Are societies resilient? Challenges faced by social insects in a changing world

Abstract

Social insects are considered to be highly successful and ecologically dominant because they comprise the majority of insect biomass in many ecosystems. One key to the success of social insects is their highly coordinated and organized behavior, which allows them to more efficiently exploit resources. However, as our world undergoes dramatic global changes, such as climate change, deforestation, and the introduction of invasive species, the very traits that have provided evolutionary advantages may become liabilities for some social insect species. Here we propose that some social traits, which are conventionally thought to be beneficial, will be detrimental in the context of rapid environmental change. We focus on four fundamental aspects of complex insect societies (coordination of cooperative behavior, worker caste organization, social immunity, and ecosystem engineering) and make predictions about how social lifestyles may become compromised in the face of ecological adversity. We intend to bring attention to the unique vulnerabilities of social insects and propose novel avenues of research to better illuminate the consequences of global change for social insects.

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References

  1. Bagneres AG, Hanus R (2015) Communication and social regulation in termites. In: Aquiloni L, Tricarico E (eds) Social regulation in invertebrates. Springer International Publishing, Switzerland, pp 193–248

    Google Scholar 

  2. Barron AB (2015) Death of the bee hive: understanding the failure of an insect society. Curr Opin Insect Sci 10:45–50

    Article  PubMed  Google Scholar 

  3. Beggs JR, Brockerhoff EG, Corley JC, Kenis M, Masciocchi M, Muller F, Rome Q, Villemant C (2011) Ecological effects and management of invasive alien Vespidae. Biocontrol 56:505–526

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  5. Blum MS (1996) Semiochemical parsimony in the Arthropoda. Annu Rev Entomol 41:353–374

    Article  PubMed  CAS  Google Scholar 

  6. Blum MS, Brand JM (1972) Social insect pheromones: their chemistry and function. Am Zool 12:553–576

    Article  CAS  Google Scholar 

  7. Bollazzi M, Kronenbitter J, Roces F (2008) Soil temperature, digging behaviour, and the adaptive value of nest depth in South American species of Acromyrmex leaf-cutting ants. Oecologia 158:165–175

    Article  PubMed  Google Scholar 

  8. Bradbury JW, Vehrencamp JW (2011) Principles of animal communication. Oxford University Press, Oxford

    Google Scholar 

  9. Cao TT, Dornhaus A (2008) Ants under crowded conditions consume more energy. Biol Lett 4:613–615

    Article  PubMed  PubMed Central  Google Scholar 

  10. Chapman RE, Bourke A (2001) The influence of sociality on the conservation biology of social insects. Ecol Lett 4:650–662

    Article  Google Scholar 

  11. Christe P, Oppliger A, Bancala F, Castella G, Chapuisat M (2003) Evidence for collective medication in ants. Ecol Lett 6:19–22

    Article  Google Scholar 

  12. Colin T, Doums C, Péronnet R, Molet M (2017) Decreasing worker size diversity does not affect colony performance during laboratory challenges in the ant Temnothorax nylanderi. Behav Ecol Sociobiol 71:92

    Article  Google Scholar 

  13. Couvillon MJ, Robinson EJH, Atkinson B, Child L, Dent KR, Ratnieks FLW (2008) En garde: rapid shifts in honey bee, Apis mellifera, guarding behavior are triggered by onslaught of conspecific intruders. Anim Behav 76:1653–1658

    Article  Google Scholar 

  14. Cremer S, Armitage SAO, Schmid-Hempel P (2007) Social immunity. Curr Biol 17:693–702

    Article  CAS  Google Scholar 

  15. d’Ettorre P, Lenoir P (2010) Nestmate recognition. In: Lach L (ed) Ant ecology. Oxford University Press, New York, pp 194–209

    Google Scholar 

  16. Downs S, Ratnieks F (1999) Adaptive shifts in honey bee (Apis mellifera L.) guarding behavior support predictions of the acceptance threshold model. Behav Ecol 11:326–333

    Article  Google Scholar 

  17. Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M, Thompson GJ, Zou Z, Hultmark D (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 15:645–656

