Has North Africa turned too warm for a Mediterranean forest pest because of climate change?

Abstract

Climate warming is inducing dramatic changes in species distribution. While many studies report the poleward range expansion of some species, some others report the range retraction and extinction risk of other species. Here we explore how climate warming affects the southern edge in North Africa of the pine processionary moth, Thaumetopoea pityocampa, which is a model insect currently expanding northwards and toward higher elevation in Europe. This Mediterranean forest insect was found in southern Tunisia until 2003. Field surveys were conducted to map the current southern edge of the species in Tunisia. Pheromone traps were installed on a north-south gradient, a translocation experiment of egg masses was conducted on this gradient, and local temperature change was analyzed. We thus proved that the pine processionary moth has disappeared from southern Tunisia, and that no more adult males were actually flying there. We also found a decrease of egg hatching and of the proportion of individuals able to reach larval stages along this gradient, while daily minimal and maximal temperatures globally increased. Furthermore, we showed that daily maximal and minimal temperatures as well as indices of extremely high temperatures have substantially increased during the study period (1980–2019). This study reveals the retraction of the pine processionary moth from southern Tunisia due to higher mortality rates that could be attributed to a significant local warming. The role of other factors (mainly the response of host trees and natural enemies to climate change) may amplify this direct effect and should be further explored.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Data availability

Most of the datasets are provided in the article and supplementary material. Other datasets are available from the corresponding author on request.

Code availability

The R code of analyses is available from the corresponding author on request.

References

  1. Andersen JC, Havill NP, Mannai Y et al (2019) Identification of winter moth (Operophtera brumata) refugia in North Africa and the Italian Peninsula during the last glacial maximum. Ecol Evol 9:13931–13941. https://doi.org/10.1002/ece3.5830

    Article  Google Scholar 

  2. Azizi Z (2015) Eclaircissement de la situation de la chenille processionnaire du pin dans le sud de sa répartition (le sud Tunisien). Master thesis, Institut National Agronomique de Tunisie, Tunis, Tunisie, pp. 66

  3. Battisti A, Stastny M, Netherer S et al (2005) Expansion of geographic range in the pine processionary moth caused by increased winter temperatures. Ecol Appl 15:2084–2096. https://doi.org/10.1890/04-1903

    Article  Google Scholar 

  4. Battisti A, Larsson S, Roques A (2017) Processionary moths and associated urtication risk: global change–driven effects. Annu Rev Entomol 62:323–342. https://doi.org/10.1146/annurev-ento-031616-034918

    Article  Google Scholar 

  5. Ben Jamâa ML (2017) Geographic area of the pine processionary moth (Thaumetopoea pityocampa Schiff, Lepidoptera) in the southern Aleppo pine forests and effect of the climatic change. Paper presented at the 125th IUFRO Anniversary Congress - Book of abstract, Freiburg, page 222. ISBN 978-3-902762-88-7. Available at: http://iufro2017.com/downloads/. Accessed 2 Jul 2020

  6. Ben Jamâa ML, Jerraya A (1999) Essai de lutte contre la processionnaire du pin : Thaumetopoea pityocampa Schiff. (Lep., Thaumetopoeïdae) à l’aide de Bacollus thuringiensis Kurstaki (ECOTECH-PRO). Ann INRF Tunisie 3:3–12

    Google Scholar 

  7. Borghetti M, Cinnirella S, Magnani F, Saracino A (1998) Impact of long-term drought on xylem embolism and growth in Pinus halepensis mill. Trees 12:187–195. https://doi.org/10.1007/PL00009709

    Article  Google Scholar 

  8. Branco M, Pereira JS, Mateus E, Tavares C, Paiva MR (2010) Water stress affects Tomicus destruens host pine preference and performance during the shoot feeding phase. Ann For Sci 67:608. https://doi.org/10.1051/forest/201021

    Article  Google Scholar 

  9. Cherif S, Ezzine O, Khouja ML, Nasr Z (2020) Comparison of the physiological responses of three pine species in different bioclimatic zones in Tunisia. Appl Ecol Environ Res 18:1–13. https://doi.org/10.15666/aeer/1801_001013

    Article  Google Scholar 

  10. Démolin G (1969) Bioécologie de la processionnaire du pin, Thaumetopoea pityocampa Schiff Incidences des facteurs climatiques Boletin del Servicio de Plagas Forestales:9–24

  11. Démolin G, Rive J (1968) La processionnaire du pin en Tunisie. Ann INRF Tunisie 1:1–19

    Google Scholar 

  12. Duputié A, Rutschmann A, Ronce O, Chuine I (2015) Phenological plasticity will not help all species adapt to climate change. Glob Chang Biol 21:3062–3073. https://doi.org/10.1111/gcb.12914

