Response of cell volume in Mytilus gill to acute salinity change

Douglas S. Neufeld, Stephen Wright

Research output: Contribution to journalArticle

30 Citations (Scopus)

Abstract

The response of gill cell volume in Mytilus californianus and Mytilus trossolus (=edulis) to acute changes in salinity was assessed using three independent indicators: optical measurement of lateral cell height, measurement of intracellular water content using radiolabeled tracers and measurement of the contents of the major osmolytes of the gills. Optical measurements indicated significant variation in the response of individual lateral cells of M. californianus to acute low-salinity shock. Lateral cell height increased by approximately 20 % shortly after abrupt exposure to 60 % artificial sea water (ASW). Following this initial swelling, we estimate that a substantial regulatory volume decrease (RVD) was present in 25 % of the trials. More commonly, however, an RVD was either absent or minimal: cell height remained elevated for at least 1 h, then returned to the control height when gills were re-exposed to 100 % ASW. Changes in the combined water space of all cells in the gill, measured as the difference between total water space and extracellular space ([14C]polyethylene glycol space), indicated that cell volume regulation in the gill as an organ was also absent or minimal. Cell water space was 2.16 mlg-1 dry mass in isolated gills of M. californianus acclimated to 100 % sea water in the laboratory and increased to 2.83mlg-1 dry mass after a 6 min exposure to 60 % ASW. Cell water space was still 2.81 mlg-1 dry mass after 1 h in 60 % ASW and returned to 2.06 mlg-1 dry mass upon re-exposure to 100 % ASW. Consistent with these observations, the gill contents of the principal cytoplasmic osmolytes (taurine, betaine and K+) were unchanged (approximately 450, 250 and 230 μmolg-1 dry mass, respectively) following exposure of gills from 100 % ASW-acclimated mussels to 60 % ASW. A decrease in cell water space to 2.66 mLg-1 dry mass after 4 weeks of acclimation to 60 % ASW corresponded with a 37 % decrease in betaine content; taurine and K+ contents were unchanged. The changes in water space and solute content of gills from freshly collected M. californianus and M. trossolus were also consistent with the absence of volume regulation; cell water space remained elevated for at least 1 h after lowsalinity exposure, and solute contents were unchanged after this period. We calculated the potential energetic cost of cell volume regulation for mussels exposed to 12 h of sinusoidal fluctuations between 100 % and 50 % sea water; solute uptake for full volume regulation in all tissues would cost a minimum of approximately 30 % of the standard metabolic rate during the period of salinity increase. The routine absence of substantial cell volume regulation in Mytilus gill may reflect the potentially high energetic cost of volume regulation in the face of the large and frequent salinity fluctuations that are regularly encountered by estuarine bivalves.

Original languageEnglish (US)
Pages (from-to)473-484
Number of pages12
JournalJournal of Experimental Biology
Volume199
Issue number2
StatePublished - Feb 1996

Fingerprint

Mytilus
Salinity
Seawater
Cell Size
gills
salinity
seawater
Water
cells
Bivalvia
solute
Betaine
Taurine
water
solutes
Costs and Cost Analysis
taurine
betaine
energetics
cost

Keywords

  • Betaine
  • Cell volume regulation
  • Mussel
  • Mytilus californianus
  • Mytilus trossolus
  • Salinity
  • Taurine

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Agricultural and Biological Sciences (miscellaneous)

Cite this

Response of cell volume in Mytilus gill to acute salinity change. / Neufeld, Douglas S.; Wright, Stephen.

In: Journal of Experimental Biology, Vol. 199, No. 2, 02.1996, p. 473-484.