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  18. Gardner A, West SA (2007) Social evolution: the decline and fall of genetic kin recognition. Curr Biol 17:810–812

    Article  CAS  Google Scholar 

  19. Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931–949

    Article  CAS  Google Scholar 

  20. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge

    Google Scholar 

  21. Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Ann Rev Ecol Syst 33:181–233

    Article  Google Scholar 

  22. Huang ZY, Robinson GE (1996) Regulation of honey bee division of labor by colony age demography. Behav Ecol Sociobiol 39:147–158

    Article  Google Scholar 

  23. Huang ZY, Robinson GE, Borst DW (1994) Physiological correlates of division of labor among similarly aged honey bees. J Comp Physiol A 174:731–739

    Article  PubMed  CAS  Google Scholar 

  24. Hughes J, Broome A (2007) Forests and wood ants in Scotland. Forestry Commission http://www.woodants.org.uk. Accessed Jun 2017

  25. Hughes WOH, Eilenberg J, Boomsma JJ (2002) Trade-offs in group living: transmission and disease resistance in leaf-cutting ants. Proc R Soc B 269:1811–1819

    Article  PubMed  Google Scholar 

  26. Jandt JM, Bengston S, Pinter-Wollman N, Pruitt JN, Raine NE, Dornhaus A, Sih A (2014) Behavioural syndromes and social insects: personality at multiple levels. Biol Rev 89:48–67

    Article  PubMed  Google Scholar 

  27. Jandt JM, Hunt EM, McGlynn TP (2015) Intraspecific food-robbing and neighborhood competition: consequences for anti-robber vigilance and colony productivity. Biotropica 47:491–496

    Article  Google Scholar 

  28. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386

    Article  Google Scholar 

  29. Jones JC, Oldroyd BP (2006) Nest thermoregulation in social insects. Adv In Insect Phys 33:153–191

    Article  Google Scholar 

  30. King JR, Warren RJ, Bradford MA (2013) Social insects dominate the Eastern US temperate hardwood forest macroinvertebrate communities in warmer regions. Plos One 8:e75843. https://doi.org/10.1371/journal.pone.0075843

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  31. Kleeberg I, Menzel F, Foitzik S (2017) The influence of slavemaking lifestyle, caste and sex on chemical profiles in Temnothorax ants: insights into the evolution of cuticular hydrocarbons. Proc R Soc B 284:20162249. https://doi.org/10.1098/rspb.2016.2249

    Article  PubMed  CAS  Google Scholar 

  32. Kudo K, Zucchi R (2008) Nestmate recognition in a Neotropical swarm-founding wasp: no effect of seasonality on tolerance of alien conspecifics. Ethol Ecol Evol 20:170–180

    Article  Google Scholar 

  33. Law JH, Wilson EO, McCloskey JA (1965) Biochemical polymorphism in ants. Science 149:544–545

    Article  PubMed  CAS  Google Scholar 

  34. Leighton GM, Charbonneau D, Dornhaus A (2016) Task switching is associated with temporal delays in Temnothorax rugatulus ants. Behav Ecol 28:319–327

    Article  PubMed  PubMed Central  Google Scholar 

  35. Leonhardt SD, Schmitt T, Bluthgen N (2011) Tree resin composition, collection behavior and selective filters shape chemical profiles of tropical bees (Apidae: Meliponini). PLOS ONE 6:e23445. https://doi.org/10.1371/journal.pone.0023445

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  36. Leonhardt S, Menzel F, Nehring V, Schmitt T (2016) Ecology and evolution of communication in social insects. Cell 164:1277–1287

    Article  PubMed  CAS  Google Scholar 

  37. Leza M, Watrous KM, Bratu J, Woodard SH (2018) Effects of neonicotinoid insecticide exposure and monofloral diet on nest founding bumblebee queens. Proc R Soc B 285:20180761

    Article  PubMed  CAS  Google Scholar 

  38. Liang D, Silverman J (2000) You are what you eat: Diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften 87:412–416

