: 10.1073/pnas.0711127105 CrossRefPubMedCentralPubMedGoogle Scholar
  29. Seid M, Traniello J (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. doi: 10.1007/s00265-006-0207-z CrossRefGoogle Scholar
  30. Sitbon G (1967) L'effet de groupe et la mortalité des abeilles d'hiver et d'été, isolées et groupées. Ann Abeille 10:203–212CrossRefGoogle Scholar
  31. Sitbon G (1968a) Les sucres totaux chez l'abeille d'hiver en fonction de l'isolement. Insect Soc 15:37–44CrossRefGoogle Scholar
  32. Sitbon G (1968b) Teneur en eau et en azote chez l'abeille en fonction de l'isolement. Insect Soc 15:413–418CrossRefGoogle Scholar
  33. Smith CR, Toth AL, Suarez AV, Robinson GE (2008) Genetic and genomic analyses of the division of labour in insect societies. Nat Rev Genet 9:735–748. doi: 10.1038/nrg2429 CrossRefPubMedGoogle Scholar
  34. Umberson D, Montez JK (2010) Social relationships and health: a flashpoint for health policy. J Health Soc Behav 51(Suppl):S54–S66. doi: 10.1177/0022146510383501 CrossRefPubMedCentralPubMedGoogle Scholar
  35. Venna VR, Xu Y, Doran SJ, Patrizz A, McCullough LD (2014) Social interaction plays a critical role in neurogenesis and recovery after stroke. Transt Psychiatry 4:e351. doi: 10.1038/tp.2013.128 CrossRefGoogle Scholar
  36. Wada-Katsumata A, Yamaoka R, Aonuma H (2011) Social interactions influence dopamine and octopamine homeostasis in the brain of the ant Formica japonica. J Exp Biol 214:1707–1713. doi: 10.1242/jeb.051565 CrossRefPubMedGoogle Scholar
  37. Wiberg GS, Grice HC (1963) Long-term isolation stress in rats. Science 142:507CrossRefPubMedGoogle Scholar
  38. Wilson E, Hölldobler B (1990) The ants. Springer, BerlinGoogle Scholar
  39. Yang YC, McClintock MK, Kozloski M, Li T (2013) Social isolation and adult mortality: the role of chronic inflammation and sex differences. J Health Soc Behav 54:183–203. doi: 10.1177/0022146513485244 CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Ecology and Evolution, Quartier UNIL-Sorge, Batiment BiophoreUniversity of LausanneLausanneSwitzerland
  2. 2.Department of Genetics, Graduate School of Pharmaceutical SciencesThe University of TokyoTokyoJapan
  3. 3.Division of NeurobiologyMRC Laboratory of Molecular BiologyCambridgeUK

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