Abstract
Urbanization often negatively impacts biological diversity. Some organisms, however, have traits that are preadapted to urban environments and thus may thrive. Reticulitermes flavipes is one such organism. Indigenous to the Eastern US, it has been introduced into multiple countries. In France, R. flavipes causes major damage to buildings. Although Paris is one of the country’s most infested cities, the factors determining R. flavipes’ distribution and propagation are poorly understood. Using data on termite occurrence, termite genetics, and environmental variables, our study aims to identify factors that explain the distribution and spread of R. flavipes within Paris. First, we explored the association between several environmental variables and the termite’s distribution pattern in Paris; since 2000, a total of 2106 infestations have been recorded. Second, we inferred termite population and colony genetic structure at 66 sample locations using 9 microsatellite loci. Third, we used least-cost models and partial Mantel tests to study the effects of environmental variables on the termite’s population genetic structure. Our analyses revealed that building-related variables were significantly associated with termite infestations and could thus help explain the termite’s spatial distribution pattern. Furthermore, railway networks also explain termite propagation and genetic patterns. Additionally, we found that the termite’s spread is likely driven by budding dispersal, which may be constrained by buildings and roads. Even if budding dispersal could facilitate R. flavipes’ spread in urban areas, it cannot explain the termite’s distribution in Paris all on its own. Indeed, termite propagation seems to be significantly driven by anthropogenic activities.
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References
Aluko GA, Husseneder C (2007) Colony dynamics of the formosan subterranean termite in a frequently disturbed urban landscape. J Econ Entomol 100:1037–1046
Andrieu D, Perdereau E, Robinet C et al (2017) Géographie des termites souterrains en région Centre-Val de Loire: le risque d’une espèce invasive. Cybergeo. https://doi.org/10.4000/cybergeo.28412
Arango RA, Marschalek DA, Green III F, Raffa KF, Berres ME (2015) Genetic analysis of termite colonies in Wisconsin. Environ Entomol 44(3):890–897
Ascunce MS, Yang C-C, Oakey J et al (2011) Global invasion history of the fire ant Solenopsis invicta. Science 331:1066–1068
Bagnères A-G, Clément J-C, Blum MS et al (1990) Cuticular hydrocarbons and defensive compounds of Reticulitermes flavipes (Kollar) and R. santonensis (Feytaud): polymorphism and chemotaxonomy. J Chem Ecol 16:3213–3244
Baudouin G, Dedeine F, Bech N, Bankhead-Dronnet S, Dupont S, Bagnères A-G (2017) An American termite in Paris: temporal colony dynamics. Genetica 145(6):491–502
Botch PS, Houseman RM (2016) Landscape patterns of colonization by subterranean termites (Isoptera: Rhinotermitidae) in Missouri neighborhoods. J Econ Entomol 109:800–808
Bourguignon T, Chisholm RA, Evans TA (2016) The termite worker phenotype evolved as a dispersal strategy for fertile wingless individuals before eusociality. Am Nat 187:372–387
Brossette L, Bagnères A-G, Millot A, Blanchard S, Dupont S, Lucas C (2017) Termite’s royal cradle: does colony foundation success differ between two subterranean species? Insect Soc 64:515–523. https://doi.org/10.1007/s00040-017-0571-x
Buchli HR (1958) L’origine des castes et les potentialités ontogéniques des Termites Européens du genre Reticulitermes (Holmgren). Masson, Paris
Buczkowski G, Bertelsmeier C (2017) Invasive termites in a changing climate: a global perspective. Ecol Evol 7:974–985
Bulmer MS, Adams ES, Traniello JFA (2001) Variation in colony structure in the subterranean termite Reticulitermes flavipes. Behav Ecol Sociobiol 49:236–243
Chambers JM, Hastie TJ (1992) Linear models. Chapter 4 of statistical models. In: Chambers JM, Hastie TJ (eds) Statistical models in S. Wadsworth & Brooks/Cole, Belmont/Pacific Grove
Clément J-L, Bagnères A-G, Uva P et al (2001) Biosystematics of Reticulitermes termites in Europe: morphological, chemical and molecular data. Insect Soc 48:202–215
