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Benson has been accepted towards fulfillment of the requirements for Ph.D. Zoology degree in % 5Z5 Egg/é/éfi/r Major professor 12 October 1978 Date — 0-7 639 'w u("tritiummargarita" A 008 EFFECTS OF ACCLIMATION TEMPERATURE ON AVIAN THERMOREGULATORY ONTOGENY By John Wellington Benson A DISSERTATION Submitted to Michigan State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Department of Zoology 1978 63/038 M ABSTRACT EFFECTS OF ACCLIMATION TEMPERATURE ON AVIAN THERMOREGULATORY ONTOGENY By John Wellington Benson The ontogeny of temperature regulation in gallg§_domesticus was studied in two series of experiments. The hypothesis tested was that acclimation temperature would influence the development of thermoregula- tion in these young birds. Acclimation temperatures were manipulated to determine their effects on endothermic (physiological) and ectothermic (behavioral) regulation of body temperature in chicks at various stages of early development. In Experimental Series I, groups of chicks were reared during early development under one of five different thermal acclimation paradigms. Endothermic capabilities of these chicks were assayed by one-hour expo- sures to 10°C on specified days during early development. Rates of endothermic ontogeny were respectively fastest to slowest in the contin- uous cold, intermediate, and continuous warm thermally-acclimated chicks. Cold thermal acclimation stimulated chick endothermic ontogeny both when presented during only the initial and only the middle stages of early development. Responses of chicks related to thermoregulatory performance changed during development in a manner reflective of contin- ual improvements in the endothermic capabilities of these chicks. John Wellington Benson However, age-related changes in these responses did not explain the demonstrated differences in endothermic performances between the groups of chicks. The superior endothermic capabilities of continuous cold, as compared to continuous warm, thermally-acclimated chicks were also demonstrated in 6-day-old birds during one-hour exposures to 18°C, and were even more pronounced during three-hour exposures to 10°C. Continu- ous and/or intermittent cold thermal acclimation stimulates the ontogeny of endothermy in the young chick. In Experimental Series II, groups of chicks were acclimated during early development to either cold or warm thermal conditions. Ecto- thermic responses of these animals were tested at specified days during early development in a multichambered thermal gradient apparatus using two different trial procedures. During the OFF trial procedure, when temperatures in the testing apparatus were uniformly cold, chicks in both acclimation groups randomly distributed themselves throughout the chambers, but were unable to maintain normal body temperatures. During the ON trials, when a range of cold to warm temperature conditions was present in the testing apparatus, chicks in both acclimation groups distributed themselves non-randomly at the warmer chamber positions. As a result of these ectothermic responses during ON trials, chicks in both acclimation groups maintained normal body temperature levels at stages of early development when endothermic capabilities alone were either ineffective or insufficient. Ectothermic responses of young chicks contribute significantly to thermoregulatory performance during the course of endothermic ontogeny. To my Parents . who made it possible. To Kimberly and Christopher . who make it worthwhile. To Susan . who makes it meaningful. ACKNOWLEDGEMENTS I wish to express my sincere gratitude to Dr. Martin Balaban for his counsel, encouragement, patience, and understanding during the protracted and difficult gestation of this investigation. I also wish to thank Drs. John A. King, James H. Asher, Jr., and E. M. Eisenstein for their many constructive suggestions and comments. The invaluable assistance of Dr. James L. Smith and the staff of the Computer Center of Muskingum College is gratefully acknowledged. Finally, my sincere appreciation is expressed to friends and family, especially my children Kimberly and Christopher, and particularly my wife Susan, without whose unwavering support this project would never have been completed. This study was supported by a NIH Predoctoral Traineeship awarded through the Animal Behavior Training Grant T01 GM01751 from the National Institute of General Medicine. Partial support for statistical analysis was provided by a grant from the Ohio University Faculty Development Fund. Sufficient space, equipment, and materials to conduct this inves- tigation were provided, in part, by the Department of Zoology and the Biology Research Center at Michigan State University. TABLE OF CONTENTS Page LIST OF TABLES ......................... vi LIST OF FIGURES ......................... ix INTRODUCTION .......................... 1 REVIEW OF LITERATURE ...................... 7 Body Temperatures in Birds ................. 7 Concepts and Terminology of Temperature Regulation ..... 11 Avian Thermoregulatory Responses to Cold .......... 16 Avian Thermoregulatory Responses to Heat .......... 22 Physiological Adaptations of Birds to Thermal Environments. 28 Ontogeny of Temperature Regulation in Birds ........ 36 GENERAL METHODS AND MATERIALS .................. 48 Animals .......................... 48 Incubation ......................... 48 Maintenance ........................ 49 EXPERIMENTAL SERIES I ....... . ............... 51 Experimental Groups .................... 51 Apparatus ......................... 53 Testing Procedures and Measurements ............ 55 Analysis of Data ...................... 62 Results .......................... 63 Discussion ......................... 90 EXPERIMENTAL SERIES II ..................... 109 Experimental Groups .................... 110 Apparatus ......................... 111 Testing Procedures and Measurements ............ 114 Analysis of Data ...................... 117 Results .......................... 117 Discussion ......................... 122 TABLE OF CONTENTS-—continued Page SUMMARY ............................. 124 BIBLIOGRAPHY .......................... 126 TABLE 10. 11. 12. LIST OF TABLES Analysis of Variance of Body Weights (gms) of Chicks Used in the Standard Trials of Experimental Series I ...... Analysis of Variance of Chick Body Temperatures (°C) at Start of 60 Minute Exposure to 10°C (Standard Trials). . . Duncan‘s Test on Mean Chick Body Temperatures (°C) at Start of 60 Minute Exposure to 10°C (Standard Trials). . . Analysis of Variance of Chick Body Temperatures (°C) at End of 60 Minute Exposure to 10°C (Standard Trials). . . . Duncan's Test on Mean Chick Body Temperatures (°C) at End of 60 Minute Exposure to 10°C (Standard Trials). . . . Analysis of Variance of Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 10°C (Standard Trials) ..................... Duncan's Test on Mean Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 10°C (Standard Trials) ..................... Analysis of Variance of Mean Chick Body Temperatures (°C) Measured at Start of Standard Trials and during the Age- Specific Body Temperature Value Determinations ...... Analysis of Variance of Chick Body Temperatures (°C) at Start of 60 Minute Exposure to 10°C ............ Duncan's Test on Mean Chick Body Temperatures (°C) at Start of 60 Minute Exposure to 10°C ............ Analysis of Variance of Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 10°C . . . . Duncan's Test on Mean Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 10°C . . . . vi Page 66 67 68 69 7O 71 72 82 82 83 83 LIST OF TABLES--continued TABLE Page 13. Analysis of Variance of Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 18°C (First Alternative Trial Procedure) ............ 