Skip to main content

Advertisement

SpringerLink
Log in

Is cold hardiness size-constrained? A comparative approach in land snails

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Body water is a major element of the cold-hardiness strategies observed in ectothermic animals, in particular in freezing avoidant species for which body ice formation is lethal. Here, we investigate the relationships, in terrestrial snails, between the temperature of crystallisation (Tc) and body water (water mass and water content), shell shape, geographic and climatic distribution, taking into account phylogenetic inertia. Phylogenetic relationships among 31 species from 13 different families of terrestrial Gastropods were studied using 28S rRNA nuclear and COI mitochondrial sequence data, together with species-specific traits. Our results provide evidence for clear relationships between Tc and absolute/relative body water: smaller species with lower water content tended to be characterized by colder temperatures of crystallisation, although some exceptions were noticeable. Environmental conditions do not appear to affect Tc significantly, as well as shell shape which is however correlated with water content. This study confirmed that supercooling ability in land snails is size-constrained, with consequences on cold-hardiness strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anker A, Baeza JA (2012) Molecular and morphological phylogeny of hooded shrimps, genera Betaeus and Betaeopsis (Decapoda, Alpheidae): testing the center of origin biogeographic model and evolution of life history traits. Mol Phylogenet Evol 64:401–415

    Article  PubMed  Google Scholar 

  • Ansart A, Vernon P (2003) Cold hardiness in molluscs. Acta Oecol 24:95–102

    Article  Google Scholar 

  • Ansart A, Vernon P (2004) Cold hardiness abilities vary with the size of the land snail Cornu aspersum. Comp Biochem Physiol A 139:205–211

    Article  CAS  Google Scholar 

  • Ansart A, Vernon P, Daguzan J (2001) Photoperiod is the main cue that triggers supercooling ability in the land snail, Helix aspersa (Gastropoda: Helicidae). Cryobiology 42:266–273

    Article  PubMed  CAS  Google Scholar 

  • Ansart A, Nicolai A, Vernon P et al (2010) Do ice nucleating agents limit the supercooling ability of the land snail Cornu aspersum? Cryoletters 31:329–340

    PubMed  CAS  Google Scholar 

  • Bailey SER, Lazaridou-Dimitriadou M (1991) Inverse temperature acclimation of heart rate in hibernating land snails. J Comp Physiol B 160:677–681

    Article  Google Scholar 

  • Bale JS, Hayward SAL (2010) Insect overwintering in a changing climate. J Exp Biol 213:980–994

    Article  PubMed  CAS  Google Scholar 

  • Bale JS, Walters KFA (2001) Overwintering biology as a guide to the establishment potential of non-native arthropods in the UK. In: Atkinson D, Thorndyke M (eds) Environment and animal development: genes, life histories and plasticity. BIOS Scientific Publishers Ltd, Oxford, pp 343–354

    Google Scholar 

  • Bartoň K (2009) MuMIn: multi-model inference. Available from http://r-forge.r-project.org/projects/mumin/. Accessed Apr 2013

  • Bigg EK (1953) The supercooling of water. Proc Phys Soc Lond B 66:688–694

    Article  Google Scholar 

  • Block W (2003) Water or ice?—the challenge for invertebrate cold survival. Sci Prog 86:77–101

    Article  PubMed  CAS  Google Scholar 

  • Blomberg SP, Garland TJ, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745

    Article  PubMed  Google Scholar 

  • Bouchet P, Rocroi J-P (2005) Classification and nomenclator of gastropod families. Malacologia 47:1–397

    Google Scholar 

  • Chown SL, Hoffmann AA, Kristensen TN et al (2010) Adapting to climate change: a perspective from evolutionary physiology. Clim Res 43:3–15

    Article  Google Scholar 

  • Costanzo JP, Moore JB, Lee RE et al (1997) Influence of soil hydric parameters on the winter cold hardiness of a burrowing beetle, Leptinotarsa decemlineata (Say). J Comp Physiol B 167:169–176

    Article  Google Scholar 

  • Costanzo JP, Litzgus JD, Iverson JB et al (1998) Soil hydric characteristics and environmental ice nuclei influence in supercooling capacity of hatchling painted turtles Chrysemys picta. J Exp Biol 201:3105–3112

