Skip to main content
SpringerLink
Log in

Anhydrobiotic Abilities of Tardigrades

  • Chapter
  • First Online:
Dormancy and Resistance in Harsh Environments

Part of the book series: Topics in Current Genetics ((TCG,volume 21))

Abstract

Tardigrades have been discovered in 1773 and are found in a variety of habitats within marine, freshwater, and terrestrial ecosystems. To survive in habitats that are prone to occasional drought, they possess the ability to enter a reversible state known as anhydrobiosis. The desiccation tolerance allows them to cope with temporal variation of available water and extended lifespan in an anhydrobiotic state with up to 20 years by producing a time shift in the age of tardigrades. The period of anhydrobiosis is limited by cumulative DNA damage and the function of repair pathways during and after rehydration. The same pathways are probably responsible for the tolerance of high doses of radiation. Heat shock proteins serve as molecular chaperones to preserve or restore the protein integrity and late embryogenesis abundant (LEA) proteins LEA proteins play an important role as well. In several desiccated species glass transition has been detected, which support the vitrification hypothesis.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alpert P (2000) The discovery, scope, and puzzle of desiccation tolerance in plants. Plant Ecol 151:5–17

    Article  Google Scholar 

  • Bahrndorff S, Tunnacliffe A, Wise MJ, McGee B, Holmstrup M, Loeschcke V (2009) Bioinformatics and protein expression analyses implicate LEA proteins in the drought response of Collembola. J Insect Physiol 55:210–217

    Article  PubMed  CAS  Google Scholar 

  • Battista JR, Park MJ, McLemore AE (2001) Inactivation of two homologues of proteins presumed to be involved in the desiccation tolerance of plants sensitizes Deinococcus radiodurans R1 to desiccation. Cryobiology 43:133–139

    Article  PubMed  CAS  Google Scholar 

  • Baumann H (1922) Die Anabiose der Tardigraden. Zool Jahrb 45:501–556

    Google Scholar 

  • Baumann H (1927) Anabiosis of tardigrades. Zool Anz 72:175–179

    Google Scholar 

  • Browne J, Tunnacliffe A, Burnell A (2002) Anhydrobiosis – plant desiccation gene found in a nematode. Nature 416:38

    Article  PubMed  CAS  Google Scholar 

  • Carpenter JF, Crowe LM, Crowe JH (1987) Stabilization of phosphofructokinase with sugars during freeze-drying characterization of enhanced protection in the presence of divalent cations. Biochim Biophys Acta 923:109–115

    Article  PubMed  CAS  Google Scholar 

  • Chandler J, Bartels D (1999) Plant desiccation. In: Lerner HR (ed) Plant Responses to Environmental Stresses: From Phytohormones to Genome Reorganization. Marcel Dekker, New York, pp 575–590

    Google Scholar 

  • Clegg JS (1965) Origin of trehalose and its significance during formation of encysted dormant embryos of Artemia salina. Comp Biochem Physiol 14:135–143

    Article  PubMed  CAS  Google Scholar 

  • Clegg JS (1967) Metabolic studies of crytobiosis in encysted embryos of Artemia salina. Comp Biochem Physiol 20:801–809

    Article  CAS  Google Scholar 

  • Clegg JS (1974) Biochemical adaptations associated with the embryonic dormancy of Artemia salina. Trans Am Microsc Soc 93:481–490

    Article  CAS  Google Scholar 

  • Clegg JS (1986) The physical properties and metabolic status of Artemia cysts at low water contents: the water replacement hypothesis. In: Leopold AC (ed) Membranes, Metabolism and Dry Organisms Cornell University Press, New York, pp 169–187

    Google Scholar 

  • Clegg JS, Jackson SA, Warner AH (1994) Extensive intracellular translocations of a major protein accompany anoxia in embryos of Artemia franciscana. Exp Cell Res 212:77–83

