Abstract
An important requirement for the management of invasive species is to identify the biological and ecological factors that influence the ability of such species to become established and spread within a new environment. Although competition is one of the key interactions determining the coexistence of species and exclusion, few studies directly examine the mechanism of competitive interactions within invasive communities. This study focused on putative competition in a social insect invader, R. flavipes, an American termite introduced into France, and an indigenous European termite, R. grassei. We first characterized and mapped a zone of sympatry between these two species. We then evaluated the degree of direct and indirect competition by comparing several life-history traits: behavioral aggression, chemical recognition and dispersion modes. Interspecific competition revealed that R. flavipes was dominant over R. grassei. Intraspecific competition was not found in R. flavipes while it appeared in varying degrees in R. grassei. These findings seemed to be correlated with the remarkable chemical homogeneity found in R. flavipes in comparison with R. grassei. Genetic analyses revealed that R. flavipes foraged over a greater distance than R. grassei colonies and might suggest a difference in the capacity to produce secondary reproductives. These findings suggest that R. flavipes has a significant advantage owing to competitive asymmetry that may enable the species to become dominant. The interspecific superiority, lack of intraspecific aggression and large extensive colonies, seem to be some of the reasons for its invasive success.
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Bagnères A-G, Clément J-C, Blum MS, Severson RF, Joulie C, Lange C (1990) Cuticular hydrocarbons and defensive compounds of Reticulitermes flavipes (Kollar) and R. santonensis (Feytaud): polymorphism and chemotaxonomy. J Chem Ecol 16:3213–3244
Bagnères A-G, Killian A, Clément J-L, Lange C (1991) Interspecific recognition among termites of the genus Reticulitermes: evidence for a role for the cuticular hydrocarbons. J Chem Ecol 17:2397–2420
Begon M, Harper JL, Townsend CR (1990) Ecology: individuals populations and communities. Blackwell Scientific, Boston
Blomquist GJ, Bagnères A-G (2010) Insect hydrocarbons: biology biochemistry and chemical ecology. Cambridge University Press, Cambridge
Bourke AFG, Francks NR (1995) Social evolution in ants. Princeton Univ Press, Princeton
Brandt M, Van Wilgenburg E, Tsutsui ND (2009) Global-scale analyses of chemical ecology and population genetics in the invasive Argentine ant. Mol Ecol 18:997–1005
Bulmer MS, Adams ES, Traniello JFA (2001) Variation in colony structure in the subterranean termite Reticulitermes flavipes. Behav Ecol Sociobiol 49:236–243
Byers JE (2000) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81:1225–1239
Cheng XY, Xie PZ, Cheng FX, Xu RM, Xie BY (2009) Competitive displacement of the native species Bursaphelenchus mucronatus by an alien species Bursaphelenchus xylophilus (Nematoda: Aphelenchida: Aphelenchoididae): a case of successful invasion. Biol Invasions 11:205–213
Clément J-L (1977) Ecologie des Reticulitermes (Holmgren) français (Isoptères). Position systématique des populations. Bull Soc Zool Fr 102:169–185
Clément J-L (1986) Open and closed societies in Reticulitermes termites (Isoptera, Rhinotermitidae): geographic and seasonal variations. Sociobiol 11:311–323
Clément J-L, 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
Cornelius ML, Osbrink WLA (2009) Bioassay design and length of time in the laboratory affect intercolonial interactions of the Formosan subterranean termite (Isoptera, Rhinotermitidae). Insectes Soc 56:203–211
Davis MA (2003) Biotic globalization: does competition from introduced species threaten biodiversity? Bioscience 53:481–489
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 13:431–441
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
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, 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