    Article  Google Scholar 

  13. Franco AMA, Hill JK, Kitschke C et al (2006) Impacts of climate warming and habitat loss on extinctions at species’ low-latitude range boundaries. Glob Chang Biol 12:1545–1553. https://doi.org/10.1111/j.1365-2486.2006.01180.x

    Article  Google Scholar 

  14. Georgiev G, Rousselet J, Laparie M et al (2020) Comparative studies of egg parasitoids of the pine processionary moth (Thaumetopoea pityocampa, Den. & Schiff.) in historic and expansion areas in France and Bulgaria. Forestry: an international journal of Forest research cpaa022. https://doi.org/10.1093/forestry/cpaa022

  15. Girard F, Vennetier M, Guibal F et al (2012) Pinus halepensis Mill. crown development and fruiting declined with repeated drought in Mediterranean France. Eur J For Res 131:919–931. https://doi.org/10.1007/s10342-011-0565-6

    Article  Google Scholar 

  16. Henriksson J, Haukioja E, Ossipov V et al (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. https://doi.org/10.1034/j.1600-0706.2003.12306.x

    Article  Google Scholar 

  17. Huchon H, Démolin G (1970) La bioécologie de la processionnaire du pin. Dispersion potentielle, dispersion actuelle. Revue For Française 151:220–234. https://doi.org/10.4267/2042/20421

    Article  Google Scholar 

  18. Imbert CE (2012) Expansion d’un ravageur forestier sous l’effet du réchauffement climatique : la processionnaire du pin affecte-t-elle la biodiversité entomologique dans les zones nouvellement colonisées ? PhD thesis, Université d’Orléans, Orléans, France. Available at: https://www.theses.fr/162101465. Accessed 29 Jul 2020

  19. 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, eds Core Writing Team, R. K. Pachauri, and L. A. Meyer (Geneva: IPCC), pp. 151. ISBN 978-92-9169-143-2. Available at: https://www.ipcc.ch/report/ar5/syr/. Accessed 29 Jul 2020

  20. Jacquet J-S, Bosc A, O’Grady AP, Jactel H (2013) Pine growth response to processionary moth defoliation across a 40-year chronosequence. For Ecol Manag 293:29–38. https://doi.org/10.1016/j.foreco.2012.12.003

    Article  Google Scholar 

  21. Johnson DM, Büntgen U, Frank DC et al (2010) Climatic warming disrupts recurrent Alpine insect outbreaks. PNAS USA 107:20576–20581. https://doi.org/10.1073/pnas.1010270107

    Article  Google Scholar 

  22. Lesk C, Coffel E, D’Amato AW et al (2017) Threats to North American forests from southern pine beetle with warming winters. Nat Clim Chang 7:713–717. https://doi.org/10.1038/nclimate3375

    Article  Google Scholar 

  23. ONERC (2010) Catalogue des indicateurs du changement climatique, Report from the French Ministry of Ecology, pp32 Available at: http://wwwobservatoireclimat-hautsdefranceorg/Les-ressources/Ressources-documentaires/Catalogue-des-indicateurs-du-changement-climatique Accessed 29 Jul 2020

  24. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. https://doi.org/10.1038/nature01286

    Article  Google Scholar 

  25. Parmesan C, Ryrholm N, Stefanescu C et al (1999) Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399:579–583. https://doi.org/10.1038/21181

    Article  Google Scholar 

  26. Parmesan C, Root TL, Willig MR (2000) Impacts of extreme weather and climate on terrestrial biota. Bull Amer Meteor Soc 81:443–450. https://doi.org/10.1175/1520-0477(2000)081%3C0443:IOEWAC%3E2.3.CO;2

    Article  Google Scholar 

  27. Peterson TC (2005) Climate change indices. World Meteorol Organ Bull 54:83–86 Available at: http://etccdi.pacificclimate.org/papers/WMO.Bulletin.April.2005.indices.pdf accessed 29 Jul 2020

    Google Scholar 

  28. Pounds JA, Fogden MPL, Campbell JH (1999) Biological response to climate change on a tropical mountain. Nature 398:611–615. https://doi.org/10.1038/19297

    Article  Google Scholar 

  29. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna URL https://www.R-project.org/

    Google Scholar 

  30. Raffa KF, Aukema BH, Bentz BJ et al (2008) Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. BioScience 58:501–517. https://doi.org/10.1641/B580607