    Article  PubMed  CAS  Google Scholar 

  • Clegg JS, Jackson SA, Liang P, Macrae TH (1995) Nuclear–cytoplasmic translocations of protein p26 during aerobic–anoxic transitions in embryos of Artemia franciscana. Exp Cell Res 219:1–7

    Article  PubMed  CAS  Google Scholar 

  • Crowe JH (1975) The physiology of cryptobiosis in tardigrades. Memorie dell'Istituto Italiano di Idrobiologia Dott Marco de Marchi 32:37–59

    Google Scholar 

  • Crowe LM (2002) Lessons from nature: The role of sugars in anhydrobiosis. Comp Biochem Physiol A Mol Integr Physiol 131:505–513

    Article  PubMed  Google Scholar 

  • Crowe JH, Clegg JS (1973) Anhydrobiosis dowden. Hutchinson and Ross, Stroudsburg, PA, p 477

    Google Scholar 

  • Crowe JH, Clegg JS (eds) (1978) Dry biological systems. Academic, New York

    Google Scholar 

  • Crowe JH, Madin KAC (1975) Anhydrobiosis in nematodes evaporative water loss and survival. J Exp Zool 193:323–334

    Article  Google Scholar 

  • Crowe JH, Crowe LM, Carpenter JF, Wistrom CA (1987) Stabilization of dry phospholipid-bilayers and proteins by sugars. Biochem J 242:1–10

    PubMed  CAS  Google Scholar 

  • Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Physiol 60:73–103

    Article  PubMed  CAS  Google Scholar 

  • Crowe JH, Crowe LM, Petrelski S, Hoekstra FA, Araujo PD, Panek AD (1997) Anhydrobiosis: cellular adaptation to extreme dehydration. In: Dantzler WH (ed) Handbook of Physiology. Oxford University Press, New York

    Google Scholar 

  • Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599

    Article  PubMed  CAS  Google Scholar 

  • de Jong WW, Caspers GJ, Leunissen JA (1998) Genealogy of the alpha-crystallin–small heat-shock protein superfamily. Int J Biol Macromol 22:151–162

    Article  PubMed  Google Scholar 

  • Doyère PLN (1842) Memoires sur les Tardigrades. Sur le facilité que possedent les Tardigrades, les rotiferes, les anguillules des toits et quelques autres animalcules, de revenir à la vie après été completement desséchées. Ann Sci Nat Zool Biol Anim 2e:5–35

    Google Scholar 

  • Ehrenberg CG (1834) Ãœber das Wiederaufleben der Moosfauna. Okens Isis 6(7):710–713

    Google Scholar 

  • Eichhorn JC (1781) Beyträge zur Naturgeschichte der kleinsten Wasserthiere, die mit blossem Auge nicht können gesehen werden und die sich in den Gewässern in und um Danzig befinden. F. Nicolai, Berlin and Stettin

    Google Scholar 

  • Ellis JR (2004) From chloroplasts to chaperones: How one thing led to another. Photosynth Res 80:333–343

    Article  CAS  Google Scholar 

  • Franceschi T (1948) Anabiosi nei tardigradi. Boll Mus Ist Biol Univ Genova 22:47–49

    Google Scholar 

  • Galau GA, Hughes DW, Dure L III (1986) Abscisic-acid induction of cloned cotton gossypium–hirsutum late embryogenesis-abundant lea messenger rna species. Plant Mol Biol 7:155–170

    Article  CAS  Google Scholar 

  • Gething MJ, Sambrook J (1992) Protein folding in the cell. Nature 355:33–45

    Article  PubMed  CAS  Google Scholar 

  • Gladyshev E, Meselson M (2008) Extreme resistance of bdelloid rotifers to ionizing radiation. Proc Natl Acad Sci USA 105:5139–5144

    Article  PubMed  CAS  Google Scholar 

  • Gnaiger E, Méndez G, Hand SC (2000) High phosphorylation efficiency and depression of uncoupled respiration in mitochondria under hypoxia. Proc Natl Acad Sci USA 97:11080–11085

