Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-22T19:06:06.514Z Has data issue: false hasContentIssue false
  • English
  • Français

Shifted phenology in the pine processionary moth affects the outcome of tree–insect interaction

Published online by Cambridge University Press:  13 June 2019

S. Rocha Open the ORCID record for S. Rocha [Opens in a new window] ,
M.C. Caldeira Open the ORCID record for M.C. Caldeira [Opens in a new window] ,
C. Burban Open the ORCID record for C. Burban [Opens in a new window] ,
C. Kerdelhué Open the ORCID record for C. Kerdelhué [Opens in a new window]  and
M. Branco Open the ORCID record for M. Branco [Opens in a new window]
S. Rocha*
Affiliation:
Forest Research Centre, School of Agriculture, University of Lisbon, Tapada da Ajuda, 1349-017 Lisboa, Portugal
M.C. Caldeira
Affiliation:
Forest Research Centre, School of Agriculture, University of Lisbon, Tapada da Ajuda, 1349-017 Lisboa, Portugal
C. Burban
Affiliation:
BIOGECO, INRA, Univ. Bordeaux, 33610 Cestas, France
C. Kerdelhué
Affiliation:
CBGP, INRA, CIRAD, IRD, Montpellier SupAgro, Univ. Montpellier, 34988 Montferriez-sur-Lez, France
M. Branco
Affiliation:
Forest Research Centre, School of Agriculture, University of Lisbon, Tapada da Ajuda, 1349-017 Lisboa, Portugal
*
*Author for correspondence Phone: 351.213653382 Fax: 351.213653185 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

In the Mediterranean and temperate regions, an increase in the frequency and intensity of drought events has been recorded, probably due to climate change. In consequence, trees will more frequently experience hydric stress, a condition that can be expected to affect insect–tree interactions, while adaptation mechanisms may be further in course. The effect of tree water stress on the performance of two allochronic populations of Thaumetopoea pityocampa was here studied. Namely, we compared a unique population of this insect, in which the larvae develop in the summer (SP), with the typical population having winter larval development (WP), to test the adaptation hypothesis to host plant status. Larvae of each population were fed on needles of young potted Pinus pinaster plants under two water supply regimes: (i) well-watered (control) and (ii) subjected to 3 months of drought stress. Compared to control, stressed plants had higher amounts of soluble sugars, phenols, and higher C/N ratio, whereas water content and chlorophylls concentrations were lower. In general, T. pityocampa larvae had lower performances on water-stressed plants, as shown by lower survival rates, lower needle consumption, and longer development times. Yet, the detrimental effects of tree stress were only significant for the WP larvae, while SP larvae were able to overcome such conditions. Results demonstrate that tree water stress can negatively affect T. pityocampa populations. Furthermore, the evidence is also provided that responses to the physiological condition of the host trees may occur at the population level, as a result of adaptation mechanisms driven by climate change.

