Skip to main content
SpringerLink
Log in

Potential spread of the invasive North American termite, Reticulitermes flavipes, and the impact of climate warming

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Reticulitermes flavipes is an invasive termite from North America that is found in several European countries, including France from north to south. It feeds on several timber species and can cause major damage when it infests lumber. Termites are urban pests: they are often found in and around towns and their expansion is closely linked to human activity. Although, by law, termite infestations must be reported and treated, R. flavipes continues to spread. To better identify areas that may soon be colonized, it is crucial to understand the mechanisms underlying the termite’s spread at a fine spatial scale. However, the complexity of the species’ dispersal dynamics (i.e., via swarming, budding, or human-mediated transport of infested material) and social organization render this process difficult. The goal of our study was to determine R. flavipes’ potential to expand its current range within a region of France: Centre-Val de Loire. We focused on one administrative department within the region—Indre and Loire—where infestations are common and data on termite presence date back to the 1980s. We developed a spatiotemporal model to study the growth and dispersal of termite colonies within favorable habitat. Habitat favorability was defined based on the density of urbanization and annual mean minimum temperature. First, we modeled temporal population dynamics, using biological parameters describing the transitions between life stages/castes within colonies; we could thus estimate alates production. Then, using this information, we modeled termite dispersal within favorable habitat, and determined the termite’s potential spread. We validated the results by comparing the model’s output with actual data on the termite’s range expansion between 1985 (when the termite was first observed in the region) and 2013. Finally, the model was used to predict the termite’s future spread given climate warming for the period from 2013 to 2030. The results show that an increase in temperature should increase the amount of favorable habitat and, as a consequence, termites could continue to spread within this region. In addition to continuing current control efforts, it will be necessary to enact preventative strategies in newly favorable habitat. In these areas, monitoring efforts should therefore be intensified, as they might be able to slow down the termite’s spread and limit its impact.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alvarez S (2016) Potential economic costs of invasive structural pests: conehead termites, Nasutitermes corniger, in Florida. J Environ Plan Manag 59(12):2145–2162

    Article  Google Scholar 

  • Andrieu D, Perdereau E, Robinet C, Suppo C, Dupont S, Cornillon M, Bagnères A-G (2017) Géographie des termites souterrains en région Centre-Val de Loire: le risque d’une espèce invasive. Cybergeo. doi:10.4000/cybergeo.28412

    Google Scholar 

  • Antier L, Demanche É, Kolarik D (2014) TermiCentre, Termites en région Centre : modélisation et représentation cartographique des données de répartition et leurs variables. École Polytechnique Universitaire—Département Aménagement, Rapport de stage de groupe, Université de Tours

  • Austin JW, Szalanski AL, Scheffrahn RH, Messenger MT, Dronnet S, Bagnères A-G (2005) Genetic evidence for the synonymy of two Reticulitermes species: Reticulitermes flavipes and Reticulitermes santonensis. Ann Entomol Soc Am 98:395–401

    Article  CAS  Google Scholar 

  • Baudouin G, Bech N, Bagnères A-G*, Dedeine F*. Spatial and genetic distribution of an American termite across the landscape of Paris (Submitted to Urban ecosystem)

  • Bertelsmeier C, Luque GM, Courchamp F (2013) Increase in quantity and quality of suitable areas for invasive species as climate changes. Conserv Biol 27(6):1458–1467

    Article  PubMed  Google Scholar 

  • Bertelsmeier C, Avril A, Blight O, Jourdan H, Courchamp F (2015) Discovery-dominance trade-off among widespread invasive ant species. Ecol Evol 5(13):2673–2683

    Article  PubMed  PubMed Central  Google Scholar 

  • Buchli H (1958) L’origine des castes et les potentialités ontogéniques des Termites européens du genre Reticulitermes. Annales des Sciences Naturelles - Zoologie et Biologie Animale 11:263–429

    Google Scholar 

  • Caloz R, Collet C (2011) Analyse spatiale de l’information géographique, Science & ingénierie de l’environnement. Presses polytechniques et universitaires romandes, Lausanne

    Google Scholar 

  • Chapman RE, Bourke AFG (2001) The influence of sociality on the conservation biology of social insects. Ecol Lett 4:650–662

    Article  Google Scholar 

  • Chouvenc T, Su NY (2014) Colony age-dependent pathway in caste development of Coptotermes formosanus Shiraki. Insectes Soc 61(2):171–182

