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Prioritization of Oxygen Delivery During Elevated Metabolic States Respiratory Physiology & Neurobiology 144 (2004) 215–224 Eat and run: prioritization of oxygen delivery during elevated metabolic states James W. Hicks∗, Albert F. Bennett Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA Accepted 25 May 2004 Abstract The principal function of the cardiopulmonary system is the matching of oxygen and carbon dioxide transport to the metabolic V˙ requirements of different tissues. Increased oxygen demands ( O2 ), for example during physical activity, result in a rapid compensatory increase in cardiac output and redistribution of blood flow to the appropriate skeletal muscles. These cardiovascular changes are matched by suitable ventilatory increments. This matching of cardiopulmonary performance and metabolism during activity has been demonstrated in a number of different taxa, and is universal among vertebrates. In some animals, large V˙ increments in aerobic metabolism may also be associated with physiological states other than activity. In particular, O2 may increase following feeding due to the energy requiring processes associated with prey handling, digestion and ensuing protein V˙ V˙ synthesis. This large increase in O2 is termed “specific dynamic action” (SDA). In reptiles, the increase in O2 during SDA may be 3–40-fold above resting values, peaking 24–36 h following ingestion, and remaining elevated for up to 7 days. In addition to the increased metabolic demands, digestion is associated with secretion of H+ into the stomach, resulting in a large metabolic − alkalosis (alkaline tide) and a near doubling in plasma [HCO3 ]. During digestion then, the cardiopulmonary system must meet the simultaneous challenges of an elevated oxygen demand and a pronounced metabolic alkalosis. This paper will compare and contrast the patterns of cardiopulmonary response to similar metabolic increments in these different physiological states (exercise and/or digestion) in a variety of reptiles, including the Burmese python, Python morulus, savannah monitor lizard, Varanus exanthematicus, and American alligator Alligator mississipiensis. © 2004 Elsevier B.V. All rights reserved. Keywords: Exercise, postprandial; Metabolism, maximum O2 uptake; Oxygen, maximum uptake; Reptiles, crocodilians; Shunt, cardiovascular 1. Introduction Increased metabolic demand in different regions of the body quickly results in a compensatory increase in cardiac output, redistribution of blood flow to the ap- ∗ Corresponding author. Tel.: +1 949 824 6386; fax: +1 949 824 2181. propriate tissues, and suitable ventilatory increments. E-mail address: [email protected] (J.W. Hicks). These increments and their physiological basis have 1569-9048/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.resp.2004.05.011 216 J.W. Hicks, A.F. Bennett / Respiratory Physiology & Neurobiology 144 (2004) 215–224 been particularly well investigated during exercise, and Table 1 the matching of cardiopulmonary performance and Similarities and differences of two elevated metabolic states: physical metabolism during activity may be universal among activity vs. digestion vertebrates (see Jones, 1994 for reviews). However, Physical activity Digestion there are other situations besides physical activity in Metabolic increment 5–10 × resting Graded (meal which the increase in the metabolic demands from size dependent) multiple organs and tissues may approach or even ex- Site of metabolic activity Skeletal muscle Gastrointestinal Metabolic pattern Catabolism Anabolism ceed the O2 transport capacity of the cardiopulmonary Acid–base disturbance Acidosis Alkalosis system. These may also pose additional physiological Activating system Somatic motor Parasympathetic challenges unrelated to O2 transport, and sometimes and sympathetic NS they may occur simultaneously with activity. Under NS the latter conditions, understanding the integrative pro- Activation time 1–5 min Hours to days cesses of prioritization during conflicting physiological V˙ −1 −1 stresses remains an important challenge in physiology O2 reaches 8 ml kg min , 32 h postfeeding, which (Jackson, 1987). is equivalent to the values measured while crawling at In carnivorous reptiles, large increments in aero- 0.4 km h−1 (Secor et al., 2000)(Fig. 1). Furthermore, bic metabolism are associated with physiological states in contrast to the relatively short duration (minutes) of V˙ other than activity. In particular, O2 increases follow- physical activity in this animal, the elevated metabolic ing feeding due to the energy requiring processes as- rates during SDA are sustained for several days (Secor sociated with prey handling, digestion and the ensuing and Diamond, 1997a,b)(Fig. 1). protein synthesis (Andrade et al., 1997; Benedict, 