84 14. Mean Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 18°C (First Alternative Trial Procedure) ..................... 84 15. Analysis of Variance of Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 10°C (Standard Trials) and to 18°C (First Alternative Trial Procedure) ..................... 86 16. Mean Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 10°C (Standard Trials) and to 18°C (First Alternative Trial Procedure) ...... 86 17. Analysis of Variance of Chick Body Temperatures (°C) after One Hour of 180 Minute Exposure to 10°C (Second Alternative Trial Procedure) ........... 87 18. Mean Chick Body Temperatures (°C) after One Hour of 180 Minute Exposure to 10°C (Second Alternative Trial Procedure) ..................... 87 19. Analysis of Variance of Chick Body Temperatures (°C) at End of 180 Minute Exposure to 10°C (Second Alternative Trial Procedure) ..................... 88 20. Mean Chick Body Temperatures (°C) at End of 180 Minute Exposure to 10°C (Second Alternative Trial Procedure). . . 88 21. Analysis of Variance of Rates of Change of Chick Body Temperature (°C) during First Hour of 180 Minute Exposure to 10°C (Second Alternative Trial Procedure). . . 89 22. Mean Rates of Change of Chick Body Temperature (°C) during First Hour of 180 Minute Exposure to 10°C (Second Alternative Trial Procedure) ........... 89 23. Analysis of Variance of Rates of Change of Chick Body Temperature (°C) during OFF and ON Procedure Trials. . . . 119 24. Duncan's Test on Mean Rates of Change of Chick Body Temperature (°C) during OFF and ON Procedure Trials. . . . 119 vii LIST OF TABLES--continued TABLE Page 25. Distribution of Chicks in Thermal Gradient Chambers during OFF and ON Procedure Trials ............ 120 26. Analysis of Independence of Chick Positions in Thermal Gradient Chambers during OFF and ON Procedure Trials . . . 121 viii LIST OF FIGURES FIGURE 1. Synopsis of avian temperature regulation (modified from Adams, 1971) ....................... Experimental manipulations and testing procedures used in Experimental Series I ................. Diagram of top view of one chamber (90 x 7 x 20 cm) of multichambered thermal gradient apparatus indicating chamber positions and chamber temperatures during OFF and ON procedure trials ................ Experimental manipulations and testing procedures used in Experimental Series II ................. Page 14 57 112 116 INTRODUCTION Homeothermy has been defined as the ability of an animal to both regulate and maintain body temperature at relatively high, constant levels under diverse thermal environments (King and Farner, 1961). This condition has traditionally been contrasted with poikilothermy in which the body temperature of an animal varies widely and directly with fluc- tuations in ambient temperature. This conceptual differentiation has resulted in the suggestion that only homeotherms could accurately regu- late their body temperature while implying that poikilotherms are capa- ble of little or no such thermoregulatory control. Although perhaps being correct in a theoretically strict and narrow sense, this interpre— tation has neglected studies (e,g,, Clench, 1966; McGinnis and Brown, 1966; Myhre and Hammel, 1969; Heath, 1970; Lillywhite, 1970, 1971; McGinnis and Voigt, 1971; Carey and Lawson, 1973; Crawshaw and Hammel, 1974; Feder and Pough, 1975; Reynolds, gt_al,, 1976; Reynolds and Casterlin, 1978) which demonstrate that certain animals traditionally categorized as poikilotherms precisely regulate their body temperature primarily through behavioral activities (Fry, 1958; DeWitt, 1967; Cabanac, 1972, 1974). Recognizing that most animals are capable of body temperature regulation, Cowles (1940) suggested the terms endothermy and ectothermy_as more realistic alternatives, respectively, to the traditional concepts of homeothermy and poikilothermy. He stressed that the primary difference between animals that regulate 1 2 their body temperature is the source of body heat, either internal (endothermy) or external (ectothermy). The regulation of body temperature in animals has been extensively studied (see reviews in Hardy, Gagge, and Stolwijk, 1970, and in Whittow, 1970, 1971). The majority of these investigations have exam- ined the primarily endothermic birds and mammals, while relatively less work has been done with the other fundamentally ectothermic animal groups. The research on thermoregulation in birds has been character- ized by laboratory experiments performed with adult animals emphasizing the determination and quantification of the physiological mechanisms involved in endothermic temperature regulation (see Dawson and Hudson, 1970; Calder and King, 1974). This research has specified the mecha- nisms of heat conservation and heat production utilized by birds during exposure to imposed cold ambient temperatures and the heat dissipating mechanisms employed by birds under hot thermal conditions. Ectothermic temperature regulation, which involves various behavioral thermoregula- tory responses, has been examined less frequently in avian species under both lab controlled and natural thermal environments. However, studies have shown the existence and utilization of such ectothermic responses in adult birds (see Bartholomew, 1964; Hafez, 1964; Bartholo- mew, 1966; Baldwin and Ingram, 1968; Guhl and Fischer, 1969; Wood—Gush, 1971; Cabanac, 1972, 1974). An extensive literature has developed on the adaptation of animals to their thermal environments (see reviews by Hart, 1957, and in Dill, 1964). These investigations have been primarily concerned with the elucidation of changes related to thermoregulation in animals that are induced by extended residence under different temperature conditions. 3 The results of such work on birds have shown numerous physical, bio— chemical, and physiological factors that are altered by both short- and long-term exposure of avian species to specified thermal conditions (Chaffee and Roberts, 1971). Although the effects of both controlled laboratory (acclimation) and natural thermal environments (acclimatiza- tjgfl) have been examined in numerous species of birds, the emphasis has again been on adults, with only a few studies regarding the effects of these same thermal conditions on younger chicks (e,g,, Ryser and Morrison, 1954; Koskimies and Lahti, 1964). There more recently has been an increasing interest shown in the ontogeny of temperature regulation in animals (see Hill, 1961, and reviews in Whittow, 1970, 1971), particularly in those organisms which show changes from the poikilothermic condition to homeothermy during development. These studies have examined the events accompanying devel- opment which are responsible for the increased thermoregulatory capabil- ities shown in the young animal from birth through the attainment of adult levels of body temperature control. Such investigations in avian species have identified maturation of the physiological mechanisms for heat generation, conservation, and dissipation as being important deter- minants of thermoregulatory ontogeny (e,g,, Dawson, Hudson, and Hill, 1972; Bernstein, 1973). Although changes in these endothermic factors have been studied under both laboratory and natural temperature conditions, there has been little work done on the ectothermic responses of young birds. Those few studies (§,g,, Bartholomew and Dawson, 1954a) examining the ectothermic activities in altricial species have emphasized the behavior of the parents in controlling the body temperature of the chick, suggesting i» 4 minimal input by the young birds themselves early in life. Examination of ectothermic responses in precocial species of birds during develop— ment under either lab controlled or natural temperature conditions has been almost completely ignored. Despite the suggestion (Poczopko, 1967a; Ogilvie, 1970) of some