Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab,Maja squinado

Abstract

Frederich, Markus, and Hans O. Pö rtner. Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am J Physiol Regulatory Integrative Comp Physiol 279: R1531-R1538, 2000.-Geographic distribution limits of ectothermal animals appear to be correlated with thermal tolerance thresholds previously identified from the onset of anaerobic metabolism. Transition to these critical temperatures was investigated in the spider crab (Maja squinado) with the goal of identifying the physiological processes limiting thermal tolerance. Heart and ventilation rates as well as PO 2 in the hemolymph were recorded on-line during progressive temperature change between 12 and 0°C (1°C/h) and between 12 and 40°C (2°C/h). Lactate and succinate were measured in tissues and hemolymph after intermediate or final temperatures were reached. High levels of hemolymph oxygenation suggest that an optimum range of aerobic performance exists between 8 and 17°C. Thermal limitation may already set in at the transition from optimum to pejus (pejus ϭ turning worse, progressively deleterious) range, characterized by the onset of a decrease in arterial PO 2 due to reduced ventilatory and cardiac performance. Hemolymph PO 2 values fell progressively toward both low and high temperature extremes until critical temperatures were reached at ϳ1 and 30°C, as indicated by low PO 2 and the onset of anaerobic energy production by mitochondria. In conclusion, the limited capacity of ventilation and circulation at extreme temperatures causes insufficient O 2 supply, thereby limiting aerobic scope and, finally, thermal tolerance. aerobic capacity; anaerobic metabolism; optodes; partial pressure of oxygen CRITICAL TEMPERATURES (T c ) have been defined for different marine invertebrate and fish species as being characterized by the onset of anaerobic metabolism, which is caused by a mismatch of O 2 demand and O 2 supply (for review, see Refs. 35 and 36). Extended exposure to temperatures above high T c or below low T c finally leads to death of the animal unless thermal acclimation, i.e., a shift of T c values, occurs (40, 51). One hypothesis is that the adjustment of mitochondrial density and capacity is involved in setting thermal tolerance limits and is therefore related to geographic distribution (35, 36). As a consequence, the relationship between O 2 availability to tissues and O 2 demand appears to be crucial for survival of exposure to temperature extremes. Study of the processes of O 2 uptake by ventilation and O 2 distribution by circulation therefore appear important to further our understanding of the O 2 limitation of thermal tolerance. Therefore, we chose to study these systemic aspects of thermal tolerance, selecting a crustacean, Maja squinado (Herbst), as a model organism. As yet, physiological studies of crustaceans have addressed temperature effects on O 2 consumption, heart and ventilatory performance, or growth (12-14, 16, 23, 34, 44). In most of these studies, temperatures were chosen wit...

Oxygen limited thermal tolerance in fish?

“…In this context, the question has regained interest whether limitations in oxygen availability or supply are involved in thermal limitation. Early evidence collected in marine invertebrates (annelids and sipunculids) demonstrated a transition to anaerobic metabolism (including mitochondrial anaerobiosis) at both cold and warm temperature extremes (Zielinski and Pörtner, 1996;Sommer et al, 1997), later on confirmed in crustaceans (Frederich and Pörtner, 2000) and molluscs, i.e. bivalves, gastropods and cephalopods (Pörtner and Zielinski, 1998;Pörtner et al, 1999;Peck et al, 2002;Sokolova and Pörtner, 2003).…”

“…A temperature dependent optimization of oxygen supply capacity was visible in the form of maximized arterial P O 2 within a limited temperature range, equivalent to the window of mean temperatures in the natural environment (Frederich and Pörtner, 2000). Limitation of both ventilatory and circulatory capacities towards thermal extremes was found to explain these patterns of body fluid oxygenation (Zielinski and Pörtner, 1996;Frederich and Pörtner, 2000).…”

“…bivalves, gastropods and cephalopods (Pörtner and Zielinski, 1998;Pörtner et al, 1999;Peck et al, 2002;Sokolova and Pörtner, 2003). Studies in a sipunculid (Sipunculus nudus, Zielinski and Pörtner, 1996) and the spider crab (Maja squinado, Frederich and Pörtner, 2000) investigated the pattern of coelomic fluid/haemolymph oxygen tensions in relation to warming and/or cooling and demonstrated development of hypoxia which preceded the onset of anaerobic metabolism towards both cold and warm temperature extremes. A temperature dependent optimization of oxygen supply capacity was visible in the form of maximized arterial P O 2 within a limited temperature range, equivalent to the window of mean temperatures in the natural environment (Frederich and Pörtner, 2000).…”

“…Studies in a sipunculid (Sipunculus nudus, Zielinski and Pörtner, 1996) and the spider crab (Maja squinado, Frederich and Pörtner, 2000) investigated the pattern of coelomic fluid/haemolymph oxygen tensions in relation to warming and/or cooling and demonstrated development of hypoxia which preceded the onset of anaerobic metabolism towards both cold and warm temperature extremes. A temperature dependent optimization of oxygen supply capacity was visible in the form of maximized arterial P O 2 within a limited temperature range, equivalent to the window of mean temperatures in the natural environment (Frederich and Pörtner, 2000). Limitation of both ventilatory and circulatory capacities towards thermal extremes was found to explain these patterns of body fluid oxygenation (Zielinski and Pörtner, 1996;Frederich and Pörtner, 2000).…”

Thermal physiology of the common eelpout (Zoarces viviparus)

“…hypoxia) only if the conductance of oxygen flow increases and there is indeed a number of mechanisms to fulfil this precondition (increasing ventilation, increasing blood circulation, etc. ; Frederich and Po¨rtner 2000). However, all of these mechanisms have certain limits of functional capacity.…”