    PubMed  CAS  Google Scholar 

  • Cruz FB, Antenucci D, Luna F et al (2011) Energetics and Liolaemini lizards: implications of a small body size and ecological conservatism. J Comp Physiol B 181:373–382

    Article  PubMed  Google Scholar 

  • David JF, Vannier G (1996) Changes in supercooling with body size, sex and season in the long-lived millipede Polyzonium germanicum (Diplopoda, Polzoniidae). J Zool Lond 240:599–608

    Article  Google Scholar 

  • Dayrat B, Tillier A, Lecointre G et al (2001) New clades of euthyneuran gastropods (mollusca) from 28S rRNA sequences. Mol Phyl Evol 19:225–235

    Article  CAS  Google Scholar 

  • Estoup A, Largiadèr CR, Perrot E et al (1996) Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Mol Mar Biol Biotechnol 5:295–298

    CAS  Google Scholar 

  • Falkner G, Obrdlík P, Castella E, Speight MCD (2001) Shelled Gastropoda of Western Europe. Friedrich-Held-Gesellschaft, München, 267 pp

  • Folmer O, Black M, Hoeh W et al (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–297

    PubMed  CAS  Google Scholar 

  • Freckleton RP (2009) The seven deadly sins of comparative analysis. J Evol Biol 22:1367–1375

    Article  PubMed  CAS  Google Scholar 

  • Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726

    Article  PubMed  CAS  Google Scholar 

  • Gargominy O, Neubert E (2011) Identifier les Clausilies de France. MalaCo HS1:109–122

    Google Scholar 

  • Gargominy O, Ripken TEJ (2011) Une collection de référence pour la malacofaune terrestre de France. MalaCo HS1:1–108

    Google Scholar 

  • Goodfriend GA (1983) Clinal variation and natural selection in the land snail Pleurodonte lucerna in western St. Ann Parish, Jamaica. PhD Dissertation, University of Florida

  • Goodfriend GA (1986) Variation in land-snail shell form and size and its causes: a review. Syst Zool 35:204–223

    Article  Google Scholar 

  • Grafen A (1989) The phylogenetic regression. Philos Trans R Soc Lond B 326:119–157

    Article  CAS  Google Scholar 

  • Grenot CJ, Garcin L, Dao J et al (2000) How does the European common lizard, Lacerta vivipara, survive the cold of winter? Comp Biochem Physiol A 127:71–80

    Article  CAS  Google Scholar 

  • Guiller A, Coutellec M-A, Madec L et al (2001) Evolutionary history of the land snail Helix aspersa in western Mediterranean: preliminary results inferred from mitochondrial DNA sequences. Mol Ecol 10:81–87

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Harmon LJ, Weir JT, Brock CD et al (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24:129–131

    Article  PubMed  CAS  Google Scholar 

  • Hausdorf B (2003) Latitudinal and altitudinal body size variation among north-west European land snail species. Global Ecol Biogeogr 12:389–394

    Article  Google Scholar 

  • Jensen D, Overgaard J, Sorensen JG (2007) The influence of developmental stage on cold shock resistance and ability to cold-harden in Drosophila melanogaster. J Insect Physiol 53:179–186

    Article  PubMed  CAS  Google Scholar 

  • Jing XH, Kang L (2003) Geographical variation in egg cold hardiness: a study on the adaptation strategies of the migratory locust Locusta migratoria L. Ecol Entomol 28:151–158

    Article  Google Scholar 

  • Kellerman V, Loeschke V, Hoffmann AA et al (2012) Phylogenetic constraints in key, functional traits behind species’ climate niches: patterns of desiccation and cold resistance across 95 Drosophila species. Evolution 66:3377–3389

    Article  Google Scholar 

  • Kerney MP, Cameron RAD (1999) Guide des escargots et limaces d’Europe. Delachaux et Niestlé, Lausanne

    Google Scholar 

  • Kerney MP, Cameron RAD, Jungbluth JH (1983) Die Landschnecken Nord- und Mitteleuropas. Parey, Hamburg

    Google Scholar 

  • Klamkin MS (1971) Elementary approximations to the area of n-dimensional ellipsoids. Am Math Mon 78:280–283

    Article  Google Scholar 

  • Klamkin MS (1976) Corrections to “Elementary approximations to the area of n-dimensional ellipsoids”. Am Math Mon 83:478

