Skip to main content
SpringerLink
Log in

Hydrostatic pressure-induced apoptosis on nauplii of Calanus sinicus

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The effect of hydrostatic pressure on embryonic development of the calanoid copepod Calanus sinicus was studied. Differences of pressure effect among blastomere stages, 1-cell, 2-cell, 4-cell, 8-cell, 16-cell, blastula and limb-bud stage, were examined under two pressurizing conditions, abruptly (10 atm/min) and gradually (0.1 atm/min) increasing. Egg hatching success, deformity frequency and apoptotic cell degradation of hatched nauplii were examined. Egg hatching success rate was not significantly different between blastomere stages, and also between pressurizing conditions. Deformity frequencies of hatched nauplii were low in the early 1-cell and 2-cell stages, and high in the later blastula and limb-bud stages, in both abrupt and gradual pressurizing conditions. On the other hand, in regard to difference in pressurizing conditions, deformity frequency in gradual pressurizing was significantly higher than that in abrupt pressurizing rate. Gradual pressure increase seems to be more harmful to C. sinicus eggs than abrupt pressure change. Apoptosis induced in nauplii by hydrostatic pressure was detected for the first time in marine zooplankton. The embryos of C. sinicus are sensitive to pressure variations, that is, these embryos are supposed to sink to deeper waters, incurring greater risk of having deformities. In the field, C. sinicus ascend to the surface and spawn at night. By looking from this upward behavior, eggs are spawned at lower pressure and warmer temperature. Probably, the harmless low pressure and warm temperature lead eggs to hatch early and to recruit successfully.

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

Similar content being viewed by others

References

  • Agar A, Hill M, Coroneo MT (1999) Pressure induced apoptosis in neurons [AR VO Abstract]. Invest Ophthalmol Vis Sci 40:S265

    Google Scholar 

  • Agar A, Yip SS, Hill MA, Coroneo MT (2000) Pressure related apoptosis in neuronal cell lines. J Neurosci Res 60:495–503

    Article  CAS  Google Scholar 

  • Ban S, Burns C, Castel J, Chaudron Y, Christou E, Escribano R, Umani SF, Gasparini S, Ruiz FG, Hoffmeyer M, Ianora A, Kang H-K, Laabir M, Lacoste A, Miralto A, Ning X, Poulet S, Rodriguez V, Runge J, Shi J, Starr M, Uye S, Wang Y (1997) The paradox of diatom-copepod interactions. Mar Ecol Prog Ser 157:287–293

    Article  Google Scholar 

  • Belka C, Marini P, Schmid B, Durand E, Rudner J, Faltin H, Bamberg M, Schulze-Osthoff K, Budach W (2001) Sensitization of resistant lymphoma cells to irradiation-induced apoptosis by the death ligand TRAIL. Nature 20:2190–2196

    CAS  Google Scholar 

  • Bossy-Wetzel E, Green DR (2000) Detection of apoptosis by Annexin V labeling, vol 322. In: Reed JC (ed) Methods in emzymology. Academic, San Diego, pp 15–18

    Google Scholar 

  • Choi DW (1995) Calcium: still center-stage in hypoxic-ischemic neuronal death. Trends Neurosci 18:58–60

    Article  CAS  Google Scholar 

  • Digby PSB (1961a) Mechanism of sensitivity to hydrostatic pressure in the prawn, Palaemonetes varians Leach. Nature 191:366–368

    Article  Google Scholar 

  • Digby PSB (1961b) Sensitivity of the shrimp Crangon vugaris to hydrostatic pressure. J. Physiol.(Lond.) 158:12–13

    Google Scholar 

  • Eibs H-G, Spielmann H (1977) Differential sensitivity of preimplantation mouse embryos to UV irradiation in vitro and evidence for postreplication repair. Radiat Res 71:367–376

    Article  CAS  Google Scholar 

  • Epel D (2003) Protection of DNA during early development: adaptations and evolutionary consequences. Evol Dev 5(1):83–88

    Article  CAS  Google Scholar 

  • Fujiki T, Toda T, Kikuchi T, Taguchi S (2003) Photoprotective response of xantophyll pigments during phytoplankton blooms in Sagami Bay, Japan. J Plankton Res 25:317–322

    Article  CAS  Google Scholar 

  • Friedrich O, Kress KR, Hartmann M, Frey B, Sommer K, Ludwig H, Fink RHA (2006) Prolonged high-pressure treatments in mammalian skeletal muscle result in loss of functional sodium channels and altered calcium channel kinetics. Cell Biochem Biophys 45:71–83

