Biological Invasions

, Volume 21, Issue 12, pp 3491–3504 | Cite as

Linking thermo-tolerances of the highly invasive ant, Wasmannia auropunctata, to its current and potential distribution

  • Carolina Coulin
  • Gerardo J. de la Vega
  • Lucila Chifflet
  • Luis A. CalcaterraEmail author
  • Pablo E. SchilmanEmail author
Original Paper


Species distribution models based on the correlation of bioclimatic variables and presence spatial data-points are useful for recognizing species habitat suitability. However, they have limitations in predicting the introduced ranges of invasive species that could be overcome by using species eco-physiological traits. By combining bioclimatic variables with thermal tolerance plasticity of the highly invasive little fire ant, Wasmannia auropunctata, we intend to better understand the mechanism underlying its current and future distributions. To this end, we performed: (1) laboratory physiological experiments to assess thermal tolerances (CTmin and CTmax) and evaluate the effect of acclimation (laboratory) and acclimatization (nature) on these variables, (2) behavioral foraging observations in the field, (3) a correlative and a simple mechanistic SDM. Briefly, physiological results showed a modulation of the CTmax and CTmin by different acclimation temperatures and by seasonal thermal acclimatization. In the field, worker foraging activity begins at environmental temperatures just above (less than 1 °C) the lowest CTmin recorded in the laboratory. At the global scale, CTmin constitutes a key physiological trait that, when linked with the minimum temperature of the coldest month, could explain the southernmost limit of W. auropunctata native distribution and its physiological capacity to expand in the Mediterranean region. The eco-physiological approach carried out here may help explain the current distribution and predict potential spread of populations when there is no certain information about the whole distribution of the species or under a changing environment. The latter is of great importance especially when analyzing invasive insects, pests or disease vectors.


Acclimation temperature CTmax and CTmin Eco-physiology Foraging activity Invasive ant distribution Thermo-tolerance plasticity 



Species distribution model


Critical thermal maximum


Critical thermal minimum


Variance inflation factor


Upper lethal temperature


Lower lethal temperature



The authors thanks Ed LeBrun, Erin Wilson-Rankin and Rodrigo Diaz for critical reading of an earlier version of the manuscript and Agencia Nacional de Promoción Científica y Técnica/Argentina (PICT2015-3491 to LC and PES) and U.S. Pacific Basin Agricultural Research Center, USDA-ARS for financial support. CC, GJdlV and LC have a PhD fellowship and PES and LAC are researchers from Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina. We also would like to thank two anonymous reviewers and the Editor for helpful suggestions that improved the manuscript.

Author contributions

CC, LAC and PES conceived the ideas and designed methodology. CC, LC and LAC collected the colonies. CC collected laboratory data. CC and GJdlV collected field data. GJdlV performed SDM. CC and GJdlV analysed the data. LAC and PES contributed reagents/materials. CC and PES led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Supplementary material

10530_2019_2063_MOESM1_ESM.pdf (875 kb)
Supplementary material 1 (PDF 875 kb)


