Climatic conditions driving a part of changes in the biochemical composition in land snails: Insights from the endangered Codringtonia(Gastropoda: Pulmonata)
Abstract
Most land snails in order to ensure their survival under adverse environmental conditions interrupt their activity entering a state of dormancy. The transition from activity to dormancy is accompanied by several changes in the animals’ physiology. To identify these changes we examined the seasonal patterns in the biochemical composition and the LDH activity of three different tissues in four endangered land snail species. Additionally, within a phylogenetic framework we investigated the correlation of the measured parameters with the spatial and climatic variables of the sampling sites. Our results indicate that there are both differences and similarities in the pattern exhibited by the four species, depending on the physiological parameter investigated and the climatic conditions of the sampling sites, which sometimes have a significant effect on the seasonal pattern exhibited. Snails can successfully deal with the winter dormancy by maintaining high metabolite concentrations and stable water content whereas there is no indication of anaerobic pathways’ activation. At the same time, they deal successfully with the low humidity and high temperatures during the summer, but they are forced to maintain low metabolite concentrations and seem to activate anaerobic pathways to meet their energy demands. Therefore, from a biochemical perspective, it seems that winter is a less stressful period for snails compared to summer. According to the prevailing climate change scenarios, the Mediterranean region is going to exhibit a sudden transition towards a dryer and longer summer. This transition will exert a very high adaptation pressure on the already vulnerable Codringtonia species. Thus, it could be that this endemic Greek genus is truly on the verge of extinction.
Acknowledgements
Our most sincere thanks to Evie Pless for her work in the linguistic editing of this manuscript. We would also like to express our gratitude to the two anonymous reviewers for their comments that greatly improved a previous version of this work.
References
Adamson K.J., Wang T., Rotgans B.A., Kuballa A.V., Storey K.B. & Cummins S.F. 2015. Differential peptide expression in the central nervous system of the land snail Theba pisana, between active and aestivated. Peptides 80: 61–71. 10.1016/j.peptides.2015.08.012Search in Google Scholar
Akaike H. 1974. A new look at statistical-model identification. IEEE Trans. Automat. Contr. 19 (6): 716–723. 10.1109/TAC.1974.1100705Search in Google Scholar
Alexis M.N., Papaparaskeva-Papoutsoglou E. & Theochari V. 1985. Formulation of practical diets for rainbow trout (Salmo gairdneri) made by partial or complete substitution of fish meal by poultry by-products and certain plant byproducts. Aquaculture 50 (1-2): 61–73. 10.1016/0044-8486(85)90153-XSearch in Google Scholar
Ansart A., Guiller A., Moine O., Martin M.-C. & Madec L. 2013. Is cold hardiness size-constrained? A comparative approach in land snails. Evol. Ecol. 28 (3): 471–493. 10.1007/s10682-013-9680-9Search in Google Scholar
Arad Z. & Avivi T.R. 1998. Ontogeny of resistance to desiccation in the bush-dwelling snail Theba pisana (Helicidae). J. Zool. 244 (4): 515–526. 10.1111/j.1469-7998.1998.tb00057.xSearch in Google Scholar
Borges E., Vuaden F.C., Cognato G.D., Fauth M.D., Bonan C.D., Turcato G., Rossi I.C.D. & Dias R.D. 2004. Effects of starvation on haemolymphatic glucose levels, glycogen contents and nucleotidase activities in different tissues of Helix aspersa (Müller, 1774) (Mollusca, Gastropoda). J. Exp. Zool. 301A (11): 891–897. 10.1002/jez.a.121Search in Google Scholar
Brooks S.P.J. & Storey K.B. 1997a. Glycolytic controls in estivation and anoxia: A comparison of metabolic arrest in land and marine molluscs. Comp. Biochem. Physiol. A 118 (4): 1103–1114. 10.1016/S0300-9629(97)00237-5Search in Google Scholar
Brooks S.P.J. & Storey K.B. 1997b. Glycolytic enzyme binding in Otala lactea hepatopancreas: Effect of taxol, colchicine and cytochalasin B and D on the in vivo enzyme distribution. Biochem. Mol. Biol. Int. 41 (4): 841–849. PMID: 911194510.1080/15216549700201881Search in Google Scholar PubMed
