All puffed out: do pufferfish hold their breath while inflated?

The inflation response of pufferfishes is one of the most iconic predator defence strategies in nature. Current dogma suggests that pufferfish inflation represents a breath-holding response, whereby gill oxygen uptake ceases for the duration of inflation and cutaneous respiration increases to compensate. Here, we show that the black-saddled pufferfish (Canthigaster valentini) has an excellent capacity for oxygen uptake while inflated, with uptake rates increasing to five-times that of resting levels. Moreover, we show that this species has negligible capacity for cutaneous respiration, concluding that the gills are the primary site of oxygen uptake while inflated. Despite this, post-deflation recovery of aerobic metabolism took an average of 5.6 h, suggesting a contribution of anaerobic metabolism during pre-inflation activity and during the act of ingesting water to achieve inflation.

Effects of body mass on physiological and anatomical parameters of mature salmon: evidence against a universal heart rate scaling exponent.

The influence of body mass (M(b)) on the physiology of large, adult fish is poorly understood, in part because of the logistical difficulties of studying large individuals. For the first time, this study quantified the influence of M(b) on the resting heart rate (f(H)), blood properties and organ masses of adults of a large-growing fish species, the Chinook salmon (Oncorhynchus tshawytscha). Surgically implanted biologgers measured f(H) and acceleration activity in sexually mature, male fish ranging in M(b) from 2.7 to 16.8 kg while they roamed freely in a controlled water body at ∼8°C. Blood parameters (at surgery and at death) and body organ masses (at death) were measured to investigate interrelationships with M(b). The scaling exponents for both f(H) and acceleration activity were not significantly different from zero. The lack of scaling of f(H) with M(b) contrasts with the situation for birds and mammals. All blood parameters were independent of M(b), while the masses of the compact myocardium, ventricle and spleen each scaled near-isometrically with M(b). These data raise the possibility that blood oxygen carrying capacity, mass-specific cardiac output and cardiac power output are maintained across M(b) in adult Chinook salmon. Biologging and biotelemetry should advance investigations into the effects of M(b) on the physiology and behaviour of large fish, where current knowledge lags far behind that of birds and mammals.

Simultaneous biologging of heart rate and acceleration, and their relationships with energy expenditure in free-swimming sockeye salmon (Oncorhynchus nerka).

Monitoring the physiological status and behaviour of free-swimming fishes remains a challenging task, although great promise stems from techniques such as biologging and biotelemetry. Here, implanted data loggers were used to simultaneously measure heart rate (f (H)), visceral temperature, and a derivation of acceleration in two groups of wild adult sockeye salmon (Oncorhynchus nerka) held at two different water speeds (slow and fast). Calibration experiments performed with individual fish in a swim tunnel respirometer generated strong relationships between acceleration, f (H), tail beat frequency and energy expenditure over a wide range of swimming velocities. The regression equations were then used to estimate the overall energy expenditure of the groups of fish held at different water speeds. As expected, fish held at faster water speeds exhibited greater f (H) and acceleration, and correspondingly a higher estimated energy expenditure than fish held at slower water speeds. These estimates were consistent with gross somatic energy density of fish at death, as determined using proximate analyses of a dorsal tissue sample. Heart rate alone and in combination with acceleration, rather than acceleration alone, provided the most accurate proxies for energy expenditure in these studies. Even so, acceleration provided useful information on the behaviour of fish and may itself prove to be a valuable proxy for energy expenditure under different environmental conditions, using a different derivation of the acceleration data, and/or with further calibration experiments. These results strengthen the possibility that biologging or biotelemetry of f (H) and acceleration may be usefully applied to migrating sockeye salmon to monitor physiology and behaviour, and to estimate energy use in the natural environment.

Reduced and reversed temperature dependence of blood oxygenation in an ectothermic scombrid fish: implications for the evolution of regional heterothermy?

Tunas (family Scombridae) are exceptional among most teleost fishes in that they possess vascular heat exchangers which allow heat retention in specific regions of the body (termed 'regional heterothermy'). Seemingly exclusive to heterothermic fishes is a markedly reduced temperature dependence of blood-oxygen (blood-O(2)) binding, or even a reversed temperature dependence where increasing temperature increases blood-O(2) affinity. These unusual binding properties have been documented in whole blood and in haemoglobin (Hb) solutions, and they are hypothesised to prevent oxygen loss from arteries to veins within the vascular heat exchangers and/or to prevent excessive oxygen unloading to the warm tissues and ensure an adequate supply of oxygen to tissues positioned efferent to the heat exchangers. The temperature sensitivity of blood-O(2) binding has not been characterised in an ectothermic scombrid (mackerels and bonitos), but the existence of the unusual binding properties in these fishes would have clear implications for their proposed association with regional heterothermy. Accordingly, the present study examined oxygenation of whole blood of the chub mackerel (Scomber japonicus) at 10, 20 and 30 degrees C and at 0.5, 1 and 2% CO(2). Oxygen affinity was generally highest at 20 degrees C for all levels of CO(2). Temperature-independent binding was observed at low (0.5%) CO(2), where the PO(2) at 50% blood-O(2) saturation (P (50)) was not statistically different at 10 and 30 degrees C (2.58 vs. 2.78 kPa, respectively) with an apparent heat of oxygenation (H degrees ) close to zero (-6 kJ mol(-1)). The most significant temperature-mediated difference occurred at high (2%) CO(2), where the P (50) at 10 degrees C was twofold higher than that at 20 degrees C with a corresponding H degrees of +43 kJ mol(-1). These results provide clear evidence of independent and reversed open-system temperature effects on blood oxygenation in S. japonicus, and it is therefore speculated that these unusual blood-O(2) binding characteristics may have preceded the evolution of vascular heat exchangers and regional heterothermy in fishes.

Sex differences in circulatory oxygen transport parameters of sockeye salmon (Oncorhynchus nerka) on the spawning ground.

Upon reaching sexual maturity, several species of male salmonids possess a relative ventricular mass (rM(V)) that may be up to 90% larger than females. This can increase maximum cardiac stroke volume and power output, which may be beneficial to increasing the oxygen transport capacity of male salmonids during the spawning period. It may be further hypothesized, therefore, that other variables within the circulatory oxygen transport cascade, such as blood oxygen-carrying capacity and heart rate, are similarly enhanced in reproductively mature male salmonids. To test this idea, the present study measured a range of circulatory oxygen transport variables in wild male and female sockeye salmon (Oncorhynchus nerka) during their spawning period, following a 150 km migration from the ocean. The rM(V) of male fish was 13% greater than females. Conversely, the haemoglobin concentration ([Hb]) of female fish was 19% higher than males, indicative of a greater blood oxygen-carrying capacity (138 vs. 116 ml O2 l(-1), respectively). Surgically implanted physiological data loggers revealed a similar range in heart rate for both sexes on the spawning ground (20-80 beats min(-1) at 10 degrees C), with a tendency for male fish to spend a greater percentage of time (64%) than females (49%) at heart rates above 50 beats min(-1). Male fish on average consumed significantly more oxygen than females during a 13-h respirometry period. However, routine oxygen consumption rates (.)MO2 ranged between 1.5 and 8.5 mg min(-1) kg(-1) for both sexes, which implies that males did not inherently possess markedly higher routine aerobic energy demands, and suggests that the higher [Hb] of female fish may compensate for the smaller rM(V). These findings reject the hypothesis that all aspects of the circulatory oxygen transport cascade are inherently superior in male sockeye salmon. Instead, it is suggested that any differences in (.)MO2 between sexually mature male and female sockeye salmon can likely be attributed to activity levels.