De Pieri F (2017) Paris Haussmann: modèle de ville/Paris Haussmann: a model’s relevance. Plan Perspect 32(4):658–659
DeHeer CJ, Vargo EL (2004) Colony genetic organization and colony fusion in the termite Reticulitermes flavipes as revealed by foraging patterns over time and space. Mol Ecol 13(2):431–441
DeHeer CJ, Vargo EL (2008) Strong mitochondrial DNA similarity but low relatedness at microsatellite loci among families within fused colonies of the termite Reticulitermes flavipes. Insect Soc 55(2):190–199
DeHeer CJ, Kutnik M, Vargo EL, Bagnères A-G (2005) The breeding system and population structure of the termite Reticulitermes grassei in southwestern France. Heredity 95:408–415
Devroye L, Wagner TJ (1982) Nearest neighbor methods in discrimination. In: Krishnaiah PR, Kanal LN (eds) Handbook of statistics. North-Holland Publishing Company, Amsterdam, pp 193–197
Dronnet S, Bagnères A-G, Juba TR, Vargo EL (2004) Polymorphic microsatellite loci in the European subterranean termite, Reticulitermes santonensis Feytaud. Mol Ecol Notes 4:127–129
Dronnet S, Chapuisat M, Vargo EL et al (2005) Genetic analysis of the breeding system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats. Mol Ecol 14:1311–1320
Dronnet S, Lohou C, Christidès J-P, Bagnères A-G (2006) Cuticular hydrocarbon composition reflects genetic relationship among colonies of the introduced termite Reticulitermes santonensis (Feytaud). J Chem Ecol 32:1027–1042
Ebdon D (1985) Statistics in geography. Blackwell, Oxford
Evans TA, Forschler BT, Grace JK (2013) Biology of invasive termites: a worldwide review. Annu Rev Entomol 58:455–474
Ewart D, Nunes L, De Troya T, Kutnik M (2017) Termite and a changing climate. In: Dhang P (ed) Climate change impact on urban pests. CABI, Wallingford, pp 80–94
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Lausanne University, Lausanne. http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 13 Dec 2016
Grace JK (1990) Mark-recapture studies with Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiology 16:297–303
Gruber B, Adamack AT (2015) landgenreport : a new R function to simplify landscape genetic analysis using resistance surface layers. Mol Ecol Resour 15:1172–1178
Guillot G, Mortier F, Estoup A (2005) GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5:712–715
Hanna C, Cook ED, Thompson AR et al (2013) Colony social structure in native and invasive populations of the social wasp Vespula pensylvanica. Biol Invasions 16:283–294
Hollander M, Wolfe DA (1973) Nonparametric statistical methods. Wiley, New York, pp 115–120
Holway DA, Lach L, Suarez AV et al (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233
Houseman RM, Gold RE, Pawson BM (2001) Resource partitioning in two sympatric species of subterranean termites, Reticulitermes flavipes and Reticulitermes hageni (Isoptera : Rhinotermitidae). Environ Entomol 30:673–685
Husseneder C, Messenger MT, Su N et al (2005) Colony social organization and population genetic structure of an introduced population of formosan subterranean termite from New Orleans, Louisiana. J Econ Entomol 98:1421–1434
Husseneder C, Powell JE, Grace JK et al (2008) Worker size in the formosan subterranean termite in relation to colony breeding structure as inferred from molecular markers. Environ Entomol 37:400–408
Husseneder C, Simms DM, Delatte JR et al (2012) Genetic diversity and colony breeding structure in native and introduced ranges of the formosan subterranean termite, Coptotermes formosanus. Biol Invasions 14:419–437
Kaspari M, Vargo EL (1995) Colony size as a buffer against seasonality Bergmann’s rule in social insects. Am Nat 145:610–632
Korb J, Hartfelder K (2008) Life history and development: a framework for understanding developmental plasticity in lower termites. Biol Rev 83:295–313
Kusaka A, Matsuura K (2017) Allee effect in termite colony formation: influence of alate density and flight timing on pairing success and survivorship. Insec Soc 65:17–24. https://doi.org/10.1007/s00040-017-0580-9