    Article  Google Scholar 

  31. Raffa KF, Aukema BH, Bentz BJ et al (2015) Responses of tree-killing bark beetles to a changing climate. In: climate change and insect pests (editors: C. Björkman, P. Niemelä). CAB International 7. pp. 173–201

  32. Rebaudo F, Rabhi V-B (2018) Modeling temperature-dependent development rate and phenology in insects: review of major developments, challenges, and future directions. Entomol Exp Appl 166:607–617. https://doi.org/10.1111/eea.12693

    Article  Google Scholar 

  33. Régnière J, St-Amant R, Duval P (2012) Predicting insect distributions under climate change from physiological responses: spruce budworm as an example. Biol Invasions 14:1571–1586. https://doi.org/10.1007/s10530-010-9918-1

    Article  Google Scholar 

  34. Rive JL (1966) La processionnaire du pin, notions de biologie et principes de lutte. Note Technique N°5, pp. 8

  35. Robinet C, Roques A (2010) Direct impacts of recent climate warming on insect populations. Integr Zool 5:132–142. https://doi.org/10.1111/j.1749-4877.2010.00196.x

    Article  Google Scholar 

  36. Robinet C, Baier P, Pennerstorfer J et al (2007) Modelling the effects of climate change on the potential feeding activity of Thaumetopoea pityocampa (Den. & Schiff.) (Lep., Notodontidae) in France. Glob Ecol Biogeogr 16:460–471. https://doi.org/10.1111/j.1466-8238.2006.00302.x

    Article  Google Scholar 

  37. Robinet C, Rousselet J, Pineau P et al (2013) Are heat waves susceptible to mitigate the expansion of a species progressing with global warming? Ecol Evol 3:2947–2957. https://doi.org/10.1002/ece3.690

    Article  Google Scholar 

  38. 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. Front Physiol 6:334. https://doi.org/10.3389/fphys.2015.00334

    Article  Google Scholar 

  39. Rocha S, Kerdelhué C, Ben Jamaa ML et al (2017) Effect of heat waves on embryo mortality in the pine processionary moth. Bull Entomol Res 107:583–591. https://doi.org/10.1017/S0007485317000104

    Article  Google Scholar 

  40. Roques A (2015) Processionary moths and climate change: an update. Springer, Dordrecht / Quae Editions, pp. 427. https://doi.org/10.1007/978-94-017-9340-7

  41. Roques A, Rousselet J, Avci M et al (2015) Climate warming and past and present distribution of the processionary moths (Thaumetopoea spp.) in Europe, Asia Minor and North Africa. In: Roques A (ed) Processionary moths and climate change : an update. Springer, Dordrecht, pp 81–161. https://doi.org/10.1007/978-94-017-9340-7_3

    Google Scholar 

  42. Rosenzweig C, Casassa G, Karoly DJ et al (2007) Assessment of observed changes and responses in natural and managed systems. Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, M.L. Parry, O.F. Canziani, J.P. Palutikof, P.J. van der Linden and C.E. Hanson, Eds., Cambridge University Press, Cambridge, UK, pp.79–131. Available at: https://www.ipcc.ch/report/ar4/wg2/historical-overview-of-climate-change-science/ Accessed 29 Jul 2020

  43. Rossi J-P, Garcia J, Roques A, Rousselet J (2016) Trees outside forests in agricultural landscapes: spatial distribution and impact on habitat connectivity for forest organisms. Landsc Ecol 31:243–254. https://doi.org/10.1007/s10980-015-0239-8

    Article  Google Scholar 

  44. Rousselet J, Imbert CE, Dekri A et al (2013) Assessing species distribution using Google street view: a pilot study with the pine processionary moth. PLoS One 8:e74918. https://doi.org/10.1371/journal.pone.0074918

    Article  Google Scholar 

  45. Rozenberg P, Pâques L, Huard F, Roques A (2020) Direct and indirect analysis of the elevational shift of larch budmoth outbreaks along an elevation gradient. Front For Glob Change 3:86. https://doi.org/10.3389/ffgc.2020.00086

    Article  Google Scholar 

  46. Santos H, Paiva MR, Tavares C et al (2011) Temperature niche shift observed in a Lepidoptera population under allochronic divergence. J Evol Biol 24:1897–1905. https://doi.org/10.1111/j.1420-9101.2011.02318.x

    Article  Google Scholar 

  47. Shuttle Radar Topography Mission (SRTM) (n.d.) Non-Void Filled (Digital Object Identifier). https://doi.org/10.5066/F7K072R7

