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Research Article

Rapid behavioral maturation accelerates failure of stressed honey bee colonies

Clint J. Perry, View ORCID ProfileEirik Søvik, Mary R. Myerscough, and Andrew B. Barron
  1. aDepartment of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia;
  2. bSchool of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom;
  3. cDepartment of Biology, Washington University in St. Louis, St. Louis, MO 63130; and
  4. dSchool of Mathematics and Statistics, The University of Sydney, Sydney, NSW 2006, Australia

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PNAS first published February 9, 2015; https://doi.org/10.1073/pnas.1422089112
Clint J. Perry
aDepartment of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia;
bSchool of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom;
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Eirik Søvik
aDepartment of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia;
cDepartment of Biology, Washington University in St. Louis, St. Louis, MO 63130; and
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  • ORCID record for Eirik Søvik
Mary R. Myerscough
dSchool of Mathematics and Statistics, The University of Sydney, Sydney, NSW 2006, Australia
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Andrew B. Barron
aDepartment of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia;
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  • For correspondence: andrew.barron@mq.edu.au
  1. Edited by Gene E. Robinson, University of Illinois at Urbana–Champaign, Urbana, IL, and approved January 21, 2015 (received for review November 18, 2014)

This article has a Correction. Please see:

  • Correction for Perry et al., Rapid behavioral maturation accelerates failure of stressed honey bee colonies - July 26, 2016
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Significance

Honey bee colony death rates are unsustainably high. While many stressors have been identified that contribute to this problem, we do not know why colonies transition so rapidly from a state of apparent health to failure. It is well known that individual bees react to nutritional and pathogen stresses by foraging precociously: our study explains how colony failure arises from the social responses of individual bees to stress. We used radio tracking to monitor performance of bees and found that workers who begin foraging prematurely perform very poorly. This compounds the stresses on the colony and accelerates failure. We suggest how colonies at risk can be identified early, and the most effective interventions to prevent failure.

Abstract

Many complex factors have been linked to the recent marked increase in honey bee colony failure, including pests and pathogens, agrochemicals, and nutritional stressors. It remains unclear, however, why colonies frequently react to stressors by losing almost their entire adult bee population in a short time, resulting in a colony population collapse. Here we examine the social dynamics underlying such dramatic colony failure. Bees respond to many stressors by foraging earlier in life. We manipulated the demography of experimental colonies to induce precocious foraging in bees and used radio tag tracking to examine the consequences of precocious foraging for their performance. Precocious foragers completed far fewer foraging trips in their life, and had a higher risk of death in their first flights. We constructed a demographic model to explore how this individual reaction of bees to stress might impact colony performance. In the model, when forager death rates were chronically elevated, an increasingly younger forager force caused a positive feedback that dramatically accelerated terminal population decline in the colony. This resulted in a breakdown in division of labor and loss of the adult population, leaving only brood, food, and few adults in the hive. This study explains the social processes that drive rapid depopulation of a colony, and we explore possible strategies to prevent colony failure. Understanding the process of colony failure helps identify the most effective strategies to improve colony resilience.

  • behavioral development
  • temporal polyethism
  • colony collapse disorder
  • compartment model
  • RFID

Footnotes

  • ↵1C.J.P. and E.S. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: andrew.barron{at}mq.edu.au.
  • Author contributions: C.J.P., E.S., and A.B.B. designed research; C.J.P., E.S., M.R.M., and A.B.B. performed research; C.J.P., E.S., and M.R.M. analyzed data; and C.J.P., E.S., M.R.M., and A.B.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1422089112/-/DCSupplemental.

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Failure of stressed honey bee colonies
Clint J. Perry, Eirik Søvik, Mary R. Myerscough, Andrew B. Barron
Proceedings of the National Academy of Sciences Feb 2015, 201422089; DOI: 10.1073/pnas.1422089112

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Failure of stressed honey bee colonies
Clint J. Perry, Eirik Søvik, Mary R. Myerscough, Andrew B. Barron
Proceedings of the National Academy of Sciences Feb 2015, 201422089; DOI: 10.1073/pnas.1422089112
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