Keywords

climate changedrought stressintra-specific variationpine processionary mothplant–insect interaction
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 1 , February 2020 , pp. 68 - 76
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderegg, W.R.L., Hicke, J.A., Fisher, R.A., Allen, C.D., Aukema, J., Bentz, B., Hood, S., Lichstein, J.W., Macalady, A.K., McDowell, N., Pan, Y., Raffa, K., Sala, A., Shaw, J.D., Stephenson, N.L., Tague, C. & Zeppel, M. (2015) Tree mortality from drought, insects, and their interactions in a changing climate. New Phytologist 208, 674–683.Google Scholar
Anjum, S.A., Xie, X., Wang, L., Saleem, M.F., Man, C. & Lei, W. (2011) Morphological, physiological and biochemical responses of plants to drought stress. African Journal of Agricultural Research 6 (9), 2026–2032.Google Scholar
Arnon, D.I. (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24 (1), 1–15.Google Scholar
Ayres, M.P. & Lombardero, M.J. (2000) Assessing the consequences of global change for forest disturbance from herbivores and pathogens. The Science of the Total Environment 262, 263–286.Google Scholar
Battisti, A., Larsson, S. & Roques, A. (2017) Processionary moths and associated urtication risk: global change-driven effects. Annual Review of Entomology 62(1), 323–342.Google Scholar
Berardi, L., Branco, M., Paiva, M.R., Santos, H. & Battisti, A. (2015) Development time plasticity of the pine processionary moth (Thaumetopoea pityocampa) populations under laboratory conditions. Entomologia 3 (273), 19–24.Google Scholar
Branco, M., Pereira, J.S., Mateus, E., Tavares, C. & Paiva, M.R. (2010) Water stress affects Tomicus destruens host pine preference and performance during the shoot feeding phase. Annals of Forest Science 67, 608.Google Scholar
Branco, M., Paiva, M.R., Santos, H.M., Burban, C. & Kerdelhué, C. (2017) Experimental evidence for heritable reproductive time in 2 allochronic populations of pine processionary moth. Insect Science 24 (2), 325–335.Google Scholar
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), 311–328.Google Scholar
Caldeira, M.C., Fernandéz, V., Tomé, J. & Pereira, J.S. (2002) Positive effect of drought on longicorn borer larval survival and growth on eucalyptus trunks. Annals of Forest Science 59, 99–106.Google Scholar
Chen, D., Wang, S., Xiong, B., Cao, B. & Deng, X. (2015) Carbon/Nitrogen imbalance associated with drought-induced leaf senescence in Sorghum bicolor. PLoS ONE 10 (8), e0137026.Google Scholar
Démolin, G. (1969) Bioecologia de la Procesionaria del pino Thaumetopoea pityocampa Schiff. Incidencia de los factores climaticos. Boletín del Servicio de Plagas Forestales 12, 9–24.Google Scholar
Després, L., David, J.P. & Gallet, C. (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends in Ecology & Evolution 22(6), 298–307.Google Scholar
Folin, O. & Ciocalteu, V. (1927) On tyrosine and tryptophane determinations in proteins. Journal of Biological Chemistry 73, 627–650.Google Scholar
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), 1288–1300.Google Scholar
Henriksson, J., Haukioja, E., Ossipov, V., Ossipova, S., Sillanpää, S, Kapari, L. & Pihlaja, K. (2003) Effects of host shading on consumption and growth of the geometrid Epirrita autumnata: interactive roles of water, primary and secondary compounds. Oikos 103, 3–16.Google Scholar
Hódar, J.A., Zamora, R. & Castro, J. (2002) Host utilization by moth and larval survival of pine processionary caterpillar Thaumetopoea pityocampa in relation to food quality in three Pinus species. Ecological Entomology 27, 292–301.Google Scholar
Hoerling, M., Eischeid, J., Perlwitz, J., Quan, X., Zhang, T. & Pegion, P. (2012) On the increased frequency of Mediterranean drought. Journal of Climate 25, 2146–2161.Google Scholar
Huberty, A.F. & Denno, R.F. (2004) Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology 85 (5), 1383–1398.Google Scholar
Inbar, M.I., Doostdar, H. & Mayer, R.T. (2001) Suitability of stressed and vigorous plants to various insect herbivores. Oikos 94, 228–235.Google Scholar
IPCC (2007) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. 996 pp in Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M. & Miller, H.L. (Eds) Cambridge, United Kingdom and New York, USA, Cambridge University Press.Google Scholar
IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. 1535 pp in Stocker, T.F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S.K., Boschung, J., Nauels, A., Xia, Y., Bex, V. & Midgley, P.M. (Eds) Cambridge, United Kingdom and New York, USA, Cambridge University Press. doi:10.1017/CBO9781107415324.Google Scholar
Jacquet, J.-S., Bosc, A., O'Grady, A. & Jactel, H. (2014) Combined effects of defoliation and water stress on pine growth and non-structural carbohydrates. Tree Physiology 00, 1–10.Google Scholar
Jactel, H., Petit, J., Desprez-Loustau, M.-L., Delzon, S., Piou, D., Battisti, A. & Koricheva, J. (2012) Drought effects on damage by forest insects and pathogens: a meta-analysis. Global Change Biology 18, 267–276.Google Scholar
Jaleel, C.A., Manivannan, P., Wahid, A., Farooq, M., Al-Juburi, H.J., Somasundaram, R. & Panneerselvam, R. (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. International Journal of Agriculture and Biology 11 (1), 100–105.Google Scholar
Jones, M.G.K., Outlaw, W.H. & Lowry, O.H. (1977) Enzymic assay of 10−7 to 10−14 moles of sucrose in plant tissues. Plant Physiology 60, 379–383.Google Scholar
Koricheva, J., Larsson, S. & Haukioja, E. (1998) Insect performance on experimentally stressed woody plants: a meta-analysis. Annual Review of Entomology 43, 195–216.Google Scholar
Kolb, T.E., Fettig, C.J., Bentz, B.J., Stewart, J.E., Weed, A.S., Hicke, J.A. & Ayres, M.P. (2016) Forest insect and fungal pathogen responses to drought. pp. 113–133 in Vose, J.M., Clark, J.S., Luce, C.H. & Patel-Weynard, T. (Eds) Effects of Drought on Forests and Rangelands in the United States: A Comprehensive Science Synthesis. General Technical Report WO-93b. Washington, USA, U.S. Department of Agriculture, Forest Service, Washington Office.Google Scholar
Larsson, S. (1989) Stressful times for the plant stress – insect performance hypothesis. Oikos 56, 277–283.Google Scholar
Leblois, R., Gautier, M., Rohfritsch, A., Foucaud, J., Burban, C., Galan, M., Loiseau, A., Saune, L., Branco, M., Gharbi, K., Vitalis, R. & Kerdelhue, C. (2017) Deciphering the demographic history of allochronic differentiation in the pine processionary moth Thaumetopoea pityocampa. Molecular Ecology 00, 1–15.Google Scholar
Loustau, D., Berbigier, P., Roumagnac, P., Arruda-Pacheco, C., David, J.S., Ferreira, M.I., Pereira, J.S. & Tavares, R. (1996) Transpiration of a 64-year-old maritime pine stand in Portugal. Oecologia 107, 33–42.Google Scholar
Mattson, W.J. & Haack, R.A. (1987) The role of drought in outbreaks of plant-eating insects. Bioscience 37, 110–118.Google Scholar
McDowell, N., Pockman, W.T., Allen, C.D., Breshears, D.D., Cobb, N., Kolb, T., Plaut, J., Sperry, J., West, A., Williams, D.G. & Yepez, E.A. (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178, 719–739.Google Scholar
Netherer, S. & Schopf, A. (2010) Potential effects of climate change on insect herbivores in European forests – general aspects and the pine processionary moth as specific example. Forest Ecology and Management 259, 831–838.Google Scholar
Rocha, S., Kerdelhue, C., Ben Jamaa, M.L., Dhahri, S., Burban, C. & Branco, M. (2017) Effect of heat waves on embryo mortality in the pine processionary moth. Bulletin of Entomological Research 107 (5): 583–591. doi: 10.1017/S0007485317000104.Google Scholar
Rouault, G., Candau, J., Lieutier, F., Nageleisen, L.-M., Martin, J.C. & Warzée, N. (2006) Effects of drought and heat on forest insect populations in relation to the 2003 drought in Western Europe. Annals of Forest Science 63, 613–624.Google Scholar
Santos, H.M.G., 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: Biological Sciences 274 (1612), 935–941.Google Scholar
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, 146–158.Google Scholar
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, 1897–1905.Google Scholar
Santos, H.M., 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 (15), 5098–5108.Google Scholar
Searle, P.L. (1984) The Berthelot or indophenol reaction and its use in the analysis chemistry of nitrogen. The Analyst 109, 549–568.Google Scholar
Stitt, M., Lilley, R.M., Gerhardt, R. & Heldt, H.W. (1989) Metabolite levels in specific cells and subcellular compartments of plant leaves. Methods in Enzymology 174, 518–552.Google Scholar
Taylor, R.S. & Friesen, V.L. (2017) The role of allochrony in speciation. Molecular Ecology 26, 3330–3342.Google Scholar
Zovi, D., Stastny, M., Battisti, A. & Larsson, S. (2008) Ecological costs on local adaptation of an insect herbivore imposed by host plants and enemies. Ecology 89 (5), 1388–1398.Google Scholar