Skip to main content
SpringerLink
Log in

Calcium translocations during the moulting cycle of the semiterrestrial isopod Ligia hawaiiensis (Oniscidea, Crustacea)

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Terrestrial isopods moult first the posterior and then the anterior half of the body. During the moulting cycle they retain a significant fraction of cuticular calcium partly by storing it in sternal CaCO3 deposits. We analysed the calcium content in whole Ligia hawaiiensis and the calcium distribution between the posterior, the anterior ventral, and the anterior dorsal cuticle during four stages of the moulting cycle. The results indicate that: (1) overall, about 80% of the calcium is retained and 20% is lost with the exuviae, (2) in premoult 68% of the calcium in the posterior cuticle is resorbed (23% moved to the anterior ventral cuticle, 17% to the anterior dorsal cuticle, and the remaining 28% to internal tissues), (3) after the posterior moult 83% of the calcium in the anterior cuticle is shifted to the posterior cuticle and possibly to internal storage sites, (4) following the anterior moult up to 54% of the calcium in the posterior cuticle is resorbed and used to mineralise the new anterior cuticle. 45Ca-uptake experiments suggest that up to 80% of calcium lost with the anterior exuviae may be regained after its ingestion. Whole body calcium of Ligia hawaiiensis is only 0.7 times that of the fully terrestrial isopods. These terrestrial species can retain only 48% of whole body calcium, suggesting that the amount of calcium that can be retained by shifting it between the anterior and posterior integument is limited. We propose that fully terrestrial Oniscidea rely to a larger degree on other calcium sources like internal stores and uptake from the ingested exuviae.

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

Similar content being viewed by others

References

  • Auzou M-L (1953) Recherches biologiques et physiologiques sur deux isopodes onisciens: Porcellio scaber Latr.et Oniscus asellus L. Ann Sci Nat 15:71–98

    Google Scholar 

  • Becker GL, Chen C-H, Greenawalt JW, Lehninger AL (1974) Calcium phosphate granules in the hepatopancreas of the blue crab Callinectes sapidus. J Cell Biol 61:316–326

    Article  PubMed  CAS  Google Scholar 

  • Becker A, Bismayer U, Epple M, Fabritius H, Hasse B, Shi J, Ziegler A (2003) Structural characterisation of X-ray amorphous calcium carbonate (ACC) in sternal deposits of the Crustacea Porcellio scaber. Dalton Trans 2003:551–555

    Article  CAS  Google Scholar 

  • Becker A, Ziegler A, Epple M (2005) The mineral phase in the cuticles of two species of Crustacea consists of magnesium calcite, amorphous calcium carbonate, and amorphous calcium phospate. Dalton Trans 2005:1814–1820

    Article  CAS  Google Scholar 

  • Breĉević L, Nielson AE (1989) Solubility of amorphous calcium carbonate. J Cryst Growth 98:504–510

    Article  Google Scholar 

  • Carefoot TH (1984) Studies on the nutrition of the supralittoral isopod Ligia pallasii using chemically defined artificial diets: assessment of vitamin,carbohydrate, fatty, acid, cholesterol and mineral requirements. Comp Biochem Physiol 79a:655–665

    Article  CAS  Google Scholar 

  • Compère P (1991) Fine structure and elaboration of the epicuticle and the pore canal system in tergite cuticle of the land isopod Oniscus asellus during a moulting cycle. In: Juchault P, Mocquard JP (eds) The biology of terrestrial isopods III. Université de Portiers, pp 169–175

  • Erhard F (1997) Das pleonale Skelet-Muskel-System von Titanethes albus (Synocheta) und weiterer Taxa der Oniscidea (Isopoda), mit Schlußfolgerungen zur Phylogenie der Landasseln. Stuttg Beitr Naturk 550:1–70

    Google Scholar 

  • Glötzner J, Ziegler A (2000) Morphometric analysis of the plasma membranes in the calcium transporting sternal epithelium of the terrestrial isopods Ligia oceanica, Ligidium hypnorum and Porcellio scaber. Arthropod Struct Dev 29:241–257

    Article  PubMed  Google Scholar 

  • Graf F, Meyran J-C (1983) Premolt calcium secretion in midgut posterior caeca of the crustacean Orchestia: ultrastructure of the epithelium. J Morphol 177:1–23

