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Effect of heat waves on embryo mortality in the pine processionary moth

  • S. Rocha (a1), C. Kerdelhué (a2), M.L. Ben Jamaa (a3), S. Dhahri (a3), C. Burban (a4) and M. Branco (a1)...


Extreme climate events such as heat waves are predicted to become more frequent with climate change, representing a challenge for many organisms. The pine processionary moth Thaumetopoea pityocampa is a Mediterranean pine defoliator, which typically lays eggs during the summer. We evaluated the effects of heat waves on egg mortality of three populations with different phenologies: a Portuguese population with a classical life cycle (eggs laid in summer), an allochronic Portuguese population reproducing in spring, and a Tunisian population from the extreme southern limit of T. pityocampa distribution range, in which eggs are laid in fall. We tested the influence of three consecutive hot days on egg survival and development time, using either constant (CT) or daily cycling temperatures (DT) with equivalent mean temperatures. Maximum temperatures (T max) used in the experiment ranged from 36 to 48°C for DT and from 30 to 42°C for CT. Heat waves had a severe negative effect on egg survival when T max reached 42°C for all populations. No embryo survived above this threshold. At high mean temperatures (40°C), significant differences were observed between populations and between DT and CT regimes. Heat waves further increased embryo development time. The knowledge we gained about the upper lethal temperature to embryos of this species will permit better prediction of the potential expansion of this insect under different climate warming scenarios.


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Angilletta, M.J., Niewiarowski, P.H. & Navas, C.A. (2002) The evolution of thermal physiology in ectotherms. Journal of Thermal Biology 27, 249268.
Bale, J.S., Masters, G.J., Hodkinson, I.D., Awmack, C., Bezemer, T.M., Brown, V.K., Butterfield, J., Buse, A., Coulson, J.C., Farrar, J., Good, J.E., Harrington, R., Hartley, S., Jones, T.H., Lindroth, R.L., Press, M.C., Symrnioudis, I., Watt, A.D. & Whittaker, J.B. (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology 8, 116.
Battisti, A. & Jactel, H. (2010) Pest insect populations in relation to climate change in forests of the Mediterranean basin. Forêt méditerranéenne 4, 385392.
Battisti, A., Stastny, M., Netherer, S., Robinet, C., Schopf, A., Roques, A. & Larsson, S. (2005) Expansion of geographic range in the pine processionary moth caused by increased winter temperatures. Ecological Applications 15, 20842096.
Bozinovic, F., Bastias, D.A., Boher, F., Clavijo-Baquet, S., Estay, S.A. & Angilletta, M.J. (2011) The mean and variance of environmental temperature interact to determine physiological tolerance and fitness. Physiological and Biochemical Zoology 84, 543552.
Branco, M., Paiva, M.R., Santos, H., Burban, C. & Kerdelhué, C. (2017) Experimental evidence for heritable reproductive time in 2 allochronic populations of pine processionary moth. Insect Science in press. doi: 10.1111/1744-7917.12287.
Burban, C., Gautier, M., Leblois, R., Landes, J., Santos, H., Paiva, M.R., Branco, M. & Kerdelhué, C. (2016) Evidence for low level hybridization between two allochronic populations of the pine processionary moth, Thaumetopoea pityocampa (Lepidoptera: Notodontidae). Biological Journal of the Linnean Society 119(2), 311328.
Chiu, M.-C., Kuo, J.-J.R. & Kuo, M.-H. (2015) Life stage-dependent effects of experimental heat waves on an insect herbivore. Ecological Entomology 40, 175181.
Clusella-Trullas, S., Blackburn, T.M. & Chown, S.L. (2011) Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change. The American Naturalist 177(6), 738751.
Clusella-Trullas, S., Boardman, L., Faulkner, K.T., Peck, L.S. & Chown, S.L. (2014) Effects of temperature on heat-shock responses and survival of two species of marine invertebrates from sub-Antarctic Marion Island. Antarctic Science 26(2), 145152.
Darwish, Y.A., Ali, A.M., Mohamed, R.A. & Khalil, N.M. (2015) Effect of extreme low and high temperatures on the almond moth, Ephestia cautella (Walker) (Lepidoptera: Pyralidae). Journal of Phytopathology and Pest Management 2(1), 3646.
