Hypoxia tolerance associated with activity reduction is a key adaptation for Laternula elliptica seasonal energetics

Abstract

Seasonal dormancy is a widespread mechanism for reducing energy expenditure during periods of low energy availability. Seasonal variation in activity and the cost of pumping water through the siphons were investigated to estimate the importance of activity regulation to the seasonal energy budget of the Antarctic clam, Laternula elliptica. In the laboratory, a metabolic rate of 26.35 micromol O(2) h(-1) was estimated for a 50-mm shell length L. elliptica pumping water at -0.4 degrees C. In the field, the proportion of time siphons were visible at the sediment surface varied seasonally (32% visible in June/July compared to 86% in December/January). L. elliptica were actively pumping for a minimum of 19% of each 24-h period during winter (August) compared to a summer maximum when animals were actively pumping for 73% of the time (February). This resulted in a 3.7-fold seasonal difference in the calculated energy consumption of a 50-mm L. elliptica (19.2 micromol O(2) h(-1) in February versus 5.0 micromol O(2) h(-1) in August), which closely matches the 3.0-fold seasonal variation in metabolic rate found previously. Seasonal variation in activity could therefore be responsible for much of the seasonal difference in energy consumption of L. elliptica. Inter-annual variation in timing of the seasonal activity maxima (January 2004 and March 1999) was correlated with variation in the timing of the summer plankton bloom in Ryder Bay. In the laboratory, periods of extended siphon closure (133 +/- 114 min, mean +/- SD) were accompanied by long periods of heart arrhythmia (167 +/- 135 min), during which time blood oxygen levels dropped to values close to zero. Heart arrhythmia is most likely part of a hypo-metabolic adaptation to reduce energy costs during extended periods of siphon closure. Physiological and behavioural dormancy, with associated hypoxia tolerance, appear to be key mechanisms controlling the seasonal energy budget of L. elliptica.

A Metabolic Model for the Ocean QuahogArctica islandica—Effects of Animal Mass and Age, Temperature, Salinity, and Geography on Respiration Rate

“…Another behavioral characteristic of Arctica are shorter lasting apneal phases (APs), which do not necessarily involve reduction of metabolic rate (MRD). These transient respiration breaks (i.e., ventilation stops) which last for no more than a couple of minutes, have already been described for other bivalve species (Morley et al 2007). …”

“…Apparently, AP is not caused by external triggers, but reflects an internal behavioral pattern in the bivalves. Apneal behavior or to the contrary short bouts of elevated respiration have already been observed in other cold adapted bivalves, such as the Antarctic mud clams Laternula elliptica (Morley et al 2007) and the protobranch Yoldia eightsi (Abele et al 2001). There is a general trend in bivalves to keep mantle water PO 2 on low and protective levels, and water breathers like Arctica islandica which live in the sediment water interface, must cope with fluctuant and up to normoxic oxygen levels in the inhaled water.…”

Bivalve models of aging and the determination of molluscan lifespans

“…Periodic times of low food intake might induce autophagic activity and possibly apoptosis in these animals, clean their cellular biochemical background from oxidized intermediates, and eliminate damaged cells and mitochondria. Regional and seasonal cold climates obviously favour frequent metabolic rate depression in bivalves like M. margaritifera (Ziuganov, 2004), L. elliptica (Morley et al, 2007) or A. islandica (Taylor, 1976). Slower growth, increased stress hardiness and shell repair in the Arctic and subarctic compared to warm adapted populations in Spain (M. margaritifera) or in the North Sea (A. islandica) support this hypothesis.…”

Extreme Phenotypic Plasticity in Metabolic Physiology of Antarctic Demosponges

“…These low food periods largely coincide with the coldest water temperatures and at polar latitudes the seasonal difference in phytoplankton productivity is amongst the highest of any ocean, whilst the shallow water temperature variation is amongst the lowest (Venables et al, 2013). Feeding, growth, and reproductive investment of primary consumers are therefore often coupled to the brief austral summer, with reduced feeding and metabolic activity for several months during winter (Gruzov, 1977;Clarke, 1988;Clarke et al, 1988;Morley et al, 2007). Whilst winter dormancy in polar species is common, and can be extreme (e.g., Bryozoan; Barnes and Peck, 2005), in other, even closely related species of suspension feeders, periods of reduced metabolic, and feeding activity can be as short as 1 month (Barnes and Clarke, 1995).…”