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.
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References
Albuquerque de Matos RM, Serra JA (1984) Taxonomic polymorphism and intrinsic factors in Helix aspersa. Brotéria-Genética 5:181–220
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
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
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. 381–391
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 41:415–428
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. 251–265
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
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
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
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
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
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
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
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
Core Team R (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
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
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
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
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
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
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
Dan N (1978) Studies on the growth and ecology of Helix aspersa Müller. PhD dissertation, University of Manchester
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 48:257–265
Denny M (1980) Locomotion: the cost of gastropod crawling. Science 208:1288–1290. doi:10.1126/science.208.4449.1288
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
Dirzo R, Young HS, Galetti M, et al. (2014) Defaunation in the Anthropocene. Science 345:401–406. doi:10.1126/science.1251817
Donihue CM, Lambert MR (2014) Adaptive evolution in urban ecosystems. Ambio 44:194–203. doi:10.1007/s13280-014-0547-2
Dunstan DJ, Hodgson DJ (2014) Snails home. Phys Scripta 89:068002. doi:10.1088/0031-8949/89/06/068002
Escofier B, Pagès J (2008) Analyses factorielles simples et multiples : Objectifs, méthodes et interprétation, 4e édition. Dunod, Paris
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
Falkner G, Obrdlik P, Castella E, Speight MCD (2001) Shelled Gastropoda of Western Europe. Friedrich Held Gesellschaft, München, Germany
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
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
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
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
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
Hamilton PV, Winter MA (1982) Behavioural responses to visual stimuli by the snail Littorina irrorata. Anim Behav 30:752–760
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
Heino M, Hanski I (2001) Evolution of migration rate in a spatially realistic metapopulation model. Am Nat 157:495–511. doi:10.1086/319927
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
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
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
Institut national de l’information géographique et forestière (2015) Géoportail http://www.geoportail.gouv.fr/accueil. Accessed 1 July 2015
Jackson HB, Fahrig L (2012) What size is a biologically relevant landscape? Landscape Ecol 27:929–941. doi:10.1007/s10980-012-9757-9
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
Kerney M-P, Cameron R-A-D (1999) Guide des escargots et limaces d’Europe. Delachaux et Niestlé, Lonay (Suisse)
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
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
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
Lind H (1990) Strategies of spatial behaviour in Helix pomatia. Ethology 86:1–18. doi:10.1111/j.1439-0310.1990.tb00414.x
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
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. 3–18
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, Amherst
McKee A, Voltzow J, Pernet B (2013) Substrate attributes determine gait in a terrestrial gastropod. Biol Bull 224:53–61
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
Packard GC (2014) Multiplicative by nature: logarithmic transformation in allometry. J Exp Zool Part B 322:202–207. doi:10.1002/jez.b.22570
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
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
Quantum GIS Development Team (2015) Quantum GIS geographic information system. Open Source Geospatial Foundation. http://qgis.osgeo.org. Accessed 1 Jul 2015
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
Service SIG de Rennes Métropole (2012) Orthophotographie aérienne 2011. http://www.data.rennes-metropole.fr. Accessed 1 July 2015
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
Shigesada N, Kawasaki K, Takeda Y (1995) Modeling stratified diffusion in biological invasions. Am Nat 146:229–251
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
Welter-Schultes F (2012) European non-marine molluscs, a guide for species identification. Planet Poster Editions, Göttingen
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
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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.
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Maxime Dahirel and Alice Séguret contributed in equal parts to this work.
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Dahirel, M., Séguret, A., Ansart, A. et al. Dispersal-related traits of the snail Cornu aspersum along an urbanisation gradient: maintenance of mobility across life stages despite high costs. Urban Ecosyst 19, 1847–1859 (2016). https://doi.org/10.1007/s11252-016-0564-y
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DOI: https://doi.org/10.1007/s11252-016-0564-y