Démolin, G. (1969) Bioecologia de la Procesionaria del pino Thaumetopoea pityocampa Schiff. Incidencia de los factores climaticos. Boletín del Servicio de Plagas Forestales 12, 924.
Denlinger, D.L. & Yocum, G.D. (1998) Physiology of heat sensitivity. pp. 753 in Hallman, G.J. & Denlinger, D.L. (Eds) Temperature Sensitivity in Insects and Application in Integrated Pest Management. Boulder, CO, Westview Press.
Deutsch, C.A., Tewksbury, J.J., Huey, R.B., Sheldon, K.S., Ghalambor, C.K., Haak, D.C. & Martin, P.R. (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences of the United States of America 105, 66686672.
Easterling, D.R., Meehl, G.A., Parmesan, C., Changnon, S.A., Karl, T.R. & Mearns, L.O. (2000) Climate extremes: observations, modelling, and impacts. Science 289, 20682074.
EEA (2012) Climate change, impacts and vulnerability in Europe 2012. European Environment Agency Report no. 12. Available online at (accessed 25 January 2016).
Folguera, G., Bastias, D.A., Caers, J., Rojas, J.M., Piulachs, M.D., Belles, X. & Bozinovic, F. (2011) An experimental test of the role of environmental temperature variability on ectotherm molecular, physiological and life-history traits: implications for global warming. Comparative Biochemistry and Physiology Part A-Molecular & Integrative Physiology 159, 242246.
Godefroid, M., Rocha, S., Santos, H., Paiva, M.-R., Burban, C., Kerdelhué, C., Branco, M., Rasplus, J.-Y. & Rossi, J.-P. (2016) Climate constrains range expansion of an allochronic population of the pine processionary moth. Diversity and Distributions 22(12), 12881300.
Gschloessl, B., Vogel, H., Burban, C, Heckel, D., Streiff, R. & Kerdelhué, C. (2014) Comparative analysis of two phenologically divergent populations of the pine processionary moth (Thaumetopoea pityocampa) by de novo transcriptome sequencing. Insect Biochemistry and Molecular Biology 46, 3142.
Hance, T., Baaren, J.-V., Vernon, P. & Boivin, G. (2007) Impact of extreme temperatures on parasitoids in a climate change perspective. Annual Review of Entomology 52, 107126.
Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 19651978.
Hoch, G., Petrucco Toffolo, E., Netherer, S., Battisti, A. & Schopf, A. (2009) Survival at low temperature of larvae of the pine processionary moth Thaumetopoea pityocampa from an area of range expansion. Agricultural and Forest Entomology 11, 313320.
Hódar, J.A. & Zamora, R. (2004) Herbivory and climatic warming: a Mediterranean outbreaking caterpillar attacks a relict, boreal pine species. Biodiversity and Conservation 13, 493500.
Hódar, J.A., Castro, J. & Zamora, R. (2003) Pine processionary caterpillar Thaumetopoea pityocampa as a new threat for relict Mediterranean Scots pine forests under climatic warming. Biological Conservation 110, 123129.
Huchon, H. & Démolin, G. (1970) La biologie de la processionnaire du pin. Dispersion potentielle – dispersion actuelle. Revue Forestière Française 22, 220234.
IPCC (2014) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. [Core Writing Team, Pachauri, R.K. & Meyer, L.A. (Eds)]. IPCC, Geneva, Switzerland, 151 pp.
Kührt, U., Samietz, J., Höhn, H. & Dorn, S. (2006) Modelling the phenology of codling moth: influence of habitat and thermoregulation. Agriculture, Ecosystems and Environment 117, 2938.
Martin, T.L. & Huey, R.B. (2008) Why “Suboptimal” is optimal: Jensen's inequality and ectotherm thermal preferences. The American Naturalist 171, E102E118.
Menéndez, R. (2007) How are insects responding to global warming? Tijdschrift voor Entomologie 150, 355365.
Mironidis, G.K. & Savopoulou-Soultani, M. (2010) Effects of heat shock on survival and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae) adults. Journal of Thermal Biology 35, 5969.
