Jeffrey B. Graham

Air-breathing fishes : evolution, diversity, and adaptation

The Biology of Air-Breathing Fishes: Introduction. Environmental Factors Affecting Air-Breathing Fishes. What is an Air-Breathing Fish? The Types of Air-Breathing Fishes. Summary and Overview. Diversity and Natural History: Introduction. The Class Osteicthyes: Families of Air-Breathing Fishes. Summary and Overview. Respiratory Organs: Introduction. Historical. Anatomy and Morphometrics. Types of Air-Breathing Organs. Lungs and Respiratory Gas Bladders. ABOs of the Higher Teleosts. Circulatory Adaptations: Introduction. Defining the Problems. Comparative Circulatory Specialization. Pulmonary Circulation: Lungfishes and Primitive Actinoperterygians. Summary and Overview. Aerial and Aquatic Gas Exchange: Introduction. Defining the Problems. Comparative Circulatory Specialization. Pulmonary Circulation: Lungfishes and Primitve Actinoperterygians. Summary and Overview. Cardiorespiratory Control: Introduction. Physical and Chemical Aspects. Comparative Aspects of Ventilatory Control: Fishes and Mammals. Studies of Bimodal Control. Studies of Central and Peripheral Control. Studies of ABO Receptors. Cardiorespiratory Reflexes. Summary and Overview. Blood Respiratory Properties: Introduction. Hemoglobin Function in Air-Breathing Fishes. Other Aspects of Air-Breathing Fish Blood Function. Summary and Overview. Metabolic Adaptations: Introduction. Oxygen Access and Intermediary Metabolism. Nitrogen Metabolism. Summary and Overview. Synthesis: Introduction. The Natural History of Fish Air Breathing. Factors Leading to the Evolution of Air Breathing. Air-Breathing Specializations. Air Breathing and Aquaculture. Fish Air Breathing and the Evolution of Tetrapods. References. Index.

Evolution and consequences of endothermy in fishes.

Regional endothermy, the conservation of metabolic heat by vascular countercurrent heat exchangers to elevate the temperature of the slow‐twitch locomotor muscle, eyes and brain, or viscera, has evolved independently among several fish lineages, including lamnid sharks, billfishes, and tunas. All are large, active, pelagic species with high energy demands that undertake long‐distance migrations and move vertically within the water column, thereby encountering a range of water temperatures. After summarizing the occurrence of endothermy among fishes, the evidence for two hypothesized advantages of endothermy in fishes, thermal niche expansion and enhancement of aerobic swimming performance, is analyzed using phylogenetic comparisons between endothermic fishes and their ectothermic relatives. Thermal niche expansion is supported by mapping endothermic characters onto phylogenies and by combining information about the thermal niche of extant species, the fossil record, and paleoceanographic conditions during the time that endothermic fishes radiated. However, it is difficult to show that endothermy was required for niche expansion, and adaptations other than endothermy are necessary for repeated diving below the thermocline. Although the convergent evolution of the ability to elevate slow‐twitch, oxidative locomotor muscle temperatures suggests a selective advantage for that trait, comparisons of tunas and their ectothermic sister species (mackerels and bonitos) provide no direct support of the hypothesis that endothermy results in increased aerobic swimming speeds, slow‐oxidative muscle power, or energetic efficiency. Endothermy is associated with higher standard metabolic rates, which may result from high aerobic capacities required by these high‐performance fishes to conduct many aerobic activities simultaneously. A high standard metabolic rate indicates that the benefits of endothermy may be offset by significant energetic costs.

Tuna comparative physiology

SUMMARY Thunniform swimming, the capacity to conserve metabolic heat in red muscle and other body regions (regional endothermy), an elevated metabolic rate and other physiological rate functions, and a frequency-modulated cardiac output distinguish tunas from most other fishes. These specializations support continuous, relatively fast swimming by tunas and minimize thermal barriers to habitat exploitation, permitting niche expansion into high latitudes and to ocean depths heretofore regarded as beyond their range.

