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Urban Ecosystems

, Volume 19, Issue 4, pp 1847–1859 | Cite as

Dispersal-related traits of the snail Cornu aspersum along an urbanisation gradient: maintenance of mobility across life stages despite high costs

  • Maxime DahirelEmail author
  • Alice Séguret
  • Armelle Ansart
  • Luc Madec
Article

Abstract

The extreme fragmentation of natural habitats due to urbanisation can influence the evolution of dispersal strategies in species persisting in cities. The brown garden snail Cornu aspersum is an anthropophilic species, capable of maintaining its populations in highly fragmented habitats despite a high cost of movement. In this species, we studied the variation of dispersal-related behaviours and traits along an urbanisation gradient characterised at two biologically relevant spatial scales (10 and 50 m), in order to identify the effects of habitat fragmentation on movement. The olfactory perceptual range was low, between 1 and 2.5 m, meaning that snails should perceive a large range of landscapes as fragmented. In line with previous results, subadults were more prone to explore than adults in the least urbanised populations. The boundary-crossing behaviour of subadults was not affected by urbanisation, while exploration propensity of adult snails increased with urbanisation at the 50 m (long-distance dispersal) scale, to reach subadult levels in more urban sites. Foot mass (a correlate of movement speed) and perceptual range were not affected by urbanisation. These results are interpreted in relation to the different levels of competition snails are likely to experience in different environments, the high risk of local extinction in urban fragmented landscapes, and the available opportunities for reproduction. They indicate that benefits of dispersal still need to be considered even in situations where movement costs are extremely important. The maintenance of relatively high mobility and its extension to the adult stage in response to anthropogenic changes may thus play a major role in the success of Cornu aspersum in urban habitats.

Keywords

Fragmentation Gastropods Helix aspersa Movement Perceptual range 

Notes

Acknowledgments

We would like to thank Hanna Cholé for her help in preliminary measures of field perceptual range, as well as two reviewers for their helpful comments.

Supplementary material

11252_2016_564_MOESM1_ESM.pdf (105 kb)
ESM 1 (PDF 105 kb)