behavioral changes indicative of ecto- thermic regulation in these young chicks, the paucity of relevant data has prevented the drawing of any definitive conclusions at this time concerning the role of behavioral thermoregulation in developing young birds and emphasizes the need for further research in this area. There have been few studies concerning the effects of acclimation temperature on the development of temperature regulation in young birds, even though environmental thermal conditions have been shown to dramati- cally influence thermoregulatory responses in many adult avian species (Chaffee and Roberts, 1971). Those investigations that have examined the ontogeny of temperature regulation in birds can be categorized into two basic types with respect to the relevant thermal conditioning param- eters. Studies of the first type, exemplified by Koskimies and Lahti (1964), have determined the thermoregulatory development in different avian species acclimated or acclimatized to different thermal environ- ments, while studies of the second type, characterized by Dawson and Evans (1957, 1960), have detailed the ontogeny of temperature regula- tion in different species of birds acclimated or acclimatized to the same thermal conditions. The effects of different temperature condi- tions on the development of thermoregulation in a single species of bird have been confounded in the first, and not even tested in the second, type of investigation as described above. The present study was designed to identify and quantify the effects 5 of acclimation temperature on the ontogeny of temperature regulation in the young chick (Gallg§_domesticus). Groups of chicks were acclimated to different thermal environments and subsequently assayed for their endothermic capabilities and ectothermic responses at various ages throughout their early development. It was hypothesized that acclima- tion temperature during early development would have a significant effect on the ontogeny of temperature regulation in the young chick. Domestic chicks were used in this investigation since most of the previous research on thermoregulatory ontogeny in birds has utilized these animals as experimental subjects (Randall, 1943; Freeman, 1965, 1967; Wekstein and Zolman, 1969; Freeman, 1970a; Nekstein and Zolman, 1971; Freeman, 1976). The use of controlled laboratory conditions in this study was dictated by a number of factors. These conditions allow- ed for precise specification of the acclimation temperatures and thermal testing parameters (e,g,, cold exposure temperatures) incorporated in the current investigation as opposed to those used in field studies, which certainly have been less rigorously controlled, in some cases undefined, and subject to the additional influence of such factors as wind, rain, and photoperiod (see Ryser and Morrison, 1954, and Hart, 1957). Furthermore, social parameters can become confounded with the thermoregulatory capabilities of the individual chick, as indicated in studies (Ricklefs and Hainsworth, 1968a; Mertens, 1969; Yarbrough, 1970; Dunn, 1976c) which have demonstrated the contributions of the parent(s) and/or sibling(s) to body temperature regulation in the young bird. Moreover, it would be extremely unlikely that a population of birds, sufficient with respect to numbers, age ranges, accessibility, similar genetic background, and, most importantly, diverse yet specified thermal 6 acclimation conditions, could be found in the natural environment that would permit execution of the present investigation as a field study. It was therefore necessary to utilize specified laboratory conditions so that the relevant factors mentioned above were either controlled or randomized, thereby providing answers to the specific questions posed in this investigation. In addition, the thermal acclimation and testing parameters utilized in the present investigation were either similar or identical to those used in earlier studies, so that direct comparisons could be made between the results of this investigation and previous work on avian thermoregulatory development. Finally, it was anticipated that the results of the present investigation would provide suggestions for future research in the area of avian thermo- regulatory ontogeny. REVIEW OF LITERATURE Temperature regulation in birds has been extensively studied from a variety of different experimental approaches. Although more research is needed to permit specification comparable to that currently available for mammals, a fairly cohesive picture has emerged concerning the impor- tant factors involved in the maintenance of body temperature in many avian species. A review of the literature on thermoregulation in birds is presented below. The body temperature levels in birds and factors which influence them will first be examined. The concepts and termi- nology utilized in research on temperature regulation are then consi- dered. This is followed by an examination of the thermoregulatory responses of birds exposed to cold and warm temperature conditions. Next will be a discussion of the effects of extended exposure to various thermal environments on the regulation of body temperature in avian species. The ontogeny of thermoregulation in birds is subsequently detailed in a critical analysis of the previous studies in this area. Finally, two series of experiments designed to determine the effects of thermal acclimation during early development on the ontogeny of temperature regulation in Gallus domesticus are presented. Body Temperatures jn_Birds The body temperatures of birds have been determined at numerous locations in the body, utilizing a variety of measurement techniques, 7 8 under many different experimental conditions (see King and Farner, 1961). These studies have demonstrated the relative stability of the central or "core” or deep body temperature as measured in the body cavity or brain case of birds, in contradistinction to the variable temperatures recorded at the periphery, on surface areas, or in the extremities, which themselves are indicative of the activity of impor- tant vasomotor thermoregulatory mechanisms (Kallir, 1930; Steen and Enger, 1957). Techniques of measurement have included the use of mercury thermometers (Fronda, 1921) and thermistor probes (Wekstein and Zolman, 1967) inserted to various depths into the cloaca or proventric- ulus while holding the live bird or, in some unavoidable cases, dead birds immediately after they have been retrieved (Palmgren, 1944). Attempting to reduce the problems associated with struggling live birds and the rapid heat loss from dead birds, more recent studies (Bligh and Hartley, 1965; Hudson and Kimzey, 1966; Coulombe, 1970; Boyd and Sladen, 1971; Cain and Wilson, 1971; Langman, 1973; Mitchell and Siegel, 1973; Southwick, 1973; Shallenberger, Whittow, and Smith, 1974; Smith, Peterson, and Thigpen, 1976) have utilized thermocouples and temperature transmitters implanted into the musculature or body cavity of the bird. While permitting more accurate measurements of body tem- perature in the unrestrained animal, these newer techniques have also imposed some additional experimental restrictions, including greater cost, limiting the number of animals that can be simultaneously mea- sured, and difficulty of equipment adaptation for use in the field situation. Body temperature measurements have been recorded under a variety of different experimental conditions, such as during the active phase in awake birds under moderate ambient temperatures, in the dark 9 at night during the postabsorptive state under thermoneutral tempera- tures with minimal disturbance to the bird, and the many possible combinations and permutations of these conditions (see King and Farner, 1961). Considering the variable methods which have been utilized and the diverse