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Origin and Development of Homoiothermy: a Case Study of Avian Energetics

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Origin and Development of Homoiothermy: a Case Study of Avian Energetics Advances in Bioscience and Biotechnology, 2013, 4, 1-17 ABB http://dx.doi.org/10.4236/abb.2013.48A1001 Published Online August 2013 (http://www.scirp.org/journal/abb/) Origin and development of homoiothermy: A case study of avian energetics Valery M. Gavrilov Department of Vertebrates Zoology and Skadovsky Zvenigorod Biological Station, Moscow State University, Moscow, Russia Email: [email protected] Received 11 June 2013; revised 12 July 2013; accepted 30 July 2013 Copyright © 2013 Valery M. Gavrilov. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. ABSTRACT temperatures which corresponded well to the environ- mental conditions on the Earth. Natural selection al- The study is based on the results of the integrated lowed animals with high energetic metabolism to in- measurement of the energy expenditure at rest and crease their diversity and abundance, but only when common activity in birds belonging to various sys- homoeothermic animals could satisfy their demands tematic groups. Homeothermy has formed in birds for food resources, that had risen manifold. That and mammals independently and in different geo- happened in the middle of Cretaceous, in time with logical ages. However, in both groups it originated as the appearance of angiosperms and expansion of re- a side effect of selection for aerobic metabolism im- lated fauna of invertebrates. provement that provided a higher level of activity. Advantages of having high and stable body tempera- Keywords: Basal Metabolism; Metabolism of Existence; ture, which were inevitably related with metabolism Homoiothermy; Erythrocytes in Birds and Mammals; intensification, led to development of thermoregula- Aerobic Supply of Activity and Sensory Systems; tory adaptations such as fur and feathers. This made Minimal Size; Parental Care it possible to retain the metabolically generated heat and reduce heat absorption in hot environments. Emergence of homeothermy with aerobic supply of 1. INTRODUCTION motion activity, possibilities to regulate the level of Maintaining a constant body temperature over wide- metabolism and thermal conductance, has opened a ranging changes in ambient temperature is achieved in lot of opportunities for homoeothermic animals. Achi- homeothermic animals by maintaining an equilibrium eving such a level of energy utilization allowed them between heat loss and heat production. A physical inter- to maintain activity for a longer time, while its sen- pretation of this phenomenon is not difficult if one ex- sory support led to complication and diversification amines the heat balance of a resting animal at low tem- of birds’ behavioral repertoire (as well as that of peratures [1], but when one examines the heat balance of mammals) facilitating the conquest of almost entire an active animal at high temperatures, this physical in- part of the biosphere that was suitable for living. This terpretation encounters a series of contradictions which process was favored by the development of nurturing as yet have not been eliminated. and passing on the information, collected throughout Birds and mammals are two classes of higher verte- the life, to new generations. Formation of high levels brates and both of them are Homoiotherms. The estab- of aerobic metabolism in birds and mammals was lishment of homoiothermy by birds and mammals during proceeding in parallel among different groups of rep- the Mesozoic is directly connected with the develop- tilian ancestors. The level of homeothermy, at which ment of high activity, which is enabled by aerobic me- aerobic metabolism was able to maintain prolonged tabolism. Homoiothermy allowed them to broaden the activity, developed in birds and mammals in different behavioral repertoire and prolong the period of activity. ways: they had got dissimilar partitioning of venous In general, long term activity and endurance are the basic and arterial networks, erythrocytes with or without a benefits of homoiothermy, which have given a selective cell nucleus, different lungs design—but, at that, simi- advantage to birds and mammals [2]. This high aerobic lar minimum metabolic power and rather close body metabolism allowed the behavioral patterns evolution in OPEN ACCESS 2 V. M. Gavrilov / Advances in Bioscience and Biotechnology 4 (2013) 1-17 birds and mammals to reach such high levels. This evo- the conditions of an equable warm (subtropical) climate lution had to be based on the preceding or parallel evolu- with small diurnal temperature variations [11,12]. This tion of metabolic systems which were capable to provide phenomenon is referred to as “inertial