References

  1. Albuquerque de Matos RM, Serra JA (1984) Taxonomic polymorphism and intrinsic factors in Helix aspersa. Brotéria-Genética 5:181–220Google Scholar
  2. Arnaud JF, Madec L, Bellido A, Guiller A (1999) Microspatial genetic structure in the land snail Helix aspersa (Gastropoda: Helicidae). Heredity 83:110–119. doi: 10.1046/j.1365-2540.1999.00565.x CrossRefPubMedGoogle Scholar
  3. Baguette M, Van Dyck H (2007) Landscape connectivity and animal behavior: functional grain as a key determinant for dispersal. Landscape Ecol 22:1117–1129. doi: 10.1007/s10980-007-9108-4 CrossRefGoogle Scholar
  4. Baguette M, Legrand D, Fréville H, et al. (2012) Evolutionary ecology of dispersal in fragmented landscape. In: Clobert J, Baguette M, Benton TG, Bullock JM (eds) Dispersal ecology and evolution. Oxford University Press, Oxford, pp. 381–391Google Scholar
  5. Bailey SER (1975) The seasonal and daily patterns of locomotor activity in the snail Helix aspersa Müller, and their relation to environmental variables. J Mollus Stud 41:415–428Google Scholar
  6. Benton TG, Bowler DE (2012) Linking dispersal to spatial dynamics. In: Clobert J, Baguette M, Benton TG, Bullock JM (eds) Dispersal ecology and evolution. Oxford University Press, Oxford, pp. 251–265CrossRefGoogle Scholar
  7. Bohrer G, Nathan R, Volis S (2005) Effects of long-distance dispersal for metapopulation survival and genetic structure at ecological time and spatial scales. J Ecol 93:1029–1040. doi: 10.1111/j.1365-2745.2005.01048.x CrossRefGoogle Scholar
  8. Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225. doi: 10.1017/S1464793104006645 CrossRefPubMedGoogle Scholar
  9. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  10. Ceballos G, Ehrlich PR, Barnosky AD, et al. (2015) Accelerated modern human–induced species losses: entering the sixth mass extinction. Science Advances. doi: 10.1126/sciadv.1400253 PubMedPubMedCentralGoogle Scholar
  11. Chase R, Pryer K, Baker R, Madison D (1978) Responses to conspecific chemical stimuli in the terrestrial snail Achatina fulica (Pulmonata: Sigmurethra). Behav Biol 22:302–315. doi: 10.1016/S0091-6773(78)92366-0 CrossRefPubMedGoogle Scholar
  12. Cheptou P-O, Carrue O, Rouifed S, Cantarel A (2008) Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. P Natl A Sci USA 105:3796–3799. doi: 10.1073/pnas.0708446105 CrossRefGoogle Scholar
  13. Ciosi M, Miller NJ, Toepfer S, et al. (2011) Stratified dispersal and increasing genetic variation during the invasion of Central Europe by the western corn rootworm, Diabrotica virgifera virgifera. Evol Appl 4:54–70. doi: 10.1111/j.1752-4571.2010.00133.x CrossRefPubMedGoogle Scholar
  14. Clarke PMR, McElreath R, Mabry KE, McEachern MB (2013) The evolution of bequeathal in stable habitats. Working paper. Accessed 29 December 2015, URL: http://xcelab.net/rmpubs/CMMM_bequeathal_2013.pdf
  15. Core Team R (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  16. Croci S, Butet A, Clergeau P (2008) Does urbanization filter birds on the basis of their biological traits? Condor 110:223–240. doi: 10.1525/cond.2008.8409 CrossRefGoogle Scholar
  17. Dahirel M, Ansart A, Madec L (2014) Stage- and weather-dependent dispersal in the brown garden snail Cornu aspersum. Popul Ecol 56:227–237. doi: 10.1007/s10144-013-0407-0 CrossRefGoogle Scholar
  18. Dahirel M, Cholé H, Séguret A, et al. (2015a) Context dependence of the olfactory perceptual range in the generalist land snail Cornu aspersum. Can J Zoolog 93:665–669. doi: 10.1139/cjz-2015-0001 CrossRefGoogle Scholar
  19. Dahirel M, Olivier E, Guiller A, et al. (2015b) Movement propensity and ability correlate with ecological specialization in European land snails: comparative analysis of a dispersal syndrome. J Anim Ecol 84:228–238. doi: 10.1111/1365-2656.12276 CrossRefPubMedGoogle Scholar
  20. Dahirel M, Ansart A, Madec L (2016a) Potential syndromes linking dispersal and reproduction in the hermaphrodite land snail Cornu aspersum. J Zool. doi: 10.1111/jzo.12328 Google Scholar
  21. Dahirel M, Vardakis M, Ansart A, Madec L (2016b) Density-dependence across dispersal stages in a hermaphrodite land snail: insights from discrete choice models. Oecologia:1–12. doi: 10.1007/s00442-016-3636-z
  22. Dan N (1978) Studies on the growth and ecology of Helix aspersa Müller. PhD dissertation, University of ManchesterGoogle Scholar
