Section: Zoology
Topic: Applied biological sciences, Population biology

Brood thermoregulation effectiveness is positively linked to the amount of brood but not to the number of bees in honeybee colonies

Corresponding author(s): Godeau, Ugoline (godeau.ugoline@gmail.com)

10.24072/pcjournal.270 - Peer Community Journal, Volume 3 (2023), article no. e42.

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To ensure the optimal development of brood, a honeybee colony needs to regulate its temperature within a certain range of values (thermoregulation), regardless of environmental changes in biotic and abiotic factors. While the set of behavioural and physiological responses implemented by honeybees to regulate the brood temperature has been well studied, less is known about the factors that may influence the effectiveness of this thermoregulation. Based on the response threshold model of task allocation, increased effectiveness of colony homeostasis should be driven by increases in group size. Therefore, we determined whether colony size (number of adult bees and amount of brood) positively influenced the effectiveness of brood thermoregulation that we measured via two criteria: (i) the brood temperature accuracy, via mean brood temperature, supposedly close to the optimum value for brood rearing, and (ii) the stability of the temperature around the mean value. Finally, within the applied perspective of honeybee colony monitoring, we assessed whether the effectiveness of thermoregulation could be used as a proxy of colony size. For that purpose, we followed 29 honeybee colonies over two years, measured both brood and adult population size regularly over the beekeeping season, and monitored the brood temperature over the 24 hours preceding the inspections of these colonies. We then studied the effect of the size of the colony (number of adult bees and number of brood cells), as well as meteorological variables, on the effectiveness of thermoregulation (mean and stability of brood temperature). We found a clear link between meteorological conditions and brood thermoregulation (mean temperature and its stability). Interestingly, mean brood temperature was also positively linked to the amount of brood, while its stability did not seem influenced by the size of the colony (number of bees or brood amount). The relationship between brood amount and mean temperature was however too weak for clearly discriminating colony population size based solely on the brood thermoregulatory effectiveness. These results demonstrate an extremely high effectiveness of honeybee colonies to thermoregulate the brood regardless of colony size.

Published online:
DOI: 10.24072/pcjournal.270
Type: Research article
Mots-clés : Apis mellifera, homeostasis, colony monitoring, colony size, beekeeping, Apis mellifera, homeostasis, colony monitoring, colony size, beekeeping

Godeau, Ugoline 1; Pioz, Maryline 1; Martin, Olivier 2; Rüger, Charlotte 3; Crauser, Didier 1; Le Conte, Yves 1; Henry, Mickael 1; Alaux, Cédric 1

1 INRAE, Abeilles et Environnement, 84914 Avignon, France
2 INRAE, Biostatistique et processus SPatiaux (BioSP), 84914 Avignon, France
3 ANSES, Epidémiologie et appui à la surveillance (EAS), 69364 Lyon Cedex 07, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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     title = {Brood thermoregulation effectiveness is positively linked to the amount of brood but not to the number of bees in honeybee colonies},
     journal = {Peer Community Journal},
     eid = {e42},
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Godeau, Ugoline; Pioz, Maryline; Martin, Olivier; Rüger, Charlotte; Crauser, Didier; Le Conte, Yves; Henry, Mickael; Alaux, Cédric. Brood thermoregulation effectiveness is positively linked to the amount of brood but not to the number of bees in honeybee colonies. Peer Community Journal, Volume 3 (2023), article  no. e42. doi : 10.24072/pcjournal.270. https://peercommunityjournal.org/articles/10.24072/pcjournal.270/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.zool.100134

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Alaux, C.; Soubeyrand, S.; Prado, A.; Peruzzi, M.; Maisonnasse, A.; Vallon, J.; Hernandez, J.; Jourdan, P.; Conte, Y. L. Measuring biological age to assess colony demographics in honeybees, PLOS ONE, Volume 13 (2018) no. 12, p. e0209192 | DOI

[2] Banner, K. M.; Higgs, M. D. Considerations for assessing model averaging of regression coefficients, Ecological Applications, Volume 27 (2017) no. 1, pp. 78-93 | DOI

[3] Bartoń, K. MuMIn: Multi-model inference (R Package), 2020 (https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf)

[4] Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting linear mixed-effects models using lme4, Journal of Statistical Software, Volume 67 (2015), pp. 1-48 | DOI

[5] Becher, M. A.; Scharpenberg, H.; Moritz, R. F. A. Pupal developmental temperature and behavioral specialization of honeybee workers (Apis Mellifera L.), Journal of Comparative Physiology A, Volume 195 (2009) no. 7, pp. 673-679 | DOI

[6] Beshers, S. N.; Fewell, J. H. Models of division of labor in social insects, Annual Review of Entomology, Volume 46 (2001) no. 1, pp. 413-440 | DOI