    Article  CAS  Google Scholar 

  • George RY (1984) Ontogenetic adaptations in growth and respiration of Euphausia superba in relation to temperature and pressure. J Crustacean Biol 4:252–262

    Article  Google Scholar 

  • George RY, Stromberg J-O (1985) Development of eggs of Antarctic krill Euphausia superba in relation to pressure. Polar Biol 4:125–133

    Article  Google Scholar 

  • Gilbert SF (2006) Developmental biology eighth edition. Sinauer Associates, Inc., Publishers Sunderland, Massachusetts, USA, pp 57–58

    Google Scholar 

  • Goldinger JM, Kang BS, Choo YE, Pagenelli CV, Hong SK (1980) Effect of hydrostatic pressure on ion transport and metabolism in human erythrocytes. J Appl Physiol 49:224–231

    Article  CAS  Google Scholar 

  • Hejnol A, Schnabel R (2004) The eutardigrade Thulinia stephaniae has an indeterminate development and the potential to regulate early blastomere ablations. Development 132:1349–1361

    Article  Google Scholar 

  • Hulsemann K (1994) Calanus sinicus Brodsky and C. jashnovi, nom. nov. (Coepoda: Calanoida) of the North-west Pacific Ocean: a comparison, with notes on the integumental pore pattern in Calanus s. str. Invertebr Tanon 8:1461–1482

    Article  Google Scholar 

  • Ianora A, Miralto A, Poulet SA, Carotenuto Y, Buttino I, Romano G, Casotti R, Pohnert G, Wichard T, Colucci-D’Amato L, Terrazzano G, Smetacek V (2004) Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature 429:403–407

    Article  CAS  Google Scholar 

  • Ikegami R, Hunter P, Yager TD (1999) Developmental activation of the capability to undergo check-point induced apoptosis in the early zebrafish embryo. Dev Biol 209:409–433

    Article  CAS  Google Scholar 

  • Islam N, Jaqqi TM, Jepsen KJ, Krray M, Welter JF, Goldberg VM, Malemud CJ (2002) Hydrostatic pressure induces apoptosis in human chondrocytes from osteoarthritic cartilage through up-regulation of tumor necrosis factor-α, inducible nitric oxide synthase, p53, c-myc, and bax-α, and suppression of bcl-2. J Cell Biochem 87:266–278

    Article  CAS  Google Scholar 

  • Isom SC, Prathre RS, Rucker EBIII (2007) Heat stress-induced apoptosis in porcine in vitro fertilized and parthenogenetic preimplantation–stage embryos. Mol Reprod Dev 74:574–581

    Article  CAS  Google Scholar 

  • Jacobson MD, Weil M, Raff MC (1997) Programmed cell death in animal development. Cell 88:347–354

    Article  CAS  Google Scholar 

  • Kashiwagi A, Handa H, Kawakami S, Kubo H, Shinkai T, Fujii H, Kashiwagi K (2003) Effects of high gravity on amphibian development. Biol Sci Space 17:215–216

    PubMed  Google Scholar 

  • Kashiwagi A, Furuno N, Kashiwagi K, Handa H, Kawakami S, Watabnabe M, Yamashita M (2005) Effect of gravity on the amphibian life cycle–morphological and molecular biological analyses of early development, morphogenesis and metamorphosis. Space Utiliz Res 21:270–273

    Google Scholar 

  • Kerr JFR, Wylie AH, Curie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implication in tissue kinetics. Br J Cancer 26:239–257

    Article  CAS  Google Scholar 

  • Klaus AV, Schawaroch V (2006) Novel methodology utilizing confocal laser scanning microscopy for systematic analysis in arthropods (Insecta). Integr Comp Biol 46:207–214

    Article  Google Scholar 

  • Kidachi T (1979) Systematics of Calanus in the Japanese waters, with special reference to morphological differentiations of Calanus in Sagami Bay. Aquabiol 1:25–31

    Google Scholar 

  • Koski M, Breteler WK, Schogt N (1998) Effect of food quality on rate of growth and development of the pelagic copepod Pseudocalanus elongatus (Copepoda, Calanoida). Mar Ecol Prog Ser 170:169–187

    Article  Google Scholar 

  • Krammer P (2000) CD95’s deadly mission in the immune system. Nature 407:789–795

