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Heat resistance variability in the Lebanese bee fauna

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Abstract

Wild bees are facing many environmental challenges that are reshaping their distributions and even causing extinctions. One of the common threats is climate change leading to a higher frequency of extreme climatic events such as heat waves. We focused on the bee fauna of the eastern Mediterranean country of Lebanon and assessed intra- and interspecific variability of the heat stress resistance in correlation with dry body weight, altitude, and collection date. We used the time before heat stupor (THS) at 40 °C in semi-controlled conditions as a proxy for heat resistance. We found significant interspecific differences in heat resistance, and a positive correlation with dry weight in some taxa. At the intraspecific level, there was a significant difference in heat resistance between sexes for some species. Also, dry/fresh weights, altitude, and collection date were correlated to a higher heat resistance in some taxa. In the context of global changes, we argue that we need heat tolerance metrics for a better understanding of bee decline and to enhance conservation measures at regional scale.

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Data Availability

 Measured variables of tested specimens with geographic coordinates of the collecting sites are available in Supplementary Material A .

Code Availability

R scripts related to the analysis of hyperthermic resistance of bees are all available on request at corresponding author.

References

  • Alboukadel K, Kosinski M, Biecek P, Fabian S (2021) R package survminer, Ver. 0.4.9. https://rpkgs.datanovia.com/survminer/index.html.

  • Andrew NR, Hart RA, Jung MP, Hemmings Z, Terblanche JS (2013) Can temperate insects take the heat? A case study of the physiological and behavioural responses in a common ant, Iridomyrmex purpureus (Formicidae), with potential climate change. J Insect Physiol 59(9):870–880

    Article  CAS  PubMed  Google Scholar 

  • Ascher JS, Pickering J (2020) Discover Life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). http://www.discoverlife.org/mp/20q?guide=Apoidea_species

  • Ayrinhac A, Debat V, Gibert P, Kister A-G, Legout H, Moreteau B, Vergilino R, David JR (2004) Cold adaptation in geographical populations of Drosophila melanogaster: phenotypic plasticity is more important than genetic variability. Funct Ecol 18:700–706

    Article  Google Scholar 

  • Bishop JA, Armbruster WS (1999) Thermoregulatory abilities of Alaskan bees: effects of size, phylogeny and ecology. Funct Ecol 13:711–724

    Article  Google Scholar 

  • Boustani M, Yammine W, Nemer N, Hammad AF, E., Michez, D., & Rasmont, P. (2020) Distribution and flower visitation records of bumblebees in Lebanon (Hymenoptera: Apidae). Annales De La Société Entomologique De France 56(2):115–124

    Article  Google Scholar 

  • Boustani M, Rasmont P, Dathe H, Ghisbain G, Kasparek M, Michez D, Müller A, Pauly A, Risch S, Straka J, Terzo M, Van Achter X, Wood T, Nemer N (2021) The bees of Lebanon (Hymenoptera: Apoidea: Anthophila). Zootaxa 4976:001–146

    Article  Google Scholar 

  • Bujan J, Roeder KA, de Beurs K, Weiser MD, Kaspari M (2020) Thermal diversity of North American ant communities: Cold tolerance but not heat tolerance tracks ecosystem temperature. Glob Ecol Biogeogr 29:1486–1494

    Article  Google Scholar 

  • Cahan SH, Nguyen AD, Stanton-Geddes J, Penick CA, Hernáiz-Hernández Y, DeMarco BB, Gotelli NJ (2017) Modulation of the heat shock response is associated with acclimation to novel temperatures but not adaptation to climatic variation in the ants Aphaenogaster picea and A. rudis. Comp Biochem Physiol 204:113–120

    Article  Google Scholar 

  • Cameron S, Sadd B (2020) Global trends in bumble bee health. Annu Rev Entomol 65. https://doi.org/10.1146/annurev-ento-011118-111847

  • Cook J (1993) Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71:421–435

    Article  Google Scholar 

  • Cui D, Liang S, Wang D (2021) Observed and projected changes in global climate zones based on Köppen climate classification. Wires Clim Change 12:e701

    Article  Google Scholar 

  • Danforth BN, Minckley RL, Neff JL, Fawcett F (2019) The solitary bees: biology, evolution. princeton university press, Conservation, p 9780691168982

