Richard W. Brill

Selective advantages conferred by the high performance physiology of tunas, billfishes, and dolphin fish☆

Abstract Tunas are extensively distributed throughout worlds oceans and grow and reproduce fast enough to support one of the worlds largest commercial fisheries. Yet they are apex predators living in the energy depauperate pelagic environment. It is often presumed that tunas evolved their specialized anatomy, physiology, and biochemistry to be capable of (a) high maximum swimming speeds, (b) high sustained swimming speeds, and/or (c) very efficient swimming, all of which help account for their wide distribution and reproductive success. However, a growing body of data on the energetics and physiological abilities of tunas do not support these assumptions. The three things demonstratively “high performance” about tunas, and probably other pelagic species such as marlin (Makaira spp. and Tetrapturus spp.) and dolphin fish (Coryphaena spp.), are (a) rates of somatic and gonadal growth, (b) rates of digestion, (c) rates of recovery from exhaustive exercise (i.e., clearance of muscle lactate and the concomitant acid load). All of these are energy consuming processes requiring rates of oxygen and substrate delivery above those needed by the swimming muscles for sustained propulsion and for other routine metabolic activities. I hypothesize that the ability of high performance pelagic species (tunas, billfishes, and dolphin fish) to deliver oxygen and metabolic substrates to the tissues at high rates evolved to permit rapid somatic and gonadal growth, rapid digestion, and rapid recovery from exhaustive exercise (abilities central to success in the pelagic environment), not exceptionally high sustained swimming speeds.

Vertical and horizontal movements of striped marlin (Tetrapturus audax) near the Hawaiian Islands, determined by ultrasonic telemetry, with simultaneous measurement of oceanic currents

We measured the vertical and horizontal movements of striped marlin (Tetrapturus audax) off the leeward coast of the Island of Hawaii between 20 November and 18 December 1992 while simultaneously gathering data on water temperature and oceanic currents. Fish movements were monitored by ultrasonic depth-sensitive transmitters, depth-temperature profiles by an expendable bathythermograph system, and oceanic current patterns by an acoustic Doppler current profiler. Like Indo-Pacific blue marlin (Makaira mazara), striped marlin near Hawaii spend >85% of their time in the mixed layer (i.e., above 90 m depth). The maximum depth for striped marlin appears to be limited by water temperatures 8 C° colder than the mixed layer, rather than by an absolute lower temperature. We also found that the horizontal displacements of some striped marlin can be strongly influenced by currents.

Predicting Postrelease Survival in Large Pelagic Fish

Abstract Sharks, turtles, billfish, and marine mammals are frequently caught accidentally in commercial fisheries. Although conservationists and fisheries managers encourage the release of these nontarget species, the long-term outcome of released animals is uncertain. Using blue sharks Prionace glauca, we developed a model to predict the long-term survival of released animals based on analysis of small blood samples. About 5% of the sharks were landed in obviously poor condition (lethargic and unresponsive to handling); these moribund sharks were sampled and euthanized. A subset of the remaining sharks was sampled and tagged with pop-up satellite archival tags (PSATs). Each of the PSATs that reported data (11 tags) showed that the sharks roamed at sea for at least 3 weeks postrelease. Five variables differentiated moribund sharks from survivors: Plasma Mg2+ (moribund, 1.57 ± 0.08 mM; survivor, 0.98 ± 0.05 mM; P < 0.00001), plasma lactate (moribund, 27.7 ± 4.1 mM; survivor, 5.80 ± 2.96 mM; P < 0.001), ery...

Oxygen transport and cardiovascular responses in skipjack tuna (Katsuwonus pelamis) and yellowfin tuna (Thunnus albacares) exposed to acute hypoxia

