Landscape Ecology

, Volume 34, Issue 8, pp 1937–1948 | Cite as

Multi-scale impacts of urbanization on species distribution within the genus Tetramorium

  • Marion CordonnierEmail author
  • Corentin Gibert
  • Arnaud Bellec
  • Bernard Kaufmann
  • Gilles Escarguel
Research Article



Urbanization is a global change which deeply impacts landscapes. Long studied through transects along urbanization gradients, ecological response to urbanization can now be investigated precisely using direct GIS-based measures. Ecological responses are strongly scale-dependent as both large- and fine-scale environments drive species distributions.


To bridge the gaps regarding the effect of multiple scales on the distribution of biodiversity in the context of urbanization, the present study questions how urbanization structures the distribution of Tetramorium ants at different spatial scales.


Based on model averaging procedures, we investigated ~ 1400 individuals belonging to four Tetramorium species at four distinct spatial scales, from urban microhabitat (1 m around the nest) to urban landscape (500 m around the nest) in 19 urban gradients in South-eastern France.


The probabilities of occurrences of Tetramorium caespitum and T. immigrans simultaneously depended on urbanization at the landscape and local scales, with T. caespitum avoiding urban microhabitats and impervious landscapes whereas T. immigrans favored them. These multi-scale impacts of urbanization were species-dependent as T. moravicum was associated with nonurban landscapes only, and T. semilaeve showed no association whatever the tested variables.


These results highlight the importance of considering several spatial scales simultaneously to study the impact of urbanization on species distributions. The highly contrasted responses to urbanization of T. immigrans and T. caespitum may indicate niche partitioning processes driven by urbanization. The future monitoring of the distribution range dynamics of these two species should provide insightful information into the impact of urbanized landscapes on species distribution.


Landscape Microhabitat Multiple scales Species distribution Tetramorium Urbanization 



This study was funded by the Conseil Départemental de l’Isère. It was also supported by the French National Research Agency (ANR) through the LABEX IMU (ANR-10-LABX-0088) of Université de Lyon, within the program “Investissements d’Avenir” (ANR-11-IDEX-0007) and through the project GEOSUD within the program “Investissements d’Avenir” (ANR-10-EWPX-20).

Supplementary material

10980_2019_842_MOESM1_ESM.pdf (379 kb)
Supplementary material 1 (PDF 379 kb)