    Article  PubMed  CAS  Google Scholar 

  39. Martin JM, Carruthers JM, Williams PH, Drijfhout FP (2010) Host specific social parasites (Psithyrus) indicate chemical recognition system in Bumblebees. J Chem Ecol 36:855–863

    Article  PubMed  CAS  Google Scholar 

  40. Mertl AL, Traniello JF (2009) Behavioral evolution in the major worker subcaste of twig-nesting Pheidole (Hymenoptera: Formicidae): does morphological specialization influence task plasticity? Behav Ecol Sociobiol 63:1411–1426

    Article  Google Scholar 

  41. Meunier J (2015) Social immunity and the evolution of group living in insects. Philos Trans R Soc B 370: 20140102. https://doi.org/10.1098/rstb.2014.0102

    Article  Google Scholar 

  42. Millennium Ecosystem Assessment (2005) Ecosystems and human well-being: synthesis. Island Press, Washington, DC

    Google Scholar 

  43. Nascimento D, Nascimento F (2012) Acceptance Threshold Hypothesis is supported by chemical similarity of cuticular hydrocarbons in a stingless bee, Melipona asilvai. J Chem Ecol 38:1432–1440

    Article  PubMed  CAS  Google Scholar 

  44. Pamminger T, Steier T, Tragust S (2016) High temperature and temperature variation undermine future disease susceptibility in a population of the invasive garden ant, Lasius neglectus. Sci Nat 103:46

    Article  CAS  Google Scholar 

  45. Pankiw T, Page RE Jr (2000) Response thresholds to sucrose predict foraging division of labor in honeybees. Behav Ecol Sociobiol 47:265–267

    Article  Google Scholar 

  46. Pankiw T, Page RE Jr (2003) Effect of pheromones, hormones, and handling on sucrose response thresholds of honey bees (Apis mellifera L.). J Comp Physiol A 189:675–684

    Article  CAS  Google Scholar 

  47. Perry CJ, Søvik E, Myerscough MR, Barron AB (2015) Rapid behavioral maturation accelerates failure of stressed honey bee colonies. Proc Natl Acad Sci USA 112:3427–3432

    Article  PubMed  CAS  Google Scholar 

  48. Pinter-Wollman N (2015) Nest architecture shapes the collective behaviour of harvester ants. Biol Lett 11:20150695. https://doi.org/10.1098/rsbl.2015.0695

    Article  PubMed  PubMed Central  Google Scholar 

  49. Purcell J, Avilés L (2007) Smaller colonies and more solitary living mark higher elevation populations of a social spider. J Anim Ecol 76:590–597

    Article  PubMed  Google Scholar 

  50. Purcell J, Vasconcellos-Neto J, Gonzaga MO, Fletcher JA, Avilés L (2012) Spatio-temporal differentiation and sociality in spiders. Plos One 7:e34592. https://doi.org/10.1371/journal.pone.0034592

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  51. Reber A, Purcell J, Buechel SD, Puri P, Chapuisat M (2011) The expression and impact of antifungal grooming in ants. J Evol Biol 24:954–964

    Article  PubMed  CAS  Google Scholar 

  52. Reeve HK (1989) The evolution of conspecific acceptance thresholds. Am Nat 133:407–435

    Article  Google Scholar 

  53. Robinson EJH (2009) Physiology as a caste-defining feature. Insectes Soc 56:1–6

    Article  Google Scholar 

  54. Robinson GE (1987) Regulation of honey bee age polyethism by juvenile hormone. Behav Ecol Sociobiol 20:329–338

    Article  Google Scholar 

  55. Robinson GE (1992) Regulation of division of labor in insect societies. Ann Rev Entomol 37:637–665

    Article  CAS  Google Scholar 

  56. Schulz DJ, Huang ZY, Robinson GE (1998) Effects of colony food shortage on behavioral development in honey bees. Behav Ecol Sociobiol 42:295–303

    Article  Google Scholar 

  57. Sih A, Ferrari MCO, Harris DJ (2011) Evolution and behavioural responses to human-induced rapid environmental change. Evol Appl 4:367–387