SummaryResponses to acute hypoxia were measured in skipjack tuna (Katsuwonus pelamis) and yellowfin tuna (Thunnus albacares) (≈1–3 kg body weight). Fish were prevented from making swimming movements by a spinal injection of lidocaine and were placed in front of a seawater delivery pipe to provide ram ventilation of the gills. Fish could set their own ventilation volumes by adjusting mouth gape. Heart rate, dorsal and ventral aortic blood pressures, and cardiac output were continuously monitored during normoxia (inhalant water (PO2>150 mmHg) and three levels of hypoxia (inhalant water PO2≈130, 90, and 50 mmHg). Water and blood samples were taken for oxygen measurements in fluids afferent and efferent to the gills. From these data, various measures of the effectiveness of oxygen transfer, and branchial and systemic vascular resistance were calculated. Despite high ventilation volumes (4–71·min-1·kg-1), tunas extract approximately 50% of the oxygen from the inhalant water, in part because high cardiac outputs (115–132 ml·min-1·kg-1) result in ventilation/perfusion conductance ratios (0.75–1.1) close to the theoretically ideal value of 1.0. Therefore, tunas have oxygen transfer factors (ml O2·min-1·mmHg-1·kg-1) that are 10–50 times greater than those of other fishes. The efficiency of oxygen transfer from water in tunas (≈65%) matches that measured in teleosts with ventilation volumes and order of magnitude lower. The high oxygen transfer factors of tunas are made possible, in part, by a large gill surface area; however, this appears to carry a considerable osmoregulatory cost as the metabolic rate of gills may account for up 70% of the total metabolism in spinally blocked (i.e., non-swimming) fish. During hypoxia, skipjack and yellowfin tunas show a decrease in heart rate and increase in ventilation volume, as do other teleosts. However, in tunas hypoxic bradycardia is not accompanied by equivalent increases, in stroke volume, and cardiac output falls as HR decreases. In both tuna species, oxygen consumption eventually must be maintained by drawing on substantial venous oxygen reserves. This occurs at a higher inhalant water PO2 (between 130 and 90 mmHg) in skipjack tuna than in yellowfin tuna (between 90 and 50 mmHg). The need to draw on venous oxygen reserves would make it difficult to meet the oxygen demand of increasing swimming speed, which is a common response to hypoxia in both species. Because yellowfin tuna can maintain oxygen consumption at a seawater oxygen tension of 90 mmHg without drawing on venous oxygen reserves, they could probably survive for extended periods at this level of hypoxia.

Ability of Archival Tags to Provide Estimates of Geographical Position Based on Light Intensity

We tested the ability of archival tags and their associated algorithms to estimate geographical position based on ambient light intensity by attaching six tags (three tags each from Northwest Marine Technologies [NMT] and Wildlife Computers [WC]) at different depths to a stationary mooring line in the Pacific Ocean (approx. 166°42′W, 24°00′N), for approximately one year (29-Aug-98 to 16-Aug-99). Upon retrieval, one tag each from the two vendors had malfunctioned: from these no data (NMT) or only partial data (WC) could be downloaded. An algorithm onboard the NMT tag automatically calculated geographical positions. For the WC tags, three different algorithms were used to estimate geographical positions from the recorded light intensity data. Estimates of longitude from all tags were significantly less variable than those for latitude. The mean absolute error for longitude estimates from the NMT tags ranged from 0.29 to 0.35°, and for the WC tags from 0.13 to 0.25°. The mean absolute error in latitude estimates from the NMT tags ranged from 1.5 to 5.5°, and for the WC tags from 0.78 to 3.50°. Ambient weather conditions and water clarity will obviously introduce errors into any geoposition algorithm based on light intensity. We show that by applying objective criteria to light level data, outliers can be removed and the variability of geographical position estimates reduced. We conclude that, although archival tags are suitable for questions of ocean basin-scale movements, they are not well suited for studies of daily fine scale movement patterns because of the likely magnitude of position estimate errors. For studies of fine scale movements in relation to specific oceanographic conditions, forage densities and distance scales of 100 km or less, other methods (e.g. acoustic tracking) remain the tool of choice.

Responses of Swimming Skipjack (Katsuwonus pelamis) and Yellowfin (Thunnus albacares) Tunas to Acute Hypoxia, and a Model of Their Cardiorespiratory Function

Heart rate and swimming-speed responses to acute hypoxia were measured in skipjack (Katsuwonus pelamis) and yellowfin tunas (Thunnus albacares). Swimming speeds began to increase in both species when O2 tension (Po2) reached approximately 124 mmHg. Bradycardia became significant in both species when Po2 reached approximately 130 mmHg. Heart rate fell with Po2 in yellowfin tuna, but, in skipjack tuna, it increased at the lowest O2 levels reached (89–70 mmHg). Bradycardia occurred in both species despite concomitant increases in swimming speed. A continuous infusion dye dilution system was used to monitor changes in ventilation volume (V̇g) during hypoxia in yellowfin tuna. As Po2 fell, V̇g increased. At the lowest O2 levels (109–90 mmHg), V̇g was 45% higher than during normoxia. Ventilation volume increased despite no concomitant increases in swimming speed. Data from these experiments were used to develop a model capable of predicting O2 demand and delivery, maximum sustainable (i.e., aerobic) swimming speeds, and minimum survivable O2 levels for yellowfin and skipjack tunas. Results from the model indicate that the cardiorespiratory system of tunas is capable of maximum rates of O2 delivery, even at low swimming speeds, that are approximately three times those of other active teleosts. We believe that, because the pelagic environment provides no place to hide and rest following exhaustive activity, the ability of the cardiorespiratory system of tunas to deliver O2 to the tissues at high rates evolved for the rapid repayment of O2 debts rather than to permit exceptionally high sustained swimming speeds.