[7] Bonoan, R. E.; Goldman, R. R.; Wong, P. Y.; Starks, P. T. Vasculature of the hive: Heat dissipation in the honey bee (Apis Mellifera) hive, Naturwissenschaften, Volume 101 (2014) no. 6, pp. 459-465 | DOI

[8] Bordier, C.; Dechatre, H.; Suchail, S.; Peruzzi, M.; Soubeyrand, S.; Pioz, M.; Pélissier, M.; Crauser, D.; Conte, Y. L.; Alaux, C. Colony adaptive response to simulated heat waves and consequences at the individual level in honeybees (Apis Mellifera), Scientific Reports, Volume 7 (2017) no. 1, p. 3760 | DOI

[9] Bujok, B.; Kleinhenz, M.; Fuchs, S.; Tautz, J. Hot spots in the bee hive, Naturwissenschaften, Volume 89 (2002) no. 7, pp. 299-301 | DOI

[10] Burnham, K. P.; Anderson, D. R. Model selection and multimodel inference: A practical information-theoretic approach, Springer, New York, 2002 | DOI

[11] Burnham, K. P.; Anderson, D. R. Multimodel inference: Understanding AIC and BIC in model selection, Sociological Methods & Research, Volume 33 (2004) no. 2, pp. 261-304 | DOI

[12] Burrill, R. M.; Dietz, A. The response of honey bees to variations in solar radiation and temperature, Apidologie, Volume 12 (1981) no. 4, pp. 319-328 | DOI

[13] Cade, B. S. Model averaging and muddled multimodel inferences, Ecology, Volume 96 (2015) no. 9, pp. 2370-2382 | DOI

[14] Christensen, R. Ordinal - regression models for ordinal data (R Package), 2019 (https://cran.r-project.org/web/packages/ordinal/ordinal.pdf)

[15] Coelho, J. R. Heat transfer and body temperature in honey bee (Hymenoptera: Apidae) drones and workers, Environmental Entomology, Volume 20 (1991) no. 6, pp. 1627-1635 | DOI

[16] Cohen, J. Statistical power analysis for the behavioral sciences, Routledge, New York, 1988 | DOI

[17] Cook, D.; Tarlinton, B.; McGree, J. M.; Blackler, A.; Hauxwell, C. Temperature sensing and honey bee colony strength, Journal of Economic Entomology (2022), p. toac034 | DOI

[18] Ellis, J. D.; Evans, J. D.; Pettis, J. Colony losses, managed colony population decline, and colony collapse disorder in the United States, Journal of Apicultural Research, Volume 49 (2010) no. 1, pp. 134-136 | DOI

[19] Esch, H.; Goller, F.; Heinrich, B. How do bees shiver?, The Science of Nature, Volume 78 (1991) no. 7, pp. 325-328 | DOI

[20] Esch, H.; Bastian, J. Mechanical and electrical activity in the indirect flight muscles of the honey bee, Zeitschrift für vergleichende Physiologie, Volume 58 (1968) no. 4, pp. 429-440 | DOI

[21] Fukuda, H.; Sakagami, S. F. Worker brood survival in honeybees, Population Ecology, Volume 10 (1968) no. 1, pp. 31-39 | DOI

[22] Graham, S.; Myerscough, M. R.; Jones, J. C.; Oldroyd, B. P. Modelling the role of intracolonial genetic diversity on regulation of brood temperature in honey bee (Apis Mellifera L.) colonies, Insectes Sociaux, Volume 53 (2006) no. 2, pp. 226-232 | DOI

[23] Groh, C.; Tautz, J.; Rössler, W. Synaptic organization in the adult honey bee brain Is influenced by brood-temperature control during pupal development, Proceedings of the National Academy of Sciences of the United States of America, Volume 101 (2004) no. 12, pp. 4268-4273 | DOI

[24] Godeau, U. Brood thermoregulation is positively linked to the amount of brood but not to the number of bees in honeybee colonies (Data), Open Science Framework, 2023a | DOI

[25] Godeau, U. Brood thermoregulation is positively linked to the amount of brood but not to the number of bees in honeybee colonies (Scripts, Code and Supplementary Materials), Open Science Framework, 2023b | DOI

[26] Heinrich, B. The hot-blooded insects: Strategies and mechanisms of thermoregulation, Springer, Berlin, Heidelberg, New York, 1993 | DOI

[27] Heinrich, B. Mechanisms of body-temperature regulation in honeybees, Apis Mellifera: II. Regulation of thoracic temperature at high air temperatures, Journal of Experimental Biology, Volume 85 (1980) no. 1, pp. 73-87 | DOI

[28] Heinrich, B. The social physiology of temperature regulation in honeybees, Experimental Behavioral Ecology and Sociobiology, Sinauer Associates, Sunderland, 1985, pp. 393-406

