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Rapid increase of the parasitic fungus Laboulbenia formicarum in supercolonies of the invasive garden ant Lasius neglectus

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Abstract

A key feature among invasive ant species is their ability to dominate vast areas by forming dense networks of connected nests in contrast to the smaller and discrete, spatially dispersed colonies of most social insects. However, it was recently proposed that such supercolonies are more vulnerable to infection by parasites and diseases as they would serve as large targets with high rates of transmission from nests to nest. We studied the invasive garden ant Lasius neglectus, a pest species currently spreading throughout Europe. Several populations are infected with an ectoparasitic fungus, Laboulbenia formicarum, itself an introduced species, yielding a new host–parasite relationship. Long-term monitoring of the prevalence and intensity of infection in two populations (supercolonies) over 4–10 years revealed epizootic spread of the parasite with a 14 % annual increase in prevalence until ca. 80 % of all ants were infected. In contrast, no other local ant species with discrete colonies carried the parasite, although a local species (Lasius niger) proved susceptible in a cross-infection experiment. These results support the hypothesis that supercolonies potentially face an important challenge from parasites and diseases, with interesting perspectives for biological control of such ant species.

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References

  • Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package version 0.999375-42. http://CRAN.R-project.org/package=lme4

  • Báthori F, Csata E, Tartally A (2015) Rickia wasmannii increases the need for water in Myrmica scabrinodis (Ascomycota: Laboulbeniales; Hymenoptera: Formicidae). J Invertebr Pathol 126:78–82

    Article  PubMed  Google Scholar 

  • Bretz F, Hothorn T, Westfall P (2011) Multiple comparisons using R. CRC Press, Boca Raton

    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 

  • Core Team R (2014) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Cremer S et al (2008) The evolution of invasiveness in garden ants. PLoS One 3:e3838

    Article  PubMed Central  PubMed  Google Scholar 

  • Csata E, Erős K, Markó B (2014) Effects of the ectoparasitic fungus Rickia wasmannii on its ant host Myrmica scabrinodis: changes in host mortality and behavior. Insectes Soc 61:247–252

  • De Kesel A (1993) Relations between host population density and spore transmission of Laboulbenia slackensis (Ascomycetes, Laboulbeniales) from Pogonus chalceus (Coleoptera, Carabidae). Belg J Bot 126:155–163

    Google Scholar 

  • Espadaler X, Santamaria S (2012) Ecto- and endoparasitc fungi on ants from the Holarctic region. Psyche Article ID 168478

  • Espadaler X, Lebas C, Wagenknecht J, Tragust S (2011) Laboulbenia formicarum (Ascomycota, Laboulbeniales), an exotic parasitic fungus, on an exotic ant in France. Vie Milieu 61:41–44

    Google Scholar 

  • Flory SL, Clay K (2013) Pathogen accumulation and long-term dynamics of plant invasions. J Ecol 101:607–613

    Article  Google Scholar 

  • Fuxa JR, Sokolova YY, Milks ML, Richter AR, Williams DF, Oi DH (2005) Prevalence, spread, and effects of the microsporidium Thelohania solenopsae released into populations with different social forms of the red imported fire ant (Hymenoptera: Formicidae). Environ Entomol 34:1139–1149

    Article  Google Scholar 

  • Hanna C, Cook ED, Thompson AR, Dare LE, Palaski AL, Foote D, Goodisman MAD (2014) Colony social structure in native and invasive populations of the social wasp Vespula pensylvanica. Biol Invasions 16:283–294

    Article  Google Scholar 

  • Helanterä H, Strassmann JE, Carrillo J, Queller DC (2009) Unicolonial ants: where do they come from, what are they and where are they going? Trends Ecol Evol 24:341–349

    Article  PubMed  Google Scholar 

  • Herraiz JA, Espadaler X (2007) Laboulbenia formicarum (Ascomycota: Laboubleniales) reaches the Mediterranean. Sociobiology 50:449–455

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Hughes DP, Pierce NE, Boomsma JJ (2008) Social insect symbionts: evolution in homeostatic fortresses. Trends Ecol Evol 23:672–677

    Article  PubMed  Google Scholar 

  • Konrad M, Grasse AV, Tragust S, Cremer S (2015) Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host. Proc R Soc Lond B Biol Sci 282:20141976

    Article  Google Scholar 

  • Leniaud L, Pichon A, Uva P, Bagnères AG (2009) Unicoloniality in Reticulitermes urbis: a novel feature in a potentially invasive termite species. Bull Entomol Res 99:1–10