    Article  CAS  Google Scholar 

  • Kuwahara SV, Ogawa H, Toda T, Kikuchi T, Taguchi S (2000a) Variability of bio-optical factors influencing the seasonal attenuation of ultraviolet radiation in temperate coastal waters of Japan. Photochem Photobiol 72(2):193–199

    Article  CAS  Google Scholar 

  • Kuwahara SV, Toda T, Hamasaki K, Kikuchi T, Taguchi S (2000b) Variability in the relative penetration of ultraviolet radiation to photosynthetically available radiation in temperate coastal waters, Japan. J Oceanogr 56:399–408

    Article  CAS  Google Scholar 

  • Liu S, Wang WX (2002) Feeding and reproductive responses of marine copepods in South China Sea to toxic and nontoxic phytoplankton. Mar Biol 140:595–603

    Article  Google Scholar 

  • Lockshin RA, Zakeri Z, Tilly JL (1998) When Cells Die: a comprehensive evaluation of apoptosis and programmed cell death. Wiley-Liss, New York, pp 289–318

    Google Scholar 

  • Marshland DA (1950) The mechanism of cell division: temperature pressure experiments on the cleaving eggs of Arbacia punctulata. J Cell Comp Physiol 36:205–227

    Article  Google Scholar 

  • McLaren IA, Sevigny J-M, Corkett CJ (1988) Body sizes, development rates, and genome sizes among Calanus species. Hydrobiologia 167(168):275–284

    Article  Google Scholar 

  • Miyaguchi H, Fujiki T, Kikuchi T, Kuwahara VS, Toda T (2006) Relationship between the bloom of Noctiluca scintillans and environmental factors in the coastal waters of Sagami Bay, Japan. J Plankton Res 28:313–324

    Article  CAS  Google Scholar 

  • Nagata S (1997) Apoptosis by death factor. Cell 88:355–365

    Article  CAS  Google Scholar 

  • Nakamura S, Arai Y, Takahashi KA, Terauchi R, Ohashi S, Osam Mazda, Imanishi J, Inoue A, Tonomura H, Kubo T (2006) Hydrostatic pressure induces apoptosis of chondrocytes cultured in alginate beads. J Orthop Res 24(4):733–739

    Article  CAS  Google Scholar 

  • Peterson WT (1980) Life history and ecology of Calanus marshallae Frost in the Oregon upwelling zone. Dissertation, Oregon State University

  • Peterson WT (1988) Rates of egg production by the copepod Calanus marshallae in the laboratory and in the sea off Oregon, USA. Mar Ecol Prog Ser 47:229–237

    Article  Google Scholar 

  • Poulet SA, Richer de Forges Cueff MA, Lennon JF (2003) Double-labelling methods used to diagnose apoptotic and necrotic cell degradations in copepod nauplii. Mar Biol 143:889–895

    Article  Google Scholar 

  • Raff JW, Glover DM (1988) Nuclear and cytoplasmic mitotic cycles continue in Drosophila embryos in which DNA synthesis is inhibited with aphidicolin. J Cell Biol 107:2009–2020

    Article  CAS  Google Scholar 

  • Romano G, Russo GL, Buttino I, Ianora A, Miralto A (2003) A marine diatom-derived aldehyde induces apoptosis in copepod and sea urchin embryos. J Exp Biol 206:3487–3494

    Article  Google Scholar 

  • Rugh R, Wohlfromm M (1962) Can the mammalian embryo be killed by X-radiation. J Exp Zool 151:227–244

    Article  CAS  Google Scholar 

  • Saito H, Tsuda A, Kasai H (2002) Nutrient and plankton dynamics in the Oyashio region of the western subarctic Pacific Ocean. Deep-Sea Res PartII 49:5463–5486

    Article  CAS  Google Scholar 

  • Salmon ED (1975) Pressure-induced depolymerization of spindle microtubules. 1. Changes in birefringence and spindle length. J Cell Biol 65:603–614

    Article  CAS  Google Scholar 

  • Shimode S, Toda T, Kikuchi T (2006) Spatio-temporal changes in diversity and community structure of planktonic copepods in Sagami Bay, Japan. Mar Biol 148:581–597

    Article  Google Scholar 

  • Tyler PA, Young CM (1998) Temperature and pressure tolerances in dispersal stages of the genus Echinus (Echinodermata: Echinoidea): prerequisites for deep-sea invasion and speciation. Deep Sea Res PartII 45:253–277