    Article  Google Scholar 

  • Graf F, Meyran J-C (1985) Calcium reabsorption in the posterior caeca of the midgut in a terrestrial crustacean, Orchestia cavimana. Cell Tissue Res 242:83–95

    Article  Google Scholar 

  • Greenaway P (1974) Calcium balance at the premoult stage of the freshwater crayfish Austropotamobius pallipes (Lereboullet). J Exp Biol 6x:27–34

    Google Scholar 

  • Greenaway P (1985) Calcium balance and moulting in the crustacea. Biol Rev 60:425–454

    CAS  Google Scholar 

  • Greenaway P (1993) Calcium and magnesium balance during moulting in land crabs. J Crust Biol 13:191–197

    Article  Google Scholar 

  • Greenaway P, Farrelly C (1991) Trans-epidermal transport and storage of calcium in Holthuisana transversa (Brachyura; Sundathelphusidae) during premoult. Acta Zool Fenn 72:29–40

    Article  Google Scholar 

  • Hadley NF, Warburg MR (1986) Water loss in three species of xeric-adapted isopods: correlations with cuticular lipids. Comp Biochem Physiol 85A:669–672

    Article  Google Scholar 

  • Harrison FM, Martin AW (1954) Calcium distribution and conservation during the molting period in Limnoria Lignorum (Rathke). J Cell Comp Physiol 43:247–256

    Article  CAS  Google Scholar 

  • Hoese B (1981) Morphologie und Funktion des Wasserleitungssystems der terrestrischen Isopoden (Crustacea, Isopoda, Oniscoidea). Zoomorph 98:135–167

    Article  Google Scholar 

  • Hoese B (1982) Der Ligia-Typ des Wasserleitungssystems bei terrestrischen Isopoden und seine Entwicklung in der Familie Ligiidae (Crustacea, Isopoda, Oniscoidea). Zool Jahrb Anat 108:225–261

    Google Scholar 

  • Lagarrigue J-G (1969) Composition ionique de l`Hemolymphe des oniscoides. Bull Soc Zool France 94:137–146

    Google Scholar 

  • Luquet G, Marin F (2004) Biomineralisations in crustaceans: storage strategies. C R P 3:515–534

    Article  Google Scholar 

  • Messner B (1965) Ein morphologisch-histologischer Beitrag zur Häutung von Porcellio scaber latr. und Oniscus asellus l. (Isopoda terrestria). Crustaceana 9:285–301

    Google Scholar 

  • Mykles DL (1980) The mechanism of fluid absorption at ecdysis in the american lobster Homarus americanus. J Exp Biol 84:89–101

    Google Scholar 

  • Neufeld DS, Cameron JN (1993) Transepithelial movement of calcium in crustaceans. J Exp Biol 184:1–16

    PubMed  CAS  Google Scholar 

  • Nicholls AG (1931) Studies on Ligia oceanica. I. A. Habitat and effect of change of environment on respiration. B. Observations on moulting and breeding. J Mar Biol Ass UK 17:655–706

    Article  Google Scholar 

  • Numanoi H (1934a) Calcium contents of the carapace and other organs of Ligia exotica during non-molting and molting phases. J Fac Sci Univ Tokyo 3:359–364

    Google Scholar 

  • Numanoi H (1934b) Calcium in the blood of Ligia exotica during non-molting and molting phases. J Fac Sci Univ Tokyo 3:351–358

    Google Scholar 

  • Passano LM (1960) Molting and its control. In: Waterman TH (ed) The physiology of Crustacea I. Academic, New York, pp 473–536

    Google Scholar 

  • Robertson JD (1960) Ionic regulation in the crab Carcinus maenas (L.) in relation to the moulting cycle. Comp Biochem Physiol 1:183–212

    Article  CAS  Google Scholar 

  • Sparkes S, Greenaway P (1984) The haemolymph as a storage site for cuticular ions during premoult in the freshwater/land crab Holthuisana transversa. J Exp Biol 113:43–54

    CAS  Google Scholar 

  • Steel CGH (1982) Stages of the intermoult cycle in the terrestrial isopod Oniscus asellus and their relation to biphasic cuticle secretion. Can J Zool 60:429–437

    Article  Google Scholar 

  • Steel CGH (1993) Storage and translocation of integumentary calcium during the moult cycle of the terrestrial isopod Oniscus asellus (L.). Can J Zool 71:4–10