experimental conditions under which these measurements have been recorded, it is not surprising that a 6-7°C total range of “normal“ deep body temperatures has been found across the various orders of birds (see Dawson and Hudson, 1970). However, it has been established that adult birds in most orders maintain their body temperatures in the more re— stricted range from 40-43°C, with chickens reportedly within the range between 41.5-42.2°C (Robinson and Lee, 1946; Whittow, 1965a), which is decidedly higher than the body temperature range found in mammalian species (McNab, 1966). Yet, studies have shown consistent differences in the body temperatures recorded not only in the different orders and species of birds, but also within individuals of the same avian species under equable thermal conditions (Lamoreux and Hutt, 1939; Udvardy, 1955; Kheireldin and Shaffner, 1957). A variety of factors have been identified which influence the body temperature level maintained in birds. Definite cycles of body tempera- ture have been found, with an amplitude range of 1-4°C, showing the highest levels during the active phase of either the nocturnal or diurnal cycle (Fronda, 1921; Baldwin and Kendeigh, 1932; Dawson, 1954; Irving, 1955; Farner, Chivers, and Riney, 1956; Dawson, 1958; Coulombe, 1970; Cheke, 1971). These cycles apparently are keyed to photoperiod rather than ambient temperature variations (Koskimies, 1950; Dawson, 1954; Goldsmith and Sladen, 1961; Veghte, 1964), although endogenous 10 components have also been demonstrated (Eklund, 1942; MacMillen and Trost, 1967). These body temperature cycles have been closely related to changes in the activity of the bird which mirror alterations in other relevant variables, such as metabolic rate (Benedict and Riddle, 1929; Benedict, Landauer, and Fox, 1932; Barott, et_gl,, 1938; Barott and Pringle, 1941; Kendeigh, 1944; Rautenberg, 1957; Merkel, 1958; Aschoff and Pohl, 1970; Pohl and West, 1973). Moreover, activity of the bird within phases of the cycle has an effect on the body tempera— ture recorded, sometimes resulting in drastic changes (Baldwin and Kendeigh, 1932; Deighton and Hutchinson, 1940; Dawson, 1954; Irving and Krog, 1954; Farner, 1956, 1958). Many studies have demonstrated the influence of ambient thermal conditions on raising or lowering body temperature in birds, especially following extended, continuous expo— sure to environmental temperatures outside the thermoneutral zone (Heywang, 1938; Wilson, 1949; Bartholomew and Dawson, 1952). A direct relationship has been shown between food intake and plane of nutrition both on metabolic rate (Mellen, Hill, and Dukes, 1954) and recorded body temperatures (Robinson and Lee, 1947; Hazelwood and Wilson, 1962). Although there may be some minor exceptions (e,g,, Winchester, 1940; Udvardy, 1955; Steen, 1958), most studies have supported the suggestion that body temperature levels are not genetically adapted to climate or physiologically adapted to seasons, since birds from the tropics and arctic areas, as well as those experimentally acclimated to different thermal conditions, maintain essentially the same body temperature year- round (e 9,, Wetmore, 1921; Scholander, et_al,, 1950a; Irving and Krog, 1954; Dawson and Schmidt-Nielsen, 1964; King and Farner, 1964; Yousef, McFarland, and Wilson, 1966; Yarbrough, 1971). Sex differences in body 11 temperature have been shown (Baldwin and Kendeigh, 1932; Riddle, Smith, and Benedict, 1932; Lamoreux and Hutt, 1939; Freeman, 1963; Whittow, Sturkie, and Stein, 1964; Gilbreath and K0, 1970) but are not pronounced and may be confounded with sex differences in other relevant factors, such as activity. While studies (§,g,, Randall, 1943; Romijn, 1954) have documented the increase in body temperatures with advancing age in young birds, the underlying causes and implications of this develop- mental change remain to be fully explored. 0n the basis of available data, Dawson and Hudson (1970) suggested the preferential specification of a restricted range of body tempera- tures, as opposed to the characterization of a single body temperature level, when describing an individual, or species of, bird. Although subsequent research has further corroborated this important point, it does not refute the demonstration of relatively stable body temperatures in an individual bird, over short periods of time in the daily tempera- ture cycle, with a variability that is obviously smaller than the 6-7°C range demonstrated at the ordinal level and certainly less than the l-4°C range shown in most avian species over the daily body temperature cycle. Moreover, this does not preclude valid comparisons of body tem- perature measurements of individual birds recorded under identical thermal conditions at the same times within the daily cycle of body temperatures. Concepts and Terminology erlemperature Regulation An understanding of the concepts and terminology used in research on temperature regulation in animals is necessary before examining further the literature in this area with respect to birds. The 12 following discussion is based on information presented in a number of good sources on this subject (e,g,, Hardy, 1961; von Euler, 1961; Hammel, 1968; Bligh, 1973; Cabanac, 1975) and draws heavily on the excellent review by Adams (1971). The concepts and terminology of thermoregulatory research, originally developed primarily from work on mammalian subjects, have been directly applied to avian species with only minor modifications (King and Farner, 1961). Since temperature is determined by heat content, an understanding of the temperature of an object requires knowledge of the factors which influence its heat content. The exchanges of thermal energy taking place between an object and its external environment, which can result in a net gain, loss, or no change in heat transferred, determine the heat content of that object. In living organisms, metabolic activity is always a source of heat gain, whereas thermal energy is always lost through the evaporation of liquids from body surfaces, given the nec- essary vapor pressure gradient between the evaporating surface and the surrounding environment. Additional avenues of heat exchange include conduction, convection, and radiation. Whether heat is gained by or lost from the living organism along these routes depends on the thermal gradient existing between that organism and its environment. If the organism has a higher temperature, it will lose heat to the environment by conduction, convection, and radiation. Alternatively, if the ambient temperature is greater, the organism will gain heat through all three of these avenues. A stable body temperature is achieved by the organism maintaining a balance between the ongoing rates of heat exchange. The level of body temperature which is maintained in the higher vertebrates is thought to be determined by the hypothalamic "set point" (Gale, 1973; Hensel, 1973). Conduction, convection, and radiation all become avenues of heat loss (j,g,, thermolysis) during exposure of an organism to cold environ- mental temperatures and, when added to the thermal losses due to evapor- ation, represent the total heat flow from that organism. The only source of heat gain to the organism under such cold conditions is from its metabolic activity (j,§,, thermogenesis). If heat gained from metabolism cannot offset the heat lost by the other combined sources, hypothermia in the organism must ensue. The physiological mechanisms employed by an organism to maintain body temperature under cold exposure are therefore directed toward increasing heat gain through enhanced metabolic activity and reducing heat loss via conductive, convective, radiative, and evaporative routes. During exposure to warm environmental temperatures, heat is gained by the organism from its own metabolic activities and, at thermal levels above body temperature, from the combined sources of conduction, convec— tion, and radiation. Under these warmer temperature conditions, the only effective route of heat loss from the organism is by evaporation. If the heat lost via evaporation is less that the sum of the heat gained by the other avenues, hyperthermia ultimately results in the animal. The maintenance of body temperature in an organism under heat exposure involves the utilization of physiological mechanisms which increase heat loss under warm temperatures and reduce heat gain under hot conditions through conductive, convective, and radiative routes and increase heat loss via evaporation under hot thermal conditions. A synopsis of temperature regulation in birds is presented in Figure 1. The limited range of environmental temperatures in which 14 .AHmmH ,mEmu< Eoew novewwoev cowum_:mwc mezucequwH cmv>m to mwmaocxm .H wezmwm 522meth 45522822.”