The cardiovascular system of tunas

Publisher Summary This chapter examines the different aspects of cardiovascular system of tunas. Tunas have high metabolic rates and are obligate ram ventilators. They suffocate rapidly if prevented from swimming, so special care must be taken to ensure that ventilatory requirements are met during all stages of an experiment. The rate of oxygen movement across the gill respiratory epitbelium is directly proportional to functional surface area and inversely proportional to the thickness of diffusion barrier. Tunas have gill surface areas approximately seven to nine times larger and gill blood–water barrier thicknesses approximately an order of magnitude less than those of rainbow trout. The maximum increase in heart rate observed in swimming yellowfin tuna matches that seen in nonswimming fish, whose vagal control of heart rate has been blocked by the injection of atropine. The routine stroke volume of skipjack and yellowfin tuna hearts approaches the maximum stroke volume of other fishes. It is found that in spite of a fixed stroke volume, the skipjack tunas high heart rate can easily accommodate its documented maximum metabolic demand.

Oxygen sensitive afferent information arising from the first gill arch of yellowfin tuna

Single nerve fiber discharge was recorded from O2 sensitive receptors in the first gill arch of the yellowfin tuna, Thunnus albacares, in vitro. These receptors were innervated by the vagus nerve and increased their discharge in response to decreasing perfusion rate, decreasing perfusion PO2 and, in most fibers, to decreasing external PO2. Fibers responding to environmental hypoxia exhibited an exponential increase in discharge to decreasing external PO2 with a sensitivity similar to that exhibited by cat carotid body chemoreceptors. Indirect evidence suggests that these receptors are located near the gill vasculature and are more sensitive to changes in arterial PO2 than water PO2. Their response characteristics and hypoxic sensitivity strongly implicate them as the afferent limb in the cardiac responses and perhaps also the ventilatory responses exhibited by tuna to environmental hypoxia.

Basic concepts relevant to heat transfer in fishes, and their use in measuring the physiological thermoregulatory abilities of tunas

SynopsisAerobic heat production and heat loss via the gills are inexorably linked in all water breathing teleosts except tunas. These processes are decoupled in tunas by the presence of vascular counter-current heat exchangers, and sustained (i.e., steady state) muscle temperatures may exceed water temperature by 10° C or more in larger individuals. The presence of vascular counter-current heat exchangers is not clearly advantageous in all situations, however. Mathematical models predict that tunas could overheat during strenuous activity unless the efficacy of vascular heat exchangers can be reduced, and that they may be activity limited in warmer waters. Tunas may likewise be forced out of potentially usable habitats as they grow because they have to occupy cooler waters. Vascular counter-current heat exchangers also slow rates of heating and cooling. A reduced rate of muscle temperature decrease is clearly advantageous when diving into colder water to chase prey or avoid predators. A reduced rate of heat gain from the environment would be disadvantageous, however, when fish return to the warmer surface waters. When subjected to changes in ambient temperature, tunas cannot defend a specific body temperature and do not thermoregulate in the mammalian sense. Yet when appropriately analyzed, data taken under steady state and non-steady state conditions indicate that tunas are not strictly prisoners of their own thermoconserving mechanisms. They apparently can modify overall efficiency of their vascular counter-current heat exchangers and thus avoid overheating during bouts of strenuous activity, retard cooling after diving into colder water, and rapidly warm their muscles after voluntarily entering warmer water. The exact physiological mechanisms employed remain to be elucidated.

Daily movements, habitat use, and submergence intervals of normal and tumor-bearing juvenile green turtles (Chelonia mydas L.) within a foraging area in the Hawaiian islands

Depth-sensitive ultrasonic transmitters monitored the horizontal and vertical movements of 12 juvenile (<65 cm carapace length) green turtles (Chelonia mydas L.) in Kaneohe Bay, Oahu (Hawaii, USA). This site was chosen because of its accessibility, its importance as a foraging area, and the high incidence (≈50%) of fibropapillomatosis, a tumor disease of unknown etiology. Our objectives were to determine the daily movements, habitat use, and submergence intervals of normal and tumor-bearing animals. The presence of tumors had no obvious effects on movement patterns or habitat use. All turtles remained within a small portion of the bay where patch reefs and shallow coral-covered areas are common, and algal growth most abundant. During daylight, two normal and two tumor-bearing animals remained within known feeding areas, all other turtles studied stayed within deep mud bottom channels or within crevices on the sides of reefs. All, except one tumor-bearing turtle, moved up on to shallow patch reefs or shallow coral-covered areas at night. Submergence intervals for both groups were short (over 90% were 33 min or less and none exceeded 66 min) compared to maximum breath-hold times (up to 5 h) measured in the laboratory by earlier workers. Juvenile green turtles in Hawaii, therefore, most likely maintain aerobic metabolism while submerged and surface before oxygen stores are significantly depleted. Tumor-bearing turtles had a higher frequency of longer submergence intervals during the night, indicating they may have been somewhat less active at night. Normal turtles showed no such day-night difference.