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Physiology of Diving of Birds and Mammals

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Physiology of Diving of Birds and Mammals PHYSIOLOOICAL REI1E'US Vol 77, No. 3. July I887 mnierl in u.Sn Physiology of Diving of Birds and Mammals PATRICK J. BUTLER AND DAVID R. JONES School of Biological Scimes, The Unidtyof Birmingham, Edgbmlon, Bidnghum, United Kingdom- and Department of Zoology, Univmity of British Columbia, Vancouver, Bitish Columbia, Camui,a I. Introduction TI. Diving Rehavior A. Birds B. Mammals I11 Metatrolic Rate and Metabolism A. Aerob~cdive limit B. Methods for determining metabolic rate of diving animals C. Birds D. Mammals I!'. I!'. Controlline Metabolism: Cardiores~iratorv" Relationshi~s Durine - Divine- A. ~ircula&yadjustments to di&g B Effiracy of cardiores1,irnror). responses lo d~ung V. Hecoven IFrom D~\ulg.t'ardiontsp~rato~~ Rt!sln)~~srs 113 Sllrf;i(.~llg VI. Control of ~ardiores~iratolyResponses VII. Concluding Comments Butler, Patrick J., and David R. Jones. Physiology of Diving of Birds and Mammals. Physiol. Rev. 77: 837-899, 1997.-This review concentrates on the physiological responses, and their control, in freely diving birds and mammals that enable them to remain submerged and sometimes quite active for extended periods of time. Recent developments in technology have provided much detailed information on the behavior of these fascinating animals. Unfortunately, the advances in technology have been insufficient to enable physiologists to obtain anything like the same level of detail on the metabolic rate and physiological adjustments that occur during natural diving. This has led to much speculation and calculations based on many assumptions concerning usable oxygen stores and metabolic rate during diving, in an attempt to explain the observed behavior. Despite their shortcomings, these calculations have provided useful insights into the degree of adaptations of various species of aquatic birds and mammals. Many of them, e.g., ducks, smaller penguins, fur seals, and Weddell seals, seem able to metabolize aerobically, when diving, at approximately the same (if not greater) rate as they do at the surface. Their enhanced oxygen stores are able to support aerobic metabolism, at what would not be considered unusually low levels, for the duration of the dives, although there are probably circulatory readjustments to ensure that the oxygen stores are managed judiciously. For other species, such as the larger pengulns, South Georgian shag, and female elephant seals, there is a -general consensus that thev must either be reducing their aerobic metabolic rate when diving. possibly by way of regional L~wotl~emlia,andlor producing ATP, at least pmtly, by anaerobiosis and metabolizing the lactic acid when at the surface (although this is hardly likely in the case of the female elephant seals). Circulation is the proximate regulator of metabolism during aerobic diving, and heart rate is the best single indicator of circulatory adjustment. During voluntary dives, heart rates range from extreme bradycardia to well above resting, rcflccting mctaholic pcrformancc. Effercnt cardiac control is largely parasympathetic. Rcflcx cardiorespiratory responses are modulated by conditioning and habituation, but reflexes predominate during extended dives and during recovery, when gas exchange is maximized. I. INTRODUCTION hundreds of meten. There are, therefore, two major prob- lems confronting many species of aquatic birds and mm- Diving bids and mammals remain submerged under- mals: relating to their limited oxygen stores and to the water for differing durations, from several seconds to large hydrostatic pressures to which they are exposed. many minutes, and, in general terms, these differing dura- With an increase of 1 atmosphere for approximately every tions relate to the depth to which the animals routinely 10-m descent into the water column, an animal at a depth dive in the water column, from a meter or so to many of 200 m will experience a pressure of 21 atmospheres. 0031-9333197 15.00 Copyright 0 1997 the Amencan Physiological Society m.7 PATRICK J. BUTLER iLND DAVID R. JONES Volume 77 The problems facing these animals are all related to the TABLE 1. Sites of oxygen storage in diving and fact that they have air-filled cavities in their bodies and nondiving l~orneothmr~s that air is compressible. There are a number of anatomic features in marine mammals that enable them to over- Myoglabin, dl00 g hissue come many of these problems, and these were all dis- Muscles cussed by Butler and Jones (53) and Kooyman (218). Be- Hummingbird (pectoralis) cause there has been little research on th's topic during Tufted duck (gastrocnemius) the past 10 years, we do not intend to discuss this aspect Tufted duck jpectoralis) Gentoo penguin (pectoralis) of diving to any great extent