Freshwater bivalves inhabit regions that can experience periods of very low oxygen tension (hypoxia). Such conditions can arise in the deeper regions of productive lakes due to oxygen utilization by respiration, and can also happen in shallower reaches when pockets of hypoxic water move into such areas by means of currents or other mixing events. Although bivalves are capable of moving, they generally remain sessile for extended periods of time, achieving gas and ion exchange, feeding and reproduction through ventilation of an internalized mantle cavity. Byrne and McMahon (1990) demonstrated that members of the freshwater bivalve group Unionidae, Anodonta grandis, could maintain oxygen uptake efficiency down to oxygen tensions as low as 10-12% air saturation (Byrne and McMahon, 1990). Below a critical oxygen tension, the freshwater bivalve would abruptly cease ventilation and would presumably rely on anaerobic means of metabolism, or depend upon limited oxygen stores within the body. Later studies (Byrne and Heiner, unpubl.) showed that freshwater bivalves under severe hypoxic conditions would indeed shut down ventilation of the mantle cavity over an extended period of time, but that brief, phasic ventilatory episodes would occur, during which some exchange of mantle cavity content with the environment was achieved. We speculate that such exchanges serve to rid the mantle cavity of accumulated wastes, in particular carbon dioxide. Byrne et al. (1991) showed that aerially exposed bivalves accumulate CO2 in the blood (hemolymph) and periodically release this load during episodic mantle cavity ventilation events in air; a very similar situation as seen in clams experiencing aquatic hypoxia.
Bivalves have a very dilute blood ionic composition, but are still much more concentrated than the freshwater medium in which they live. During hypoxia clams must maintain internal physiological stability in order to carry out essential life functions. They must keep adequate quantities of mineral ions within the body despite losses to the environment. Byrne and McMahon (1994) summarized previous studies that showed freshwater clams maintaining ionic homeostasis even under conditions of extended aerial exposure. Accumulated CO2 resulted in an acidosis which was buffered by mobilization of shell components, in particular calcium and bicarbonate. On return to freshwater, bivalves demonstrated increased rates of ion transport, as well as a return to pre-exposure conditions within a short time period (Byrne et al. 1991). During an aquatic hypoxic event energy stores inside the animal are presumably reduced, thereby affecting energy requiring mechanisms, e.g. ion transport. Also, reduced access to the environment may disrupt ionic homeostasis as a result of CO2 accumulation, in that the acidosis that would ensue may cause changes in the calcium and bicarbonate buffers in the hemolymph.
We examined the change in blood ionic composition during hypoxia in a local clam, Lampsilis radiata, as well as the progress of recovery in normally oxygenated water. During a 96h period of severe hypoxia blood levels of both sodium and chloride declined, whereas calcium levels increased. Chloride levels declined from 10.2 ± 0.2 mmol/L to 7.8 ± 0.2 after 96h (P<0.05) whereas sodium concentrations went from 28.2 ± 0.3 to 20.8 ± 0.4 mmol/L (P<0.05) in the same period. During recovery in normoxic water, hemolymph sodium and chloride returned to control values within 6h (P>0.05). Hemolymph calcium content increased during hypoxia (4.29±0.3 to 7.1±0.3 after 96h; P<0.05) suggesting that acidosis was taking place with accumulation of respiratory CO2. Hemolymph calcium also returned to control conditions within 6h of recovery in freshwater.
Using radiolabelled sodium (22Na) we partitioned the sodium flux during and after hypoxia. These specific ion flux studies showed that the losses were due to declines in active transport of ions rather than increases in the rate of ion loss. Sodium influx declined from 4.39 ± 1.21 µmol/g/h to 1.90± 0.30 after 96h hypoxia, but was elevated to 5.85 ± 0.50 within 2h of recovery, and returned to control values within 24h. There was no significant change in rate of efflux of sodium as a result of hypoxia suggesting that losses of hemolymph ions are due to reductions in epithelial ion transport rather than increases in ion loss. We also showed that bivalves are in a net ion loss situation for other ions (calcium, potassium, magnesium) during hypoxia, but that much of this loss is recovered within a short time in normoxic conditions.
Our study demonstrated that freshwater bivalves loose essential ions during hypoxia and that this loss is primarily due to reductions in the rate of ion transport from the medium to the animal. This may be due to reduction in energy stores, or mantle cavity ventilation, or both. These ions are replaced within a very short time under normal oxygen conditions, partially as a result of elevated rates of epithelial ion transport. As bivalves must withstand extended periods of hypoxia, their strategy seems to be reduction in energy utilization while protecting existing ionic stores through closure of valves. Periodic gaping may be a method for removing accumulated CO2 as calcium levels in the hemolymph rise significantly, or other wastes. Rapid recovery in normoxia returns animals to pre-hypoxic conditions within a very short time. Freshwater bivalves maintain ionic homeostasis during and after hypoxia.
References
Byrne, R.A., B.N. Shipman, N.J. Smatresk, T.H. Dietz and R.F. McMahon. (1991). Acid-base balance during emergence in the freshwater bivalve, Corbicula fluminea. Physiological Zoology 64: 748-766.
Byrne, R.A. and R.F. McMahon. (1994). Behavioral and physiological responses to emersion in freshwater bivalves. American Zoologist: 34: 194-204.
Byrne, R.A. and B.R. McMahon. (1990). Acid-base and ion regulatory responses to environmental O2 and CO2 in a freshwater bivalve. American Zoologist 30: