Thermal Tolerance of Honeybees (Apis mellifera L.) Changes Across an Elevation Gradient in the Mexican Transition Zone
DOI:
https://doi.org/10.13102/sociobiology.v71i1.10155Keywords:
thermal tolerance range, environmental gradients,, body size, thermal variability, intrapopulation variation.Abstract
The objective of this study was to determine the critical thermal minimum [CTmin], critical thermal maximum [CTmax], and thermal tolerance range of A. mellifera at three different elevations located in the Mexican Transition Zone: 11; 1,324, and 3,304 m.a.s.l. In general, we found that the CTmin of A. mellifera was lower at the site with the highest elevation (i.e., they tolerate colder temperatures). At the same time, the CTmax remained constant across the three studied elevations, revealing higher plasticity for cold tolerance rather than heat. Moreover, we did not find evidence that the body mass of the individuals was associated with their thermal tolerance at any of the three sampled elevations. Our findings suggest processes of local adaptation of A. mellifera populations in environmentally contrasting sites, allowing them to expand their range of distribution, which could be useful in predicting responses to future environmental change.
Downloads
References
Addo-Bediako, A., Chown, S.L. & Gaston, K.J. (2000). Thermal tolerance, climatic variability, and latitude. Proceedings of the Royal Society B: Biological Sciences, 267: 739-745.
Aizen, M.A. & Harder. L.D. (2009). The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Current Biology, 19: 915-918.
Al-Kahtani, S.N. & Taha, E.K.A. (2021). Morphometric study of Yemeni (Apis mellifera jemenitica) and Carniolan (A. m. carnica) honeybee workers in Saudi Arabia. Plos One, 16: e0247262.
Angilletta, M.J. (2009). Thermal adaptation: a theoretical and empirical synthesis. Oxford: Oxford University Press.
Baena-Díaz, F., Chévez, E., Ruiz de la Merced, F., & Porter-Bolland, L. (2022). Apis mellifera en México: producción de miel, flora melífera y aspectos de polinización. Revista Mexicana de Ciencias Pecuarias, 13: 525- 548.
Bellard, C., Bertelsmeier, C., Leadley, P., Thuiller, W. & Courchamp, F. (2012). Impacts of climate change on the future of biodiversity. Ecology Letters, 15: 365-377.
Bennett, J.M., Sunday, J., Calosi, P., Villalobos, F., Martínez, B., Molina-Venegas, R. et al. (2021) The Evolution of Critical Thermal Limits of Life on Earth. Nature Communications, 12: id1198.
Bergmann, C. (1847). Ueber die Verhaltnisse der Warmeokonomie der Thierezuihrer Grosse. Gottinger Studien, 3: 595-708.
Bernier, P. & Schoene, D. (2009). Adapting forests and their management to climate change: an overview. Unasylva, 60: 231-232.
Bishop, J.A. & Armbruster. W.S. (1999). Thermoregulatory abilities of Alaskan bees: effects of size, phylogeny and ecology. Functional Ecology, 13: 711-724.
Bishop, T.R., Robertson, M.P., Van Rensburg, B.J. & Parr, C.L. (2017). Coping with the Cold: Minimum Temperatures and Thermal Tolerances Dominate the Ecology of Mountain Ants. Ecological Entomology, 42: 105-114.
Blanckenhorn, W.U. (2000). The evolution of body size: what keeps organisms small? The Quarterly Review of Biology, 75: 385-407.
Brett, J.R. (1956). Some Principles in the Thermal Requirements of Fishes. The Quarterly Review of Biology, 31: 75-87.
Castillo-Campos, G. (2006). Las selvas. Entornos veracruzanos: la costa de La Mancha, P. Moreno-Casasola (ed.). Instituto de Ecología, Xalapa, Veracruz, 221-229.
Castillo, G. & Medina, M.E. (2002). Árboles y arbustos de la Reserva Natural de La Mancha, Veracruz. Instituto de Ecología, A.C. Xalapa, Veracruz, 144 p.
Chown, S.L., Chown, S. & Nicolson, S. (2004). Insect physiological ecology: mechanisms and patterns. Oxford: Oxford University Press.
Conrad, K.M., Peters, V.E., & Rehan, S.M. (2021). Tropical bee species abundance differs within a narrow elevational gradient. Scientific Reports, 11: id23368.
Cortina, C.A., Aslan, C.E., & Litson, S.J. (2019). Importance of Non-Native Honeybees (Apis mellifera) as Flower Visitors to the Hawaiian Tree’ Ōhi ‘a Lehua (Metrosideros polymorpha) Across an Elevation Gradient. Pacific Science, 73: 345-355.