in this review. Thoroughbred horse (psoas) Regarding their linriled oxygen stores, the central Beaver question is: What physiological and metabolic processes Ribbon seal Weddell seal enable these air-breathing, homeothcrmic endothenns to Elephant seal remain submerged and, maybe, active for extended peri- Bottlenose dolphin ods? Two vely important aspects of the answer to this Porpoise (psoas) Sperm whale question relate to the amount of oxygen that can be stored Bottlenose whale in the body for use underwater (and, conversely, the amount of carbon dioxide that can be stored during sub- Volume, ml BTPSkg mersion for removal at the surface) and the rate at which Respiratorz~S?istm that oxygen is used during the period of submersion. Re- lated to the latter is how the stored oxygen is distributed Mallard duck 112 Tufted duck (lesser sraup) 180 (355) to the various organs and tissues to meet their different Adhlie penguin 165 requirements and to what extent living andlor diving in Dog 61 cold (maybe around 0°C) water and eating cold food af- Human 74 Beaver 60 fects the metabolic rate of these endothermic homeo- Weddell seal 48 them. Although temperature regulation and adaptations Harbor porpoise 59 Bottlenose whale 26 to low temperature were also discussed in some detail in -- Reference 53 and are not covered to any great extent in Volume, mV Oxygen Capacity, the current review, we intend to highlight some exciting 100 g body Hb, g1100 rnl ml OdlOO rnl recent observations that indicate that regional hypother- mass blood blood mia may be an important factor in reducing overall oxygen Circulatory requirements during diving, in at least some species of Pigeon 9.2 marine birds and mammals. Another important aspect, Mallard 9. I particularly as far as foraging is concerned, is the rapidity Tufted duck 11.4 Chinstrap penguin with which the oxygen stores can be replaced (and the E~rlperorpenguin carbon dioxide removed) when the animals are at the Human 't.7 surface. Beaver 6.6 Weddell seal 21.0 It is possible to identify three distinct phases in the Bladdernose seal evolution of the answer to the above question. Initially, Elephant seal 21.7 data were obtained from restrained animals that were Bottlenose porpoise 7.1 Dall porpoise 14.3 forcihly submerged. These studies go hack well over 100 Sperm whale years, but perhaps the most influential publications were those of Irving (195, 196) and Scholander (346). These Hb, hemoglobin; BTPS, body temperature and pressure, saturated. and subscqucnt publications by thc samc authors and 0th Data are from the following sources: Ref. 49; lesser scaup, Ref. 364; elephant seal, Ref. 218; Weddell seal, Ref. 324. crs using rcstraincd animals have been rcviewed many times (3,28,45,53,69, 135,218), so it is not the intention here to produce another review of this material. vasoconstriction causing a reduction in the perfusion of all The model that emerged from these studies is that, parts of the body except the oxygensensitive tissues, the although the oxygen stored in the body is greater in diving central nervous system, and heart [note, there is no reduc- than in nondiving species (Table I), it is insufficient to tion in coronary flow in forcibly submerged ducks (204), enable aquatic bids and mammals to maintain aerobic me- whereas in seals it does decrease in proportion to the re- tabolism and remain submerged for the durations obtained duction in cardim ontput (27, 30, 424)l. during the experiments. Consequently, there is an overall Thus, in the underperfused tissues, which includes reduction in the level of aerobic metabolism so that the the skeletal muscles in these restrained animals, there is oxygen stores are conserved for those tissues that cannot a net accumulation of lactic acid that is flushed into the survive hypoxia This is achieved by selective peripheral blood soon after the animal is surfaced. As well as the Iz~ly1997 PHYSIOLOGY OF DIVING OF BIRDS AND MAMMALS 839 A shown in Figure 1. Of particular importance is the fact 100 that it takes approximately six times the duration of the forced submersion for the concentration of blood lactate i 60 o to return to the predive level (see also Ref. 53). 4 20 This hypothesis of large-scale peripheral vasocon- .-C striction, reduced aerobic metabolism, and a substantial g -20 c increase in anaerobic metabolism during voluntruy sub- -60 mersion was challenged during the late 1970s and early 8 -100 1980s, initially as a result of studies on two species, the tufted duck, Aythya fuligula, and the Weddell seal, Lep- 8 &'..f&*.$ tonychotes weddeUii (59, 235, 414), although it must be $A6@ said that Scholander, himself, was not too certain of the ,j V. universality of the IrvingScholander hypothesis. In his 1940 paper (346), he says that it would "be of great interest Submew to compare the circulation in a
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