    Article  Google Scholar 

  • Clark PJ, Evans FC (1954) Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35(4):445–453

    Article  Google Scholar 

  • Clément JL, Bagnères A-G, Uva P, Wilfert L, Quintana A, Reinhard J, Dronnet S (2001) Biosystematics of Reticulitermes termites in Europe: morphological, chemical and molecular data. Insectes Soc 48:202–215

    Article  Google Scholar 

  • Dedeine F, Dupont S, Guyot S, Matsuura K, Wang C, Habibpour B, Bagnères A-G, Mantovani B, Luchetti A (2016) Historical biogeography of Reticulitermes termites (Isoptera: Rhinotermitidae) inferred from analyses of mithocondrial and nuclear loci. Mol Phylogenet Evol 94:778–790

    Article  PubMed  Google Scholar 

  • Dronnet S, Chapuisat M, Vargo EL, Lohou C, Bagnères A-G (2005) Genetic analysis of the breeding system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats. Mol Ecol 14:1311–1320

    Article  CAS  PubMed  Google Scholar 

  • Duan JJ, Bauer LS, Abell KJ, Ulyshen MD, Van Driesche RG (2015) Population dynamics of an invasive forest insect and associated natural enemies in the aftermath of invasion: implications for biological control. J Appl Ecol 52(5):1246–1254

    Article  Google Scholar 

  • Epanchin-Niell RS, Wilen JE (2014) Individual and cooperative management of invasive species in human-mediated landscapes. Am J Agr Econ 97(1):180–198

    Article  Google Scholar 

  • Evans TA, Forschler BF, Grace JK (2013) Biology of invasive termites: a worldwide review. Annu Rev Entomol 58:455–474

    Article  CAS  PubMed  Google Scholar 

  • Ewart D, Nunes L, de Troya T, Kutnik M (2017) Termites and a changing climate. In: Dhang P (ed) Climate change impacts on urban pests. CABI, Wallingford, pp 80–94. doi:10.1079/9781780645377.0080

  • Facon B, Genton BJ, Shykoff J, Jarne P, Estoup A, Davis P (2006) A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol Evol 21(3):130–135

    Article  PubMed  Google Scholar 

  • Facon B, Mailleret L, Renault D, Roques L (2015) Biological invasion processes: evaluation and prediction. Revue d’Ecologie (Terre et Vie) 70:110–113

    Google Scholar 

  • Feytaud J (1946) Le peuple des Termites. Ed. Presses universitaires de France

  • Ghesini S, Messenger MT, Pilon N, Marini M (2010) First report of Reticulitermes flavipes (Isoptera: Rhinotermitidae) in Italy. Florida Entomological Society 93:327–328

    Article  Google Scholar 

  • Haury J, Tassin J, Renault D, Atlan A (2015) Socio-economic management of biological invasions. Revue d’Ecologie (Terre et Vie) 70:172–174

    Google Scholar 

  • Kenis M, Roy HE, Zindel R, Majerus MEN (2008) Current and potential management strategies against Harmonia axyridis. Biocontrol 53:235–252

    Article  CAS  Google Scholar 

  • Kollar V (1837) Naturgeschichte des schädlichen Insekten. Verhandlungen Landwirthschaft Gesellshaft in Wien 5:411–413

    Google Scholar 

  • Langlois P, Lajoie G (1998) Cartographie par carroyage et précision spatiale. M@ppemonde 49:20–22

    Google Scholar 

  • Liebhold AM, Berec L, Brockerhoff EG, Epanchin-Niell RS, Hastings A, Herms DA, Kean JM, McCullough DG, Suckling DM, Tobin PC, Yamanaka T (2016) Eradication of invading insect populations: from concepts to applications. Annu Rev Entomol 61:335–352

    Article  CAS  PubMed  Google Scholar 

  • Nuninger L, Bertoncello F, Favory F (2011) Dynamiques socio-environnementales dans la longue durée. In: Rodier X. (dir.) Information spatiale et archéologie, Paris, France: Éd. Errance

  • Ouzeau G, Déqué M, Jouini M, Planton S, Vautard R (2014) Le climat de la France au XXIe siècle. Volume 4: Scénarios régionalisés: édition 2014 pour la métropole et les régions d’outre-mer. Rapport du Ministère de l’Ecologie, du Développement durable et de l’Energie, p 64, www.developpement-durable.gouv.fr