Chevan A. & Sutherland M. 1991. Hierarchical Partitioning. The American Statistician 45 (2): 90–96. 10.2307/2684366Search in Google Scholar
Cook A. 2001. Behavioural ecology: on doing the right thing, in the right place at the right time, pp. 447–487. In: Barke G.M. (ed.), The Biology of Terrestrial Molluscs, CABI Publishing, Oxford, 558 pp. ISBN: 0851993184, 9780851993188Search in Google Scholar
Felsenstein J. 1985. Phylogenies and the Comparative Method. Am. Nat. 125(1): 1–15. 10.1086/284325Search in Google Scholar
Fields J.H.A. 1992. The effects of aestivation on the catalytic and regulatory properties of pyruvate kinase from Helix aspersa. Comp. Biochem. Physiol. B 102 (1): 77–82. 10.1016/0305-0491(92)90275-VSearch in Google Scholar
Gao X.J. & Giorgi F. 2008. Increased aridity in the Mediterranean region under greenhouse gas forcing estimated from high resolution simulations with a regional climate model. Global Planet Change 62 (3-4): 195–209. 10.1016/j.gloplacha.2008.02.002Search in Google Scholar
Giannakopoulos C., Kostopoulou E., Varotsos K.V., Tziotziou K. & Plitharas A. 2011. An integrated assessment of climate change impacts for Greece in the near future. Reg. Environ. Change 11 (4): 829–843. 10.1007/s10113-011-0219-8Search in Google Scholar
Giokas S., Karkoulis P., Pafilis P. & Valakos E. 2007. Relictual physiological ecology in the threatened land snail Codringtonia helenae: A cause for decline in a changing environment? Acta Oecol. 32 (3): 269–278. 10.1016/j.actao.2007.05.008Search in Google Scholar
Giokas S., Pafilis P. & Valakos E. 2005. Ecological and physiological adaptations of the land snail Albinaria caerulea (Pulmonata: Clausiliidae). J. Mollusc. Stud. 71 (1): 15–23. 10.1093/mollus/eyi001Search in Google Scholar
Goodfriend G.A. 1986. Variation in land snail shell form and size and its causes: a Review. Syst. Biol. 35 (2): 204–223. 10.1093/sysbio/35.2.204Search in Google Scholar
Hadjicharalambous E. 1996. Contribution to the study of the ecology and biology of the genus Codringtonia Kobelt, 1898 (Gastropoda, Pulmonata). PhD Thesis, Department of Biology. University of Athens, Athens, 286 pp.Search in Google Scholar
Hijmans R.J., Cameron S.E., Parra J.L., Jones P.G. & Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25 (15): 1965–1978. 10.1002/joc.1276Search in Google Scholar
Kornberg A. 1955. Lactic dedydrogenase of muscle, pp. 441–443. In: Colowick S.P. & Kaplan N.O. (eds), Methods of Enzymology, Vol. 1, Academic Press, New York and London, 835 pp. ISBN: 978-0-12-181801-210.1016/0076-6879(55)01072-0Search in Google Scholar
Kotsakiozi P., Pafilis P., Giokas S. & Valakos E. 2012a. A comparison of the physiological responses of two land snail species with different distributional ranges. J. Mollusc. Stud. 78 (2): 217–224. 10.1093/mollus/eys003Search in Google Scholar
Kotsakiozi P., Parmakelis A., Aggeli I.-K., Gaitanaki C., Giokas S. & Valakos E.D. 2015. Water balance and expression of heat-shock protein 70 in Codringtonia species: A study within a phylogenetic framework. J. Mollusc. Stud. 81 (1): 24–36. 10.1093/mollus/eyu042Search in Google Scholar
Kotsakiozi P., Parmakelis A., Giokas S., Papanikolaou I. & Valakos E.D. 2012b. Mitochondrial phylogeny and biogeographic history of the Greek endemic land-snail genus Codringtonia Kobelt 1898 (Gastropoda, Pulmonata, Helicidae). Mol. Phylogenet. Evol. 62 (2): 681–692. 10.1016/j.ympev.2011.11.012Search in Google Scholar
Kotsakiozi P., Rigal F., Valakos E.D. & Parmakelis A. 2013. Disentangling the effects of intraspecies variability, phylogeny, space, and climate on the evolution of shell morphology in endemic Greek land snails of the genus Codringtonia. Biol. J. Linn. Soc. 110 (4): 796–813. 10.1111/Bij.12169Search in Google Scholar
Layne E. 1957. Spectrophotometric and turbidimetric methods for measuring proteins. Methods in Enzymology 3: 447–454. 10.1016/S0076-6879(57)03413-8Search in Google Scholar
Lazaridou-Dimitriadou M. & Saunders D.S. 1986. The influence of humidity, photoperiod, and temperature on the dormancy and activity of Helix lucorum (Gastropoda, Pulmonata). J. Mollusc. Stud. 52 (3): 180–189. 10.1093/mollus/52.3.180Search in Google Scholar