  23. Dan N, Bailey SER (1982) Growth, mortality, and feeding rates of the snail Helix aspersa at different population densities in the laboratory, and the depression of activity of helicid snails by other individuals, or their mucus. J Mollus Stud 48:257–265Google Scholar
  24. Denny M (1980) Locomotion: the cost of gastropod crawling. Science 208:1288–1290. doi: 10.1126/science.208.4449.1288 CrossRefPubMedGoogle Scholar
  25. Dirzo R, Raven PH (2003) Global state of biodiversity and loss. Annu Rev Env Resour 28:137–167. doi: 10.1146/annurev.energy.28.050302.105532 CrossRefGoogle Scholar
  26. Dirzo R, Young HS, Galetti M, et al. (2014) Defaunation in the Anthropocene. Science 345:401–406. doi: 10.1126/science.1251817 CrossRefPubMedGoogle Scholar
  27. Donihue CM, Lambert MR (2014) Adaptive evolution in urban ecosystems. Ambio 44:194–203. doi: 10.1007/s13280-014-0547-2 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Dunstan DJ, Hodgson DJ (2014) Snails home. Phys Scripta 89:068002. doi: 10.1088/0031-8949/89/06/068002 CrossRefGoogle Scholar
  29. Escofier B, Pagès J (2008) Analyses factorielles simples et multiples : Objectifs, méthodes et interprétation, 4e édition. Dunod, ParisGoogle Scholar
  30. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol S 34:487–515. doi: 10.1146/annurev.ecolsys.34.011802.132419 CrossRefGoogle Scholar
  31. Falkner G, Obrdlik P, Castella E, Speight MCD (2001) Shelled Gastropoda of Western Europe. Friedrich Held Gesellschaft, München, GermanyGoogle Scholar
  32. Fletcher RJJ, Maxwell CWJ, Andrews JE, Helmey-Hartman WL (2013) Signal detection theory clarifies the concept of perceptual range and its relevance to landscape connectivity. Landscape Ecol 28:57–67. doi: 10.1007/s10980-012-9812-6 CrossRefGoogle Scholar
  33. Friedenberg NA (2003) Experimental evolution of dispersal in spatiotemporally variable microcosms. Ecol Lett 6:953–959. doi: 10.1046/j.1461-0248.2003.00524.x CrossRefGoogle Scholar
  34. Gandon S, Michalakis Y (1999) Evolutionarily stable dispersal rate in a metapopulation with extinctions and kin competition. J Theor Biol 199:275–290. doi: 10.1006/jtbi.1999.0960 CrossRefPubMedGoogle Scholar
  35. Groffman PM, Cavender-Bares J, Bettez ND, et al. (2014) Ecological homogenization of urban USA. Front Ecol Environ 12:74–81. doi: 10.1890/120374 CrossRefGoogle Scholar
  36. Guiller A, Martin M-C, Hiraux C, Madec L (2012) Tracing the invasion of the mediterranean land snail Cornu aspersum aspersum becoming an agricultural and garden pest in areas recently introduced. PLoS ONE 7:e49674. doi: 10.1371/journal.pone
  37. Hamilton PV, Winter MA (1982) Behavioural responses to visual stimuli by the snail Littorina irrorata. Anim Behav 30:752–760CrossRefGoogle Scholar
  38. Hamilton PV, Winter MA (1984) Behavioural responses to visual stimuli by the snails Tectarius muricatus, Turbo castanea, and Helix aspersa. Anim Behav 32:51–57. doi: 10.1016/S0003-3472(82)80147-4 CrossRefGoogle Scholar
  39. Heino M, Hanski I (2001) Evolution of migration rate in a spatially realistic metapopulation model. Am Nat 157:495–511. doi: 10.1086/319927 CrossRefPubMedGoogle Scholar
  40. Henriques-Silva R, Boivin F, Calcagno V, et al. (2015) On the evolution of dispersal via heterogeneity in spatial connectivity. P Roy Soc Lond B Bio 282:20142879. doi: 10.1098/rspb.2014.2879 CrossRefGoogle Scholar
  41. Husson F, Josse J, Le S, Mazet J (2015) R package FactoMineR: Multivariate exploratory data analysis and data mining. http://factominer.free.fr/index.html. Accessed 1 Jul 2015
  42. Iglesias J, Castillejo J (1999) Field observations on feeding of the land snail Helix aspersa Müller. J Molluscan Stud 65:411–423. doi: 10.1093/mollus/65.4.411 CrossRefGoogle Scholar
  43. Institut national de l’information géographique et forestière (2015) Géoportail http://www.geoportail.gouv.fr/accueil. Accessed 1 July 2015Google Scholar
  44. Jackson HB, Fahrig L (2012) What size is a biologically relevant landscape? Landscape Ecol 27:929–941. doi: 10.1007/s10980-012-9757-9 CrossRefGoogle Scholar
  45. Jess S, Marks RJ (1995) Population density effects on growth in culture of the edible snail Helix aspersa Var. maxima. J Molluscan Stud 61:313–323. doi: 10.1093/mollus/61.3.313 CrossRefGoogle Scholar
  46. Kerney M-P, Cameron R-A-D (1999) Guide des escargots et limaces d’Europe. Delachaux et Niestlé, Lonay (Suisse)Google Scholar