  1. Aho K, Derryberry D, Peterson T (2014) Model selection for ecologists: the worldviews of AIC and BIC. Ecology 95:631–636CrossRefPubMedGoogle Scholar
  2. Alberti M (2008) Modeling the urban ecosystem: a conceptual framework. Urban ecology. Springer, Boston, pp 623–646CrossRefGoogle Scholar
  3. Alberti M, Botsford E, Cohen A (2001) Quantifying the urban gradient: linking urban planning and ecology. Avian ecology and conservation in an urbanizing world. Springer, Boston, pp 89–115CrossRefGoogle Scholar
  4. Bartoń K (2016) MuMIn: multi-model inference, version 1.15. 6. URL: Accessed 23 Mar 2018
  5. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1: 1-23Google Scholar
  6. Bjornstad ON (2018) Ncf: spatial covariance functions. R package version 1: 2-4Google Scholar
  7. Borowiec L, Galkowski C, Salata S (2015) What is Tetramorium semilaeve André, 1883? (Hymenoptera, Formicidae). ZooKeys 512:39CrossRefGoogle Scholar
  8. Brian MV, Elmes GW (1974) Production by the ant Tetramorium caespitum in a southern English heath. J Anim Ecol 1:889–903.CrossRefGoogle Scholar
  9. Buczkowski G, Richmond DS (2012) The effect of urbanization on ant abundance and diversity: a temporal examination of factors affecting biodiversity. PLoS ONE 7:22–25CrossRefGoogle Scholar
  10. Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304CrossRefGoogle Scholar
  11. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143CrossRefGoogle Scholar
  12. Concepción ED, Moretti M, Altermatt F, Nobis MP, Obrist MK (2015) Impacts of urbanisation on biodiversity: the role of species mobility, degree of specialisation and spatial scale. Oikos 124:1571–1582CrossRefGoogle Scholar
  13. Cordonnier M, Bellec A, Dumet A, Escarguel G, Kaufmann B (2019) Range limits in sympatric cryptic species: a case study in Tetramorium pavement ants (Hymenoptera: Formicidae) across a biogeographical boundary. Insect Conserv Divers 12:109–120.CrossRefGoogle Scholar
  14. Deguines N, Julliard R, De Flores M, Fontaine C (2012) The whereabouts of flower visitors: contrasting land-use preferences revealed by a country-wide survey based on citizen science. PLoS ONE 7:e45822CrossRefPubMedPubMedCentralGoogle Scholar
  15. Deguines N, Julliard R, De Flores M, Fontaine C (2016) Functional homogenization of flower visitor communities with urbanization. Ecol Evol 6:1967–1976CrossRefPubMedPubMedCentralGoogle Scholar
  16. Egerer MH, Arel C, Otoshi MD, Quistberg RD, Bichier P, Philpott SM (2017) Urban arthropods respond variably to changes in landscape context and spatial scale. J Urban Ecol 3:1–10CrossRefGoogle Scholar
  17. Forman RT (2014) Urban ecology: science of cities. Cambridge University Press, CambridgeGoogle Scholar
  18. Garden J, Mcalpine C, Peterson ANN, Jones D, Possingham H (2006) Review of the ecology of Australian urban fauna: a focus on spatially explicit processes. Aust Ecol 31:126–148CrossRefGoogle Scholar
  19. Gippet JM, Mondy N, Diallo-Dudek J, Bellec A, Dumet A, Mistler L, Kaufmann B (2017) I’m not like everybody else: urbanization factors shaping spatial distribution of native and invasive ants are species-specific. Urban Ecosyst 20:157–169CrossRefGoogle Scholar
  20. Grant BW, Middendorf G, Colgan MJ, Ahmad H, Vogel MB (2011) Ecology of urban amphibians and reptiles: urbanophiles, urbanophobes, and the urbanoblivious. Urban ecology. Oxford University Press, Oxford, pp 167–178CrossRefGoogle Scholar
  21. Grimm NB, Foster D, Groffman P, Grove JM, Hopkinson CS, Nadelhoffer KJ, Pataki DE, Peters DP (2008) The changing landscape: ecosystem responses to urbanization and pollution across climatic and societal gradients. Front Ecol Environ 6:264–272CrossRefGoogle Scholar
  22. Hammer Ø, Harper DAT, Ryan PD (2001) PAST-Palaeontological statistics. acessado em 25: 2009Google Scholar
  23. Hartley S, Krushelnycky PD, Lester PJ (2010) Integrating physiology, population dynamics and climate to make multi-scale predictions for the spread of an invasive insect: the Argentine ant at Haleakala National Park, Hawaii. Ecography 33:83–94CrossRefGoogle Scholar