    Article  PubMed  PubMed Central  Google Scholar 

  58. Simone-Finstrom M, Borba RS, Wilson M, Spivak M (2017) Propolis Counteracts Some Threats to Honey Bee Health. Insects 8:e46. https://doi.org/10.3390/insects8020046

    Article  PubMed  Google Scholar 

  59. Steinmetz I, Schmolz E (2005) Nest odor dynamics in the social wasp Vespula vulgaris. Naturwiss 92:414–418

    Article  PubMed  CAS  Google Scholar 

  60. Stuart RJ, Alloway TM (1985) Behavioural evolution and domestic degeneration in obligatory slave-making ants (Hymenoptera: Formicidae: Leptothoracini). Anim Behav 33:1080–1088

    Article  Google Scholar 

  61. Theraulaz G, Bonabeau E, Beneubourg J (1998) The origin of nest complexity in social insects. Complexity 3:15–25

    Article  Google Scholar 

  62. Tylianakis JM, Diham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363

    Article  PubMed  Google Scholar 

  63. Ushitani T, Perry CJ, Cheng K, Barron AB (2016) Accelerated behavioural development changes fine-scale search behaviour and spatial memory in honey bees (Apis mellifera L.). J Exp Biol 219:412–418

    Article  PubMed  Google Scholar 

  64. van Zweden JS, Brask JB, Christensen JH, Boomsma JJ, Linksvayer TA, d'Ettorre P (2010) Blending of heritable recognition cues among ant nestmates creates distinct colony gestalt odours but prevents within-colony nepotism. J Evol Biol 23:1498–1508

    Article  PubMed  CAS  Google Scholar 

  65. van Zweden JS, d’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ, Bagnères A-G (eds) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge, pp 222–243

    Google Scholar 

  66. Wagner D, Tissot M, Gordon D (2001) Task-related environment alters the cuticular hydrocarbon composition of harvester ants. J Chem Ecol 27:1805–1819

    Article  PubMed  CAS  Google Scholar 

  67. Waser NM (1998) Task-matching and short-term size shifts in foragers of the harvester ant, Messor pergandei (Hymenoptera: Formicidae). J Insect Behav 11:451–462

    Article  Google Scholar 

  68. Wenzel JW (1998) A generic key to the nests of hornets, yellowjackets, and paper wasps worldwide (Vespidae, Vespinae, Polistinae). Am Museum Novit 3224:39

    Google Scholar 

  69. Wilson MB, Spivak M, Hegeman AD, Rendahl A, Cohe JD (2013) Metabolomics reveals the origins of antimicrobial plant resins collected by honey bees. Plos One 8:e77512. https://doi.org/10.1371/journal.pone.0077512

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  70. Wilson EO (1971) The insect societies. Harvard University Press, Cambridge

    Google Scholar 

  71. Wilson EO (1983) Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). Behav Ecol Sociobiol 14:47–54

    Article  Google Scholar 

  72. Wilson EO (1990) Success and dominance in ecosystems: the case of the social insects. Ecology Institute, Oldendorf

    Google Scholar 

  73. Wittwer B, Hefetz A, Simon T, Murphy LEK, Elgar MA, Pierce NE, Kocher SD (2017) Solitary bees reduce investment in communication compared with their social relatives. Proc Natl Acad Sci USA 114:6569–6574

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors thank Kevin Loope, Amanda Hale, Madison Sankovitz, Daniel Pierce, and two anonymous reviewers for their thoughtful comments and suggestions. This work was supported in part by University of California Agricultural Experiment Station funds to J. Purcell and S.H. Woodard.

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Correspondence to S. Hollis Woodard or Jessica Purcell.

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Fisher, K., West, M., Lomeli, A.M. et al. Are societies resilient? Challenges faced by social insects in a changing world. Insect. Soc. 66, 5–13 (2019). https://doi.org/10.1007/s00040-018-0663-2

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Keywords

  • Land conversion
  • Invasive species
  • Conservation
  • Anthropocene
  • Chemical communication
  • Task allocation