. 3.835 P V 3838 .2 \ .. .. x .. .. .\ a I: 1* $0, Lopez L.“ at; 332810;“: “an“; a t:****#* E82 .3 mm.» if figyfifi ~ In aaaifiaw? ea \ \Il unnuuuu-.. 20.5333 u.. «.4 av 1: ss :1 “NW 8.8; 0:832: lawful: flat 3? * I | \ \ Am I; \ . ~ .1. I|| \ .5. b. a s O I: 832853 av a s o If It a??? 25m :85 a; X ss 00 if: 1W 1% X \s 00 .1. . i. any 1: .. I | \ O 1.51.; ea c. a aaaaaaaaaa on met 0 oouoooo 00.... 832353 02.00 0.. 0000» was: to 000 o 0 been 960 000 00000 Page: a a. a o a 0 MW 00 1' 8.8.8.323; IV 0 _ 00 5.3876 5.50.7528 on 1 -32, AzfiEusmcoEewfi VT -32, _ . V I ‘ .0 o>5mcoaw>mlll| $3636.6ch ofionfimz V . .Anllllll =36??? I'llIJAiSEmS? .1 3:26:23»: 32558»: £315”.on Y Y All!‘ 15 body temperature is maintained with minimal implementation of the physiological thermoregulatory mechanisms is defined as the thermo- neutral zone. Exposure of a bird to progressively colder external temperatures below the zone of thermoneutrality initially invokes primarily ”physical” regulation by heat conserving mechanisms includ- ing peripheral vasoconstriction and ptiloerection, which are sufficient to maintain thermal balance down to the lower critical temperature. Environmental temperatures below the lower critical temperature neces- sitate the addition of ”chemical" regulation by heat producing mecha- nisms such as shivering to permit successful thermoregulation under these cold conditions. Hypothermia, identified by precipitous decreases in body temperature and metabolic rate, develops when the physiological mechanisms of the bird are unable to maintain a balance of heat ex- changes at even colder ambient temperatures. Exposure of a bird to progressively warmer external temperatures above the thermoneutral zone initially evokes ”physical" regulation by heat dissipating mechanisms including peripheral vasodilation and, to a lesser extent, ptilodeflection, which are adequate to maintain body temperature below the upper critical temperature. Ambient temperatures above the upper critical temperature require an additional increase in evaporative heat loss to sustain effective thermoregulation under these warm conditions. At even warmer environmental temperatures, hyper- thermia, indicated by a rapid rise in body temperature and a dramatic decrease in evaporative heat loss, results when heat balance cannot be achieved by additional activity of the physiological thermoregulatory mechanisms of the bird. It should be noted here that the overview presented above has been 16 based on the traditional concept of homeothermy with respect to body temperature regulation in birds.‘ Consequently, the emphasis has been placed on endothermic control and its related physiological mechanisms, reflecting priorities evident in the past and current research in this area. Ectothermic responses and their input into such a thermoregula- tory scheme therefore have, at best, been relegated to a rather minor role in modifying the ongoing rates of heat exchange by conduction, convection, and radiation, and, at worst, have been virtually neglected as a potentially valuable and perhaps even the only means of body tem- perature regulation in the absence of effective endothermic control. Avian Thermoregulatory Responses 39 Cold The previous discussion has indicated that, as the environmental temperature decreases, a bird is faced with reduction in body tempera- ture due to heat loss through conductive, convective, radiative, and evaporative routes. Under these colder temperature conditions, thermal energy can accrue to the organism only from the heat produced by its own metabolic activities. The physiological responses of birds exposed to cold environmental temperatures have been shown to include mechanisms which both reduce thermolysis and increase thermogenesis (King and Farner, 1961). Behavioral responses have also been identified which contribute to the maintenance of thermal balance in birds during expo- sure to cold ambient temperatures (Hafez, 1964; Cabanac, 1974). Al- though decreases in body temperature and cold torpor have been docu- mented in some birds under cold environmental temperatures (e,g,, Bartholomew, Howell, and Cade, 1957; Ramsey, 1970; Wolf and Hainsworth, 1972), adaptive hypothermia ddes not appear to be widespread among 17 avian species. Considerable reduction in thermolysis in birds under cold thermal conditions is afforded by peripheral vasoconstriction which retards heat flux through conduction and radiation by decreasing the thermal gradient between the body surface and the external environment (Johansen and Tonneson, 1969; Jones and Johansen, 1972). Greatly depressed skin tem- peratures have been recorded on the legs, feet, beaks, and heads of many avian species during cold exposure (Kallir, 1930; Wilson, Hellerman, and Edwards, 1952; Bartholomew and Dawson, 1954b; Irving and Krog, 1955; Bartholomew and Cade, 1957; Ederstrom and Brumleve, 1964; Malhotra and Clayton, 1965; Steen and Steen, 1965; Drent and Stonehouse, 1971). These results indicate the extensive utilization of vasomotor adjust- ments under these poorly or non-feathered surfaces (von Saint Paul and Aschoff, 1968; van Kampen, 1971) which represent potentially critical sites of heat loss under cold environmental temperatures. Anatomical modifications of peripheral vasculature have also been demonstrated (Grant and Bland, 1931; Irving and Krog, 1955; Ederstrom and Brumleve, 1964; Whittow, 1965a) which permit countercurrent heat exchange (Scho— lander and Krog, 1957) that further augments reduced heat loss in the extremities. At a minimal metabolic cost, these vasomotor responses contribute to the increased overall insulation measured in birds during cold exposure, thereby constituting an efficient mechanism for reduction in thermolysis under these cold temperature conditions (Bartholomew and Cade, 1957; West, 1962; Hudson and Brush, 1964; King, 1964; West and Hart, 1966). In contrast to the decreased temperatures recorded on poorly insu— lated areas, the body surfaces of birds that are effectively covered 18 with feathers have been shown to remain at relatively high temperatures even under severe cold stress (Kallir, 1930; Wilson and Plaister, 1951; Bartholomew and Dawson, 1954b; Irving and Krog, 1955; Steen and Enger, 1957; Irving, 1964; Veghte, 1964; Boone, 1968; Rautenberg, 1969; Richards, 1971). These warmer body surface temperatures may be due to changes in peripheral blood flow and/or to the presence of feathers on these surface areas. Although the existence and importance of peripher- al vasomotor activities under feather-covered body surfaces of birds remains to be fully determined, the plumage alone apparently contributes significantly to overall insulation in many avian species (Benedict, gt al,, 1932; Deighton and Hutchinson, 1940; Hutchinson, 1954a; Herreid and Kessel, 1967). Birds with heavier plumage retain heat better than birds