Feytaud DJ (1924) Le termite de Saintonge. Comptes-Rendus de l’Académie des Sciences 171:203–205
Fournier D, Biseau JC, Aron S (2009) Genetics, behaviour and chemical recognition of the invading ant Pheidole megacephala. Mol Ecol 18:186–199
Gause GF (1934) The struggle for existence. Williams and Wilkins, Baltimore
Gherardi F, Daniels WH (2004) Agonism and shelter competition between invasive and indigenous crayfish species. Can J Zool 82:1923–1932
Ghesini S, Messenger MT, Pilon N, Marini M (2010) First report of Reticulitermes flavipes (Isoptera: Rhinotermitidae) in Italy. Fla Entomol 93:327–328
Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci USA 99:6075–6079
Goudet J (1995) FSTAT (vers 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Grace JK (1996) Absence of overt agonistic behavior in a northern population of Reticulitermes flavipes (Isoptera: Rhinotermitidae). Sociobiol 28:103–110
Grube S, Forschler BT (2004) Census of monogyne and polygyne laboratory colonies illuminates dynamics of population growth in Reticulitermes flavipes (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 97:466–475
Hardin G (1960) Competitive exclusion principle. Science 131:1292–1297
Hayashi Y, Kitade O, Kojima JI (2002) Microsatellite loci in the Japanese subterranean termite, Reticulitermes speratus. Mol Ecol Notes 2:518–520
Holway DA (1999) Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecology 80:238–251
Holway DA, Suarez AV (1999) Animal behavior: an essential component of invasion biology. Trends Ecol Evol 14:328–330
Holway DA, Lach L, Suarez AV, Case TJ (1998) Loss of intraspecific aggression in the success of a widespread invasive social insect. Science 282:949–952
Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233
Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393
Hu XP, Zhu F (2003) Aggressive relationship between two subterranean termites. Acta Zool Sinica 49:296–302
Husseneder C, Grace JK (2001) Evaluation of DNA fingerprinting, aggression tests and morphometry as tools for colony delineation of the Formosan subterranean termite. J Insect Behav 14:173–186
Husseneder C, Messenger MT, Su N-Y, Grace JK, Vargo EL (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
Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314
Jones SC, Trosset MW (1991) Interference competition in desert subterranean termites. Entomol Exp Appl 61:83–90
Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204
Korb J, Heinze J (2008) Ecology of social evolution. Springer, Berlin
Kutnik M, Uva P, Brinkworth L, Bagnères A-G (2004) Phylogeography of two European Reticulitermes (Isoptera) species: the Iberian refugium. Mol Ecol 13:3099–3113
Lalzar I, Simon T, Meer RKV, Hefetz A (2010) Alteration of cuticular hydrocarbon composition affects heterospecific nestmate recognition in the carpenter ant Camponotus fellah. Chemoecol 20:19–24
Le Breton J, Delabie JHC, Chazeau J, Dejean A, Jourdan H (2004) Experimental evidence of large-scale unicoloniality in the tramp ant Wasmannia auropunctata (Roger). J Insect Behav 17:263–271
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, Dedeine F, Pichon A, Dupont S, Bagnères A-G (2010) Geographical distribution, genetic diversity and social organization of a new European termite, Reticulitermes urbis (Isoptera: Rhinotermitidae). Biol Invasions 12:1389–1402
Leniaud L, Darrouzet E, Dedeine F, Ahn K, Huang Z, Bagnères A-G (2011) Ontogenic potentialities of the worker caste in two subterranean termites in France. Evol Dev 13(2) (in press)
Lenz M, Barrett RA (1982) Neotenic formation in field colonies of Coptotermes lacteus (Froggatt) in Australia, with comments on the roles of neotenics in the genus Coptotermes (Isoptera, Rhinotermitidae). Sociobiol 7:47–59
Lorenzi MC, Bagnères A-G, Clément J-L, Turillazzi S (1997) Polistes biglumis bimaculatus epicuticular hydrocarbons and nestmate recognition (Hymenoptera, Vespidae). Insectes Soc 44:123–138
Lowe S, Browne M, Boudjelas S, De Poorter M (2001) 100 of the world’s worst invasive alien species: a selection from the global invasive species database. Species Survival Commission. World Conservation Union, New Zealand