    Article  PubMed  CAS  Google Scholar 

  • Goeze JAE (1773) Herrn Karl Bonnets Abhandlungen aus der Insektologie aus d. Franz. übers. u. mit einigen Zusätzen hrsg. v. Joh. August Ephraim Goeze Gebauer, Halle. p 414

    Google Scholar 

  • Goyal K, Tisi L, Basran A, Browne J, Burnell A, Zurdo J, Tunnacliffe A (2003) Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. J Biol Chem 278:12977–12984

    Article  PubMed  CAS  Google Scholar 

  • Goyal K, Pinelli C, Maslen SL, Rastogi RK, Stephens E, Tunnacliffe A (2005) Dehydration-regulated processing of late embryogenesis abundant protein in a desiccation-tolerant nematode. FEBS Lett 579:4093–4098

    Article  PubMed  CAS  Google Scholar 

  • Grzelezak ZF, Sattalo MH, Hanley-Bowdoin LK, Kennedy TD, Lane BG (1982) Synthesis and turnover of proteins and mRNA in germinating wheat embryos. Can J Biochem Physiol 60(3):389–397

    Article  Google Scholar 

  • Guidetti R, Jönsson KI (2002) Long-term anhydrobiotic survival in semi-terrestrial micrometazonas. J Zool (1987) 257:181–187

    Article  Google Scholar 

  • Hand SC (1998) Quiescence in Artemia franciscana embryos: reversible arrest of metabolism and gene expression at low oxygen levels. J Exp Biol 201:1233–1242

    PubMed  CAS  Google Scholar 

  • Hand SC, Hardewig I (1996) Downregulation of cellular metabolism during environmental stress: Mechanisms and implications. Annu Rev Physiol 58:539–563

    Article  PubMed  CAS  Google Scholar 

  • Hengherr S, Brümmer F, Schill RO (2008a) Anhydrobiosis in tardigrades and its effects on longevity traits. J Zool (1987) 275:216–220

    Article  Google Scholar 

  • Hengherr S, Heyer AG, Brümmer F, Schill RO (2008b) Trehalose as protecting agent in aquatic invertebrates during dormancy induced by desiccation. Comp Biochem Physiol A Comp Physiol 151:S34

    Google Scholar 

  • Hengherr S, Heyer AG, Köhler HR, Schill RO (2008c) Trehalose and anhydrobiosis in tardigrades – evidence for divergence in responses to dehydration. FEBS J 275:281–288

    Article  PubMed  CAS  Google Scholar 

  • Hengherr S, Worland MR, Reuner A, Brümmer F, Schill RO (2009) High-temperature tolerance in anhydrobiotic tardigrades is limited by glass transition. Physiol Biochem Zool 82:749–755

    Article  PubMed  CAS  Google Scholar 

  • Hightower LEH (1993) A brief perspective on the heat-shock response and stress proteins. Mar Environ Res 35:79–83

    Article  CAS  Google Scholar 

  • Hoekstra FA, Crowe JH, Crowe LM (1992a) Germination and ion leakage are linked with phase transitions of membrane lipids during imbibition of Typha latifolia pollen. Physiol Plant 84:29–34

    Article  CAS  Google Scholar 

  • Hoekstra FA, Crowe JH, Crowe LM, van Roekel T, Vermeer E (1992b) Do phospholipids and sucrose determine membrane phase transitions in dehydrating pollen species? Plant Cell Environ 15(5):601–606

    Article  CAS  Google Scholar 

  • Horikawa DD, Sakashita T, Katagiri C, Watanabe M, Kikawada T, Nakahara Y, Hamada N, Wada S, Funayama T, Higashi S, Kobayashi Y, Okuda T, Kuwabara M (2006) Radiation tolerance in the tardigrade Milnesium tardigradum. Int J Radiat Biol 82:843–848