Research output: Contribution to journalArticle

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abstract = "The response of gill cell volume in Mytilus californianus and Mytilus trossolus (=edulis) to acute changes in salinity was assessed using three independent indicators: optical measurement of lateral cell height, measurement of intracellular water content using radiolabeled tracers and measurement of the contents of the major osmolytes of the gills. Optical measurements indicated significant variation in the response of individual lateral cells of M. californianus to acute low-salinity shock. Lateral cell height increased by approximately 20 {\%} shortly after abrupt exposure to 60 {\%} artificial sea water (ASW). Following this initial swelling, we estimate that a substantial regulatory volume decrease (RVD) was present in 25 {\%} of the trials. More commonly, however, an RVD was either absent or minimal: cell height remained elevated for at least 1 h, then returned to the control height when gills were re-exposed to 100 {\%} ASW. Changes in the combined water space of all cells in the gill, measured as the difference between total water space and extracellular space ([14C]polyethylene glycol space), indicated that cell volume regulation in the gill as an organ was also absent or minimal. Cell water space was 2.16 mlg-1 dry mass in isolated gills of M. californianus acclimated to 100 {\%} sea water in the laboratory and increased to 2.83mlg-1 dry mass after a 6 min exposure to 60 {\%} ASW. Cell water space was still 2.81 mlg-1 dry mass after 1 h in 60 {\%} ASW and returned to 2.06 mlg-1 dry mass upon re-exposure to 100 {\%} ASW. Consistent with these observations, the gill contents of the principal cytoplasmic osmolytes (taurine, betaine and K+) were unchanged (approximately 450, 250 and 230 μmolg-1 dry mass, respectively) following exposure of gills from 100 {\%} ASW-acclimated mussels to 60 {\%} ASW. A decrease in cell water space to 2.66 mLg-1 dry mass after 4 weeks of acclimation to 60 {\%} ASW corresponded with a 37 {\%} decrease in betaine content; taurine and K+ contents were unchanged. The changes in water space and solute content of gills from freshly collected M. californianus and M. trossolus were also consistent with the absence of volume regulation; cell water space remained elevated for at least 1 h after lowsalinity exposure, and solute contents were unchanged after this period. We calculated the potential energetic cost of cell volume regulation for mussels exposed to 12 h of sinusoidal fluctuations between 100 {\%} and 50 {\%} sea water; solute uptake for full volume regulation in all tissues would cost a minimum of approximately 30 {\%} of the standard metabolic rate during the period of salinity increase. The routine absence of substantial cell volume regulation in Mytilus gill may reflect the potentially high energetic cost of volume regulation in the face of the large and frequent salinity fluctuations that are regularly encountered by estuarine bivalves.",
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AB - The response of gill cell volume in Mytilus californianus and Mytilus trossolus (=edulis) to acute changes in salinity was assessed using three independent indicators: optical measurement of lateral cell height, measurement of intracellular water content using radiolabeled tracers and measurement of the contents of the major osmolytes of the gills. Optical measurements indicated significant variation in the response of individual lateral cells of M. californianus to acute low-salinity shock. Lateral cell height increased by approximately 20 % shortly after abrupt exposure to 60 % artificial sea water (ASW). Following this initial swelling, we estimate that a substantial regulatory volume decrease (RVD) was present in 25 % of the trials. More commonly, however, an RVD was either absent or minimal: cell height remained elevated for at least 1 h, then returned to the control height when gills were re-exposed to 100 % ASW. Changes in the combined water space of all cells in the gill, measured as the difference between total water space and extracellular space ([14C]polyethylene glycol space), indicated that cell volume regulation in the gill as an organ was also absent or minimal. Cell water space was 2.16 mlg-1 dry mass in isolated gills of M. californianus acclimated to 100 % sea water in the laboratory and increased to 2.83mlg-1 dry mass after a 6 min exposure to 60 % ASW. Cell water space was still 2.81 mlg-1 dry mass after 1 h in 60 % ASW and returned to 2.06 mlg-1 dry mass upon re-exposure to 100 % ASW. Consistent with these observations, the gill contents of the principal cytoplasmic osmolytes (taurine, betaine and K+) were unchanged (approximately 450, 250 and 230 μmolg-1 dry mass, respectively) following exposure of gills from 100 % ASW-acclimated mussels to 60 % ASW. A decrease in cell water space to 2.66 mLg-1 dry mass after 4 weeks of acclimation to 60 % ASW corresponded with a 37 % decrease in betaine content; taurine and K+ contents were unchanged. The changes in water space and solute content of gills from freshly collected M. californianus and M. trossolus were also consistent with the absence of volume regulation; cell water space remained elevated for at least 1 h after lowsalinity exposure, and solute contents were unchanged after this period. We calculated the potential energetic cost of cell volume regulation for mussels exposed to 12 h of sinusoidal fluctuations between 100 % and 50 % sea water; solute uptake for full volume regulation in all tissues would cost a minimum of approximately 30 % of the standard metabolic rate during the period of salinity increase. The routine absence of substantial cell volume regulation in Mytilus gill may reflect the potentially high energetic cost of volume regulation in the face of the large and frequent salinity fluctuations that are regularly encountered by estuarine bivalves.

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KW - Mytilus trossolus

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