with lighter feathers (Irving, 1960; Whittow, 1965a). Defeathered birds lose heat faster, and have shorter survival times, than birds with intact plumage under the same cold thermal conditions (Baldwin and Kendeigh, 1932; Lee, et_al,, 1945; Streicher, Hackel, and Fleischmann, 1950; Brush, 1965), even though their metabolic rates increase (Hoffman and Shaffner, 1950). Birds with defective plumage are less cold toler- ant than normally feathered individuals (Wallgren, 1954). Moreover, alteration of the feather arrangement through ptiloerection enhances the insulative properties of the plumage, as demonstrated by Kendeigh (1939) and Delane and Hayward (1975) and also suggested by other observations (Hutchinson, 1954a; Irving, 1960; McFarland and Baher, 1968). Although the input of natural ptilomotor responses into the maintenance of ther- mal balance in avian species has only begun to be quantified (McFarland and Budgell, 1970), these responses are obviously involved in the reduction of heat loss by conductive, convective, and radiative routes 19 with minimal energy expenditure in birds exposed to cold environmental conditions (Irving, 1960). Evaporation represents an additional avenue of thermolysis in avian species during cold exposure. Because birds do not have any sweat glands, the majority of evaporative heat loss has been assumed to occur via the respiratory system and associated structures. Further research is necessary to ascertain the mechanisms involved, but it has become clear that most birds maintain a low level of evaporative water loss similar to that shown in the thermoneutral zone (Kendeigh, 1944; King and Farner, 1964; Bartholomew and Trost, 1970; Moldenhauer, 1970), and in some cases even show decreases below this level (Lasiewski and Dawson, 1964; Lasiewski, 1972), upon exposure to cold environmental temperatures, thereby achieving a reduction of evaporative heat loss. There is some question as to the route over which such reduced heat flux actually occurs however, since cutaneous non-respiratory water loss may be a significant factor in overall evaporation (Bernstein, 1969; Smith and Suthers, 1969; Bernstein, 1971b). Vasomotor, ptilomotor, and supposedly respiratory mechanisms which can effect a reduction of thermolysis become incapable of maintaining thermal balance in a bird below the the lower critical temperature, necessitating thermogenesis to permit continued body temperature control under these cold thermal conditions. Increases in heat production above basal levels in birds exposed to such cold environmental temperatures have been documented in many avian species (Benedict and Lee, 1937; Kendeigh, 1939; Barott and Pringle, 1946; Howell and Bartholomew, 1962b; Ivacic and Labisky, 1973; Rasmussen and Brander, 1973; Smith and Prince, 1973; Goldstein, 1974; Holmes and Sawyer, 1975). The available data 20 suggests that this additional thermogenesis results primarily from in- creased muscular activity that initially appears as enhanced regional muscle tonus which expands to more pronounced whole-body shivering with further decreases in ambient temperature (Steen and Enger, 1957; Hart, 1962). The close, direct relationship found between intensity of shiv— ering and level of thermogenesis in birds exposed to progressively colder temperatures has demonstrated the importance of muscular heat production in the maintenance of thermal balance in birds under these cold temperature conditions (West, 1965). Although implicated in some adults (Kayser, 1929; El Halawani, Wilson, and Burger, 1970) and par- ticularly in young chicks (Wekstein and Zolman, 1968), non-shivering thermogenesis does not appear to be utilized in most avian species (Hart, 1962; Chaffee, §t_a1,, 1963), at least not to the extent that has been demonstrated in mammals (Smith and Horwitz, 1969). This may be related to the fact that birds do not have brown adipose tissue (Freeman, 1967; Hissa and Palokangas, 1970; Johnston, 1971) which has been shown to be of critical importance in the non-shivering thermo— genesis of many mammalian species. Moreover, avian adipose tissue ap- pears to be insensitive to the calorigenic effects of catecholamines (Hazelwood, 1972). Indicative of the increased rate of heat production with falling ambient thermal conditions, temperature coefficients (j,§,, increases in metabolism above basal rate upon exposure to cold tempera- tures below the thermoneutral zone) measured in many avian species have demonstrated that metabolism may be increased as much as fivefold for several hours (Lasiewski and Dawson, 1967). Such an intense metabolic increase over extended periods of time would place a severe drain on bodily energy reserves which must ultimately be replenished by food 21 intake. The specific dynamic action of ingested food, as well as acti- vities associated with feeding, may constitute useful additional sources of heat to birds exposed to cold, as suggested by Groebbels (1928), Barott, 93.91: (1938), Berman and Snapir (1965), and Brooks (1968). An increase in locomotor activity has been found in some avian species under cold environmental conditions (esg,, Morrison, 1962; Pohl, 1969; Spurr, 1978) which may provide an alternative source of heat production that could substitute for shivering calorigenesis in such a cold thermal environment. However, the resultant savings in heat production required to maintain thermal balance under these cold conditions may be obviated by a concomitant increase in thermal conductance due to such voluntary responses (West and Hart, 1966). Other studies have, in fact, shown decreased activity rates in birds as ambient temperatures become cold- er (§,g,, Grubb, 1978). A number of behavioral responses which facilitate temperature regu- lation in birds exposed to cold environmental conditions have been documented (Hafez, 1964; Baldwin and Ingram, 1968; Wood-Gush, 1971). Hutchinson (1954a) has described the responses of fowl to cold tempera- tures. These animals tend to remain in a crouched position even when moving and hold their wings close to the body, with the feathers erected whenever the bird is inactive or sleeping (Moore, 1945). Protection of poorly insulated surfaces is accomplished through such activities as tucking the head under the wing or sitting the body upon the legs and feet, thereby effectuating considerable reduction in thermolysis (Deighton and Hutchinson, 1940; Goldsmith and Sladen, 1961; Alder, 1963; Veghte and Herreid, 1965; Jones and Johansen, 1972; Evans and Moen, 1975). Huddling behavior demonstrated in adult and young birds 22 (Lehmann, 1941; Bartholomew and Dawson, 1952; Lohrl, 1955; Irving, 1964; Pulliam, gt_gl., 1974), as well as communal roosting (Knorr, 1957; Frazier and Nolan, 1959; Brenner, 1965), effectively reduces the meta- bolic cost of thermoregulation in the cold (Kleiber and Winchester, 1933; Kendeigh, 1960; Case, 1973). The maintenance of thermal balance in cold-exposed birds is assisted by the utilization of burrows and other forms of natural shelter (Kendeigh, 1934; Wetmore, 1945; Cade, 1953; Pearson, 1953; Kluyver, 1957; French, 1959; Dawson, 1962; Irving, 1964; King and Wales, 1964; Calder, 1971; Kilham, 1971; Calder and Booser, 1973; White, Bartholomew, and Kinney, 1978). Sunbathing has been shown in birds (Hauser, 1957; Heath, 1962; Morton, 1967; Teager, 1967; Kennedy, 1969; King, 1970; Kahl, 1971; Mueller, I972; Cade, 1973; Leck, 1974; White, Bartholomew, and Howell, 1975) which contributes to thermoregulation by the addition of solar heat. However, any external source of radiant energy apparently can substitute for increased meta— bolic rate in birds during cold stress (Hamilton and Heppner, 1967; Lustick, I969; Heppner, 1970; Lustick, 1970, 1971; Ohmart and Lasiewski, 1971). In general though, relatively few ectothermic responses of birds