  47. Kuhn M, Weston S, Wing J, et al (2013) R package contrast: A collection of contrast methods. https://cran.r-project.org/web/packages/contrast/. Accessed 1 Jul 2015
  48. Le Mitouard E, Bellido A, Guiller A, Madec L (2009) Spatial structure of shell polychromatism in Cepaea hortensis in relation to a gradient of landscape fragmentation in western France. Landscape Ecol 25:123–134. doi: 10.1007/s10980-009-9406-0 CrossRefGoogle Scholar
  49. Liker A, Papp Z, Bókony V, Lendvai ÁZ (2008) Lean birds in the city: body size and condition of house sparrows along the urbanization gradient. J Anim Ecol 77:789–795. doi: 10.1111/j.1365-2656.2008.01402.x CrossRefPubMedGoogle Scholar
  50. Lind H (1990) Strategies of spatial behaviour in Helix pomatia. Ethology 86:1–18. doi: 10.1111/j.1439-0310.1990.tb00414.x CrossRefGoogle Scholar
  51. Martin AE, Fahrig L (2015) Matrix quality and disturbance frequency drive evolution of species behavior at habitat boundaries. Ecol Evol 5:5792–5800. doi: 10.1002/ece3.1841 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Matthysen E (2012) Multicausality of dispersal: a review. In: Clobert J, Baguette M, Benton TG, Bullock JM (eds) Dispersal ecology and evolution. Oxford University Press, Oxford, pp. 3–18CrossRefGoogle Scholar
  53. McGarigal K, Cushman SA, Ene E (2012) FRAGSTATS v4: spatial pattern analysis program for categorical and continuous maps. Computer software program produced by the authors at the University of Massachusetts, AmherstGoogle Scholar
  54. McKee A, Voltzow J, Pernet B (2013) Substrate attributes determine gait in a terrestrial gastropod. Biol Bull 224:53–61CrossRefPubMedGoogle Scholar
  55. Öckinger E, Van Dyck H (2012) Landscape structure shapes habitat finding ability in a butterfly. PLoS One 7:e41517. doi: 10.1371/journal.pone.0041517 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Packard GC (2014) Multiplicative by nature: logarithmic transformation in allometry. J Exp Zool Part B 322:202–207. doi: 10.1002/jez.b.22570 CrossRefGoogle Scholar
  57. Pe’er G, Kramer-Schadt S (2008) Incorporating the perceptual range of animals into connectivity models. Ecol Model 213:73–85. doi: 10.1016/j.ecolmodel.2007.11.020 CrossRefGoogle Scholar
  58. Perea J, Garcia A, Gomez G, et al. (2007) Effect of light and substratum structural complexity on microhabitat selection by the snail Helix aspersa Müller. J Mollus Stud 73:39–43. doi: 10.1093/mollus/eyl031 CrossRefGoogle Scholar
  59. Quantum GIS Development Team (2015) Quantum GIS geographic information system. Open Source Geospatial Foundation. http://qgis.osgeo.org. Accessed 1 Jul 2015
  60. Selander RK, Kaufman DW (1975) Genetic structure of populations of the brown snail (Helix aspersa). I Microgeographic variation Evolution 29:385. doi: 10.2307/2407252 Google Scholar
  61. Service SIG de Rennes Métropole (2012) Orthophotographie aérienne 2011. http://www.data.rennes-metropole.fr. Accessed 1 July 2015
  62. Shibuya S, Kikvidze Z, Toki W, et al. (2014) Ground beetle community in suburban Satoyama — a case study on wing type and body size under small scale management. J Asia Pac Entomol 17:775–780. doi: 10.1016/j.aspen.2014.07.013 CrossRefGoogle Scholar
  63. Shigesada N, Kawasaki K, Takeda Y (1995) Modeling stratified diffusion in biological invasions. Am Nat 146:229–251CrossRefGoogle Scholar
  64. Sih A, Ferrari MCO, Harris DJ (2011) Evolution and behavioural responses to human-induced rapid environmental change. Evol Appl 4:367–387. doi: 10.1111/j.1752-4571.2010.00166.x CrossRefPubMedPubMedCentralGoogle Scholar
  65. Welter-Schultes F (2012) European non-marine molluscs, a guide for species identification. Planet Poster Editions, GöttingenGoogle Scholar
  66. Williams NSG, Morgan JW, McDonnell MJ, McCarthy MA (2005) Plant traits and local extinctions in natural grasslands along an urban–rural gradient. J Ecol 93:1203–1213. doi: 10.1111/j.1365-2745.2005.01039.x CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Maxime Dahirel
    • 1
    • 2
    Email author
  • Alice Séguret
    • 1
    • 3
  • Armelle Ansart
    • 1
  • Luc Madec
    • 1
  1. 1.CNRS/ University of Rennes 1RennesFrance
  2. 2.Department of BiologyGhent University, Terrestrial Ecology unitGhentBelgium
  3. 3.Martin-Luther-University Halle-Wittenberg, Institute for BiologyHalle (Saale)Germany

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