    Book  Google Scholar 

  • Di Pasquale G, Salignon M, Le Conte Y, Belzunces LP, Decourtye A, Kretzschmar A, Suchai S, Brunet J-L, Alaux C (2013) Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PLoS ONE 8(8):e72016

    Article  PubMed  PubMed Central  Google Scholar 

  • Dirzo A, Young HS, Galetti M, Ceballos G, Isaac NJB, Collen B (2014) Defaunation in the Anthropocene. Science 345(6195):401–406

    Article  CAS  PubMed  Google Scholar 

  • Gérard M, Martinet B, Maebe K, Marshall L, Smagghe G, Vereecken NJ, Vray S, Rasmont P, Michez D (2020) Shift in size of bumblebee queens over the last century. Glob Change Biol 26:1185–1195

    Article  Google Scholar 

  • Ghisbain G, Thiery W, Massonnet F, Erazo D, Rasmont P, Michez D, Dellicour S (2023) Projected decline in European bumblebee populations in the twenty-first century. Nature. https://doi.org/10.1038/s41586-023-06471-0

    Article  PubMed  Google Scholar 

  • Gonzalez VH, Hranitz JM, Percival CR, Pulley KL, Tapsak ST, Tscheulin T, Petanidou T, Barthell JF (2020) Thermal tolerance varies with dim-light foraging and elevation in large carpenter bees (Hymenoptera: Apidae: Xylocopini). Ecol Entomol 45:688–696

    Article  Google Scholar 

  • Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347(6229):1255957

    Article  PubMed  Google Scholar 

  • Hayes T, López-Martínez G (2021) Resistance and survival to extreme heat shows circadian and sex-specific patterns in A cavity nesting bee. Curr Res Insect Sci 1(100020)

  • Heinrich B (1975) Thermoregulation in bumblebees. II. Energetics of warmup and free flight. J Comp Physiol 96:155–166

    Article  Google Scholar 

  • Heinrich B, Heinrich MJE (1983) Size and caste in temperature regulation by bumblebees. Physiol Zool 56:552–562

    Article  Google Scholar 

  • Hodkinson ID (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev 80:489–513

    Article  PubMed  Google Scholar 

  • Iltis C, Louâpre P, Vogelweith F, Thiéry D, Moreau J (2021) How to stand the heat? Post-stress nutrition and developmental stage determine insect response to a heat wave. J Insect Physiol 131:104214

    Article  CAS  PubMed  Google Scholar 

  • IUCN (2023) The IUCN Red List of Threatened Species. Version 2023-1. https://www.iucnredlist.org. Accessed 9 Sept 2023

  • Jenkins CN, Sanders NJ, Andersen AN, Arnan X, Brühl CA, Cerda X, Ellison AM, Fisher BL, Fitzpatrick MC, Gotelli NJ, Gove AD, Guénard B, Lattke JE, Lessard J-P, McGlynn TP, Menke SB, Parr CL, Philpott SM, Vasconcelos HL, Weiser MD, Dunn RR (2011) Global diversity in light of climate change: the case of ants. Divers Distrib 17:652–662

    Article  Google Scholar 

  • Jetz W, Wilcove DS, Dobson AP (2007) Projected impacts of climate and land-use change on the global diversity of birds. PLoS Biol 5(6):e157

    Article  PubMed  PubMed Central  Google Scholar 

  • Kellermann V, Overgaard J, Hoffmann AA, Fløjgaard C, Svenning JC, Loeschcke V (2012) Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically. Proc Natl Acad Sci USA 109(40):16228–16233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kierat J, Szentgyörgyi H, Czarnoleski M, Woyciechowski M (2017) The thermal environment of the nest affects body and cell size in the solitary red mason bee (Osmia bicornis L.). J Therm Biol 68:39–44

    Article  PubMed  Google Scholar 

  • Kingsolver JG, Buckley LB (2017) Quantifying thermal extremes and biological variation to predict evolutionary responses to changing climate. Philos Trans R Soc B 372(1723):20160147

    Article  Google Scholar 

  • Kingsolver JG, Diamond SE, Buckley LB (2013) Heat stress and the fitness consequences of climate change for terrestrial ectotherms. Funct Ecol 27:1415–1423

    Article  Google Scholar 

  • Kiritani K (2013) Different effects of climate change on the population dynamics of insects. Appl Entomol Zool 48:97–104