[29] Heinrich, B.; Esch, H. Thermoregulation in Bees, American Scientist, Volume 82 (1994) no. 2, pp. 164-170

[30] Hernandez, J.; Maisonnasse, A.; Cousin, M.; Beri, C.; Le Quintrec, C.; Bouetard, A.; Castex, D.; Decante, D.; Servel, E.; Buchwalder, G.; Brunet, F.; Feschet-Destrella, E.; de Bellescize, K.; Kairo, G.; Frontero, L.; Pédehontaa-Hiaa, M.; Buisson, R.; Pouderoux, T.; Aebi, A.; Kretzschmar, A. ColEval: Honeybee COLony Structure EVALuation for field surveys, Insects, Volume 11 (2020) no. 1, p. 41 | DOI

[31] Himmer, A. Die Temperaturverhältnisse bei den sozialen Hymenopteren, Biological Reviews, Volume 7 (1932) no. 3, pp. 224-253 | DOI

[32] Jones, J. C.; Oldroyd, B. P. Nest thermoregulation in social insects, Advances in Insect Physiology, Volume 33 (2006), pp. 153-191 | DOI

[33] Jones, J. C.; Helliwell, P.; Beekman, M.; Maleszka, R.; Oldroyd, B. P. The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis Mellifera, Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, Volume 191 (2005) no. 12, pp. 1121-1129 | DOI

[34] Jones, J. C.; Myerscough, M. R.; Graham, S.; Oldroyd, B. P. Honey bee nest thermoregulation: Diversity promotes stability, Science, Volume 305 (2004) no. 5682, pp. 402-404 | DOI

[35] Kassambara, A. Rstatix: Pipe-friendly framework for basic statistical tests (R Package), 2021 ( https://cran.r-project.org/web/packages/rstatix/rstatix.pdf)

[36] Kleinhenz, M.; Bujok, B.; Fuchs, S.; Tautz, J. Hot bees in empty broodnest cells: Heating from within, Journal of Experimental Biology, Volume 206 (2003) no. 23, pp. 4217-4231 | DOI

[37] Koeniger, N. Das Wärmen der Brut bei der Honigbiene (Apis Mellifera L.), Apidologie, Volume 9 (1978) no. 4, pp. 305-320 | DOI

[38] Kovac, H.; Käfer, H.; Stabentheiner, A.; Costa, C. Metabolism and upper thermal limits of Apis Mellifera Carnica and A. m. Ligustica, Apidologie, Volume 45 (2014) no. 6, pp. 664-677 | DOI

[39] Kronenberg, F.; Heller, H. C. Colonial thermoregulation in honey bees (Apis Mellifera), Journal of Comparative Physiology, Volume 148 (1982) no. 1, pp. 65-76 | DOI

[40] Lattorff, M. Precision and accuracy of honeybee thermoregulation (Recommendation), PCI Zoolgy, 2023 | DOI

[41] Lindauer, M. The water economy and temperature regulation of the honeybee colony, Bee World, Volume 36 (1955) no. 5, pp. 81-92 | DOI

[42] López-Uribe, M. M.; Ricigliano, V. A.; Simone-Finstrom, M. Defining pollinator health: A holistic approach based on ecological, genetic, and physiological factors, Annual Review of Animal Biosciences, Volume 8 (2020) no. 1, pp. 269-294 | DOI

[43] Marchal, P.; Buatois, A.; Kraus, S.; Klein, S.; Gomez-Moracho, T.; Lihoreau, M. Automated monitoring of bee behaviour using connected hives: Towards a computational apidology, Apidologie, Volume 51 (2020) no. 3, pp. 356-368 | DOI

[44] Meikle, W. G.; Holst, N. Application of continuous monitoring of honeybee colonies, Apidologie, Volume 46 (2015) no. 1, pp. 10-22 | DOI

[45] Meikle, W. G.; Weiss, M.; Maes, P. W.; Fitz, W.; Snyder, L. A.; Sheehan, T.; Mott, B. M.; Anderson, K. E. Internal hive temperature as a means of monitoring honey bee colony health in a migratory beekeeping operation before and during winter, Apidologie, Volume 48 (2017) no. 5, pp. 666-680 | DOI

[46] Meikle, W. G.; Weiss, M.; Stilwell, A. R. Monitoring colony phenology using within-day variability in continuous weight and temperature of honey bee hives, Apidologie, Volume 47 (2016) no. 1, pp. 1-14 | DOI

[47] Neumann, P.; Carreck, N. L. Honey bee colony losses, Journal of Apicultural Research, Volume 49 (2010) no. 1, pp. 1-6 | DOI

[48] Potts, S. G.; Roberts, S. P. M.; Dean, R.; Marris, G.; Brown, M. A.; Jones, R.; Neumann, P.; Settele, J. Declines of managed honey bees and beekeepers in europe, Journal of Apicultural Research, Volume 49 (2010) no. 1, pp. 15-22 | DOI