  • Perdereau E, Bagnères A-G, Dupont S, Dedeine F (2010) High occurrence of colony fusion in a European population of the American termite Reticulitermes flavipes. Insectes Soc 57:393–402

    Article  Google Scholar 

  • Perdereau E, Dedeine F, Christides JP, Dupont S, Bagnères A-G (2011) Competition between invasive and indigenous species: an insular case study of subterranean termites. Biol Invasions 13:1457–1470

    Article  Google Scholar 

  • Perdereau E, Bagnères A-G, Bankhead-Dronnet S, Dupont S, Zimmermann M, Vargo EL, Dedeine F (2013) Global genetic analysis reveals the putative native source of the invasive termite, Reticulitermes flavipes, in France. Mol Ecol 22:1105–1119

    Article  CAS  PubMed  Google Scholar 

  • Perdereau E, Bagnères A-G, Vargo EL, Baudouin G, Xu Y, Labadie P, Dupont S, Dedeine F (2015) Relationship between invasion success and colony breeding structure in a subterranean termite. Mol Ecol 24:2125–2142

    Article  CAS  PubMed  Google Scholar 

  • Petit O, Billon P, Follin J-M (2012) Évaluation de la qualité des données OpenStreetMap sur la Sarthe et réflexion sur le processus de contribution. Revue XYZ 131:37–47

    Google Scholar 

  • Pin B, Yengué J-L, Andrieu D, Servain S, Génin A (2013) Analyse multicritères de la diversité des espaces verts, approche méthodologique et décryptage fonctionnel: le cas du schéma de cohérence territoriale de Tours (Indre-et-Loire). CTHS. Nature et composition urbaine, CTHS, p 125, Actes des congrès nationaux des sociétés historiques et scientifiques

  • Pluess T, Jarošík V, Pyšek P, Cannon R, Pergl J, Breukers A, Bacher S (2012) Which factors affect the success or failure of eradication campaigns against alien species? PLoS ONE 7(10):e48157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pumain D (2012) Une théorie géographique pour la loi de Zipf. Région et développement 36:33–57

    Google Scholar 

  • R Development Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN: 3-900051-07-0. http://www.R-project.org

  • Ripa R, Castro L (2000) Presencia de la termita subterranea Reticulitermes santonensis de Feytaud (Isoptera: Rhinotermitidae) en la comuna de Quillota. In: XXII Chilean Congress of Entomology, Valdivia

  • Roques A, Auger-Rozenberg M-A, Blackburn TM, Garnas J, Pyšek P, Rabitsch W, Richardson DM, Wingfield MJ, Liebhold AM, Duncan RP (2016) Temporal and interspecific variation in rates of spread for insect species invading Europe during the last 200 years. Insect Invasions 18:907–920

    Article  Google Scholar 

  • Scaduto DA, Garner SR, Leach EL, Thompson GJ (2012) Genetic evidence for multiple invasions of the eastern subterranean termite into Canada. Environ Entomol 41(6):1680–1686

    Article  PubMed  Google Scholar 

  • Scharf ME, Wu-Scharf D, Pittendrigh BR, Bennett GW (2003) Caste- and development-associated gene expression in a lower termite. Genome Biol 4(10):R62

    Article  PubMed  PubMed Central  Google Scholar 

  • Shelton TG, Hu XP, Appel AG, Wagner TL (2006) Flight speed of tethered Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae) alates. J Insect Behav 19:115–128

    Article  Google Scholar 

  • Su NY (2013) How to become a successful invader. Fla Entomol 96(3):765–769

    Article  Google Scholar 

  • Su NY, Ye WM, Ripa R, Scheffrahn RH, Giblin-Davis RM (2006) Identification of Chilean Reticulitermes (Isoptera: Rhinotermitidae) inferred from three mitochondrial gene DNA sequences and soldier morphology. Ann Entomol Soc Am 99:352–363

    Article  CAS  Google Scholar 

  • Thorne BL (1998) Biology of subterranean termites. NPCA research report on subterranean termites. National Pest Control Association, Virginia, pp 1–30

    Google Scholar 

  • Thorne BL, Traniello JFA, Adams ES, Bulmer M (1999) Reproductive dynamics and colony structure of subterranean termites of the genus Reticulitermes (Isoptera Rhinotermitidae): a review of the evidence from behavioral, ecological, and genetic studies. Ethol Ecol Evol 11:149–169