    Article  Google Scholar 

  • Kline O, Joshi NK (2020) Mitigating the effects of habitat loss on solitary bees in agricultural ecosystems. Agriculture 10(4):115

    Article  CAS  Google Scholar 

  • Leclair AT, Drake DAR, Pratt TC, Mandrak NE (2020) Seasonal variation in thermal tolerance of redside dace Clinostomus elongatus. Conserv. Physiol. 8(1):coaa081

    Article  PubMed  PubMed Central  Google Scholar 

  • Lenoir J, Gégout JC, Marquet PA, de Ruffray P, Brisse H (2008) A significant upward shift in plant species optimum elevation during the 20th century. Science 320(5884):1768–1771

    Article  CAS  PubMed  Google Scholar 

  • Lutterschmidt WI, Hutchison VH (1997) The critical thermal maximum: data to support the onset of spasms as the definitive end point. Can J Zool 75:1553–1560

    Article  Google Scholar 

  • Maebe K, De Baets A, Vandamme P, Vereecken NJ, Michez D, Smagghe G (2021) Impact of intraspecific variation on measurements of thermal tolerance in bumble bees. J Therm Biol 99:103002

    Article  PubMed  Google Scholar 

  • Martinet B, Lecocq T, Smet J, Rasmont P (2015) A protocol to assess insect resistance to heat waves, applied to bumblebees (Bombus Latreille, 1802). PLoS ONE 10(3):e0118591

    Article  PubMed  PubMed Central  Google Scholar 

  • Martinet B, Zambra E, Przybyla K, Lecocq T, Anselmo A, Nonclercq D, Rasmont P, Michez D, Hennebert E (2020) Mating under climate change: Impact of simulated heatwaves on the reproduction of model pollinators. Funct Ecol 35:739–752

    Article  Google Scholar 

  • Martinet B, Dellicour S, Ghisbain G, Przybyla K, Zambra E, Lecocq T, Boustani M, Baghirov R, Michez D, Rasmont P (2021) Global effects of extreme temperatures on wild bumblebees. Conserv Biol 35(5):1507–1518

    Article  PubMed  Google Scholar 

  • May ML, Casey TM (1983) Thermoregulation and heat exchange in euglossine bees. Physiol Biochem Zool 56:541–551

    Google Scholar 

  • McAfee A, Chapman A, Higo H, Underwood R, Milone J, Foster LJ, Guarna MM, Tarpy DR, Pettis JS (2020) Vulnerability of honey bee queens to heat-induced loss of fertility. Nat Sustain 3:367–376

    Article  Google Scholar 

  • McKinstry M, Chung C, Truong H, Johnston BA, Snow JW (2017) The heat shock response and humoral immune response are mutually antagonistic in honey bees. Sci. Rep. 7:8850

    Article  PubMed  PubMed Central  Google Scholar 

  • Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997

    Article  CAS  PubMed  Google Scholar 

  • Meeus I, Brown MJF, De Graaf DC, Smagghe G (2011) Effects of invasive parasites on bumble bee declines. Conserv Biol 25:662–671

    Article  PubMed  Google Scholar 

  • Nacko S, Hall MA, Gloag R, Lynch RE, Spooner-Hart RN, Cook JM, Riegler M (2023) Heat stress survival and thermal tolerance of Australian stingless bees. J Therm Biol 117:103671

    Article  PubMed  Google Scholar 

  • Neven LG (2000) Physiological responses of insects to heat. Postharvest Biol Technol 21(1):103–111

    Article  CAS  Google Scholar 

  • Nieto A, Roberts SPM, Kemp J, Rasmont P, Kuhlmann M, García Criado M, Biesmeijer JC, Bogusch P, Dathe HH, De la Rúa P, De Meulemeester T, Dehon M, Dewulf A, Ortiz-Sánchez FJ, Lhomme P, Pauly A, Potts SG, Praz C, Quaranta M, Radchenko VG, Scheuchl E. Smit, J., Straka J., Terzo M., Tomozii B., Window J., Michez, D. (2014) European Red List of bees. Publication Office of the European Union, Luxembourg

    Google Scholar 

  • Oliveira BF, Yogo WI, Hahn DA, Yongxing J, Scheffers BR (2021) Community-wide seasonal shifts in thermal tolerances of mosquitoes. Ecology 102(7):e03368