    Article  PubMed  CAS  Google Scholar 

  • Hufeland CW (1817) Makrobiotik – Die Kunst das menschliche Leben zu verlängern. Fleischhauer, Reutlingen

    Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403

    Article  PubMed  CAS  Google Scholar 

  • Jönsson KI, Bertolani R (2001) Facts and fiction about long-term survival in tardigrades. J Zool (Lond) 255:121–123

    Article  Google Scholar 

  • Jönsson KI, Schill RO (2007) Induction of Hsp70 by desiccation, ionising radiation and heat-shock in the eutardigrade Richtersius coronifer. J Comp Physiol B 146:456–460

    Google Scholar 

  • Jönsson KI, Harms-Ringdahl M, Torudd J (2005) Radiation tolerance in the eutardigrade Richtersius coronifer. Int J Radiat Biol 81:649–656

    Article  PubMed  Google Scholar 

  • Jørgensen A, Møbjerg N, Kristensen RM (2007) A molecular study of the tardigrade Echiniscus testudo (Echiniscidae) reveals low DNA sequence diversity over a large geographical area. J Limnol 66:77–83

    Article  Google Scholar 

  • Keilin D (1959) The Leeuwenhoek Lecture. The problem of anabiosis or latent life: History and current concept. Proc R Soc Lond B Biol Sci 150:149–191

    Article  PubMed  CAS  Google Scholar 

  • Kikawada T, Nakahara Y, Kanamori Y, Iwata K, Watanabe M, McGee B, Tunnacliffe A, Okuda T (2006) Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid. Biochem Biophys Res Commun 348:56–61

    Article  PubMed  CAS  Google Scholar 

  • Lapinski J, Tunnacliffe A (2003) Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Lett 553:387–390

    Article  PubMed  CAS  Google Scholar 

  • Liang P, MacRae TH (1999) The synthesis of a small heat shock/alpha-crystallin protein in Artemia and its relationship to stress tolerance during development. Dev Biol 207:445–456

    Article  PubMed  CAS  Google Scholar 

  • Liang P, Amons R, Clegg JS, MacRae TH (1997a) Molecular characterization of a small heat shock alpha-crystallin protein in encysted Artemia embryos. J Biol Chem 272:19051–19058

    Article  PubMed  CAS  Google Scholar 

  • Liang P, Amons R, Macrae TH, Clegg JS (1997b) Purification, structure and in vitro molecular-chaperone activity of Artemia p26, a small heat-shock/alpha-crystallin protein. Eur J Biochem 243:225–232

    Article  PubMed  CAS  Google Scholar 

  • Madin KAC, Crowe JH (1975) Anhydrobiosis in nematodes – carbohydrate and lipid-metabolism during dehydration. J Exp Zool 193:335–342

    Article  CAS  Google Scholar 

  • McGee B, Schill RO, Tunnacliffe A (2004) Hydrophilic proteins in invertebrate anhydrobiosis. Integr Comp Biol 44:679–679

    Google Scholar 

  • Neumann S, Reuner A, Brümmer F, Schill RO (2009) DNA damage in storage cells of anhydrobiotic tardigrades. Comp Biochem Physiol A Mol Integr Physiol 153(4):425–429

    Article  PubMed  Google Scholar 

  • Okuda T, Watanabe M, Kikawada T, Fujita A, Forczek E (2004) Cryptobiosis in the african chironomid: Physiological mechanism to survive complete dehydration. Proc Arthropod Embryol Soc Jpn 39:1–7

    Google Scholar 

  • Potts M (2001) Desiccation tolerance: a simple process? Trends Microbiol 9:553–559

    Article  PubMed  CAS  Google Scholar 

  • Örstan A (1998) Factors affecting long-term survival of dry bdelloid rotifers: a preliminary study. Hydrobiologia 387/388:327–331

    Article  Google Scholar 

  • Rahm P (1921) Effect of very low temperatures on the fauna of moss. Proc K Ned Akad Wet Ser C Biol Med Sci 23:235–248