    Article  Google Scholar 

  • Tonini F, Hochmair HH, Scheffrahn RH, Deangelis DL (2013) Simulating the spread of an invasive termite in an urban environment using a stochastic individual-based model. Environ Entomol 42(3):412–423

    Article  PubMed  Google Scholar 

  • Tonini F, Divino F, Lasinio GL, Hochmair HH, Scheffrahn R (2014) Predicting the geographical distribution of two invasive termite species from occurrence data. Environ Entomol 43(5):1135–1144

    Article  PubMed  Google Scholar 

  • Uva P, Clément J-L, Austin JW, Aubert J, Zaffagnini V, Quintina A, Bagnères A-G (2004) Origin of a new Reticulitermes termite (Isoptera, Rhinotermitidae) inferred from mitochondrial and nuclear DNA data. Mol Phylogenet Evol 30:344–353

    Article  CAS  PubMed  Google Scholar 

  • Vargo EL (2014) Molecular ecology meets urban entomology: How molecular biology is changing urban pest management. In: Dhang P (ed) Urban insect pests: sustainable management strategies. CAB International, Wallingford, pp 166–180

    Google Scholar 

  • Vargo EL, Husseneder C (2008) Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annu Rev Entomol 54:379–403

    Article  Google Scholar 

  • Vargo EL, Leniaud L, Swoboda LE, Diamond S, Weiser MD, Miller DM, Bagnères A-G (2013) Clinal variation on colony breeding structure and level of inbreeding in the subterranean termites Reticulitermes flavipes and R. grassei. Mol Ecol 22:1447–1462

    Article  PubMed  Google Scholar 

  • Walther GR, Roques A, Hulme PE, Sykes MT, Pyšek P, Kühn I, Zobel M, Bacher S, Botta-Dukát Z, Bugmann H, Czúcz B, Dauber J, Hickler T, Jarošík V, Kenis M, Klotz S, Minchin D, Moora M, Nentwig W, Ott J, Panov VE, Reineking B, Robinet C, Semenchenko V, Solarz W, Thuiller W, Vilà M, Vohland K, Settele J (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24(12):686–693

    Article  PubMed  Google Scholar 

  • Weidner H (1937) Termiten in Hamburg. Zeitschrift für Pflanzenkrankheiten 47:593–596

    Google Scholar 

Download references

Acknowledgements

We wish to thank Innophyt (M. Cornillon and I. Arnault), the different cities of the Centre-Val de Loire region, various PCO companies, and the FDGDON Center (M.-P. Dufresne) for their help with sample and data collection. We would also like to thank the three students who greatly contributed to the identification of favorable termite habitat and the potential effects of climate warming: Lolita Antier, Elise Demanche, and Daphné Kolarik (MHS, Tours, France). Alain Roques (INRA, URZF, Orléans, France) provided helpful comments during model development and expertise when it came to estimating several parameters. We are grateful to Agroclim (INRA, Avignon, France) and Météo France for providing monthly temperature and relative humidity data for the study area. Funding was provided by a grant (TermiCentre) from the Centre-Val de Loire region to Anne-Geneviève Bagnères.

Author information

Authors and Affiliations

  1. Institut de Recherche sur la Biologie de l’Insecte, UMR 7261, CNRS, Université François-Rabelais, 37200, Tours, France

    Christelle Suppo, Elfie Perdereau & Anne-Geneviève Bagnères

  2. INRA, UR633 Zoologie Forestière, 45075, Orléans, France

    Christelle Robinet

  3. Université François-Rabelais, USR 3501 MSH Val de Loire, 37204, Tours, France

    Dominique Andrieu

  4. Centre d’Ecologie Fonctionnelle et Evolutive, UMR 5175, CNRS, 34293, Montpellier, France

    Anne-Geneviève Bagnères

Authors
  1. Christelle Suppo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christelle Robinet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elfie Perdereau
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dominique Andrieu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anne-Geneviève Bagnères
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christelle Suppo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Suppo, C., Robinet, C., Perdereau, E. et al. Potential spread of the invasive North American termite, Reticulitermes flavipes, and the impact of climate warming. Biol Invasions 20, 905–922 (2018). https://doi.org/10.1007/s10530-017-1581-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-017-1581-3

Keywords

Search

Navigation