    Article  Google Scholar 

  • Strus J, Blejec A (2001) Microscopic anatomy of the integument and digestive system during the molt cycle in Ligia italica (Oniscidea). In: Kensley B, Brusca RC (eds) Isopod systematcis and evolution. A.A.Balkema, Brookfield, pp 343–352

    Google Scholar 

  • Travis DF (1955) The molting cycle of the spiny lobster, Panulirus argus Latreille. III. Physiological changes which occur in the blood and urine during the normal molting cycle. Biol Bull 109:484–503

    Google Scholar 

  • Travis DF (1960) The deposition of skeletal structures in the crustacea. I. The histology of the gastrolith skeletal tissue complex and the gastrolith in the crayfish, orconectes (cambarus) virilis hagen- decapoda. Biol Bull 118:137–149

    Google Scholar 

  • Wheatly MG, Ayers J (1995) Scaling of calcium, inorganic contents, and organic contents to body mass during the molting cycle of the fresh-water crayfish Procambarus clarkii (Girard). J Crust Biol 15:409–417

    Article  Google Scholar 

  • Wheatly MG, Gannon AT (1995) Ion regulation in crayfish: freshwater adaptations and the problem of molting. Am Zool 35:49–59

    CAS  Google Scholar 

  • Ziegler A (1994) Ultrastructure and electron spectroscopic diffraction analysis of the sternal calcium deposits of Porcellio scaber Latr. (Isopoda, Crustacea). J Struct Biol 112:110–116

    Article  Google Scholar 

  • Ziegler A (2003) Variations of calcium deposition in terrestrial isopods. Crustaceana Monographs ed Leiden: Koninklijke Brill NV

  • Ziegler A, Grospietsch T, Carefoot TH, Danko JP, Zimmer M, Zerbst-Boroffka I, Penning SC (2000) Hemolymph ion composition and volume changes in the supralittoral isopod Ligia pallasii Brandt, during molt. J Comp Physiol B 170:329–336

    Article  PubMed  CAS  Google Scholar 

  • Ziegler A, Miller B (1997) Ultrastructure of CaCO3 deposits of terrestrial isopods (crustacea, oniscidea). Zoomorph 117:181–187

    Article  Google Scholar 

  • Ziegler A, Scholz FHE (1997) The ionic hemolymph composition of the terrestrial isopod Porcellio scaber Latr. during molt. J Comp Physiol B 167:536–542

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by research grants to A. Ziegler from the Deutsche Forschungsgemeinschaft (Zi 368/3–3), to G. Ahearn from the U.S. National Science Foundation (IBN04-21986), and to T. Carefoot from Natural Sciences and Engineering Research Council of Canada. Experiments comply with the current Animal Care laws and guidelines of the U.S. and Canada. We thank Michael Hadfield, Director of the Kewalo Marine Laboratory of Hawaii, and his staff and students, for providing research facilities and general assistance during the course of our studies. We are grateful to Bert Mueller, Amy Woo, and Maureen Soon of Earth and Ocean Sciences at the University of British Columbia for their technical expertise in doing the calcium analyses.

Author information

Authors and Affiliations

  1. Central Facility for Electron Microscopy, University of Ulm, 89069, Ulm, Germany

    Andreas Ziegler

  2. Départment de Biochimie, Université de Genève, 1211, Genève-4, Switzerland

    Monica Hagedorn

  3. Department of Biology, University of North Florida, 4567 St. Johns Bluff Road, South, Jacksonville, FL, 32223, USA

    Gregory A. Ahearn

  4. Department of Zoology, University of British Columbia, Vancouver, BC, Canada, V6T 1Z4

    Thomas H. Carefoot

Authors
  1. Andreas Ziegler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monica Hagedorn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gregory A. Ahearn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas H. Carefoot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andreas Ziegler.

Additional information

Communicated by I.D. Hume

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ziegler, A., Hagedorn, M., Ahearn, G.A. et al. Calcium translocations during the moulting cycle of the semiterrestrial isopod Ligia hawaiiensis (Oniscidea, Crustacea). J Comp Physiol B 177, 99–108 (2007). https://doi.org/10.1007/s00360-006-0112-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-006-0112-9

Keywords

Search

Navigation