to cold environmental conditions have thus far been adequately de- scribed. Moreover, quantification of the precise thermoregulatory effects of ectothermic responses remains to be determined for most avian species. Avian Thermoregulatory Responses 39 Heat It was previously indicated that a bird becomes liable to increased body temperature as the environmental temperature rises. This organism always gains heat from its own metabolic activity and, under hot thermal 23 conditions, also along conductive, convective, and radiative routes. Heat loss is achieved by conduction, convection, and radiation under warm thermal conditions, while at hot ambient temperatures, evaporation affords the only effective avenue of thermolysis available to the bird. The physiological responses of avian species exposed to increased environmental temperatures have been shown to include mechanisms which reduce heat gain under hot thermal conditions and increase heat loss at both warm and hot temperatures (King and Farner, 1961). Heat pro- duction does not decrease under these warm thermal conditions and, in fact, becomes exacerbated due to 010 effects (King and Farner, 1964; Whittow, 1965b; Calder and King, 1974). Behavioral responses have been identified which contribute to the maintenance of thermal balance in birds exposed to heat (Hafez, 1964; Baldwin and Ingram, 1968; Cabanac, 1974). Increasing the thermal gradient between the body surfaces and the external environment enhances heat loss from poorly insulated body surfaces of the bird during exposure to warm environmental temperatures. Peripheral vasodilation has been demonstrated in the extremities of many avian species (Bartholomew and Cade, 1957; Bartholomew and Dawson, 1958; Howell and Bartholomew, 1961a; Kahl, 1963; Whittow, Sturkie, and Stein, 1964; Steen and Steen, 1965; Lasiewski and Bartholomew, 1966), as well as in the combs and wattles of fowl (Yeates, Lee, and Hines, 1941; van Kampen, 1971), by the increased temperatures measured at these body surfaces under warm thermal conditions. Wilson (1949) and Whittow §t_§1, (1964) have shown the thermoregulatory importance of the combs and wattles in fowl under heat stress. Ptilodeflection has also been shown in birds exposed to warm thermal conditions which facilitates 24 thermolysis from feather-covered surfaces (Dawson, 1954). Removal of the feathers has been shown to increase the heat tolerance of birds (Lee, gt_gl., I945). Wallgren (1954) demonstrated that birds with defective feathers are more heat tolerant than normally—feathered individuals. Vasomotor and ptilomotor responses contribute to the enhanced thermal conductance, demonstrated in many avian species (Kendeigh, 1944; Wallgren, 1954; Dawson, 1958; Fisher, Griminger, and Weiss, 1965; Greenwald, Stone, and Cade, 1967; Trost, 1972; MacMillen, 1974), which progressively increases to a maximal value in birds exposed to even warmer ambient temperatures. Many birds have also shown a moderate hyperthermia coincident with the rise in thermal conductance which augments favorable heat exchange under these warm temperature conditions (Kendeigh, 1944; Bartholomew and Dawson, 1954a; Dawson, 1954; Bartholomew and Cade, 1957; Bartholomew and Dawson, 1958; Dawson, 1958; Dawson and Schmidt-Nielsen, 1964; King and Farner, 1964; Marder, 1973a; Calder and King, 1974). When rising environmental thermal conditions surpass body tempera- ture, conduction, convection, and radiation all become avenues of heat gain to a bird. However, since there is an upper limit to the amount of heat that can safely be stored by adaptive hyperthermia (Moreng and Shaffner, 1951; Calder, 1964), further increases in body temperature to reduce heat gain are precluded. Maintenance of thermal balance in birds exposed to these excessively warm thermal conditions necessitates the activation of mechanisms which prevent additional heat influx from the environment. Pronounced ptiloerection, described in some birds subject to very high ambient thermal conditions (Weller, 1958; Calder and Schmidt-Nielsen, 1967; Crawford and Schmidt-Nielsen, 1967; 25 Shallenberger, gt_gl,, 1974), serves to retard heat gain from such a hot environment (Misch, 1960; Hinds and Calder, 1973; Marder, 1973b). Con- comitant alterations in peripheral vasomotor responses in birds have not only been demonstrated (Yeates, gt p1,, 1941; Bartholomew and Cade, 1957; Bartholomew and Dawson, 1958; Hatch, 1970), but also have been shown to be important avenues of heat loss under these warm thermal conditions (Kahl, 1963; Steen and Steen, 1965; Johansen and Tonneson, 1969; Jones and Johansen, 1972). During intense as well as moderate heat stress, evaporation becomes the only significant avenue of thermolysis by which birds can success- fully maintain body temperature. There has been some indication that cutaneous non-respiratory water loss may contribute to thermoregulation in some birds during heat exposure (Bernstein, 1969; Smith and Suthers, 1969; Bernstein, 1971a, b; Lasiewski, Bernstein, and Ohmart, 1971; Lee and Schmidt-Nielsen, 1971; van Kampen, 1971) even though these organisms do not have any sweat glands. However, the surfaces of the respiratory system and buccal cavity have been identified as the most significant sites of evaporative water loss in virtually all avian species studied to date (Kayser, 1930; Baldwin and Kendeigh, 1932; Barott and Pringle, 1946; Dawson and Schmidt-Nielsen, 1964; King and Farner, 1964). Since the amount of water evaporated from a surface is related to the extent of air movement over that area, given a sufficient water vapor pressure gradient (Hutchinson, 1954b), modulation of respiratory rates consti- tutes an important physiological mechanism by which evaporative heat loss is controlled in avian species (Kendeigh, 1944; Dawson, 1958; Richards, 1970). Many birds show a direct relationship between body temperature and the respiratory rate above the thermoneutral zone 26 (Salt, 1964; Lasiewski, Dawson, and Bartholomew, 1970; Henderson, 1971), with many avian species exhibiting a relatively high, species-typical rate of breathing characterized as panting which commences when body temperature reaches and exceeds some critical level (von Saalfeld, 1936; Randall and Hiestand, 1939; Boni, 1942; Randall, 1943; Kendeigh, 1944; Frankel, Hollands, and Weiss, 1962; Linsley and Burger, 1964; Lasiewski and Bartholomew, 1966; Crawford and Schmidt-Nielsen, 1967; Siegel and Drury, 1968a, b; Schmidt-Nielsen, §t_gl., 1969; Smith, 1972; Weathers, 1972; Mosher and White, 1978). Gular flutter is also employed by some birds and has been shown to greatly increase evaporative water loss by more effectively utilizing the moist surfaces of the pharyngeal cavity (Cowles and Dawson, 1951; Bartholomew, Dawson, and O'Neill, 1953; Bartholomew and Dawson, 1954b; Howell and Bartholomew, 1962a; MacMillen and Trost, 1967; Bartholomew, Lasiewski, and Crawford, 1968; Calder and Schmidt-Nielsen, 1968; Lasiewski, 1969; Lasiewski and Snyder, 1969; Bartholomew and Trost, 1970; Lasiewski and Seymour, 1972; Smith, 1972). Panting and gular flutter mechanisms probably require minimal energy expenditure (Bartholomew, Hudson, and Howell, 1962; Lasiewski, 1969; Lasiewski and Seymour, 1972) since their operation is thought to occur at or near the natural resonant frequency of these respective appara- tusses (Dawson and Schmidt-Nielsen,.l964; Crawford and Kampe, 1971; Brackenbury, 1973). Although the attendant muscular activity adds to the metabolic heat load, panting and gular flutter mechanisms have demonstrated extreme efficiency in permitting birds not only to main- tain thermal balance under severe heat stress (Bartholomew and Dawson, 1954b; Bartholomew, gt_al,, 1962; Howell and Bartholomew, 1962a; Calder and-King, 1963; Marder, 1973a; Marder, Arad, and Gafni, 1974), but