Landguth EL, Cushman SA, Schwartz MK et al (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191
Lee S-H, Su N-Y, Bardunias P (2007) Exploring landscape structure effect on termite territory size using a model approach. Biosystems 90:890–896
Leniaud L, Pichon A, Uva P, Bagnères A-G (2009) Unicoloniality in Reticulitermes urbis: a novel feature in a potentially invasive termite species. Bull Entomol Res 99:1–10
Leniaud L, Darrouzet E, Dedeine F et al (2011) Ontogenic potentialities of the worker caste in two sympatric subterranean termites in France. Evol Dev 13:138–148
Lenz M, Kard B, Evans TA et al (2009) Differential use of identical food resources by Reticulitermes flavipes (Isoptera : Rhinotermitidae ) in two types of habitats. Entomol Soc Am 38:35–42
Lohou C, Burban G, Clément J-L (1997) Protection des arbres d’alignement contre les termites souterrains: l’expérience menée à Paris. Phytoma - la défense des végétaux 492:42–44
Long C, Thorne BL (2006) Resource fidelity, brood distribution and foraging dynamics in complete laboratory colonies of Reticulitermes flavipes (Isoptera: Rhinotermitidae). Ethol Ecol Evol 18:113–125
Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197
Matsuura K, Himuro C, Yokoi T, Yamamoto Y, Vargo EL, Keller L (2010) Identification of a pheromone regulating caste differentiation in termites. PNAS 107(29):12963–12968
McDonnell MJ, Hahs AK (2015) Adaptation and adaptedness of organisms to urban environments. Annu Rev Ecol Evol Syst 46:261–280
McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 27:247–206
McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11:161–176
McRae BH (2006) Isolation by resistance. Evolution 60:1551–1561
Moller H (1996) Lessons for invasion theory from social insects. Biol Conserv 78:125–142
Møller AP (2009) Successful city dwellers: a comparative study of the ecological characteristics of urban birds in the western Palearctic. Oecologia 159:849–858
Nei M (1987) Molecular evolutionary genetics. Columbia university press, New York
Nobre T, Nunes L, Bignell DE (2008) Colony interactions in Reticulitermes grassei population assessed by molecular genetic methods. Insect Soc 55:66–73
Paulmier I, Vauchot B, Pruvost A, et al (1997) Evaluation of two populations of Reticulitermes santonensis Feytaud (Isoptera) by triple mark-recapture procedure. In: 28th Annual meeting of the international group of wood preservation. Whistler, pp 25–30
Pecheux J (1975) L’Age d’or du rail Européen 1850–1900. Berger-Lev, Paris, p 253
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. Insect Soc 57:393–402
Perdereau E, Dedeine F, Christidès J-P et al (2011) Competition between invasive and indigenous species : an insular case study of subterranean termites. Biol Invasions 13:1457–1470
Perdereau E, Bagnères A-G, Bankhead-Dronnet S et al (2013) Global genetic analysis reveals the putative native source of the invasive termite, Reticulitermes flavipes, in France. Mol Ecol 22:1105–1119
Perdereau E, Bagnères A-G, Vargo EL et al (2015) Relationship between invasion success and colony breeding structure in a subterranean termite. Mol Ecol 24:2125–2142
Pichon A, Kutnik M, Leniaud L et al (2007) Development of experimentally orphaned termite worker colonies of two Reticulitermes species (Isoptera : Rhinotermitidae). Sociobiology 50:1015–1034
Pumain D (2012) Une théorie géographique pour la loi de Zipf. Région et Développement 36:31–54
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and Ecumenicism. J Hered 86:248–249
Rust MK, Su N (2012) Managing social insects of urban importance. Annu Rev Entomol 57:355–375
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
Spear SF, Storfer A (2010) Anthropogenic and natural disturbance lead to differing patterns of gene flow in the Rocky Mountain tailed frog, Ascaphus montanus. Biol Conserv 143:778–786
Su N-Y, Scheffrahn RH (1990) Economically important termites in the United States and their control. Sociobiology 17:77–94
Su N-Y, Ban PM, Scheffrahn RH (1993) Foraging populations and territories of the eastern subterranean termite (Isoptera: Rhinotermitidae) in southeastern Florida. Entomol Sci 22:1113–1117