    Article  Google Scholar 

  • Klein Tank AMG, Wijngaard JB, Können GP et al (2002) Daily dataset of 20th-century surface air temperature and precipitation series for the European Climate Assessment. Int J Clim 22:1441–1453

    Article  Google Scholar 

  • Koene JM, Schulenburg H (2005) Shooting darts: co-evolution and counter-adaptation in hermaphroditic snails. BMC Evol Biol 5:25. doi:10.1186/1471-2148-5-25

    Article  PubMed Central  PubMed  Google Scholar 

  • Kosnik ME, Jablonski D, Lockwood R et al (2006) Quantifying molluscan body size in evolutionary and ecological analyses: maximizing the return on data-collection efforts. Palaios 21:588–597

    Article  Google Scholar 

  • Koštál V, Rozsypal J, Pavel P et al (2013) Physiological and biochemical responses to cold and drought in the rock-dwelling pulmonate snail, Chondrina avenacea. J Comp Physiol B. doi:10.1007/s00360-013-0749-0

  • Kukal O, Duman JG (1989) Switch in the overwintering strategy of two insect species and latitudinal differences in cold hardiness. Can J Zool 67:825–827

    Article  Google Scholar 

  • Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18

    Google Scholar 

  • Lee RE, Costanzo JP (1998) Biological ice nucleation and ice distribution in cold-hardy ectothermic animals. Ann Rev Physiol 60:55–72

    Article  CAS  Google Scholar 

  • Machin J (1967) Structural adaptations for reducing water-loss in three species of terrestrial snail. J Zool Lond 152:55–65

    Article  Google Scholar 

  • MacKenzie AP (1977) Non-equilibrium freezing behaviour of aqueous systems. Philos Trans R Soc Lond B 278:167–189

    Article  CAS  Google Scholar 

  • Moine O, Rousseau D–D, Jolly D et al (2002) Paleoclimatic reconstruction using mutual climatic range on terrestrial mollusks. Quat Res 57:162–172

    Article  Google Scholar 

  • Moran AL (2004) Egg size evolution in tropical American arcid bivalves: the comparative method and the fossil record. Evolution 58:2718–2733

    Article  PubMed  Google Scholar 

  • Nicolai A, Vernon P, Lee M et al (2005) Supercooling ability in two populations of the land snail Helix pomatia (Gastropoda: Helicidae) and ice-nucleating activity of gut bacteria. Cryobiology 50:48–57

    Article  PubMed  Google Scholar 

  • Nicolai A, Filser J, Lenz R et al (2011) Adjustment of metabolite composition in the haemolymph to seasonal variations in the land snail Helix pomatia. J Comp Physiol B 181:457–466

    PubMed  CAS  Google Scholar 

  • Nunn CL (2011) The comparative approach in evolutionary anthropology and biology. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Nyamukondiwa C, Terblanche JS, Marshall KE et al (2011) Basal cold but not heat tolerance constrains plasticity among Drosophila species (Diptera: Drosophilidae). J Evol Biol 24:1927–1938

    Article  PubMed  CAS  Google Scholar 

  • Nylander JAA (2004) MrAIC.pl. Program distributed by the author. Evol Biol Center, Uppsala University. http://www.abc.se/~nylander/mraic/mraic.html

  • Orme CDL, Freckleton RP, Thomas GH et al (2012) CAPER: comparative analyses of phylogenetics and evolution in R. Available from http://cran.r-project.org/web/packages/caper/. Accessed Apr 2013

  • Örstan A (2011) A method to measure snail shell volumes. Triton 23:31–32

    Google Scholar 

  • Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    Article  PubMed  CAS  Google Scholar 

  • Pakay JL, Withers PC, Hobbs AA et al (2002) In vivo downregulation of protein synthesis in the snail Helix aspersa during estivation. Am J Physiol Regul Integr Comp Physiol 283:197–204

    Google Scholar 

  • Pither J (2003) Climate tolerance and interspecific variation in geographic range size. Proc R Soc Lond B 270:475–481

    Article  Google Scholar 

  • Powell EN, Stanton RJJ (1985) Estimating biomass and energy flow of molluscs in palaeo-communities. Palaeontology 28:1–34

    Google Scholar 

  • Ramløv H (2000) Aspects of natural cold tolerance in ectothermic animals. Hum Reprod 15:24–26

