Cardiovascular and respiratory physiology of tuna: adaptations for support of exceptionally high metabolic rates

Abstract

Both physical and physiological modifications to the oxygen transport system promote high metabolic performance of tuna . The large surface area of the gills and thin blood-water barrier means that 02 utilization is high (30-50%) even when ram ventilation approaches 101 min-'kg-' . The heart is extremely large and generates peak blood pressures in the range of 70-100 mmHg at frequencies of 1-5 Hz . The blood 02 capacity approaches 16 ml dl-'and a large Bohr coefficient (-0 .83 to -1 .17) ensures adequate loading and unloading of 02 from the well buffered blood (20.9 slykes) . Tuna muscles have aerobic oxidation rates that are 3-5 times higher than in other teleosts and extremely high glycolytic capacity (150 µmot g' lactate generated) due to enhanced concentration of glycolytic enzymes . Gill resistance in tuna is high and may be more than 50% of total peripheral resistance so that dorsal aortic pressure is similar to that in other active fishes such as salmon or trout . An 0, delivery/demand model predicts the maximum sustained swimming speed of small yellowfin and skipjack tuna is 5 .6 BL s' and 3 .5 BL sec', respectively. The surplus 0, delivery capacity at lower swimming speeds allows tuna to repay large oxygen debts while swimming at 2-2 .5 BL s -' . Maximum oxygen consumption (7-9 x above the standard metabolic rate) at maximum exercise is provided by approximately 2 x increases in each of heart rate, stroke volume, and arterial-venous 02 content difference .

Moving with the beat: heart rate and visceral temperature of free-swimming and feeding bluefin tuna

“…These maximum values agree with previous predictions and are exceptional among fishes at the same temperature (Brill & Bushnell 1991bBushnell & Jones 1994;Farrell 1996;), primarily due to the large cardiac stroke volume resulting from the large relative ventricular mass of tuna (Bushnell & Jones 1994). Additionally, tuna have blood oxygen carrying capacities that rival mammalian values ( Jones et al 1986;Brill & Bushnell 1991a,b;Graham & Dickson 2004;Clark et al 2008), and so it is evident how they may achieve extremely high rates of oxygen consumption without extraordinarily high f H .…”

Cardiorespiratory physiology and swimming energetics of a high-energy-demand teleost, the yellowtail kingfish (Seriola lalandi)

“…This species has been reported to have a SMR greater than most other high performance fishes and approaching that of the tunas (Yamamoto et al, 1981;Korsmeyer and Dewar, 2001), although these data may have been affected by stress due to heavy instrumentation and confinement to a small static respirometer. Interestingly, the published resting f H value of this species at 25°C is approximately 90·beats·min -1 (Ishimatsu et al, 1990;Lee, K. S. et al, 2003a), which is quite high for a resting teleost, and may reflect a high maximum f H considering that a twofold increase during exercise is not uncommon (Bushnell and Jones, 1994;Korsmeyer et al, 1997a;Altimiras and Larsen, 2000;Clark et al, 2005).…”

“…Gallaugher et al, 2001;Beaumont et al, 2003;Blank et al, 2004), implies that highly regulated blood flows are of secondary importance to an enhanced blood oxygen-carrying capacity and tissue oxygen extraction. Values given in parentheses are from the present study for S. lalandi, whereas all other values are for S. quinqueradiata [~20°C data compiled from (Yamamoto et al, 1981;Yamamoto, 1991;Lee, K. S. et al, 2003b); 25°C data compiled from (Ishimatsu et al, 1990;Ishimatsu et al, 1997;Lee, K. S. et al, 2003a)]; data for rainbow trout were compiled from Randall et al, 1967;Stevens and Randall, 1967;Kiceniuk and Jones, 1977;Brill and Bushnell, 1991;Farrell and Jones, 1992;Gallaugher et al, 1995;Altimiras and Larsen, 2000;Brill and Bushnell, 2001); data for tunas (skipjack and yellowtail) were compiled from (Bushnell et al, 1990;Brill and Bushnell, 1991;Jones et al, 1993;Bushnell and Jones, 1994;Korsmeyer et al, 1997a;Korsmeyer et al, 1997b;Brill and Bushnell, 2001). …”

“…Some high performance species possess an enhanced blood oxygen-carrying capacity owing to higher levels of haemoglobin, which acts to augment (Ca O 2-Cv O 2) such that extraordinary increases in V b are not necessary to attain maximum levels of M O 2 (Brill and Bushnell, 2001;Graham and Dickson, 2004). Nevertheless, many teleosts utilize similar proportional increases in V b and (Ca O 2-Cv O 2) to satisfy an increase in M O 2 with exercise (Brill and Bushnell, 1991;Bushnell and Jones, 1994;Korsmeyer et al, 1997b).…”

Swimming performance studies on the eastern Pacific bonitoSarda chiliensis, a close relative of the tunas (family Scombridae) I. Energetics

“…In addition, there may be functional costs requiring a high SMR, such as the osmoregulatory load imposed by a larger gill surface area (Brill, 1987(Brill, , 1996Benetti et al, 1995;. Tunas also have the added costs associated with the aerobic requirements of a larger and thicker-walled ventricle that has both a high cardiac output and a high systolic pressure (Graham et al, 1983;Bushnell, 1991, 2001;Bushnell and Jones, 1994;Graham and Dickson, 2000). Added to these may be a higher aerobic cost associated with the more aerobic white muscle of tunas.…”