Population Ecology

, Volume 56, Issue 1, pp 227–237 | Cite as

Stage- and weather-dependent dispersal in the brown garden snail Cornu aspersum

Original article

Abstract

Dispersal decisions are often condition-dependent, influenced by the interaction of individual phenotype and environmental conditions. Terrestrial Gastropods are simultaneous hermaphrodites, a reproductive system rarely studied in the context of dispersal. Moreover, the energetic cost of their movement is one of the highest among animals. Despite these features, which make them valuable models to understand the trade-offs between dispersal and other life-history traits, their dispersal strategies have been barely explored. We studied the movements of subadults and adults of the brown garden snail Cornu aspersum in a semi-natural 4-patch network, for 2 months in 2011 (a dry year) and 1 month in 2012 (a wet year). We assessed the effects of life-history stage (subadult/adult) and weather conditions on dispersal propensity and dispersal speed. Snails were more mobile under humid and warm weather, but nearly all individuals left patches when the relative humidity was close to 100 % in 2012. Because such humidity levels are potentially lethal to C. aspersum, we argue these extreme emigration rates might be an emergency escape response to harmful conditions. Despite a theoretically higher cost of movement, we found that subadults emigrated more, and dispersed faster and further, than adults. Thus, and contrary to what was expected, direct costs of movement do not play the main role in shaping dispersal in C. aspersum. Observed differences between subadults and adults in dispersal behaviour are discussed in the context of intraspecific competition, inbreeding avoidance and relative costs of male and female reproduction.

Keywords

Dispersal distances Helix aspersa Life-history strategies Natal dispersal Phenotype-dependent dispersal 