Musolin, D.L., Tougou, D. & Fujisaki, K. (2010) Too hot to handle? Phenological and life-history responses to simulated climate change of the southern green stink bug Nezara viridula (Heteroptera: Pentatomidae). Global Change Biology 16, 7387.
Paaijmans, K.P., Heinig, R.L., Seliga, R.A., Blanford, J.I., Blanford, S., Murdock, C.C. & Thomas, M.B. (2013) Temperature variation makes ectotherms more sensitive to climate change. Global Change Biology 19, 23732380.
Potter, K.A., Davidowitz, G. & Woods, H.A. (2011) Cross-stage consequences of egg temperature in the insect Manduca sexta . Functional Ecology 25, 548556.
Qayyum, A. & Zalucki, P. (1987) Effects of high temperature on survival of eggs of Heliothis armigera (Hubner) and H. punctigera Wallengren (Lepidoptera: Noctuidae). Journal of the Australian Entomological Society 26, 295296.
Robinet, C. & Roques, A. (2010) Direct impacts of recent climate warming on insect populations. Integrative Zoology 5, 132142.
Robinet, C., Baier, P., Pennerstorfer, J., Schopf, A. & Roques, A. (2007) Modelling the effects of climate change on the potential feeding activity of Thaumetopoea pityocampa (Den. & Schiff.) (Lepidoptera: Notodontidae) in France. Global Ecology and Biogeography 16, 460471.
Robinet, C., Rousselet, J., Pineau, P., Miard, F. & Roques, A. (2013) Are heat waves susceptible to mitigate the expansion of a species progressing with global warming? Ecology and Evolution 3(9), 29472957.
Robinet, C., Laparie, M. & Rousselet, J. (2015) Looking beyond the large scale effects of global change: local phenologies can result in critical heterogeneity in the pine processionary moth. Frontiers in Physiology 6, 334.
Root, T.L., Price, J.T., Hall, K.R., Schneider, S.H., Rosenzweig, C. & Pounds, J.A. (2003) Fingerprints of global warming on wild animals and plants. Nature 421, 5760.
Salpiggidis, G., Navrozidis, E. & Copland, M.J. (2004) Effect of temperature on the egg viability and duration of egg development of Parahypopta caestrum . Phytoparasitica 32(4), 367369.
Santos, H., Rousselet, J., Magnoux, E., Paiva, M.R., Branco, M. & Kerdelhué, C. (2007) Genetic isolation through time: allochronic differentiation of a phenologically atypical population of the pine processionary moth. Proceedings of the Royal Society of London B 274, 935941.
Santos, H., Burban, C., Rousselet, J., Rossi, J.-P., Branco, M. & Kerdelhué, C. (2011 a) Incipient allochronic speciation in the pine processionary moth (Thaumetopoea pityocampa, Lepidoptera, Notodontidae). Journal of Evolutionary Biology 24, 146158.
Santos, H., Paiva, M.R., Tavares, C., Kerdelhué, C. & Branco, M. (2011 b) Temperature niche shift observed in a Lepidoptera population under allochronic divergence. Journal of Evolutionary Biology 24, 18971905.
Santos, H., Paiva, M.R., Rocha, S., Kerdelhué, C. & Branco, M. (2013) Phenotypic divergence in reproductive traits of a moth population experiencing a phenological shift. Ecology and Evolution 3, 50985108.
Simonato, M., Battisti, A., Kerdelhué, C., Burban, C., Lopez-Vaamonde, C., Pivotto, I., Salvato, P. & Negrisolo, E. (2013) Host and phenology shifts in the evolution of the social moth genus Thaumetopoea . PLoS ONE 8(2), e57192. doi: 10.1371/journal.pone.0057192
Vasseur, D.A., DeLong, J.P., Gilbert, B., Greig, H.S., Harley, C.D.G., McCann, K.S., Savage, V., Tunney, T.D. & O'Connor, M.I. (2014) Increased temperature variation poses a greater risk to species than climate warming. Proceedings of the Royal Society of London B 281, 20132612. Available online at
Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Fromentin, J.M., Hoegh-Guldberg, O. & Bairlein, F. (2002) Ecological responses to recent climate change. Nature 416, 389395.



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