    Article  Google Scholar 

  • Uye S (1996) Induction of reproductive failure in the planktonic copepod Calanus pacificus by diatoms. Mar Ecol Prog Ser 133:89–97

    Article  Google Scholar 

  • Uye S, Huang C, Onbe T (1990) Ontogenetic diel vertical migration of the planktonic copepod Calanus sinicus in the Inland Sea of Japan. Mar Biol 104:389–396

    Article  Google Scholar 

  • Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C (1995) A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods 184:39–51

    Article  CAS  Google Scholar 

  • Wichard T, Poulet SA, Halsband-link C, Albaina A, Harris R, Liu D, Pohnert G (2005) Survey of the chemical defence potential of diatoms: screening of fifty-one species for α, β, γ, δ-unsaturated aldehydes. J Chem Ecol 31(4):949–958

    Article  CAS  Google Scholar 

  • Yamada T, Ohyama H, Tone S, Kizaki H, Tanuma S (1995) Apoptosis.; Nikkei Science Press, pp 52–53

  • Yoshida T, Toda T, Kuwahara V, Taguchi S, Othman BHR (2003) Rapid response to changing light environment of the calanoid copepod Calanus sinicus. Mar Biol 145:505–513

    Google Scholar 

  • Yoshiki T, Toda T, Yoshida T, Shimizu A (2006) A new hydrostatic pressure apparatus for studies of marine zooplankton. J Plankton Res 28:563–570

    Article  Google Scholar 

  • Young CM, Tyler PA (1993) Embryos of the deep-sea echinoid Echinus affinis require high pressure for development. Limnol Oceanogr 38(1):178–181

    Article  Google Scholar 

  • Young CM, Tyler PA, Fenaux L (1997) Potential for deep sea invasion by Mediterranean shallow water echinoids: pressure and temperature as stage-specific dispersal barriers. Mar Ecol Prog Ser 154:197–209

    Article  Google Scholar 

  • Young CM, Tyler PA, Gage JD (1996) Vertical distribution correlates with pressure tolerances of early embryos in the deep-sea asteroid Plutonaster bifrons. J Mar Biol Assoc U.K. 76:749–757

    Article  Google Scholar 

  • Yu SP, Canzoniero LMT, Choi DW (2001) Ion homeostasis and apoptosis. Curr Opin in Cell Biol 13:405–411

    Article  CAS  Google Scholar 

  • Zhang B, Spanda DF, Roman A (2002) E5 protein of human papillomavirus type 16 protests human foreskin keratinocytes from UV B-irradiation-induced apoptosis. J Virol 76:220–231

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. T. Yoshida, University Kebangsaan Malaysia, and Dr. H. Miyaguchi and Ms. S. P. Kok, Soka Univerisity, for their valuable suggestions that improved the article. Our gratitude is extended to Prof. S. Taguchi, Drs. N. Nagao and Y. Onoue, Soka University, for their helpful comments in this manuscript. We are also indebted to Mr. Y. Asakura and the crew of the R. V. “Tachibana”, Manazuru Marine Laboratory for Science Education, Yokohama National University, for their support in collecting samples. This research was partially funded by the University joint Research Project for Private Universities: matching fund subsidy from MEXT (Ministry of Education, Culture Sports, Science and Technology), 2004–2008.

Author information

Authors and Affiliations

  1. Department of Environmental Engineering for Symbiosis, Faculty of Engineering, Soka University, Tangi-cho, Hachioji, Tokyo, 192-8577, Japan

    Tomoko Yoshiki, Banri Yamanoha, Akio Shimizu & Tatsuki Toda

  2. Department of Hydrographic Science, Faculty of Education and Human Science, Yokohama National University, Tokiwadai, Hodogaya-ku, Yokohama, 240-8501, Japan

    Tomohiko Kikuchi

Authors
  1. Tomoko Yoshiki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Banri Yamanoha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tomohiko Kikuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Akio Shimizu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tatsuki Toda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tomoko Yoshiki.

Additional information

Communicated by X. Irigoien.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yoshiki, T., Yamanoha, B., Kikuchi, T. et al. Hydrostatic pressure-induced apoptosis on nauplii of Calanus sinicus . Mar Biol 156, 97–106 (2008). https://doi.org/10.1007/s00227-008-1066-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-008-1066-0

Keywords

Search

Navigation