Supplementary material

10144_2013_407_MOESM1_ESM.pdf (353 kb)
Supplementary material 1 (PDF 352 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. Aubry S, Labaune C, Magnin F, Roche P, Kiss L (2006) Active and passive dispersal of an invading land snail in Mediterranean France. J Anim Ecol 75:802–813PubMedCrossRefGoogle Scholar
  3. Baeza JA (2007) Male mating opportunities affect sex allocation in a protandric-simultaneous hermaphroditic shrimp. Behav Ecol Sociobiol 61:365–370CrossRefGoogle Scholar
  4. Baguette M, Van Dyck H (2007) Landscape connectivity and animal behavior: functional grain as a key determinant for dispersal. Landscape Ecol 22:1117–1129CrossRefGoogle 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. Bailey SER (1989) Daily cycles of feeding and locomotion in Helix aspersa. Haliotis 19:23–31Google Scholar
  7. Barker GM (2001a) The biology of terrestrial molluscs. CABI Publishing, WallingfordCrossRefGoogle Scholar
  8. Barker GM (2001b) Gastropods on land: phylogeny, diversity and adaptive morphology. In: Barker GM (ed) The biology of terrestrial molluscs. CABI Publishing, Wallingford, pp 1–146CrossRefGoogle Scholar
  9. Barker GM (2002) Molluscs as crop pests. CABI Publishing, WallingfordCrossRefGoogle Scholar
  10. Barker GM (2004) Natural enemies of terrestrial molluscs. CABI Publishing, WallingfordCrossRefGoogle Scholar
  11. Bartoń KA (2012) R package MuMIn: model selection and model averaging based on information criteria (AICc and alike). http://mumin.r-forge.r-project.org/
  12. Bates D, Maechler M, Bolker B (2011) R package lme4: linear mixed-effects models using S4 classes. http://lme4.r-forge.r-project.org/
  13. Baur B (1990) Egg cannibalism in hatchlings of the land snail Helix pomatia: nutritional advantage may outweigh lack of kin recognition. Malacol Rev 23:103–105Google Scholar
  14. Baur A (1993a) Effects of food availability and intraspecific and interspecific interactions on the dispersal tendency in the land snail Chondrina clienta. J Zool 230:87–100CrossRefGoogle Scholar
  15. Baur B (1993b) Population structure, density, dispersal and neighbourhood size in Arianta arbustorum. Ann Naturhist Mus Wien 94(95):307–321Google Scholar
  16. Baur B, Baur A (1997) Random mating with respect to relatedness in the simultaneously hermaphroditic land snail Arianta arbustorum. Invertebr Biol 116:294CrossRefGoogle Scholar
  17. Benard MF, McCauley SJ (2008) Integrating across life-history stages: consequences of natal habitat effects on dispersal. Am Nat 171:553–567PubMedCrossRefGoogle Scholar
  18. Bitume EV, Bonte D, Ronce O, Bach F, Flaven E, Olivieri I, Nieberding CM (2013) Density and genetic relatedness increase dispersal distance in a subsocial organism. Ecol Lett 16:430–437PubMedCrossRefGoogle Scholar
  19. Bonte D, Van Dyck H, Bullock JM, Coulon A, Delgado M, Gibbs M, Lehouck V, Matthysen E, Mustin K, Saastamoinen M, Schtickzelle N, Stevens VM, Vandewoestijne S, Baguette M, Barton K, Benton TG, Chaput-Bardy A, Clobert J, Dytham C, Hovestadt T, Meier CM, Palmer SCF, Turlure C, Travis JMJ (2012) Costs of dispersal. Biol Rev 87:290–312PubMedCrossRefGoogle Scholar
  20. Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225PubMedCrossRefGoogle Scholar
  21. Bowler DE, Benton TG (2009) Variation in dispersal mortality and dispersal propensity among individuals: the effects of age, sex and resource availability. J Anim Ecol 78:1234–1241PubMedCrossRefGoogle Scholar
  22. Bride J, Gomot L (1991) Asynchronisme du développement du tractus génital de l’escargot Helix aspersa pendant la croissance et la reproduction. Reprod Nut Dev 31:81–96 (in French with English abstract)CrossRefGoogle Scholar
  23. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  24. Clobert J, Baguette M, Benton TG, Bullock JM (2012) Dispersal ecology and evolution. Oxford University Press, OxfordGoogle Scholar
  25. Cook A (2001) Behavioural ecology: on doing the right thing, in the right place at the right time. In: Barker GM (ed) The biology of terrestrial molluscs. CABI Publishing, Wallingford, pp 447–488CrossRefGoogle Scholar
  26. Costello CM, Creel SR, Kalinowski ST, Vu NV, Quigley HB (2008) Sex-biased natal dispersal and inbreeding avoidance in American black bears as revealed by spatial genetic analyses. Mol Ecol 17:4713–4723PubMedCrossRefGoogle Scholar
  27. Cowie RH (2011) Snails and slugs. In: Simberloff D, Rejmanek M (eds) Encyclopedia of biological invasions. University of California Press, Berkeley, pp 634–643Google Scholar
  28. Dale S (2001) Female-biased dispersal, low female recruitment, unpaired males, and the extinction of small and isolated bird populations. Oikos 92:344–356CrossRefGoogle Scholar
  29. Dan N (1978) Studies on the growth and ecology of Helix aspersa Müller. PhD thesis, University of Manchester, ManchesterGoogle Scholar
  30. 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
  31. Danchin E, Cam E (2002) Can non-breeding be a cost of breeding dispersal? Behav Ecol 51:153–163CrossRefGoogle Scholar
  32. Debeffe L, Morellet N, Cargnelutti B, Lourtet B, Bon R, Gaillard JM, Hewison AJM (2012) Condition-dependent natal dispersal in a large herbivore: heavier animals show a greater propensity to disperse and travel further. J Anim Ecol 81:1327–1337PubMedCrossRefGoogle Scholar
  33. Delattre T (2010) Influence de la structure du paysage et des conditions météorologiques sur le comportement de dispersion de Maniola jurtina (Lepidoptera: Nymphalidae, L.) dans un agroécosystème bocager. PhD thesis, Université de Rennes 1/Université Européenne de Bretagne, Rennes (in French with chapters in English)Google Scholar