    Article  CAS  PubMed  Google Scholar 

  • Mitchell CE, Blumenthal D, Jarosik V, Puckett EE, Pysek P (2010) Controls on pathogen species richness in plants’ introduced and native ranges: roles of residence time, range size and host traits. Ecol Lett 13:1525–1535

    Article  PubMed Central  PubMed  Google Scholar 

  • Moller H (1996) Lessons for invasion theory from social insects. Biol Conserv 78:125–142

    Article  Google Scholar 

  • Myers JH, Simberloff D, Kuris AM, Carey JR (2000) Eradication revisited: dealing with exotic species. Trends Ecol Evol 15:316–320

    Article  PubMed  Google Scholar 

  • Nuhn TP, Van Dyke CG (1979) Laboulbenia formicarum Thaxter (Ascomycotina: Laboulbeniales) on ants (Hymenoptera: Formicidae) in Raleigh, North Carolina with a new host record. Proc Entomol Soc Wash 81:101–104

    Google Scholar 

  • Pedersen JS, Krieger MJ, Vogel V, Giraud T, Keller L (2006) Native supercolonies of unrelated individuals in the invasive Argentine ant. Evolution 60:782–791

    Article  PubMed  Google Scholar 

  • Raak-van den Berg CL, van Wielink PS, de Jong PW, Gort G, Haelewaters D, Helder J, van Lenteren JC (2014) Invasive alien species under attack: natural enemies of Harmonia axyridis in the Netherlands. Biocontrol 59:229–240

    Article  Google Scholar 

  • Rust MK, Su NY (2012) Managing social insects of urban importance. Annu Rev Entomol 57:355–375

    Article  CAS  PubMed  Google Scholar 

  • Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton

    Google Scholar 

  • Schneider SS, DeGrandi-Hoffman G, Smith DR (2004) The African honey bee: factors contributing to a successful biological invasion. Annu Rev Entomol 49:351–376

    Article  CAS  Google Scholar 

  • Shapiro-Ilan DI, Bruck DJ, Lacey LA (2012) Principles of epizootiology and microbial control. In: Vega FE, Kaya HK (eds) Insect pathology. Academic Press, London, pp 91–201

    Google Scholar 

  • Silverman J, Brightwell RJ (2008) The Argentine ant: challenges in managing an invasive unicolonial pest. Annu Rev Entomol 53:231–252

    Article  CAS  PubMed  Google Scholar 

  • Simberloff D, Gibbons L (2004) Now you see them, now you don’t!—population crashes of established introduced species. Biol Invasions 6:161–172

    Article  Google Scholar 

  • Ugelvig LV, Cremer S (2012) Effects of social immunity and unicoloniality on host–parasite interactions in invasive insect societies. Funct Ecol 26:1300–1312

    Article  Google Scholar 

  • Ugelvig LV, Drijfhout FP, Kronauer DJC, Boomsma JJ, Pedersen JS, Cremer S (2008) The introduction history of invasive garden ants in Europe: integrating genetic, chemical and behavioural approaches. BMC Biol 6:11–25

    Article  PubMed Central  PubMed  Google Scholar 

  • Vogel V, Pedersen JS, d’Ettorre P, Lehmann L, Keller L (2009) Dynamics and genetic structure of Argentine ant supercolonies in their native range. Evolution 63:1627–1639

    Article  CAS  PubMed  Google Scholar 

  • Weir A, Blackwell M (2005) Fungal biotrophic parasites of insects and other arthropods. In: Vega FE, Blackwell M (eds) Insect–fungal associations: ecology and evolution. Oxford University Press, Oxford, pp 119–145

    Google Scholar 

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Acknowledgments

We thank Nabila Devos, Tim Engelkes, Tatiana Giraud, Sandy Weidlich and Bernard Le Roux for help with ant collection, Martin Otto Schmitt for part of the data acquisition, Pina Brinker and Oliver Otti for discussion, and Jon Shik and four anonymous reviewers for constructive comments on previous versions of the manuscript. This study was partly supported by the Danish National Research Foundation (Grant DNRF57; J.S.P.).

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Correspondence to Simon Tragust.

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Tragust, S., Feldhaar, H., Espadaler, X. et al. Rapid increase of the parasitic fungus Laboulbenia formicarum in supercolonies of the invasive garden ant Lasius neglectus . Biol Invasions 17, 2795–2801 (2015). https://doi.org/10.1007/s10530-015-0917-0

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