Crawley. M.J. (2012). The R book. John Wiley & Sons.
Cruz, C.P., Luna, P., Guevara, R., Hinojosa-Díaz, I.A., Villalobos, F. & Dáttilo, W. (2022). Climate and human influence shape the interactive role of the honeybee in pollination networks beyond its native distributional range. Basic and Applied Ecology, 63: 186-195.
Colinet, H., Sinclair, B.J., Vernon, P., & Renault, D. (2015). Insects in fluctuating thermal environments. Annual Review of Entomology, 60: 123-140.
Dutton, R.W., Ruttner, F., Berkeley, A. & Manley, M.J.D. (1981). Observations on the morphology, relationships and ecology of Apis mellifera of Oman. Journal of Apicultural Research, 20: 201- 214.
Fischman, B.J., Pitts-Singer, T.L., & Robinson, G.E. (2017). Nutritional regulation of phenotypic plasticity in a solitary bee (Hymenoptera: Megachilidae). Environmental Entomology, 46: 1070-1079.
García-Robledo, C., Kuprewicz, E.K., Staines, C.L., Erwin, T.L. & Kress, W.J. (2016). Limited tolerance by insects to high temperatures across tropical elevational gradients and the implications of global warming for extinction. Proceedings of the National Academy of Sciences USA, 113 :680-685.
Gaston, K.J., Chown, S.L., Calosi, P., Bernardo, J., Bilton, D.T. et al. (2009). Macrophysiology: a conceptual reunification. American Naturalist, 174: 595-612.
Gerard, M., Michez, D., Debat, V., Fullgrabe, L., Meeus, I., Piot, N. et al. (2018) Stressful conditions reveal decrease in size, modification of shape but relatively stable asymmetry in bumblebee wings. Scientific Reports, 8: e15169.
Greenleaf, S.S., Williams, N.M., Winfree, R. & Kremen, C. (2007). Bee foraging ranges and their relationship to body size. Oecologia, 153: 589-596.
Gonzalez, V.H., Oyen, K., Aguilar, M.L., Herrera, A., Martin, R.D. & Ospina, R. (2022). High Thermal Tolerance in High-Elevation Species and Laboratory-Reared Colonies of Tropical Bumble Bees. Ecology and Evolution, 12: e9560.
González-Tokman,. D, Gil-Pérez, Y., Servín-Pastor, M., Alvarado, F., Escobar, F., Baena-Díaz, F. & Martínez, I. (2021). Effect of chemical pollution and parasitism on heat tolerance in dung beetles (Coleoptera: Scarabaeinae). Journal of Economic Entomology, 114: 462-467.
Gutiérrez-Pesquera, L.M., Tejedo, M., Olalla-Tárraga, M.A., Duarte, H., Nicieza, A. & Solé, M. (2016). Testing the climate variability hypothesis in thermal tolerance limits of tropical and temperate tadpoles. Journal of Biogeography, 43: 1166-1178.
Han, F., Wallberg, A. & Webster, M. T. (2012). From where did the Western honeybee (Apis mellifera) originate? Ecology and Evolution, 2: 1949-1957.
Harrison, J.F. & Fewell, J.H. (2002). Environmental and genetic influences on flight metabolic rate in the honey bee, Apis mellifera. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology, 133: 323-333.
Hodkinson, I.D. (2005). Terrestrial insects along elevation gradients: species and community responses to altitude. Biological Review, 80: 489-513.
Hoiss, B., Krauss, J., Potts, S.G., Roberts, S. & Steffan-Dewenter, I. (2012). Altitude acts as an environmental filter on phylogenetic composition, traits and diversity in bee communities. Proceedings of the Royal Society B: Biological Sciences, 279: 4447-4456.
Janzen, D.H. (1967). Why mountain passes are higher in the tropics. American Naturalist, 101:
-249.
Lovejoy, T.E. & Hannah, L. (2005). Climate change and biodiversity. Yale University Press, New Haven, Connecticut, USA.
Maleszka, R. (2018). Beyond Royalactin and a master inducer explanation of phenotypic plasticity in honey bees. Communications Biology, 1: id8.
McCabe, L.M., Aslan, C.E. & Cobb, N.S. (2022). Decreased bee emergence along an elevation gradient: Implications for climate change revealed by a transplant experiment. Ecology, 103: e03598.
Molina-Montenegro, M.A. & Naya, D.E. (2012)., Latitudinal patterns in phenotypic plasticity and fitness-related traits: assessing the climatic variability hypothesis (CVH) with an invasive plant species. PLoS One, 7: e47620.