  34. Denny M (1980) Locomotion: the cost of gastropod crawling. Science 208:1288–1290PubMedCrossRefGoogle Scholar
  35. Dörge N, Walther C, Beinlich B, Plachter H (1999) The significance of passive transport for dispersal in terrestrial snails (Gastropoda, Pulmonata). Z Ökologie u Naturschutz 8:1–10Google Scholar
  36. Fearnley RH (1993) Sexual selection, dispersal and reproductive behaviour in hermaphrodite land snails, with particular reference to Helix aspersa Müller (Pulmonata: Gastropoda). PhD thesis, University of Manchester, ManchesterGoogle Scholar
  37. González O, Pérez Camargo G, Membiela M, Frezza D, Bartoloni N, Vieites C (2008) Effect of population density on snail productivity (Helix aspersa) in an open sky system fed with Swiss chard and a balanced food supplement. Cien Inv Agr 35:251–257Google Scholar
  38. Guerra PA (2011) Evaluating the life-history trade-off between dispersal capability and reproduction in wing dimorphic insects: a meta-analysis. Biol Rev 86:813–835PubMedCrossRefGoogle Scholar
  39. 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:e49674PubMedCentralPubMedCrossRefGoogle Scholar
  40. Hanski I (2012) Dispersal and eco-evolutionary dynamics in the Glanville fritillary butterfly. In: Clobert J, Baguette M, Benton TG, Bullock JM (eds) Dispersal ecology and evolution. Oxford University Press, UK, pp 290–303Google Scholar
  41. Haynes KJ, Cronin JT (2006) Interpatch movement and edge effects: the role of behavioral responses to the landscape matrix. Oikos 113:43–54CrossRefGoogle Scholar
  42. Henry P-Y, Jarne P (2007) Marking hard-shelled gastropods: tag loss, impact on life-history traits, and perspectives in biology. Invertebr Biol 126:138–153CrossRefGoogle Scholar
  43. Honek A, Martinkova Z (2011) Body size and the colonisation of cereal crops by the invasive slug Arion lusitanicus. Ann Appl Biol 158:79–86CrossRefGoogle Scholar
  44. Iglesias J, Castillejo J (1999) Field observations on feeding of the land snail Helix aspersa Müller. J Mollus Stud 65:411–423CrossRefGoogle Scholar
  45. Ims RA, Hjermann DØ (2001) Condition-dependent dispersal. In: Clobert J, Danchin E, Dhondt A, Nichols J (eds) Dispersal. Oxford University Press, Oxford, pp 203–216Google Scholar
  46. Klein-Rollais D (1993) Contribution à l’étude de la balance hydrique et de sa régulation chez l’escargot Petit-Gris, Helix aspersa Müller (Mollusque Gastéropode Pulmoné). PhD thesis, Université de Rennes 1, Rennes (in French)Google Scholar
  47. Kupfernagel S, Baur B (2011) Sperm utilization in subadult and adult simultaneous hermaphrodite snails mating in the wild. Can J Zool 89:1041–1049CrossRefGoogle Scholar
  48. Mathieu J, Barot S, Blouin M, Caro G, Decaëns T, Dubs F, Dupont L, Jouquet P, Nai P (2010) Habitat quality, conspecific density, and habitat pre-use affect the dispersal behaviour of two earthworm species, Aporrectodea icterica and Dendrobaena veneta, in a mesocosm experiment. Soil Biol Biochem 42:203–209CrossRefGoogle Scholar
  49. Miller TEX, Inouye BD (2013) Sex and stochasticity affect range expansion of experimental invasions. Ecol Lett 16:354–361PubMedCrossRefGoogle Scholar
  50. Oosterhoff LM (1977) Variation in growth rate as an ecological factor in the landsnail Cepaea nemoralis (l.). Neth J Zool 27:1–132CrossRefGoogle Scholar
  51. Perrin N, Goudet J (2001) Inbreeding, kinship, and the evolution of natal dispersal. In: Clobert J, Danchin E, Dhondt A, Nichols J (eds) Dispersal. Oxford University Press, Oxford, pp 123–142Google Scholar
  52. Peschel M, Straub V, Teyke T (1996) Consequences of food-attraction conditioning in Helix: a behavioral and electrophysiological study. J Comp Physiol A 178:317–327Google Scholar
  53. R Development Core Team (2011) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna. http://www.R-project.org
  54. Reynolds AM, Bohan DA, Bell JR (2007) Ballooning dispersal in arthropod taxa: conditions at take-off. Biol Lett 3:237–240PubMedCentralPubMedCrossRefGoogle Scholar
  55. Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38:231–253CrossRefGoogle Scholar
  56. Saccheri IJ, Brakefield PM (2002) Rapid spread of immigrant genomes into inbred populations. Proc R Soc Lond B 269:1073–1078CrossRefGoogle Scholar
  57. Sæther B-E, Engen S, Lande R (1999) Finite metapopulation models with density–dependent migration and stochastic local dynamics. Proc R Soc Lond B 266:113–118CrossRefGoogle Scholar
  58. Schooley RL, Wiens JA (2004) Movements of cactus bugs: patch transfers, matrix resistance, and edge permeability. Landscape Ecol 19:801–810CrossRefGoogle Scholar
  59. Starrfelt J, Kokko H (2012) The theory of dispersal under multiple influences. In: Clobert J, Baguette M, Benton TG, Bullock JM (eds) Dispersal ecology and evolution. Oxford University Press, Oxford, pp 19–28Google Scholar
  60. Stratton LW (1964) The non-marine Mollusca of the Parish of Dale. Field Stud 2:41–52Google Scholar
  61. Tomiyama K, Nakane M (1993) Dispersal patterns of the giant African snail, Achatina fulica (Férussac) (Stylommatophora: achatinidae), equipped with a radio-transmitter. J Mollus Stud 59:315–322CrossRefGoogle Scholar
  62. Tuda M, Shima K (2002) Relative importance of weather and density dependence on the dispersal and on-plant activity of the predator Orius minutus. Popul Ecol 44:0251–0257CrossRefGoogle Scholar
  63. Turchin P (1998) Quantitative analysis of movement: measuring and modeling population redistribution in animals and plants. Sinauer Associates, SunderlandGoogle Scholar

Copyright information

© The Society of Population Ecology and Springer Japan 2013

Authors and Affiliations

  1. 1.Université de Rennes 1, UMR CNRS 6553 EcobioRennes CedexFrance

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