    Article  PubMed  Google Scholar 

  • Owen EL, Bale JS, Hayward SA (2013) Can winter-active bumblebees survive the cold? Assessing the cold tolerance of Bombus terrestris audax and the effects of pollen feeding. PLoS One. 8(11)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oyen KJ, Giri S, Dillon ME (2016) Altitudinal variation in bumble bee (Bombus) critical thermal limits. J Therm Biol 59:52–57

    Article  PubMed  Google Scholar 

  • Oyen KJ, Dillon ME (2018) Critical thermal limits of bumblebees (Bombus impatiens) are marked by stereotypical behaviors and are unchanged by acclimation, age or feeding status. J Exp Biol 221(8):jeb165589

    Article  PubMed  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology. Evol Syst 37:637–669

    Article  Google Scholar 

  • Pereboom JJ, Biesmeijer JC (2003) Thermal constraints for stingless bee foragers: the importance of body size and coloration. Oecologia 137:42–50

    Article  CAS  PubMed  Google Scholar 

  • Perez R, Aron S (2020) Adaptations to thermal stress in social insects: recent advances and future directions. Biol Rev 95(6):1535–1553

    Article  PubMed  Google Scholar 

  • Pimsler ML, Oyen KJ, Herndon JD, Jackson JM, Strange JP, Dillon ME, Lozier JD (2020) Biogeographic parallels in thermal tolerance and gene expression variation under temperature stress in a widespread bumble bee. Sci Rep 10(1):17063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Potts SG, Imperatriz-Fonseca V, Ngo HT, Aizen MA, Biesmeijer JC, Breeze TD, ... & Vanbergen AJ (2016) Safeguarding pollinators and their values to human well-being. Nature 540(7632):220–229

    Article  CAS  PubMed  Google Scholar 

  • Ragone F, Wouters J, Bouchet F (2018) Computation of extreme heat waves in climate models using a large deviation algorithm. Proc Nat Acad Sci 115:24–29

    Article  CAS  PubMed  Google Scholar 

  • Rasmont P, Franzen M, Lecocq T, Harpke A, Roberts SPM, Biesmeijer K, Castro L, Cederberg B, Dvorak L, Fitzpatrick U, Gonseth Y, Haubruge E, Mahe G, Manino A, Michez D, Neumayer J, Odegaard F, Paukkunen J, Pawlikowski T, Potts S, Reemer M, Settele J, Straka J, Schweiger O (2015) Climatic risk and distribution atlas of european bumblebees. Biorisk Special Issue 10:1–246

    Google Scholar 

  • Richner N, Holderegger R, Linder HP, Walter T (2015) Reviewing change in the arable flora of Europe: a meta-analysis. Weed Res 55:1–13

    Article  Google Scholar 

  • Sales K, Vasudeva R, Gage MJG (2021) Fertility and mortality impacts of thermal stress from experimental heatwaves on different life stages and their recovery in a model insect. R Soc Open Sci 8:201717

    Article  PubMed  PubMed Central  Google Scholar 

  • Sheikh AA, Rehman NZ, Kumar R (2017) Diverse adaptations in insects: A Review. J Entomol Zool Stud 5(2):343–350

    Google Scholar 

  • Soroye P, Newbold T, Kerr J (2020) Climate change contributes to widespread declines among bumble bees across continents. Science 367(6478):685–688

    Article  CAS  PubMed  Google Scholar 

  • Straub L, Strobl V, Yañez O, Albrecht M, Brown MJF, Neumann P (2022) Do pesticide and pathogen interactions drive wild bee declines? Int J Parasitol Parasites Wildl 18:232–243

    Article  PubMed  PubMed Central  Google Scholar 

  • Terblanche JS, Deere JA, Clusella-Trullas S, Charlene J, Chown SL (2007) Critical thermal limits depend on methodological context. Proc r Soc B Biol Sci 274:2935–2943

    Article  Google Scholar 

  • Vanderplanck M, Martinet B, Carvalheiro LG, Rasmont P, Barraud A, Renaudeau C, Michez D (2019) Ensuring access to high-quality resources reduces the impacts of heat stress on bees. Sci Rep 9:12596