Anatomical and physiological specializations for endothermy

Publisher Summary This chapter discusses the anatomical and physiological specializations for endothermy in fishes. Tunas are endothermic, which means that they utilize metabolic heat to elevate and maintain regional body temperatures that are warmer than the ambient seawater temperature. Tuna red muscle (RM) is both more anterior and nearer to the vertebral column and is completely surrounded by white muscle This RM position and its specialized connective-tissue linkage to the caudal fin affects swimming mechanics and results in the unique tuna swimming mode, which is termed as “thunniform locomotion.” The features of the thunniform locomotion pattern include minimal lateral body flexion and changes in the relationships between muscle activation and the strain cycle. It is found that in the four species— Euthynnus lineatus, Katsuwonus pelamis, Thunnus albacares, and Thunnus alalunga —the rete arterial vessel walls contain two or three layers of smooth muscle, while the venule walls have a single layer. Varying the contractile state of the vascular smooth muscle provides a possible mechanism whereby vessel diameter, and thus blood-flow and heat-exchange effectiveness may be adjusted in vivo . The link among tuna vascular anatomy, activity level, and an elevated body temperature is also described in the chapter.

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.

The aerobic capacity of tunas: Adaptation for multiple metabolic demands

Abstract Tunas are pelagic, continuous swimmers, with numerous specializations for achieving a high aerobic scope. Tunas must maintain a high rate of energy turnover, and therefore require elevated levels of aerobic performance in multiple physiological functions simultaneously. Based on a model of oxygen demand and delivery to the swimming musculature, the yellowfins total oxygen consumption at the predicted maximum sustainable (aerobic) swimming velocity is well below estimates of its maximum oxygen consumption. This suggests that the high aerobic scope of tunas may be a specialization that permits continuous swimming in addition to supplying oxygen to other metabolic functions. Estimates of the metabolic costs of oxygen-debt repayment, growth, and specific dynamic action have been combined with this model of aerobic swimming performance to evaluate the total energy budget in relation to the aerobic scope of the yellowfin tuna. Repayment of the oxygen debt incurred during burst swimming is potentially a large component of tuna respiratory metabolism and the relatively high aerobic capacity of tuna white muscle may be a specialization for rapid lactate clearance.

Breathing Air in Air: In What Ways Might Extant Amphibious Fish Biology Relate to Prevailing Concepts about Early Tetrapods, the Evolution of Vertebrate Air Breathing, and the Vertebrate Land Transition?*

The air‐breathing fishes have heuristic importance as possible models for the Paleozoic evolution of vertebrate air breathing and the transition to land. A recent hypothesis about this transition suggests that the diverse assemblage of marine amphibious fishes occurring primarily in tropical, high intertidal zone habitats are analogs of early tetrapods and that the intertidal zone, not tropical freshwater lowlands, was the springboard habitat for the Devonian land transition by vertebrates. Here we argue that selection pressures imposed by life in the intertidal zone are insufficient to have resulted in the requisite aerial respiratory capacity or the degree of separation from water required for the vertebrate land transition. The extant marine amphibious fishes, which occur mainly on rocky shores or mudflats, have reached the limit of their niche expansion onto land and remain tied to water by respiratory structures that are less efficient in air and more vulnerable to desiccation than lungs. We further argue that evolutionary contingencies actuated by the Devonian origin of the tetrapods marked a critical point of divergence for a way of life in which selection pressures would operate on the physiology, morphology, and natural history of the different vertebrate groups. While chronically hypoxic and shallow water conditions in the habitats of some primitive bony fishes and some amphibians appear similar to the conditions that prevailed in the Devonian, markedly different selection pressures have operated on other amphibians and bony fishes over the 300 million years since the vertebrate land transition. For example, both egg development and larval metamorphosis in extant amphibians are geared mainly toward compensating for the uncertainty of habitat water quality or even the absence of water by minimizing the time required to develop there. In contrast, reproduction by most intertidal (and amphibious) fishes, all of which are teleosts, remains dependent on a planktonic larval phase and is characterized by specializations (brooding) that minimize overdispersal and maximize recruitment back to the littoral habitat.