Legakis A., Maragou, P. 2009. The Red Data Book of the Threatened Animal Species of Greece. Hellenic Zoological Society, Athens, 525 pp. ISBN: 978-960-85298-8-5 [In Greek]Search in Google Scholar
Michaelidis B., Loumbourdis N.S. & Kapaki E. 2002. Analysis of monoamines, adenosine and GABA in tissues of the land snail Helix lucorum and lizard Agama stellio stellio during hibernation. J. Exp. Biol. 205 (8): 1135–1143. PMID: 1191927210.1242/jeb.205.8.1135Search in Google Scholar PubMed
Michaelidis B., Pallidou A. & Vakouftsi P. 1999a. Effects of anoxia on the extra- and intracellular acid-base status in the land snail Helix lucorum (L.): Lack of evidence for a relationship between pyruvate kinase down-regulation and acid-base status. J. Exp. Biol. 202 (12): 1667–1675. PMID: 1033351210.1242/jeb.202.12.1667Search in Google Scholar PubMed
Michaelidis B., Rofalikou E. & Grieshaber M.K. 1999b. The effects of hypercapnia on force and rate of contraction and intracellular pH of perfused ventricles from the land snail Helix lucorum (L.). J. Exp. Biol. 202 (21): 2993–3001. PMID: 1051848010.1242/jeb.202.21.2993Search in Google Scholar PubMed
Michaelidis B., Vavoulidou D., Rousou J. & Portner H.O. 2007. The potential role of CO2 in initiation and maintenance of estivation in the land snail Helix lucorum. Physiol. Biochem. Zool. 80 (1): 113–124. 10.1086/509210Search in Google Scholar PubMed
Nally R.M. 2002. Multiple regression and inference in ecology and conservation biology: further comments on identifying important predictor variables. Biodivers. Conserv. 11 (8): 1397–1401. 10.1023/A:1016250716679Search in Google Scholar
Nicolai A., Filser J., Lenz R., Bertrand C. & Charrier M. 2011. Adjustment of metabolite composition in the haemolymph to seasonal variations in the land snail Helix pomatia. J. Comp. Physiol. B 181 (4): 457–466. 10.1007/s00360-010-0539-xSearch in Google Scholar PubMed
Nowakowska A., Caputa M. & Rogalska J. 2010. Natural aestivation and antioxidant defence in Helix pomatia: effect of acclimation to various external conditions. J. Mollusc. Stud. 76: 354–359. 10.1093/mollus/eyq024Search in Google Scholar
Nowakowska A., Swiderska-Kolacz G., Rogalska J. & Caputa M. 2009. Antioxidants and oxidative stress in Helix pomatia snails during estivation. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 150 (4): 481–486. 10.1016/j.cbpc.2009.07.005Search in Google Scholar
Olea P.P., Mateo-Tomas P. & Frutos A.D. 2010. Estimating and modelling bias of the hierarchical partitioning public-domain software: Implications in environmental management and conservation. PLoS One 5 (7): e11698. 10.1371/journal.pone.0011698.Search in Google Scholar
Pakay J.L., Withers P.C., Hobbs A.A. & Guppy M. 2002. In vivo downregulation of protein synthesis in the snail Helix aspersa during estivation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283 (1): R197–R204. 10.1152/ajpregu.00636.2001Search in Google Scholar
Paradis E., Claude J. & Strimmer K. 2004. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20 (2): 289–290. 10.1093/bioinformatics/btg412Search in Google Scholar
Porcel D., Bueno J.D. & Almendros A. 1996. Alterations in the digestive gland and shell of the snail Helix aspersa Muller (Gastropoda, Pulmonata) after prolonged starvation. Comp. Biochem. Physiol. A 115 (1): 11–17. 10.1016/0300-9629(95)02069-1Search in Google Scholar
Prior D.J. 1985. Water-regulatory behavior in terrestrial gastropods. Biol. Rev. 60 (3): 403–424. 10.1111/j.1469-185X.1985.tb00423.xSearch in Google Scholar
Ramnanan C.J., Allan M.E., Groom A.G. & Storey K.B. 2009. Regulation of global protein translation and protein degradation in aerobic dormancy. Mol. Cell. Biochem. 323 (1-2): 9–20. 10.1007/s11010-008-9959-2Search in Google Scholar PubMed
Rees B.B. & Hand S.C. 1990. Heat dissipation, gas exchange and acid base status in the land snail Oreohelix during short term estivation. J. Exp. Biol. 152 (1): 77–92.10.1242/jeb.152.1.77Search in Google Scholar