  24. Heterick BE, Lythe M, Smithyman C (2013) Urbanisation factors impacting on ant (Hymenoptera: Formicidae) biodiversity in the Perth metropolitan area, Western Australia: two case studies. Urban Ecosyst 16:145–173CrossRefGoogle Scholar
  25. Hortal J, Roura-Pascual N, Sanders NJ, Rahbek C (2010) Understanding (insect) species distributions across spatial scales. Ecography 33:51–53CrossRefGoogle Scholar
  26. Kark S, Iwaniuk A, Schalimtzek A, Banker E (2007) Living in the city: can anyone become an ‘urban exploiter’? J Biogeogr 34:638–651CrossRefGoogle Scholar
  27. Kasimova RG, Tishin D, Obnosov YV, Dlussky GM, Baksht FB, Kacimov AR (2014) Ant mound as an optimal shape in constructal design: solar irradiation and circadian brood/fungi-warming sorties. J Theor Biol 355:21–32CrossRefPubMedGoogle Scholar
  28. Lessard JP, Buddle CM (2005) The effects of urbanization on ant assemblages (Hymenoptera: Formicidae) associated with the Molson Nature Reserve, Quebec. Can Entomol 137:215–225CrossRefGoogle Scholar
  29. Lowry H, Lill A, Wong B (2013) Behavioural responses of wildlife to urban environments. Biol Rev 88:537–549CrossRefPubMedGoogle Scholar
  30. Marzluff JM, Bowman R, Donnelly R (2001) A historical perspective on urban bird research: trends, terms, and approaches. Avian ecology and conservation in an urbanizing world. Springer, New York, pp 1–17CrossRefGoogle Scholar
  31. McDonnell MJ, Hahs AK (2008) The use of gradient analysis studies in advancing our understanding of the ecology of urbanizing landscapes: current status and future directions. Landsc Ecol 23:1143–1155CrossRefGoogle Scholar
  32. McDonnell MJ, Pickett ST (1990) Ecosystem structure and function along urban-rural gradients: an unexploited opportunity for ecology. Ecology 71(4):1232–1237CrossRefGoogle Scholar
  33. McGarigal K, Wan HY, Zeller KA, Timm BC, Cushman SA (2016) Multi-scale habitat selection modeling: a review and outlook. Landsc Ecol 31:1161–1175CrossRefGoogle Scholar
  34. McIntyre NE (2000) Ecology of urban arthropods: a review and a call to action. Ann Entomol Soc Am 93:825–835CrossRefGoogle Scholar
  35. McKinney ML (2002) Urbanization, biodiversity, and conservation: the impacts of urbanization on native species are poorly studied, but educating a highly urbanized human population about these impacts can greatly improve species conservation in all ecosystems. Bioscience 52:883–890CrossRefGoogle Scholar
  36. McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260CrossRefGoogle Scholar
  37. Mehrabi Z, Slade EM, Solis A, Mann DJ (2014) The importance of microhabitat for biodiversity sampling. PLoS ONE 9:e114015CrossRefPubMedPubMedCentralGoogle Scholar
  38. Menke SB, Guénard B, Sexton JO, Weiser MD, Dunn RR, Silverman J (2011) Urban areas may serve as habitat and corridors for dry-adapted, heat tolerant species; an example from ants. Urban Ecosyst 14:135–163CrossRefGoogle Scholar
  39. Mikheyev AS, Tschinkel WR (2004) Nest architecture of the ant Formica pallidefulva: structure, costs and rules of excavation. Insectes Soc 51:30–36CrossRefGoogle Scholar
  40. Müller N, Ignatieva M, Nilon CH, Werner P, Zipperer WC (2013) Patterns and trends in urban biodiversity and landscape design. Urbanization, biodiversity and ecosystem services: challenges and opportunities. Springer, Dordrecht, pp 123–174CrossRefGoogle Scholar
  41. Munshi-South J, Kharchenko K (2010) Rapid, pervasive genetic differentiation of urban white-footed mouse (Peromyscus leucopus) populations in New York City. Mol Ecol 19:4242–4254CrossRefPubMedGoogle Scholar
  42. Newbold T, Hudson LN, Hill SL, Contu S, Lysenko I, Senior RA, Börger L, Bennett DJ, Choimes A, Collen B, Day J, De Palma A, Díaz S, Echeverria-Londoño S, Edgar MJ, Feldman A, Garon M, Harrison MLK, Alhusseini T, Ingram DJ, Itescu Y, Kattge J, Kemp V, Kirkpatrick L, Kleyer M, Laginha Pinto Correia D, Martin CD, Meiri S, Novosolov M, Pan Y, Phillips HRP, Purves DW, Robinson A, Simpson J, Tuck SL, Weiher E, White HJ, Ewers RM, Mace GM, Scharlemann JPW, Purvis A (2015) Global effects of land use on local terrestrial biodiversity. Nature 520:45CrossRefGoogle Scholar