  1. Addo-Bediako A, Chown SL, Gaston KJ (2000) Thermal tolerance, climatic variability and latitude. Proc R Soc B 267:739–745CrossRefPubMedPubMedCentralGoogle Scholar
  2. Araújo MB, Peterson AT (2012) Uses and misuses of bioclimatic envelope modelling. Ecology 93:1527–1539CrossRefPubMedPubMedCentralGoogle Scholar
  3. Araújo MB, Ferri-Yáñez F, Bozinovic F, Marquet P, Valladares F, Chown SL (2013) Heat freezes niche evolution. Ecol Lett 16:1206–1219CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ayrinhac A, Debat V, Gibert P, Kister A-G, Legout H, Moreteau B, Vergilino R, David JR (2004) Cold adaptation in geographical populations of Drosophila melanogaster: phenotypic plasticity is more important than genetic variability. Funct Ecol 18:700–706CrossRefGoogle Scholar
  5. Bewick S, Stuble KL, Lessard JP, Dunn RR, Adler FR, Sanders NJ (2014) Predicting future coexistence in a North American ant community. Ecol Evol 4:1804–1819CrossRefPubMedPubMedCentralGoogle Scholar
  6. Byrne MJ, Coetzee J, McConnachie AJ, Parasram W, Hill MP (2004) Predicting climate compatibility of biological control agents in their region of introduction. In: Cullen JM, Briese DT, Kriticos DJ, Lonsdale WM, Morin L, Scott JK (eds) Proceedings of the XI international symposium on biological control of weeds, pp 351–352Google Scholar
  7. Calosi P, Bilton DT, Spicer JI (2008) Thermal tolerance, acclimatory capacity and vulnerability to global climate change. Biol Lett 4:99–102CrossRefPubMedPubMedCentralGoogle Scholar
  8. Calosi P, Bilton DT, Spicer JI, Votier SC, Atfield A (2010) What determines a species’ geographical range? Thermal biology and latitudinal range size relationships in European diving beetles (Coleoptera: Dytiscidae). J Anim Ecol 79:194–204. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cerdá X (2001) Behavioural and physiological traits to thermal stress tolerance in two Spanish desert ants. Etología 9:15–27Google Scholar
  10. Cerdá X, Retana J, Cros S (1998) Critical thermal limits in Mediterranean ant species: trade-off between mortality risk and foraging performance. Funct Ecol 12:45–55CrossRefGoogle Scholar
  11. Chanthy P, Martin RJ, Gunning RV, Andrew NR (2012) The effects of thermal acclimation on lethal temperatures and critical thermal limits in the green vegetable bug, Nezara viridula (L. (Hemiptera: Pentatomidae). Front Physiol 3:465CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chifflet L, Rodriguero MS, Calcaterra LA, Rey O, Dinghi PA, Baccaro FB, Souza JL, Follett P, Confalonieri VA (2016) Evolutionary history of the little fire ant Wasmannia auropunctata before global invasion: inferring dispersal patterns, niche requirements, and past and present distribution within its native range. J Evol Biol 29(4):790–809. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chifflet L, Guzmán NV, Rey O, Confalonieri VA, Calcaterra LA (2018) Southern expansion of the invasive ant Wasmannia auropunctata within its native range and its relation with clonality and human activity. PLoS ONE 13(11):e0206602CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chown SL, Nicolson SW (2004) Insect physiological ecology: mechanisms and patterns. Oxford University Press, OxfordCrossRefGoogle Scholar
  15. Clark DB, Guayasamin C, Pazmino O, Donoso C, Paez de Villacis Y (1982) The tramp ant Wasmannia auropunctata: autecology and effects on ant diversity and distribution on Santa Cruz Island, Galapagos. Biotropica 14:196–207CrossRefGoogle Scholar
  16. Cuezzo F, Calcaterra L, Chifflet L, Follet P (2015) Wasmannia Forel (Hymenoptera: Formicidae: Myrmicinae) in Argentina: systematics and distribution. Sociobiology 62:246–265Google Scholar
  17. Cunningham HR, Rissler LJ, Buckley LB, Urbanet MC (2015) Abiotic and biotic constraints across reptile and amphibian ranges. Ecography 38:001–008CrossRefGoogle Scholar
  18. David JR, Gibert P, Moreteau B, Gilchrist GW, Huey RB (2003) The fly that came in from the cold: geographic variation of recovery time from low-temperature exposure in Drosophila subobscura. Funct Ecol 17:425–430CrossRefGoogle Scholar
  19. de la Vega GJ, Schilman PE (2017) Using ecophysiological traits to understand the Realized Niche: the role of desiccation tolerance in Chagas disease vectors. Oecologia 185:607–618. CrossRefPubMedPubMedCentralGoogle Scholar