Reuner A., Brümmer F. & Schill R.O. 2008. Heat shock proteins (Hsp70) and water content in the estivating Mediterranean Grunt Snail (Cantareus apertus). Comp. Biochem. Physiol. B 151 (1): 28–31. 10.1016/j.cbpb.2008.05.004Search in Google Scholar PubMed
Solomon S., Qin D., Manning M., Chen Z., Marquis M., Averyt B., Tignor M. & Miller H.L. (eds). 2007. Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, 996 pp. ISBN: 978 0521 88009-1Search in Google Scholar
Steinberger Y., Grossman S. & Dubinsky Z. 1982. Changes in organic storage compounds during the active and inactive periods in a desert snail, Sphincterochila prophetarum. Comp. Biochem. Physiol. A 71 (1): 41–46. 10.1016/0300-9629(82)90364-4Search in Google Scholar
Storey K.B. 2002. Life in the slow lane: molecular mechanisms of estivation. Comp. Biochem. Physiol. A 133 (3): 733–754. 10.1016/S1095-6433(02)00206-4Search in Google Scholar
Stuart J.A., Ooi E.L. & Ballantyne J.S. 1998. Maximal activities of enzymes of intermediary metabolism in the estivating terrestrial snail Cepaea nemoralis. Comp. Biochem. Physiol. B 120 (2): 417–423. 10.1016/S0305-0491(98)10027-5Search in Google Scholar
Sulikowska-Drozd A. & Maltz T.K. 2014. Experimental drought affects the reproduction of the brooding clausiliid Alinda biplicata (Montagu, 1803). J. Mollusc. Stud. 80 (3): 265–271. 10.1093/mollus/eyu030Search in Google Scholar
Sun J., Mu H., Zhang H., Chandramouli K.H., Qian P.-Y., Wong C.K.C. & Qiu J.-W. 2013. Understanding the regulation of estivation in a freshwater snail through iTRAQ-based comparative proteomics. J. Proteome Res. 12 (11): 5271–5280. 10.1021/pr400570aSearch in Google Scholar
Wieser W. 1978. Initial stage of anaerobic metabolism in snail, Helix pomatia L. FEBS Lett. 95 (2): 375–378. 10.1016/0014-5793(78)81033-3Search in Google Scholar
Wieser W. & Wright E. 1978. D-Lactate formation, D-LDH activity and glycolytic potential of Helix pomatia L. J. Comp. Physiol. B 126 (3): 249–255. 10.1007/BF00688934Search in Google Scholar
Wieser W. & Wright E. 1979. Effects of season and temperature on D-Lactate dehydrogenase, pyruvate kinase and arginine kinase in the foot of Helix pomatia. Hoppe Seylers Z. Physiol. Chem. 360 (4): 533–542. PMID: 3545710.1515/bchm2.1979.360.1.533Search in Google Scholar PubMed
Withers P., Pedler S. & Guppy M. 1997. Physiological adjustments during aestivation by the Australian land snail Rhagada tescorum (Mollusca: Pulmonata: Camaenidae). Austr. J. Zool. 45 (6): 599–611. 10.1071/ZO97009Search in Google Scholar
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Articles in the same Issue
- Cellular and Molecular Biology
- Mitochondrial clock: moderating evolution of early eukaryotes in light of the Proterozoic oceans
- Cellular and Molecular Biology
- Induced sterility in fish and its potential and challenges for aquaculture and germ cell transplantation technology: a review
- Botany
- Human impact on sandy beach vegetation along the southeastern Adriatic coast
- Botany
- Temporal dynamics in the genetic structure of a natural population of Picea abies
- Botany
- Ecotypic adaptations in Bermuda grass (Cynodon dactylon) for altitudinal stress tolerance
- Botany
- Zinc sulfide nanoparticle mediated alterations in growth and anti-oxidant status of Brassica juncea
- Zoology
- Climatic conditions driving a part of changes in the biochemical composition in land snails: Insights from the endangered Codringtonia(Gastropoda: Pulmonata)
- Zoology
- New and little known ptyctimous mites (Acari: Oribatida) with a key to known species of Oribotritia from the Australasian Region
- Zoology
- Using radio telemetry to track ground beetles: Movement of Carabus ullrichii
- Zoology
- Trophic relations between adult water beetles from the Dytiscidae family and non-biting midges (Diptera: Chironomidae)
- Zoology
- Role of the invasive Chinese sleeper Perccottus glenii (Actinopterygii: Odontobutidae) in the distribution of fish parasites in Europe: New data and a review
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- Translocations of tropical and subtropical marine fish species into the Mediterranean. A case study based on Siganus virgatus (Teleostei: Siganidae)
- Zoology
- Distribution, habitats and abundance of the herb field mouse (Apodemus uralensis) in Lithuania