    Article  PubMed  PubMed Central  Google Scholar 

  • Vogt FD (1986) Thermoregulation in bumblebee colonies, I: thermoregulatory versus brood-maintenance behaviors during acute changes in ambient temperatures. Physiol Biochem Zool 59:55–59

    Google Scholar 

  • Wagner DL (2020) Insect declines in the anthropocene. Ann Rev Entomol 65:457–480

    Article  CAS  Google Scholar 

  • Willmer PG (1986) Foraging patterns and water balance: problems of optimization for a xerophilic bee. Chalicodoma Sicula J Ani Ecol 55(3):941–962

    Article  Google Scholar 

  • Woodcock B, Isaac N, Bullock J, Roy DB, Garthwaite DG, Crowe A, Pywell RF (2016) Impacts of neonicotinoid use on long-term population changes in wild bees in England. Nat Comm 7:12459

    Article  CAS  Google Scholar 

  • Wright GA, Nicolson SW, Shafir S (2018) Nutritional Physiology and Ecology of Honey Bees. Ann Rev Entomol 63:327–344

    Article  CAS  Google Scholar 

  • Yan W-Y, Gan H-Y, Li S-Y, Hu J-H, Wang ZL, Wu X-B, Zeng Z-J (2016) Morphology and transcriptome differences between the haploid and diploid drones of Apis cerana. J Asia Pac Entomol 19(4):1167–1173

    Article  Google Scholar 

  • Zhao H, Li G, Guo D, Li H, Liu Q, Xu B, Guo X (2021) Response mechanisms to heat stress in bees. Apidologie 52:388–399

    Article  Google Scholar 

  • Zizzari ZV, Ellers J (2011) Effects of exposure to short-term heat stress on male reproductive fitness in a soil arthropod. J Insect Physiol 57(3):421–426

    Article  CAS  PubMed  Google Scholar 

  • Zwiener I, Blettner M, Hommel G (2011) Survival analysis: part 15 of a series on evaluation of scientific publications. Deutsches Arzteblatt International 108(10):163–169

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank the three people who were directly involved in the field work facilitation: Challita Tanios (Director of Tannourine Cedar Nature Reserve), Sandra Koussa Saba (Director of Horch Ehden Nature Reserve) and Charbel Tawk (Committee of the Cedar Forest Friends, Bcharre). Our thanks go to the people who assisted in the field collections, Antoine Gekière, Jad Jabbour, Mariam Fakhry, Nancy Abi Khalil, and Xavier Van Achter. We thank Thomas James Wood (University of Mons) for proofreading this paper.

Funding

MB was funded by the University of Mons for her Ph-D research. BM was funded by Fonds National de la Recherche Scientifique (postdoctoral researcher, Chargé de Recherche, F.R.S.-FNRS). DM was supported in this work by the Fonds National de la Recherche Scientifique (F.R.S.-FNRS) and the Fonds Wetenschappelijk Onderzoek (FWO) joint programme “EOS – Excellence Of Science” (Belgium) for the project named “CliPS: Climate change and its effects on Pollination Services (project 30947854)". ¨PR was funded by the University of Mons. NN was funded by the Holy Spirit University of Kaslik.

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Authors and Affiliations

  1. Laboratory of Zoology, Institute for Biosciences, University of Mons, Place du Parc, 20, 7000, Mons, Belgium

    Mira Boustani, Denis Michez & Pierre Rasmont

  2. Evolutionary Biology & Ecology, Université Libre de Bruxelles, Avenue Paul Héger - CP 160/12, 1000, Brussels, Belgium

    Baptiste Martinet

  3. Department of Agriculture and Food Engineering, Holy Spirit University of Kaslik, PO Box 446, Jounieh, Lebanon

    Nabil Nemer

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  1. Mira Boustani
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Contributions

MB: Conceptualization, Data curation, Formal analysis, Writing—Original Draft. BM: Conceptualization, Formal analysis, Writing- Reviewing and Editing. DM: Funding acquisition, Writing- Reviewing and Editing. NN: Supervision, Writing- Reviewing and Editing. PR: Conceptualization, Funding acquisition, Supervision.

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Correspondence to Mira Boustani.

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Boustani, M., Martinet, B., Michez, D. et al. Heat resistance variability in the Lebanese bee fauna. Apidologie 55, 29 (2024). https://doi.org/10.1007/s13592-024-01070-y

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