  20. de la Vega GJ, Schilman PE (2018) Ecological and physiological thermal niches in vectors of Chagas disease. Med Vet Entomol 32:1–13. CrossRefGoogle Scholar
  21. de la Vega GJ, Medone P, Ceccarelli S, Rabinovich J, Schilman PE (2015) Geographical distribution, climatic variability and thermo-tolerance of Chagas disease vectors. Ecography 38:851–860. CrossRefGoogle Scholar
  22. Delsinne TD, Roisin Y, Leponce M (2007) Spatial and temporal foraging overlaps in a Chacoan ground-foraging ant assemblage. J Arid Environ 71:29–44CrossRefGoogle Scholar
  23. Diamond SE, Sorger DM, Hulcr J, Pelini SL, Del Toro I, Hirsch C, Oberg E, Dunn RR (2012) Who likes it hot? A global analysis of the climatic, ecological, and evolutionary determinants of warming tolerance in ants. Global Change Biol 18:448–456CrossRefGoogle Scholar
  24. Elith J, Kearney M, Phillips S (2010) The art of modelling range-shifting species. Methods Ecol Evol 1:330–342CrossRefGoogle Scholar
  25. Espadaler X, Pradera C, Santana JA (2018) The first outdoor-nesting population of Wasmannia auropunctata in continental Europe (Hymenoptera, Formicidae). Iberomyrmex 10:1–8Google Scholar
  26. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282CrossRefPubMedPubMedCentralGoogle Scholar
  27. Fitzpatrick MC, Weltzin JF, Sanders NJ, Dunn RR (2007) The biogeography of prediction error: why does the introduced range of the fire ant over-predict its native range? Global Ecol Biogeogr 16:24–33CrossRefGoogle Scholar
  28. Foucaud J, Rey O, Robert S, Crespin L, Orivel J, Facon B, Loiseau A, Jourdan H, Kenne M, Masse PS, Tindo M, Vonshak M, Estoup A (2013) Thermotolerance adaptation to human-modified habitats occurs in the native range of the invasive ant Wasmannia auropunctata before long-distance dispersal. Evol Appl 6:721–734. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Gaston K, Blackburn T (2000) Pattern and process in macroecology. Blackwell, OxfordCrossRefGoogle Scholar
  30. Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8:993–1009CrossRefGoogle Scholar
  31. Hijmans RJ, Elith J (2012) dismo: species distribution modeling. R package version 0.7-2. Accessed 23 Sept 2018
  32. Hill M, Hoffmann A, Macfadyen S, Umina P, Elith J (2012) Understanding niche shifts: using current and historical data to model the invasive redlegged earth mite, Halotydeus destructor. Divers Distrib 18(2):191–203CrossRefGoogle Scholar
  33. Hoffmann AA, Shirriffs J, Scott M (2005) Relative importance of plastic vs genetic factors in adaptive differentiation: geographical variation for stress resistance in Drosophila melanogaster from eastern Australia. Funct Ecol 19:222–227CrossRefGoogle Scholar
  34. Kaspari M, Clay NA, Lucas J, Yanoviak SP, Kay A (2015) Thermal adaptation generates a diversity of thermal limits in a rainforest ant community. Global Change Biol 21(3):1092–1102CrossRefGoogle Scholar
  35. Kearney M, Porter WP (2009) Mechanistic niche modelling: combining physiological and spatial data to predict species’ ranges. Ecol Lett 12:334–350CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kumar S, LeBrun EG, Stohlgren TJ, Stabach JA, McDonald DL, Oi DH, LaPolla JS (2015) Evidence of niche shift and global invasion potential of the Tawny Crazy ant, Nylanderia fulva. Ecol Evol 5:4628–4641CrossRefPubMedPubMedCentralGoogle Scholar
  37. Lancaster LT (2016) Widespread range expansions shape latitudinal variation in insect thermal limits. Nat Clim Change 6:618–621. CrossRefGoogle Scholar
  38. MacArthur RH (1972) Geographical ecology: patterns in the distribution of species. Harper and Row, New YorkGoogle Scholar
  39. Mikheyev AS, Mueller UG (2007) Genetic relationships between native and introduced populations of the little fire ant Wasmannia auropunctata. Divers Distrib 13:573–579CrossRefGoogle Scholar
  40. Mitchell JD, Hewitt PH, Van Der Linde TCDK (1993) Critical thermal limits and temperature tolerance in the harvester termite Hodotermes mossambicus (Hagen). J Insect Physiol 39:523–528CrossRefGoogle Scholar
  41. Pearson RG, Dawson TP (2003) Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Global Ecol Biogeogr 12:361–371CrossRefGoogle Scholar
  42. Penick CA, Diamond SE, Sanders NJ, Dunn RR (2017) Beyond thermal limits: comprehensive metrics of performance identify key axes of thermal adaptation in ants. Funct Ecol 31(5):1091–1100CrossRefGoogle Scholar