homoiothermy.” high activity. The basis of homoiothermy is in the com- Several biophysical models have been constructed to bination of high heat production and low thermal con- assess the possible body temperature of large dinosaurs ductance [2,3]. [13,14]; their estimates are 30˚C - 47˚C. Advances in ra- The goal of this work was to propose a possible evolu- dioisotope research methods have allowed us to asses the tionary and ecological scenario for the causes and condi- body temperature in discovered extinct dinosaurs with tions underlying the establishment of homoiothermy and various degrees of accuracy [15-20]. All of the isotope- the colonization of major ecological niches by homoio- based estimates for the body temperature of dinosaurs therms. The paper is based on a set of experimental data mainly fall into the range predicted by biophysical mod- on the energetics of the extant vertebrates, its theoretical els. Nonetheless, the question on the true endothermy of substantiation, and an analysis of the relevant literature dinosaurs remains open [17,19-21]. Most frequently, they on the major events in the Mesozoic era. are compared to contemporary crocodiles, which display This study utilizes the results of an integrated meas- certain attempts at endothermy. However, there is no urement of the energy expenditure at rest (assessed ac- final evidence that the metabolism of dinosaurs differed cording to oxygen consumption) and common activity, from the metabolism of extant reptiles [17,19-22]. Cor- i.e., the so called existence metabolism (assessed ac- respondingly, it is quite adequate to assume that the me- cording to food consumption), as well as the energy ex- tabolism of extinct reptiles had no serious differences penditures in flight and at a maximal loading in birds from the metabolisms of recent forms [9,11,23-30], de- belonging to various systematic groups that display con- spite the publications that imply such a difference (for siderable variations in their body sizes. The main atten- example, [31]) that constantly appear in prestigious jour- tion was focused on clarifying the balance between the nals. minimal metabolic capacity (basal metabolic rate, BMR) Differences in metabolism are naturally reflected in and other levels of energy expenditures, such as the the food consumption, which remains in the reptiles by standard (resting) metabolic rate and energy expenditures over one order of magnitude lower compared to mam- for the existence at different ambient temperatures (TA). mals and birds. The establishment of homoiothermy was To estimate the maximal potential of birds in dissipating directly connected with the development of high activity, excess heat, we had to estimate the maximal and produc- which is enabled by aerobic metabolism. This high aero- tive metabolic rates, as well as the energy expenditures bic metabolism made the evolution of complex behave- for activity in various passerine and non-passerine spe- ioral patterns feasible in birds and mammals. This evolu- cies. Thus, this paper is an attempt to understand the tion had to be based on the preceding evolution of meta- scenario of homoiothermy origination from the stand- bolic systems capable of providing high activity. This point of ecological energetics. resulted in an increased standard (resting) metabolic rate (SMR), which became the minimal capacity level. The 2. ECOLOGICAL ENERGETICS OF SMR increased in order to enable even higher levels of RECENT VERTEBRATE ANIMALS work intensity in homoiotherms [2,9,11,32-38]. AND ORIGIN OF HOMOIOTHERMY On the other hand, an increase in the energy expendi- tures cannot be subject to the positive control of natural 2.1. The Hypotheses on the Reason and the selection, since an increase in the energy expenditures Effects for Origin Homoiothermy per se is disadvantageous for an organism. How, then, in the Evolution does natural selection control an increase in the capacity The evolution of homoiothermy is usually discussed in of energy metabolism? What are the ecological advan- the literature in the context of the advantages conferred tages gained by the animals with a high metabolism? by a stable body temperature (diurnal activity, enzyme What is the cost of possessing a high metabolism? And functions, and tolerance to freezing) and thermoregula- why did homoiothermy not emerge with lower body tion [4-8]. Only some researchers pay attention to the temperature? Researchers studying the ecological ener- increase in activity and fatigue resistance in homoio- getics of modern vertebrate groups face all of these ques- therms [9-11]. The author also believes that thermoregu- tions and, in their answers, will give deeper insight into lation is not the only selective advantage in the evolution the origin of homoiothermy.
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