  48. Thomas CD, Lennon JJ (1999) Birds extend their ranges northwards. Nature 399:213. https://doi.org/10.1038/20335

    Article  Google Scholar 

  49. Thomas CD, Cameron A, Green RE et al (2004) Extinction risk from climate change. Nature 427:145–148. https://doi.org/10.1038/nature02121

    Article  Google Scholar 

  50. Tsankov G, Schmidt GH, Mirchev P (1996) Structure and parasitism of egg-batches of a processionary moth population different from Thaumetopoea pityocampa (Den. & Schiff.) (Lep. Thaumetopoeidae) found in Bulgaria. Bullettino di Zoologia agraria e di Bachiccoltura, Ser II 28:195–207 Available at : https://www.researchgate.net/publication/259622330_Structure_and_parasitism_of_egg-batches_of_a_processionary_moth_population_different_from_Thaumetopoea_pityocampa_Den_Schiff_Lep_Thaumetopoeidae_found_in_Bulgaria. Accessed 29 Jul 2020

    Google Scholar 

  51. Urban MC (2015) Accelerating extinction risk from climate change. Science 348:571–573. https://doi.org/10.1126/science.aaa4984

    Article  Google Scholar 

  52. Verner D, Wilby R, Breisinger C et al (2013) Tunisia in a changing Climate: Assessment and Actions for Increased Resilience and Development. The World Bank, Washington. https://doi.org/10.1596/978-0-8213-9857-9 Available at: http://documents.worldbank.org/curated/en/989681468313213278/Tunisia-in-a-changing-climate-assessment-and-actions-for-increased-resilience-and-development. Accessed 29 Jul 2020

    Book  Google Scholar 

  53. Vicente-Serrano SM, Lasanta T, Gracia C (2010) Aridification determines changes in forest growth in Pinus halepensis forests under semiarid Mediterranean climate conditions. Agric For Meteorol 150:614–628. https://doi.org/10.1016/j.agrformet.2010.02.002

    Article  Google Scholar 

  54. Walther G-R, Post E, Convey P et al (2002) Ecological responses to recent climate change. Nature 416:389–395. https://doi.org/10.1038/416389a

    Article  Google Scholar 

  55. Zhang X, Yang F (2004) RClimDex 1.0: user manual. Climate Research Branch Environment. Downs view, Ontario, p 23p Available at: http://etccdi.pacificclimate.org/software.shtml. Accessed 29 Jul 2020

    Google Scholar 

Download references

Acknowledgements

We are grateful to Jérôme ROUSSELET (INRAE-URZF, Orléans, France) for insightful advice on mapping the edge of species distribution and translocation experiment, to Olfa EZZINE and Samir DHAHRI (INRGREF, Tunis, Tunisia) for general discussions and support in the frame of the PhD of Asma BOUROUGAAOUI, and to Adel BEN ABADA (INRGREF, Tunis, Tunisia) for his valuable help in the field. Pheromone traps and protective suits were kindly provided by Jean Claude MARTIN (INRAE-UEFM, Avignon, France). The distribution of pine stands was kindly provided by the General Direction of Forests in Tunis, and a part of the temperature datasets by the National Institute of Meteorology (INM) in Tunis.

Funding

This study was supported by funding from the University of Carthage (Tunisia): the University provided two grants to Asma BOUROUGAAOUI to spend her internships (two months/grant) at INRAE-URZF in France in 2018 and 2019 in the frame of her PhD. It was also supported by the ANR project PHENEC (grant number 19-CE32-0007-01).

Author information

Affiliations

Authors

Contributions

CR and MBJ designed the study. AB conducted the field experiments, the laboratory analysis, and the statistical analyses. CR and MBJ supervised her work. AB, MBJ, and CR wrote and revised the article.

Corresponding author

Correspondence to Christelle Robinet.

Ethics declarations

Ethics approval

This study was conducted on an insect species (the pine processionary moth, Thaumetopoea pityocampa), which is a pest species commonly controlled. In addition, this is a model species for science which has been exempted from any declaration regarding the Nagoya protocol.

Consent to participate

Not applicable.

Consent for publication

The authors of this article consent to publish the study.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(DOCX 2379 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bourougaaoui, A., Ben Jamâa, M.L. & Robinet, C. Has North Africa turned too warm for a Mediterranean forest pest because of climate change?. Climatic Change 165, 46 (2021). https://doi.org/10.1007/s10584-021-03077-1

Download citation

Keywords

  • Pine processionary moth
  • Thaumetopoea pityocampa
  • Climate warming
  • Range retraction
  • Pinus
  • Tunisia