    Google Scholar 

  • Ramløv H, Westh P (2001) Cryptobiosis in the eutardigrade Adorybiotus (Richtersius) coronifer: Tolerance to alcohols, temperature and de novo protein synthesis. Zool Anz 240:517–523

    Article  Google Scholar 

  • Rebecchi L, Guidetti R, Borsari S, Altiero T, Bertolani R (2006) Dynamics of long-term anhydrobiotic survival of lichen-dwelling tardigrades. Hydrobiologia 558:23–30

    Article  Google Scholar 

  • Ricci C (1998) Anhydrobiotic capabilities of bdelloid rotifers. Hydrobiologia 387(388):321–326

    Article  Google Scholar 

  • Ricci C, Caprioli M (1998) Stress during dormancy: Effect on recovery rates and life-history traits of anhydrobiotic animals. Aquat Ecol 32:353–359

    Article  Google Scholar 

  • Ricci C, Caprioli M (2005) Anhydrobiosis in bdelloid species, populations and individuals. Integr Comp Biol 45:759–763

    Article  PubMed  Google Scholar 

  • Ricci C, Covino C (2005) Anhydrobiosis of Adineta ricciae: Costs and Benefits. Hydrobiologia 546:307–314

    Article  Google Scholar 

  • Ricci C, Pagani M (1997) Desiccation of Panagrolaimus rigidus (nematoda): Survival, reproduction and the influence on the internal clock. Hydrobiologia 347:1–13

    Article  Google Scholar 

  • Ricci C, Vaghi L, Manzini ML (1987) Desiccation of rotifers (Macrotrachela quadricornifera): Survival and reproduction. Ecology 68:1488–1494

    Article  Google Scholar 

  • Sakurai M, Furuki T, K-i A, Tanaka D, Nakahara Y, Kikawada T, Watanabe M, Okuda T (2008) Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki. Proc Natl Acad Sci USA 105:5093–5098

    Article  PubMed  CAS  Google Scholar 

  • Schill RO, Fritz GB (2008) Desiccation tolerance in embryonic stages of the tardigrade Milnesium tardigradum. J Zool (Lond) 276:103–107

    Article  Google Scholar 

  • Schill R, Steinbrück G, Köhler H (2004) Stress gene (hsp70) sequences and quantitative expression in Milnesium tardigradum (Tardigrada) during active and cryptobiotic stages. J Exp Biol 207:1607–1613

    Article  PubMed  CAS  Google Scholar 

  • Schill RO, Neumann S, Reuner A, Brümmer F (2008) Detection of DNA damage with single-cell gel electrophoresis in anhydrobiotic tardigrades. Comp Biochem Physiol A Comp Physiol 151:S32

    Google Scholar 

  • Schöneich C (1999) Reactive oxygen species and biological aging: amechanistical approach. Exp Gerontol 34:19–34

    Article  Google Scholar 

  • Schultze CAS (1834) Macrobiotus hufelandii, animale e crustaceorum classe novum, Berlin, p 8

    Google Scholar 

  • Spallanzani L (1776) Opuscoli di Fisica Animale e Vegetabile. Modena: Società Tipografica, pp 203–285

    Google Scholar 

  • Sun Y, MacRae TH (2005) Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci 62:2460–2476

    Article  PubMed  CAS  Google Scholar 

  • Sun WQ, Irving TC, Leopold AC (1984) The role of sugar, vitrification and membrane phase transition in seed desiccation tolerance. Physiol Plant 90(4):621–628

    Article  Google Scholar 

  • Tomos D (1992) Life without water. Curr Biol 2:594–596

    Article  PubMed  CAS  Google Scholar 

  • Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94:791–812

    Article  PubMed  CAS  Google Scholar 

  • Tunnacliffe A, Lapinski J, McGee B (2005) A putative LEA protein, but no trehalose, is present in anhydrobiotic bdelloid rotifers. Hydrobiologia 546:315–321