Nooten, S.S. & Rehan, S.M. (2020). Historical changes in bumble bee body size and range shift of declining species. Biodiversity and Conservation, 29: 451-467.
Obeso, J.R. & Herrera, J.M. (2018). Polinizadores y cambio climático. Ecosistemas, 27: 52-59.
Oyen, K.J., Giri, S. & Dillon, M.E. (2016). Altitudinal variation in bumble bee (Bombus) critical thermal limits. Journal of Thermal Biology, 59: 52-57.
Overgaard, J., Kristensen, T.N., Mitchel, K.A. & Hoffmann, A.A. (2011). Thermal tolerance of widespread tropical Drosophila species: does phenotypic plasticity increase with latitude? American Naturalist, 178: 80-96.
Parker, R., Melathopoulos, A.P., White, R., Pernal, S.F., Guarna, M.M. & Foster, L.J. (2010). Ecological adaptation of diverse honey bee (Apis mellifera) populations. PLoS One, 5: e11096.
Pepin, N.C., Arnone, E., Gobiet, A., Haslinger, K., Kotlarski, S., Notarnicola, C. & Adler, C. (2022). Climate changes and their elevational patterns in the mountains of the world. Reviews of Geophysics, 60: e2020RG000730.
Pereboom, J.J.M. & Biesmeijer, J.C. (2003). Thermal constraints for stingless bee foragers: the importance of body size and coloration. Oecologia, 137: 42- 50.
Peters, M.K. Peisker, J., Steffan-Dewenter, I. & Hoiss, B. (2016). Morphological traits are linked to the cold performance and distribution of bees along elevational gradients. Journal of Biogeography, 43: 2040-2049.
R Development Core Team, (2023). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Viena, Austria. https://www.R-project.org/
Rabe, M.J., Rosenstock, S.S. & Nielsen, D.I. (2005). Feral Africanized honey bees (Apis mellifera) in Sonoran desert habitats of southwestern Arizona. Southwest Naturalist, 50: 307-311.
Reis-Jr, R., Oliveira, M.L. & Borges, G.R.A. (2015). RT4Bio: R tools for biologists (RT4Bio). R package version 1.0.
Rensch, B. (1938). Some problems of geographical variation and species formation. Proceedings of the Linnean Society of London, 150: 275-285.
Sánchez-Echeverría, K., Castellanos, I., Mendoza-Cuenca, L., Zuria, I., & Sánchez-Rojas, G. (2019) Reduced thermal variability in cities and its impact on honey bee thermal tolerance. PeerJ, 7: e7060.
Shah, A.A., Woods, H.A., Havird, J.C., Encalada, A.C., Flecker, A.S., Funk, W.C. & Ghalambor, C.K. (2021). Temperature dependence of metabolic rate in tropical and temperate aquatic insects: support for the climate variability hypothesis in mayflies but not stoneflies. Global Change Biology, 27: 297-311.
Stevens, G.C. (1989). The latitudinal gradients in geographical range: how so many species co-exist in the tropics. American Naturalist, 133: 240-256.
Smith, R.D., Higgins, J., Burton, J. & Cobb, N.S. (2015). Bee diversity and abundance along an elevational gradient in Northern Arizona. In Huenneke, L.F., van Riper, C. & Hays-Gilpin, K.A. (eds) The Colorado Plateau VI: Science and Management at the Landscape Scale. University of Arizona Press. p. 159-189.
Sunday, J.M., Bates, A.E., Kearney, M.R., Colwell, R.K., Dulvy, N.K., Longino, J.T. & Huey, R.B. (2014). Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proceedings of the National Academy of Sciences USA, 111: 5610-5615.
Villegas, P.R., Muñoz, R.C., Muñoz, J., Gallo, G.C.A., & Ponce, R.J. (2011). Tasa de cambio de uso del suelo en el Parque Nacional Pico de Orizaba, Veracruz, México en el periodo 2003–2011. CONANP-INECOL. Xalapa Veracruz, México.
Wilmer, P.G. & Unwin, D.M. (1981). Field analysis of insect heat budgets: reflectance, size and heating rates. Oecologia, 50: 250-255
Woyke, J., Wilde, J. & Wilde, M. (2003). Flight activity reaction to temperature changes in Apis dorsata, Apis laboriosa and Apis mellifera. Journal of Apicultural Science, 47: 73-80.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 José Benito Barreiro, Brenda Ratoni, Fernanda Baena-Díaz, Daniel González-Tokman, Wesley Dáttilo
This work is licensed under a Creative Commons Attribution 4.0 International License.
Sociobiology is a diamond open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
eISSN 2447-8067