Sukopp H (2008) On the early history of urban ecology in Europe. In: Marzluff J, Shulenberger E, Endlicher W et al (eds) Urban ecology. An international perspective on the interaction between humans and nature. Springer Science + Business Media, New York, pp 79–97
Suppo C, Robinet C, Perdereau E, Andrieu D, Bagnères AG (2017) Potential spread of the invasive North American termite, Reticulitermes flavipes, and the impact of climate warming. Biol Invasions :1–18. https://doi.org/10.1007/s10530-017-1581-3
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
Vargo EL (2000) Polymorphism at trinucleotide microsatellite loci in the subterranean termite Reticulitermes flavipes. Mol Ecol 9:817–820
Vargo EL (2003) Hierarchical analysis of colony and population genetic structure of the eastern subterranean termite, Reticulitermes flavipes, using two classes of molecular markers. Evolution 57:2805–2818
Vargo EL, Carlson JR (2006) Comparative study of breeding systems of sympatric subterranean termites (Reticulitermes flavipes and R. hageni) in central North Carolina using two classes of molecular genetic markers. Environ Entomol 35:173–187
Vargo EL, Husseneder C (2009) Biology of subterranean termites: insights from molecular studies of Reticulitermes and Coptotermes. Annu Rev Entomol 54:379–403
Vargo EL, Husseneder C, Grace JK (2003) Colony and population genetic structure of the formosan subterranean termite, Coptotermes formosanus, in Japan. Mol Ecol 12:2599–2608
Vargo EL, Leniaud L, Swoboda LE et al (2013) Clinal variation in colony breeding structure and level of inbreeding in the subterranean termites Reticulitermes flavipes and R. grassei. Mol Ecol 22:1447–1462
Vieau F (1993) Le termite de Saintonge Reticulitermes santonensis Feytaud: Termite urbain. Bull Société Zool Fr 118:125–133
Vieau F (2001) Comparison of the spatial distribution and reproductive cycle of Reticulitermes santonensis Feytaud and Reticulitermes lucifugus grassei Clément (Isoptera, Rhinotermitidae) suggests that they represent introduced and native species, respectively. Insect Soc 48:57–62
Vitousek P, Mooney H, Lubchenko J, Melillo J (1997) Human domination of earth’s ecosystems. Science 277(80):494–499
Wasserman TN, Cushman SA, Schwartz MK, Wallin DO (2010) Spatial scaling and multi-model inference in landscape genetics : Martes americana in northern Idaho. Landsc Ecol 25:1601–1612
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wilkinson GN, Rogers CE (1973) Symbolic descriptions of factorial models for analysis of variance. Appl Stat 22:392–399
Williams NSG, Hahs AK, Vesk PA (2015) Urbanisation, plant traits and the composition of urban floras. Perspect Plant Ecol Evol Syst 17:78–86
Wright S (1969) Evolution and the genetics of populations, vol 2. The theory of gene frequencies. University of Chicago Press, Chicago
Acknowledgements
This study is part of G. Baudouin’s PhD research. We are grateful to Simon Dupont for providing samples. We are also grateful to Tony Dié and Matthieu Vachon of Pharmabois for providing some of the 2016 samples. We wish to thank Claude Marès and Sylvain Genty of Paris City Hall for sharing their knowledge about termite in Paris. We also wish to thank J. Pearce for her English editing services, Dominique Andrieu for his comments on the first draft of the manuscript, and Stephanie Bankhead-Dronnet and Christelle Suppo for their helpful comments. This work was funded by a contract (to A-G Bagnères) that was established between the French National Center for Scientific Research (CNRS) and the city of Paris (Direction du Logement et de l’Habitat).
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Baudouin, G., Bech, N., Bagnères, AG. et al. Spatial and genetic distribution of a north American termite, Reticulitermes flavipes, across the landscape of Paris. Urban Ecosyst 21, 751–764 (2018). https://doi.org/10.1007/s11252-018-0747-9
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DOI: https://doi.org/10.1007/s11252-018-0747-9
Keywords
- Urban pest
- Landscape genetics
- Human-mediated dispersal
- Biological invasions
- Breeding structure