High net calcium uptake explains the hypersensitivity of the freshwater pulmonate snail, Lymnaea stagnalis, to chronic lead exposure

Martin Grosell, Kevin V. Brix

Research output: Contribution to journalArticle

32 Citations (Scopus)

Abstract

Previous studies have shown that freshwater pulmonate snails of the genus Lymnaea are exceedingly sensitive to chronic Pb exposure. An EC20 of <4 μg l-1 Pb for juvenile snail growth has recently been determined for Lymnaea stagnalis, which is at or below the current USEPA water quality criterion for Pb. We characterized ionoregulation and acid-base balance in Pb-exposed L. stagnalis (young adults ∼1 g) to investigate the mechanisms underlying this hypersensitivity. After 21-day exposure to 18.9 μg l-1 Pb, Ca2+ influx was significantly inhibited (39%) and corresponding net Ca2+ flux was significantly reduced from 224 to -23 nmol g-1 h-1. An 85% increase in Cl- influx was also observed, while Na+ ion transport appeared unaffected. Finally, a marked alkalosis of extracellular fluid was observed with pH increasing from 8.35 in the control to 8.65 in the 18.9 μg l-1 Pb-exposed group. Results based on direct measurement of Ca2+ influx in 1 g snails gave an influx nearly an order of magnitude higher (750 nmol g-1 h-1) than in comparably sized fish in similar water chemistry. Under control conditions, specific growth rate in newly hatched snails was estimated at 16.7% per day over the first 38-day post-hatch and whole body Ca2+ concentrations were relatively constant at ∼1100 nmol g-1 over this period. Based on these data, it is estimated that newly hatched snails have net Ca2+ uptake rates on the order of 7600 nmol g-1 h-1. A model was developed integrating these data and measured inhibition of Ca2+ influx rates of 13.4% and 38.7% in snails exposed to 2.7 and 18.9 μg l-1 Pb, respectively. The model estimates 45% and 83% reductions in newly hatched snail growth after 30-day exposure in these two Pb-exposed groups. These results compare well with previous direct measurements of 47% and 90% reductions in growth at similar Pb concentrations, indicating the high net Ca2+ uptake is the controlling factor in observed Pb hypersensitivity.

Original languageEnglish
Pages (from-to)302-311
Number of pages10
JournalAquatic Toxicology
Volume91
Issue number4
DOIs
StatePublished - Mar 9 2009

Fingerprint

Lymnaea
Lymnaea stagnalis
Snails
Fresh Water
hypersensitivity
snail
snails
Hypersensitivity
calcium
Calcium
uptake mechanisms
Growth
water quality criteria
United States Environmental Protection Agency
Alkalosis
acid-base balance
extracellular fluids
Acid-Base Equilibrium
Water Quality
Extracellular Fluid

Keywords

  • Biotic ligand model
  • Ionoregulation
  • Lead
  • Snails

ASJC Scopus subject areas

  • Aquatic Science
  • Health, Toxicology and Mutagenesis

Cite this

High net calcium uptake explains the hypersensitivity of the freshwater pulmonate snail, Lymnaea stagnalis, to chronic lead exposure. / Grosell, Martin; Brix, Kevin V.

In: Aquatic Toxicology, Vol. 91, No. 4, 09.03.2009, p. 302-311.

