Peter G. Bushnell

An automated swimming respirometer

Abstract An automated respirometer is described that can be used for computerized respirometry of trout and sharks.

2 – The Arterial System

This chapter describes the arterial system of fishes. The primary circulation of fishes follows the typical vertebrate pattern in that a heart forces blood into a ventral aorta, which then gives off paired vessels that arch upward among successive gill clefts and rejoin to form the dorsal aorta. The primary circulation is remarkably constant in general form in cyclostomes, elasmobranchs, and teleosts. Major modifications of the posterior branchial arteries occur in air-breathing fishes. For efficient gas exchange, water flow over the gills and blood flow through the gills should be continuous. Continuous blood flow may be achieved by the elastic recoil of blood vessel walls stretched during systolic ejection. The best estimate of the extent of this windkessel function of the ventral aortic system is from flow measurements made on the main vessel, either just outside the conus or bulbus or between pairs of branchial arteries. Recordings from these situations show major differences between flow patterns in cyclostomes and elasmobranchs on the one hand and teleosts on the other, although these flow patterns may not be truly indicative of gill blood flow. The pressure and flow relationships in the ventral and dorsal aortas are also elaborated in the chapter.

Oxygen consumption in four species of teleosts from Greenland: no evidence of metabolic cold adaptation

Standard metabolic rate of Greenland cod or uvak, Gadus ogac, polar cod, Boreogadus saida, Atlantic cod, Gadus morhua, and sculpin, Myxocephalus scorpius, caught in the same geographical area on the west coast of Greenland was measured at 4.5°C, the temperature at which the fish were caught. The present data does not support the Metabolic Cold Adaptation theory in the traditional sense of the standard metabolic rate being 2–4 times higher for Arctic fishes than for temperate species. The standard metabolic rate of the two exclusively Arctic species of teleosts was only 10% and 26% higher, respectively, than the two species that occur in temperate as well as Arctic areas. The critical oxygen tension, with respect to oxygen consumption, of resting uvak was between 50 and 60 mmHg, and the lethal oxygen tension 20–25 mmHg at 4.5°C, which is considerably higher than for Atlantic cod from a temperate area measured at the same temperature.

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.

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.

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

SynopsisBoth 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 O2 utilization is high (30–50%) even when ram ventilation approaches 101 min−1kg−1. 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 O2 capacity approaches 16 ml dl−1 and a large Bohr coefficient (−0.83 to −1.17) ensures adequate loading and unloading of O2 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 μmol g−1 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 O2 delivery/demand model predicts the maximum sustained swimming speed of small yellowfin and skipjack tuna is 5.6 BL s−1 and 3.5 BL sec−1, respectively. The surplus O2 delivery capacity at lower swimming speeds allows tuna to repay large oxygen debts while swimming at 2–2.5 BL s−1. Maximum oxygen consumption (7–9 × above the standard metabolic rate) at maximum exercise is provided by approximately 2 × increases in each of heart rate, stroke volume, and arterial-venous O2 content difference.

Exercise metabolism in two species of cod in arctic waters

The northern range of Atlantic cod (Gadus morhua), overlaps the southern range of the Greenland cod (Gadus ogac), in the coastal waters of Western Greenland. The availability of a temperate water species (G. morhua) in the same area and oceanographic conditions as a polar species (G. ogac) presented us with the ideal circumstances to test the hypothesis of metabolic cold adaptation (MCA) since many of the problems associated with MCA studies (adaptation of the animals beyond their normal temperature range or mathematical extrapolation of data to common temperatures) could thus be avoided. We therefore used a swim tunnel to measure oxygen consumption in fish at 4°C over a range of swimming speeds and following exhaustion, monitored the size of the oxygen debt and time of oxygen debt repayment. There were no significant differences in standard (60–72 mg O2 kg−1· hr−1), routine (76 mg O2 kg−1·hr−1), active (137mg O2 kg−1·hr−1), or maximal (157 mg O2 kg−1·hr−1) metabolic rate, metabolic scope (2.5) or critical swimming speed (2.2 BL·s−1) between the two species. Following exhaustive swimming, however, the half-time for oxygen debt repayment in G. ogac (43 min) was almost twice that of G. morhua (25 min). Despite its circumpolar distribution, therefore, there was no evidence of MCA in G. ogac.

Design and setup of intermittent‐flow respirometry system for aquatic organisms

Intermittent-flow respirometry is an experimental protocol for measuring oxygen consumption in aquatic organisms that utilizes the best features of closed (stop-flow) and flow-through respirometry while eliminating (or at least reducing) some of their inherent problems. By interspersing short periods of closed-chamber oxygen consumption measurements with regular flush periods, accurate oxygen uptake rate measurements can be made without the accumulation of waste products, particularly carbon dioxide, which may confound results. Automating the procedure with easily available hardware and software further reduces error by allowing many measurements to be made over long periods thereby minimizing animal stress due to acclimation issues. This paper describes some of the fundamental principles that need to be considered when designing and carrying out automated intermittent-flow respirometry (e.g. chamber size, flush rate, flush time, chamber mixing, measurement periods and temperature control). Finally, recent advances in oxygen probe technology and open source automation software will be discussed in the context of assembling relatively low cost and reliable measurement systems.

Eye lens radiocarbon reveals centuries of longevity in the Greenland shark (Somniosus microcephalus)

Deep living for centuries We tend to think of vertebrates as living about as long as we do, give or take 50 to 100 years. Marine species are likely to be very long-lived, but determining their age is particularly difficult. Nielsen et al. used the pulse of carbon-14 produced by nuclear tests in the 1950s—specifically, its incorporation into the eye during development—to determine the age of Greenland sharks. This species is large yet slow-growing. The oldest of the animals that they sampled had lived for nearly 400 years, and they conclude that the species reaches maturity at about 150 years of age. Science, this issue p. 702 Greenland sharks can live to be 400 years old and only become sexually mature at 150, raising conservation concerns. The Greenland shark (Somniosus microcephalus), an iconic species of the Arctic Seas, grows slowly and reaches >500 centimeters (cm) in total length, suggesting a life span well beyond those of other vertebrates. Radiocarbon dating of eye lens nuclei from 28 female Greenland sharks (81 to 502 cm in total length) revealed a life span of at least 272 years. Only the smallest sharks (220 cm or less) showed signs of the radiocarbon bomb pulse, a time marker of the early 1960s. The age ranges of prebomb sharks (reported as midpoint and extent of the 95.4% probability range) revealed the age at sexual maturity to be at least 156 ± 22 years, and the largest animal (502 cm) to be 392 ± 120 years old. Our results show that the Greenland shark is the longest-lived vertebrate known, and they raise concerns about species conservation.