1932; Thus, in certain animals, both activity and diges- Cruz-Neto et al., 2001; Houlihan, 1991; Overgaard tion can result in metabolic rates five or more times et al., 2002; Secor and Diamond, 1995, 1997a,b; Wang above resting levels and require similar levels of O2 V˙ et al., 2002). This large increase in O2 is referred to consumption and carbon dioxide excretion. This equiv- as “specific dynamic action” (SDA) (Rubner, 1902). In alence in gas exchange during these two physiological terms of relative metabolic rates, SDA is far more pro- conditions might suggest that similar patterns of car- nounced in ectothermic vertebrates than in endother- diopulmonary response would be appropriate for both mic birds and mammals because of the substantially hypermetabolic states. However, other aspects of these greater maintenance metabolic costs of the latter. The metabolic states differ profoundly (Table 1). Skeletal V˙ increase in O2 during SDA in some reptiles may re- muscle activity is catabolic and acidotic and is regu- semble or even exceed that during physical activity. lated by an increase sympathetic tone. Digestion may For example, in the Burmese python, Python molurus, involve considerable synthesis and is thus primarily an Fig. 1. Oxygen consumption during maximal activity and 32 h postfeeding in the python (mean ± 1 S.E.). Note: maximal activity is sustained V˙ for only several minutes, in contrast to postprandial O2 , which is sustained for days (right panel). Redrawn from Secor et al. (2000). J.W. Hicks, A.F. Bennett / Respiratory Physiology & Neurobiology 144 (2004) 215–224 217 anabolic process. The secretion of large quantities of excess (above resting levels) energy expenditure dur- protons into the stomach results in profound “alkaline ing digestion or as the ratio of this value to total energy tides” in the blood, and the entire digestion process is in the meal. In addition, the factorial metabolic incre- largely controlled by the parasympathetic nervous sys- ment, the ratio of peak to preingestion metabolic rate, tem. Further, the time course of the activity response in- is also frequently measured. SDA is very dependent on volves much more rapid activation, achieving maximal food composition, being approximately 30% for pro- levels within 1–2 min and its duration is only several tein, 13% for fat, and 10% for carbohydrate (Rubner, minutes to an hour. Maximal metabolic rates during 1902; Brody, 1945; Secor et al., 1994; Secor and digestion by contrast do not occur until 1–2 days after Diamond, 1997a,b). Thus, in particular, protein re- ingestion and may be profoundly elevated for a week quires a major energetic investment prior to acquisition (Secor and Diamond, 1998; Wang et al., 2001a). of energy within the food consumed (designated “pay The cardiopulmonary response to similar metabolic before pumping” by Secor and Diamond, 1995). demands during these different physiological states The largest postprandial metabolic increments have could be either stereotyped or flexible. In the former been found in carnivorous reptiles. Benedict (1932) case, equal metabolic increments (e.g., ml O2 or J) in and, more recently and thoroughly, Secor and Diamond either the skeletal muscle or the gastrointestinal track and their coworkers have undertaken an extensive se- would elicit an equal increment in the cardiac response ries of investigations on the topic in several reptiles, (heart rate and stroke volume, with appropriate re- principally in snakes. They have found that the impact distribution of blood flow) and ventilatory response on reptilian energetics is very large for two reasons, (breathing frequency and tidal volume), regardless of enormous protein-rich meals and low resting metabolic the physiological state generating the demand. In the rates. Many large carnivorous reptiles naturally eat very latter case, the cardiopulmonary system might have a rarely, sometimes only once a month or less (Secor variety of state-dependent and -appropriate responses et al., 1994; Secor and Diamond, 1995). They tolerate that result in the same level of gas exchange. In such long periods of fasting, exceeding one year in large in- a flexible system, the convective components (either dividuals (Benedict, 1932; Secor et al., 1994). During cardiac output or lung ventilation) might be markedly this time, intestinal tissue regresses, curtailing mainte- state-dependent, appropriate to matching more subtle nance costs (Secor and Diamond, 1997a,b). These an- regulatory factors other than simple energetic demands. imals are then capable of consuming enormous meals, Here we review what is known about the patterns which are primarily protein, generating a very high of gas exchange, ventilation and systemic blood flow SDA. The magnitude of
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