    Google Scholar 

  • Raup DM, Graus RR (1972) General equations for volume and surface area of a logarithmically coiled shell. Math Geol 4:307–316

    Article  Google Scholar 

  • Revell LJ (2010) Phylogenetic signal and linear regression on species data. Methods Ecol Evol 1:319–329

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck J (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Sinclair BJ, Marshall DJ, Singh S et al (2004) Cold tolerance of Littorinidae from southern Africa: intertidal snails are not constrained to freeze tolerance. J Comp Physiol B 174:617–624

    Article  PubMed  Google Scholar 

  • Slotsbo S, Hansen LM, Jordaens K et al (2012) Cold tolerance and freeze-induced glucose accumulation in three terrestrial slugs. Comp Biochem Physiol A 161:443–449

    Article  CAS  Google Scholar 

  • Storey KB, Storey JM (1990) Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation and estivation. Quart Rev Biol 65:145–174

    Article  PubMed  CAS  Google Scholar 

  • Storey KB, Storey JM (2004) Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev 79:207–233

    Article  PubMed  Google Scholar 

  • Storey KB, Storey JM, Churchill TA (2007) Freezing and anoxia tolerance of slugs: a metabolic perspective. J Comp Physiol B 177:833–840

    Article  PubMed  Google Scholar 

  • Strachan LA, Tarnowski-Garner HE, Marshall KE et al (2011) The evolution of cold tolerance in Drosophila larvae. Physiol Biochem Zool 84:43–53

    Article  PubMed  Google Scholar 

  • Vernon P, Vannier G, Luce JM (1997) Diminution de la capacité de surfusion au cours de l’embryogenèse et du développement larvaire chez un coléoptère. C R Acad Sci 320:359–366

    Article  CAS  Google Scholar 

  • Voituron Y, Barré H, Ramlov H et al (2009) Freeze tolerance evolution among anurans: frequency and time of appearance. Cryobiology 58:241–247

    Article  PubMed  Google Scholar 

  • Wilson PW, Heneghan AF, Haymet ADJ (2003) Ice nucleation in nature: supercooling points (SCP) measurements and the role of heterogeneous nucleation. Cryobiology 46:88–98

    Article  PubMed  CAS  Google Scholar 

  • Zachariassen KE, Kristiansen E (2000) Ice nucleation and antinucleation in nature. Cryobiology 41:257–279

    Article  PubMed  CAS  Google Scholar 

  • Zachariassen KE, Kristiansen E, Pedersen SA et al (2004) Ice nucleation in solutions and freeze-avoiding insects—homogeneous or heterogeneous? Cryobiology 48:309–321

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We are thankful to Nicole Limondin-Lozouet and Olivier Gargominy for their help in species identification, to Yann Rantier for extraction of geographic information on species, to Philippe Vernon and anonymous referees for constructive comments and to all the people who collected snails for this study purpose, in particular Annegret Nicolai, Mathieu Daëron and Thomas Geslin. This work benefited from the ATBI (All Taxa Biodiversity Inventory) Mercantour program and was partly supported by MAPGEO project, funded by the INSU/INEE PALEO2 program of Centre National de la Recherche Scientifique (CNRS).

Author information

Authors and Affiliations

  1. UMR 6553 Ecobio, Université de Rennes 1, bâtiment 14A, 263 Avenue du Général Leclerc, CS 74205, 35042, Rennes Cedex, France

    Armelle Ansart, Marie-Claire Martin & Luc Madec

  2. UMR 6553 Ecobio, Laboratoire de Parasitologie Pharmaceutique, Université de Rennes 1, bâtiment 6, Avenue du Professeur Léon Bernard, 35043, Rennes Cedex, France

    Annie Guiller

  3. Laboratoire de Géographie Physique, UMR CNRS 8591, 1 place Aristide Briand, 92195, Meudon Cedex, France

    Olivier Moine

Authors
  1. Armelle Ansart
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Annie Guiller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Olivier Moine
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marie-Claire Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luc Madec
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Armelle Ansart.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ansart, A., Guiller, A., Moine, O. et al. Is cold hardiness size-constrained? A comparative approach in land snails. Evol Ecol 28, 471–493 (2014). https://doi.org/10.1007/s10682-013-9680-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-013-9680-9

Keywords

Search

Navigation