Metabolic rate of the albacore tuna Thunnus alalunga

The oxygen consumption rates ( VO2) of 6 specimens (6 to 13 kg) of the albacore tuna Thunnus alalunga were measured at sea, using specimens collected 300 km west of San Diego, California (USA) during July and August, 1981. Fish were tested in a closed continuous-flow respirometer, where they swam at about 1.3 body lengths s-1 velocity in 15° to 19°C water. The albacore tuna is a temperate pelagic species experiencing water temperatures from about 10° to 20°C and attaining a maximum weight of 45 kg. The VO2 ranged from 1 249 to 3 336 ml h-1 (the mean VO2 for the 6 fish was 2 228 ml h-1); such values approach those of mammals of a similar size and are 3 to 4 times those of most active fishes (e.g. sockeye salmon). Among fishes, the only higher VO2 values yet recorded were for the skipjack tuna Katsuwonus pelamis, a tropical species. The remarkably high metabolic rates of tunas are presumably correlated with their continuous swimming activity and the maintenance of endothermy. The exponent relating VO2 to body weight (1.18), although large, is not statistically different from the exponents for most other active vertebrates.

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

SUMMARY A large swim tunnel respirometer was used to quantify the swimming energetics of the eastern Pacific bonito Sarda chiliensis (tribe Sardini) (45–50 cm fork length, FL) at speeds between 50 and 120 cm s-1 and at 18±2°C. The bonito rate of oxygen uptake (V̇O2)–speed function is U-shaped with a minimum V̇O2 at 60 cm s-1, an exponential increase in V̇O2 with increased speed, and an elevated increase in V̇O2 at 50 cm s-1 where bonito swimming is unstable. The onset of unstable swimming occurs at speeds predicted by calculation of the minimum speed for bonito hydrostatic equilibrium (1.2 FL s-1). The optimum swimming speed (Uopt) for the bonito at 18±2°C is approximately 70 cm s-1 (1.4 FL s-1) and the gross cost of transport at Uopt is 0.27 J N-1 m-1. The mean standard metabolic rate (SMR), determined by extrapolating swimming V̇O2 to zero speed, is 107±22 mg O2 kg-1 h-1. Plasma lactate determinations at different phases of the experiment showed that capture and handling increased anaerobic metabolism, but plasma lactate concentration returned to pre-experiment levels over the course of the swimming tests. When adjustments are made for differences in temperature, bonito net swimming costs are similar to those of similar-sized yellowfin tuna Thunnus albacares (tribe Thunnini), but the bonito has a significantly lower SMR. Because bonitos are the sister group to tunas, this finding suggests that the elevated SMR of the tunas is an autapomorphic trait of the Thunnini.

Gill morphometrics in relation to gas transfer and ram ventilation in high-energy demand teleosts: Scombrids and billfishes

This comparative study of the gill morphometrics in scombrids (tunas, bonitos, and mackerels) and billfishes (marlins, swordfish) examines features of gill design related to high rates of gas transfer and the high‐pressure branchial flow associated with fast, continuous swimming. Tunas have the largest relative gill surface areas of any fish group, and although the gill areas of non‐tuna scombrids and billfishes are smaller than those of tunas, they are also disproportionally larger than those of most other teleosts. The morphometric features contributing to the large gill surface areas of these high‐energy demand teleosts include: 1) a relative increase in the number and length of gill filaments that have, 2) a high lamellar frequency (i.e., the number of lamellae per length of filament), and 3) lamellae that are long and low in profile (height), which allows a greater number of filaments to be tightly packed into the branchial cavity. Augmentation of gill area through these morphometric changes represents a departure from the general mechanism of area enhancement utilized by most teleosts, which lengthen filaments and increase the size of the lamellae. The gill design of scombrids and billfishes reflects the combined requirements for ram ventilation and elevated energetic demands. The high lamellar frequencies and long lamellae increase branchial resistance to water flow which slows and streamlines the ram ventilatory stream. In general, scombrid and billfish gill surface areas correlate with metabolic requirements and this character may serve to predict the energetic demands of fish species for which direct measurement is not possible. The branching of the gill filaments documented for the swordfish in this study appears to increase its gill surface area above that of other billfishes and may allow it to penetrate oxygen‐poor waters at depth. J. Morphol. 2010.