McNatty A, Abbott KL, Lester PJ (2009) Invasive ants compete with and modify the trophic ecology of hermit crabs on tropical islands. Oecologia 160:187–194
Messenger MT, Su NY (2005) Agonistic behavior between colonies of the Formosan subterranean termite (Isoptera: Rhinotermitidae) from Louis Armstrong Park, New Orleans, Louisiana. Sociobiol 45:331–345
Moller H (1996) Lessons for invasion theory from social insects. Biol Conserv 78:125–142
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. Insectes Soc 55:66–73
Noirot C (1959) Reparques sur l’écologie des termites. Soc R Zool Belg 89:151–169
O’Dowd DJ, Green PT, Lake PS (2003) Invasional ‘meltdown’ on an oceanic island. Ecol Lett 6:812–817
Paini DR, Funderburk JE, Reitz SR (2008) Competitive exclusion of a worldwide invasive pest by a native. Quantifying competition between two phytophagous insects on two host plant species. J Anim Ecol 77:184–190
Perdereau E, Bagnères A-G, Dupont S, Dedeine F (2010a) High occurrence of colony fusion in a European population of the American termite Reticulitermes flavipes. Insectes Soc 57:393–402
Perdereau E, Dedeine F, Christidès J-P, Bagnères A-G (2010b) Variations in worker cuticular hydrocarbons and soldier isoprenoid defensive secretions within and among introduced and native populations of the subterranean termite, Reticulitermes flavipes. J Chem Ecol 36:1189–1198
Petren K, Case TJ (1996) An experimental demonstration of exploitation competition in an ongoing invasion. Ecology 77:118–132
Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275
Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283
Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Biodiversity—global biodiversity scenarios for the year 2100. Science 287:1770–1774
Sambrook J, Fritcsh EF, Maniatis T (1989) Molecular cloning. 2nd Ed. Cold Spring Harbor Lab Press, Cold Spring Harbor
Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176
Shinen JS, Morgan SG (2009) Mechanisms of invasion resistance: competition among intertidal mussels promotes establishment of invasive species and displacement of native species. Mar Ecol Prog Ser 383:187–197
Suarez AV, Holway DA, Liang D, Tsutsui ND, Case TJ (2002) Spatiotemporal patterns of intraspecific aggression in the invasive Argentine ant. Anim Behav 64:697–708
Thorne BL, Haverty MI (1991) A review of intracolony, intraspecific, and interspecific agonism in termites. Sociobiol 19:115–145
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 9:817–829
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, 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, Woodson D, Waldvogel MG, Grace JK (2006) Genetic analysis of colony and population genetic structure of three introduced populations of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in the Continental United States. Environ Entomol 35:151–166
Vauchot B, Provost E, Bagnères A-G, Clément J-L (1996) Regulation of the chemical signatures of two termite species, Reticulitermes santonensis and Reticulitermes lucifugus grassei, living in mixed experimental colonies. J Insect Physiol 42:309–321
Vieau F (1993) Le termite de Saintonge Reticulitermes santonensis Feytaud: termite urbain. Bull Soc 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. Insectes Soc 48:57–62
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wood TG, Lee KE (1971) Abundance of mounts and competition among colonies of some Australian termite species. Pedobiologia 11:341–366
Acknowledgments
We would like to thank Marjorie Labedan for her help as genetic assistant. We are grateful to Yann Bourgeois, Maxime Traineau and Jérémy Dion for their help in behavioral tests. We also wish to thank Tony Tebby for helping to improve the English of the manuscript. This work was part funded by a CNRS-PICS grant.
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Perdereau, E., Dedeine, F., Christidès, JP. et al. Competition between invasive and indigenous species: an insular case study of subterranean termites. Biol Invasions 13, 1457–1470 (2011). https://doi.org/10.1007/s10530-010-9906-5
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DOI: https://doi.org/10.1007/s10530-010-9906-5