    Article  CAS  Google Scholar 

  • van Breukelen F, Hand SC (2000) Characterization of ATP-dependent proteolysis in embryos of the brine shrimp, Artemia franciscana. J Comp Physiol B 170:125–133

    Article  PubMed  Google Scholar 

  • van Breukelen F, Maier R, Hand SC (2000) Depression of nuclear transcription and extension of mRNA half-life under anoxia in Artemia franciscana embryos. J Exp Biol 203:1123–1130

    PubMed  Google Scholar 

  • van Leeuwenhoek A (1702) On certain animalcules found in the sediments in gutters of the roofs of houses. Letter 144. The Selected Works of Anton van Leeuwenhoek, London, pp 207–213

    Google Scholar 

  • Vertucci CW, Farrant JM (1995) Acquisition and loss of desiccation Marcel Dekker: New York

    Google Scholar 

  • Watanabe M, Kikawada T, Minagawa N, Yukuhiro F, Okuda T (2002) Mechanism allowing an insect to survive complete dehydration and extreme temperatures. J Exp Biol 205:2799–2802

    PubMed  CAS  Google Scholar 

  • Watanabe M, Kikawada T, Okuda T (2003) Increase of internal ion concentration triggers trehalose synthesis associated with cryptobiosis in larvae of Polypedilum vanderplanki. J Exp Biol 206:2281–2286

    Article  PubMed  CAS  Google Scholar 

  • Webb SJ (1964) Bound water, metabolites and genetic continuity. Nature 203:374–377

    Article  PubMed  CAS  Google Scholar 

  • Webb SJ, Dumasia MD, Bhorjee JS (1965) Bound Water, Inositol, and the Biosynthesis of Temperate and Virulent Bacteriophages by Air-Dried Escherichia coli. Can J Microbiol 11:141–150

    Article  PubMed  CAS  Google Scholar 

  • Westh P, Ramlov H (1991) Trehalose accumulation in the tardigrade Adorybiotus coronifer during anhydrobiosis. J Exp Zool 258:303–311

    Article  CAS  Google Scholar 

  • Westh P, Ramløv H (1988) Cryptobiosis in Arctic tardigrades with special attention to the appearance of trehalose. In: Höpner Petersen G (ed) Grönland Exkursion 2.–25., August 1987. Institut für Polarökologie, Kiel, pp 227–245

    Google Scholar 

  • Wharton DA (2002) Nematode survival strategies. In: Lee DL (ed) The biology of nematodes. Taylor and Francis, London, pp 389–411

    Google Scholar 

  • Womersley C (1981) Biochemical and physiological aspects of anhydrobiosis. Comp Biochem Physiol B Biochem Mol Biol 70:669–678

    Google Scholar 

  • Wright JC, Westh P, Ramlov H (1992) Cryptobiosis in Tardigrada. Biol Rev 67:1–29

    Article  Google Scholar 

  • Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, Biological Institute, University of Stuttgart, Stuttgart, Germany

    Ralph O Schill

Authors
  1. Ralph O Schill
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ralph O Schill .

Editor information

Editors and Affiliations

  1. Israel Oceanographic and Limnological Re, Haifa, 31080, Israel

    Esther Lubzens

  2. Tecnologia Agroalimentaries, Center of Aquaculture, IRTA Institut de Recerca i, Ctra. Poble Nou km 6, San Carlos de la Rapita, 43540, Spain

    Joan Cerda

  3. , Ecosystems, British Antarctic Survey, Madingley Road, Cambridge, CB3 0ET, United Kingdom

    Melody Clark

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Schill, R.O. (2010). Anhydrobiotic Abilities of Tardigrades. In: Lubzens, E., Cerda, J., Clark, M. (eds) Dormancy and Resistance in Harsh Environments. Topics in Current Genetics, vol 21. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-12422-8_8

Download citation

Publish with us

Policies and ethics

Search

Navigation