[49] Prange, H. D. Evaporative cooling in insects, Journal of Insect Physiology, Volume 42 (1996) no. 5, pp. 493-499 | DOI

[50] R Core Team R: A language and environment for statistical computing, 2021 (https://www.R-project.org)

[51] Schmickl, T.; Crailsheim, K. Inner nest homeostasis in a changing environment with special emphasis on honey bee brood nursing and pollen supply, Apidologie, Volume 35 (2004) no. 3, pp. 249-263 | DOI

[52] Seeley, T. Honeybee ecology: A study of adaptation in social life, Princeton University Press, Princeton, NJ, 1985

[53] Seeley, T.; Heinrich, B. Regulation of temperature in the nests of social insects, Insect Thermoregulation, Wiley, New York, 1981, pp. 160-234

[54] Siegel, A. J.; Hui, J.; Johnson, R. N.; Starks, P. T. Honey bee workers as mobile insulating units, Insectes Sociaux, Volume 52 (2005) no. 3, pp. 242-246 | DOI

[55] Southwick, E. E. Allometric relations, metabolism and heart conductance in clusters of honey bees at cool temperatures, Journal of Comparative Physiology B, Volume 156 (1985) no. 1, pp. 143-149 | DOI

[56] Stabentheiner, A.; Kovac, H.; Mandl, M.; Käfer, H. Coping with the cold and fighting the heat: Thermal homeostasis of a superorganism, the honeybee colony, Journal of Comparative Physiology A, Volume 207 (2021) no. 3, pp. 337-351 | DOI

[57] Stabentheiner, A.; Kovac, H.; Brodschneider, R. Honeybee colony thermoregulation – regulatory mechanisms and contribution of individuals in dependence on age, location and thermal stress, PLOS ONE, Volume 5 (2010) no. 1, p. e8967 | DOI

[58] Starks, P. T.; Gilley, D. C. Heat shielding: A novel method of colonial thermoregulation in honey bees, Naturwissenschaften, Volume 86 (1999) no. 9, pp. 438-440 | DOI

[59] Starks, P. T.; Johnson, R. N.; Siegel, A. J.; Decelle, M. M. Heat shielding: A task for youngsters, Behavioral Ecology, Volume 16 (2005) no. 1, pp. 128-132 | DOI

[60] Tautz, J.; Maier, S.; Groh, C.; Rössler, W.; Brockmann, A. Behavioral performance in adult honey bees Is influenced by the temperature experienced during their pupal development, Proceedings of the National Academy of Sciences, Volume 100 (2003) no. 12, pp. 7343-7347 | DOI

[61] Theraulaz, G.; Bonabeau, E.; Denuebourg, J.-N. Response threshold reinforcements and division of labour in insect societies, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 265 (1998) no. 1393, pp. 327-332 | DOI

[62] Ulrich, Y.; Saragosti, J.; Tokita, C. K.; Tarnita, C. E.; Kronauer, D. J. C. Fitness benefits and emergent division of labour at the onset of group living, Nature, Volume 560 (2018) no. 7720, pp. 635-638 | DOI

[63] Vicens, N.; Bosch, J. Weather-dependent pollinator activity in an apple orchard, with special reference to Osmia Cornuta and Apis Mellifera (Hymenoptera: Megachilidae and Apidae), Environmental Entomology, Volume 29 (2000) no. 3, pp. 413-420 | DOI

[64] Wang, Q.; Xu, X.; Zhu, X.; Chen, L.; Zhou, S.; Huang, Z. Y.; Zhou, B. Low-temperature stress during capped brood stage increases pupal mortality, misorientation and adult mortality in honey bees, PLOS ONE, Volume 11 (2016) no. 5, p. e0154547 | DOI

[65] Weidenmüller, A. The control of nest climate in bumblebee (Bombus Terrestris) colonies: Interindividual variability and self reinforcement in fanning response, Behavioral Ecology, Volume 15 (2004) no. 1, pp. 120-128 | DOI

[66] Winston, M. L. The biology of the honey bee, Harvard University Press, Harvard, 1987

[67] Zacepins, A.; Meitalovs, J.; Komasilovs, V.; Stalidzans, E. Temperature sensor network for prediction of possible start of brood rearing by indoor wintered honey bees, 12th International Carpathian Control Conference (ICCC) (2011) | DOI

[68] Zacepins, A.; Stalidzans, E.; Meitalovs, J. Application of information technologies in precision apiculture, 11th International Conference on Precision Agriculture, Indianapolis, Indiana USA. , 2012 (https://www.ispag.org/proceedings/?action=abstract&id=1023&title=Application+of+Information+Technologies+in+Precision+Apiculture)

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