  43. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259CrossRefGoogle Scholar
  44. Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97CrossRefGoogle Scholar
  45. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  46. Rey O, Estoup A, Vonshak M, Loiseau A, Blanchet S, Calcaterra L, Chifflet L, Rossi JP, Kergoat GJ, Foucaud J, Orivel J, Leponce M, Schultz T, Facon B (2012) Where do adaptive shifts occur during invasion? A multidisciplinary approach to unravelling cold adaptation in a tropical ant species invading the Mediterranean area. Ecol Lett 15:1266–1275CrossRefPubMedPubMedCentralGoogle Scholar
  47. Roger J (1863) Die neu aufgeführten Gattungen und Arten meines Formiciden-Verzeichnisses nebst Ergänzung einiger früher gegebenen Beschreibungen. Berliner Entomologische Zeitschrift 7:131–214CrossRefGoogle Scholar
  48. Roura-Pascual N, Hui C, Ikeda T, Leday G, Richardson DM, Carpintero S, Espadaler X, Gómez C, Guénard B, Hartley S, Krushelnycky P, Lester PJ, McGeoch MA, Menke SB, Pedersen JS, Pitt JP, Reyes J, Sanders NJ, Suarez AV, Touyama Y, Ward D, Ward PS, Worner SP (2011) Relative roles of climatic suitability and anthropogenic influence in determining the pattern of spread in a global invader. Proc Natl Acad Sci USA 108:220–225CrossRefPubMedPubMedCentralGoogle Scholar
  49. Schilman PE, Lightn JRB, Holway DA (2005) Respiratory and cuticular water loss in insects with continuous exchange: comparison across five ant species. J Insect Physiol 51:1295–1305CrossRefPubMedPubMedCentralGoogle Scholar
  50. Schilman PE, Lightn JRB, Holway DA (2007) Water balance in the Argentine ant (Linepithema humile) compared to five native ant species from southern California. Physiol Entomol 32(1):1–7CrossRefGoogle Scholar
  51. Sinclair BJ, Coello Alvarado LE, Ferguson LV (2015) An invitation to measure insect cold tolerance: methods, approaches, and workflow. J Therm Biol 53:180–197CrossRefPubMedPubMedCentralGoogle Scholar
  52. Swets JA (1988) Measuring the accuracy of diagnostic systems. Science 240:1285–1293CrossRefPubMedPubMedCentralGoogle Scholar
  53. Terblanche JS, Chown SL (2006) The relative contributions of developmental plasticity and adult acclimation to physiological variation in the tsetse fly, Glossina pallidipes (Diptera, Glossinidae). J Exp Biol 209:1064–1073CrossRefPubMedPubMedCentralGoogle Scholar
  54. van Heerwaarden B, Kellermann V, Sgrò CM (2016) Limited scope for plasticity to increase upper thermal limits. Funct Ecol 30(12):1947–1956. CrossRefGoogle Scholar
  55. Villemant C, Barbet-Massin M, Perrard A, Muller F, Gargominy O, Jiguet F, Rome Q (2011) Predicting the invasion risk by the alien bee-hawking Yellow-legged hornet Vespa velutina nigrithorax across Europe and other continents with niche models. Biol Conserv 144:2142–2150CrossRefGoogle Scholar
  56. Vonshak M, Dayan T, Ionescu-Hirsh A, Freidberg A, Hefetz A (2010) The little fire ant Wasmannia auropunctata: a new invasive species in the Middle East and its impact on the local arthropod fauna. Biol Invasions 12:1825–1837CrossRefGoogle Scholar
  57. Vonshak M, Dayan T, Hefetz A (2012) Interspecific displacement mechanisms by the invasive little fire ant Wasmannia auropunctata. Biol Invasions 14:851–861CrossRefGoogle Scholar
  58. Wetterer JK (2013) Worldwide spread of the little fire ant, Wasmannia auropunctata (Hymenoptera: Formicidae). Terr Arthropod Rev 6(3):173–184CrossRefGoogle Scholar
  59. Wetterer JK, Porter SD (2003) The little fire ant Wasmannia auropunctata: distribution, impact and control. Sociobiology 42:1–41Google Scholar
  60. Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, BerlinCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Fundación para el Estudio de Especies Invasivas (FuEDEI)Buenos AiresArgentina
  2. 2.Laboratorio de Ecofisiología de Insectos, Departamento de Biodiversidad y Biología Experimental (DBBE), Facultad de Ciencias Exactas y Naturales (FCEN)Universidad de Buenos Aires (UBA) and IBBEA (CONICET-UBA)Buenos AiresArgentina
  3. 3.Grupo de Investigación de Filogenias Moleculares y Filogeografía, Departamento de Ecología, Genética y Evolución (EGE), FCENUBA and IEGEBA (CONICET-UBA)Buenos AiresArgentina
  4. 4.Instituto de Investigaciones en Recursos Naturales, Agroecología y Desarrollo Rural (IRNAD)Universidad Nacional de Rio Negro-CONICETSan Carlos de BarilocheArgentina

Personalised recommendations