4.7 Article

Physiological responses to temperature and haeme synthesis modifiers in earthworm Lumbricus terrestris (Annelida: Oligochaeta)

Journal

ENVIRONMENTAL TOXICOLOGY
Volume 27, Issue 1, Pages 1-10

Publisher

WILEY
DOI: 10.1002/tox.20604

Keywords

temperature; earthworm; respiration; hemoglobin; electron transport system

Funding

  1. NIGMS [GM-06344-01]

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Earthworms (Lumbricus terrestris) acclimated at 2 degrees and 6 degrees C above their average habitat temperature (10 degrees C) had respectively 15 and 40% higher rate of respiration than those at habitat temperature. At 14 degrees C, the rate of respiration and blood hemoglobin (Hb) concentration both increased by similar to 60 and 50%, respectively, of the values at habitat temperature. At higher temperatures the rate of respiration and Hb synthesis started decreasing. At 20-23 degrees C, the respiration and Hb concentration decreased respectively by about 85% and 35% of that at 14 degrees C. Decrease in blood Hb concentration at higher temperatures appeared to be due to the lowering of the activity of blood enzyme delta-aminolaevulinic acid dehydratase (ALAD). Exposure of 20-23 degrees C-acclimated pale worms to ALAD inhibitor (lead), lowered the already compromised rate of respiration and blood Hb concentration; while exposure to hexachlorobenzene (HCB, inducer of haeme synthesis) and ferric chloride (enhancer of haeme synthesis) did not overcome the inhibitory effect of high temperature on Hb synthesis. At 2023 degrees C the affinity of Hb for oxygen also decreased as indicated by the lowering of oxy-Hb (HbO) concentration in blood. The lowering of concentration of blood Hb and its affinity for oxygen may lower the amount of oxygen delivered to cells, which may limit the level of aerobic metabolism (glycolysis, oxidative phosphorylation), as indicated by an increase in blood glucose concentration and a decrease in in vitro activities of mitochondrial electron transport system components (ETS) namely NADH-cytochrome c reductase, succinate dehydrogenase, cytochrome c oxidase, and ATPases. Although the oxygen concentration in air, at sea level, does not decrease significantly from 6 degrees to 20-23 degrees C (lack of hypoxia), lowering of both Hb and HbO concentrations by high temperature may cause significant hypoxemia. The latter may lead to inhibition of the activity of muscle mitochondrial respiratory enzymes (ETS). The resulting inhibition of ATP synthesis and hydrolysis may cause deficit of energy needed for peristalsis/fictive locomotion of body and heart muscles (as indicated by a decrease in heart rate) to facilitate diffusion and transport of gases. The upper critical temperature (20-23 degrees C) also slows down the heart rate and causes hyperosmotic stress (hypovolemia). Thus, a rise in soil temperature above 18 degrees C, which inhibits Hb synthesis, Hb oxygenation, and mitochondrial ETS activity, and slows down the heart rate and causes hyperosmotic stress, can make this and higher temperatures lethal to populations of these earthworms, especially in the presence of metabolic inhibitors and respiratory poisons. (c) 2010 Wiley Periodicals, Inc. Environ Toxicol, 2012.

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