Research output: Contribution to journalArticle

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abstract = "Previous studies have shown that freshwater pulmonate snails of the genus Lymnaea are exceedingly sensitive to chronic Pb exposure. An EC20 of <4 μg l-1 Pb for juvenile snail growth has recently been determined for Lymnaea stagnalis, which is at or below the current USEPA water quality criterion for Pb. We characterized ionoregulation and acid-base balance in Pb-exposed L. stagnalis (young adults ∼1 g) to investigate the mechanisms underlying this hypersensitivity. After 21-day exposure to 18.9 μg l-1 Pb, Ca2+ influx was significantly inhibited (39{\%}) and corresponding net Ca2+ flux was significantly reduced from 224 to -23 nmol g-1 h-1. An 85{\%} increase in Cl- influx was also observed, while Na+ ion transport appeared unaffected. Finally, a marked alkalosis of extracellular fluid was observed with pH increasing from 8.35 in the control to 8.65 in the 18.9 μg l-1 Pb-exposed group. Results based on direct measurement of Ca2+ influx in 1 g snails gave an influx nearly an order of magnitude higher (750 nmol g-1 h-1) than in comparably sized fish in similar water chemistry. Under control conditions, specific growth rate in newly hatched snails was estimated at 16.7{\%} per day over the first 38-day post-hatch and whole body Ca2+ concentrations were relatively constant at ∼1100 nmol g-1 over this period. Based on these data, it is estimated that newly hatched snails have net Ca2+ uptake rates on the order of 7600 nmol g-1 h-1. A model was developed integrating these data and measured inhibition of Ca2+ influx rates of 13.4{\%} and 38.7{\%} in snails exposed to 2.7 and 18.9 μg l-1 Pb, respectively. The model estimates 45{\%} and 83{\%} reductions in newly hatched snail growth after 30-day exposure in these two Pb-exposed groups. These results compare well with previous direct measurements of 47{\%} and 90{\%} reductions in growth at similar Pb concentrations, indicating the high net Ca2+ uptake is the controlling factor in observed Pb hypersensitivity.",
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N2 - Previous studies have shown that freshwater pulmonate snails of the genus Lymnaea are exceedingly sensitive to chronic Pb exposure. An EC20 of <4 μg l-1 Pb for juvenile snail growth has recently been determined for Lymnaea stagnalis, which is at or below the current USEPA water quality criterion for Pb. We characterized ionoregulation and acid-base balance in Pb-exposed L. stagnalis (young adults ∼1 g) to investigate the mechanisms underlying this hypersensitivity. After 21-day exposure to 18.9 μg l-1 Pb, Ca2+ influx was significantly inhibited (39%) and corresponding net Ca2+ flux was significantly reduced from 224 to -23 nmol g-1 h-1. An 85% increase in Cl- influx was also observed, while Na+ ion transport appeared unaffected. Finally, a marked alkalosis of extracellular fluid was observed with pH increasing from 8.35 in the control to 8.65 in the 18.9 μg l-1 Pb-exposed group. Results based on direct measurement of Ca2+ influx in 1 g snails gave an influx nearly an order of magnitude higher (750 nmol g-1 h-1) than in comparably sized fish in similar water chemistry. Under control conditions, specific growth rate in newly hatched snails was estimated at 16.7% per day over the first 38-day post-hatch and whole body Ca2+ concentrations were relatively constant at ∼1100 nmol g-1 over this period. Based on these data, it is estimated that newly hatched snails have net Ca2+ uptake rates on the order of 7600 nmol g-1 h-1. A model was developed integrating these data and measured inhibition of Ca2+ influx rates of 13.4% and 38.7% in snails exposed to 2.7 and 18.9 μg l-1 Pb, respectively. The model estimates 45% and 83% reductions in newly hatched snail growth after 30-day exposure in these two Pb-exposed groups. These results compare well with previous direct measurements of 47% and 90% reductions in growth at similar Pb concentrations, indicating the high net Ca2+ uptake is the controlling factor in observed Pb hypersensitivity.

AB - Previous studies have shown that freshwater pulmonate snails of the genus Lymnaea are exceedingly sensitive to chronic Pb exposure. An EC20 of <4 μg l-1 Pb for juvenile snail growth has recently been determined for Lymnaea stagnalis, which is at or below the current USEPA water quality criterion for Pb. We characterized ionoregulation and acid-base balance in Pb-exposed L. stagnalis (young adults ∼1 g) to investigate the mechanisms underlying this hypersensitivity. After 21-day exposure to 18.9 μg l-1 Pb, Ca2+ influx was significantly inhibited (39%) and corresponding net Ca2+ flux was significantly reduced from 224 to -23 nmol g-1 h-1. An 85% increase in Cl- influx was also observed, while Na+ ion transport appeared unaffected. Finally, a marked alkalosis of extracellular fluid was observed with pH increasing from 8.35 in the control to 8.65 in the 18.9 μg l-1 Pb-exposed group. Results based on direct measurement of Ca2+ influx in 1 g snails gave an influx nearly an order of magnitude higher (750 nmol g-1 h-1) than in comparably sized fish in similar water chemistry. Under control conditions, specific growth rate in newly hatched snails was estimated at 16.7% per day over the first 38-day post-hatch and whole body Ca2+ concentrations were relatively constant at ∼1100 nmol g-1 over this period. Based on these data, it is estimated that newly hatched snails have net Ca2+ uptake rates on the order of 7600 nmol g-1 h-1. A model was developed integrating these data and measured inhibition of Ca2+ influx rates of 13.4% and 38.7% in snails exposed to 2.7 and 18.9 μg l-1 Pb, respectively. The model estimates 45% and 83% reductions in newly hatched snail growth after 30-day exposure in these two Pb-exposed groups. These results compare well with previous direct measurements of 47% and 90% reductions in growth at similar Pb concentrations, indicating the high net Ca2+ uptake is the controlling factor in observed Pb hypersensitivity.

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