  43. Niemela J, Kotze DJ (2009) Carabid beetle assemblages along urban to rural gradients: a review. Landsc Urban Plan 92:65–71CrossRefGoogle Scholar
  44. Penone C, Kerbiriou C, Julien JF, Julliard R, Machon N, Le Viol I (2013) Urbanisation effect on Orthoptera: which scale matters? Insect Conserv Divers 6:319–327CrossRefGoogle Scholar
  45. Philpott SM, Perfecto I, Armbrecht I, Parr CL (2010) Ant diversity and function in disturbed and changing habitats. Ant ecology. Oxford University Press, New York, pp 137–157Google Scholar
  46. R development Core Team (2016) R: a language and environment for statistical computing. Vienna, Austria. URL Accessed 23 Mar 2018
  47. Santamouris M, Synnefa A, Karlessi T (2011) Using advanced cool materials in the urban built environment to mitigate heat islands and improve thermal comfort conditions. Sol Energy 85:3085–3102CrossRefGoogle Scholar
  48. Sattler T, Borcard D, Arlettaz R, Bontadina F, Legendre P, Obrist MK, Moretti M (2010) Spider, bee, and bird communities in cities are shaped by environmental control and high stochasticity. Ecology 91:3343–3353CrossRefPubMedGoogle Scholar
  49. Schlick-Steiner BC, Steiner FM, Sanetra M, Heller G, Stauffer C, Christian E, Seifert B (2005) Queen size dimorphism in the ant Tetramorium moravicum (Hymenoptera, Formicidae): morphometric, molecular genetic and experimental evidence. Insectes Soc 52:186–193CrossRefGoogle Scholar
  50. Schlick-Steiner BC, Steiner FM, Moder K, Seifert B, Sanetra M, Dyreson E, Stauffer C, Christian E (2006) A multidisciplinary approach reveals cryptic diversity in Western Palearctic Tetramorium ants (Hymenoptera: Formicidae). Mol Phylogenet Evol 40:259–273CrossRefPubMedGoogle Scholar
  51. Seress G, Lipovits Á, Bókony V, Czúni L (2014) Quantifying the urban gradient: a practical method for broad measurements. Landsc Urban Plan 131:42–50CrossRefGoogle Scholar
  52. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W.H. Freeman and Company, New YorkGoogle Scholar
  53. Thogmartin WE, Knutson MG (2007) Scaling local species-habitat relations to the larger landscape with a hierarchical spatial count model. Landsc Ecol 22:61–75CrossRefGoogle Scholar
  54. Threlfall CG, Law B, Banks PB (2012) Influence of landscape structure and human modifications on insect biomass and bat foraging activity in an urban landscape. PLoS ONE 7:e38800CrossRefPubMedPubMedCentralGoogle Scholar
  55. Uno S, Cotton J, Philpott SM (2010) Diversity, abundance, and species composition of ants in urban green spaces. Urban Ecosyst 13:425–441CrossRefGoogle Scholar
  56. Vonshak M, Gordon DM (2015) Intermediate disturbance promotes invasive ant abundance. Biol Conserv 186:359–367CrossRefGoogle Scholar
  57. Wagner HC, Arthofer W, Seifert B, Muster C, Steiner FM, Schlick-Steiner BC (2017) Light at the end of the tunnel: integrative taxonomy delimits cryptic species in the Tetramorium caespitum complex (Hymenoptera: Formicidae). Myrmecol News 25:95–129Google Scholar
  58. Warren RJ, Reed K, Olejnizcak M, Potts DL (2018) Rural land use bifurcation in the urban-rural gradient. Urban Ecosyst 21:577–583CrossRefGoogle Scholar
  59. Wu J (2007) Scale and scaling: a cross-disciplinary perspective. In: Wu J, Hobbs R (eds) Key topics in landscape ecology. Cambridge University Press, Cambridge, pp 115–142CrossRefGoogle Scholar
  60. Wu J, Li H (2006) Concepts of scale and scaling. Scaling and uncertainty analysis in ecology. Springer, Dordrecht, pp 3–15CrossRefGoogle Scholar
  61. Wu JG, Loucks OL (1995) From balance of nature to hierarchical patch dynamics: a paradigm shift in ecology. Q Rev Biol 70:439–466CrossRefGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Université de Lyon, UMR5023 Ecologie des Hydrosystèmes Naturels et Anthropisés, ENTPE, CNRSLyonFrance
  2. 2.Université de Lyon, UMR5600 Environnement Ville Société, CNRSLyon Cedex 07France

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