also 27 to even reduce body temperature in some species exposed to these hot thermal conditions (Crawford and Schmidt-Nielsen, 1967; Lasiewski, 1969). A number of behavioral responses which contribute to avian thermo- regulation during exposure to heat have been deScribed (Hafez, 1964; Baldwin and Ingram, 1968). Postural adjustments which facilitate heat loss, such as standing (Deighton and Hutchinson, 1940), holding the wings away from the body (Dawson, 1954; Hutchinson, 1954a; Bartholomew, 1966; Kahl, 1971; Marder, 1973b), exposing the legs and feet to con- vective air currents (Howell and Bartholomew, 1961a), and lying down on the cool ground with head extended (Hafez, 1964) have been observed. Birds may also shade or fan themselves (Weller, 1958) and bathe in water, mud, or dust to augment thermolysis (Wilson, gt_gl,, 1952; Bartholomew, _e_t_ 31., 1953; Calderwood, 1953; Dawson, 1954; Hutchinson, 1954a; Slessers, 1970). The tendency of avian species to decrease locomotor activity under heat stress (Calder and Schmidt-Nielsen, 1967; MacMillen and Trost, 1967; Austin, 1976), or at least to reduce or even refrain from activity during the warmest portions of the daily activity cycle (Dawson, 1954; Calder, 1968; Ricklefs and Hainsworth, 1968b; Kavanau and Ramos, 1970), has been established. When active under warm thermal conditions, many birds will utilize shaded locales or shelters (Dawson, 1954; Hensley, 1954; Hudson, 1962; Smyth and Bartholomew, 1966; Crawford and Schmidt-Nielsen, 1967; Johnson, 1968; Ligon, 1968; Serventy, 1971; Marder, 1973c; Austin, 1976; MacMillen, gt_al,, 1977), while some birds may fly to cooler areas (Madsen, 1930; Pennycuick, 1972). The use, construction, and orientation of the nest may itself aid thermoregulation under warm conditions (Bartholomew, 28 White, and Howell, 1976; Walsberg and King, 1978). Reduction in feeding has been demonstrated in avian species during heat stress (Persons, Wilson, and Harms, 1967; Brooks, 1968; Swain and Farrell, 1975), whereas drinking usually increases and is often accompanied by the splashing of water on various body surfaces (Yeates, gt_al,, 1941; Lee, gt gl,, 1945; Robinson and Lee, 1946; Wilson, 1948; Seibert, 1949; Fox, 1951; Wilson and Edwards, 1952; Bartholomew and Dawson, 1954a; Dawson, 1954; Bartholomew and Cade, 1956; Wilson, McNally, and Ota, 1957; Parker, Boone, and Knechtges, 1972). Defecation and urination may also afford birds some relief from extreme heat (Wilson, gt_gl,, 1957; Kahl, 1963; Hatch, 1970), although the thermoregulatory importance of urohidrosis has been questioned (King and Farner, 1964; Berger and Hart, 1974). It is of interest to note that many more behavioral responses that may affect thermoregulation have been described in birds during heat stress than when exposed to cold thermal conditions, which may be related to the observation that physiological temperature regulating mechanisms in birds appear to have evolved mainly along lines of enhancing heat pro- duction and heat retention rather than towards increasing thermolysis. Physiological Adaptations pf_Birds tp_Thermal Environments An extensive amount of work has been done on the adaptation of birds to different thermal environments (Hart, 1957; see reviews in Dill, 1964). Since the ability of a bird to regulate its body tempera- ture, and the manner in which this is achieved, can be influenced by the prior thermal history of that organism, it is important to under- stand the effects of these temperature experiences on the maintenance of thermal balance in avian species exposed to diverse environmental 29 temperatures. Previous research has identified a number of physical, biochemical, and physiological changes related to thermoregulation that are induced in birds by their residence in cold as well as warm environ- ments (Chaffee and Roberts, 1971). However, because differences have been found between the effects of laboratory-controlled as compared to seasonal temperature conditions, it is necessary to examine the influ- ence of both of these thermal conditions and to differentiate between the effects of acclimation or temperature conditioning and those which result from natural acclimatization. Alterations in metabolic, insula- tive, evaporative, and other pertinent factors relating to avian thermo- regulation which contribute to the adaptation of birds to diverse ther- mal environments have been extensively documented (see Dawson and Hudson, 1970). Although a variety of changes have been shown in birds subjected to different thermal conditions, a rather confusing and sometimes con- tradictory picture has emerged concerning the effects of both short- and long-term exposure to cold environmental temperatures on the para- meters of avian thermoregulation. For example, some studies have documented a significant increase in the insulative indices of birds maintained under cold environmental temperatures in the lab (West and Hart, 1966) and as a result of seasonal changes (Riddle, Smith, and Benedict, 1934; Scholander, et al,, 1950c; Wallgren, 1954; Hart, 1962; Veghte, 1964; Veghte and Herreid, 1965; Coulombe, 1970; West, 1972a; Kendeigh and Blem, 1974). These insulative increases may be due to alteration of the plumage (Kendeigh, 1934; Wallgren, 1954; Irving, 1960; Hart, 1964), vasomotor adjustments (Ederstrom and Brumleve, 1964; Veghte, 1964; Hissa and Palokangas, 1970), or changes in the thickness 30 of subcutaneous fat depots (King and Farner, 1965, 1966; King, 1972). However, other investigations (Davis, 1955; Hart, 1962, 1964; Rauten- berg, 1969; Mugaas and Templeton, 1970; Dawson and Bennett, 1973) have failed to confirm such increases in insulation during cold acclimation or acclimatization and some studies (Irving, Krog, and Monson, 1955; Hart, 1957; Whittow, Sturkie, and Stein, 1966; Sturkie, 1967) have shown that alterations may occur in the direction of decreased insula— tion under-cold temperature regimes. The effects of extended exposure to cold on rates of evaporative water loss in birds have not been examined in sufficient detail to allow the drawing of conclusive state- ments at this time, even though adaptively decreased levels of evapora- tive heat loss could significantly enhance the maintenance of thermal balance in birds under cold conditions. Numerous studies have shown upward shifts in the basal metabolic rate in birds acclimated to cold ambient temperatures (Dontcheff and Kayser, 1934; Gelineo, 1934; Miller, 1939; Wallgren, 1954; Gelineo, 1955; Hart, 1957; Steen, 1957; Chaffee, gt_gl,, 1963; Gelineo, 1964; Hart, 1964; Harrison and Biellier, 1969; Rautenberg, 1969; Siegel, 1969; El Halawani, §t_gl,, 1970; Pohl, 1971; Pohl and West, 1973), although the thermoregulatory importance and desirability of such alterations has been questioned (King and Farner, 1961; Dawson and Hudson, 1970). The direct influence of the thyroid gland on these metabolic increases has been established (Miller, 1939; Williams, 1958; Dawson and Allen, 1960; Wilson and Farner, 1960). While changes in basal metabolic rates, indicative of increased meta- bolic levels during the coldest times of the year, have been demon- strated in some species (Dontcheff and Kayser, 1934; Kendeigh, 1934; Miller, 1939; Winchester, 1940; Davis, 1955; Saxena, 1957; Steen, 1958; 31 West, 1962; Irving, 1964; West, 1972b; Rising and Hudson, 1974), many investigations have failed to substantiate similar effects of cold acclimatization on either basal metabolism (Riddle, gt_gl,, 1934; Odum, 1943; Dawson, 1954; Wallgren, 1954; Irving, gt_al,, 1955; Rautenberg, 1957; Dawson, 1958; Hart, 1964; Veghte, 1964; Rising, 1969; Hissa and Palokangas, 1970; Mugaas and Templeton, 1970; Pohl, 1971; Delane and Hayward, 1975; Schwan and Williams, 1978) or thyroid activity (Wilson and Farner, 1960). However, temperature coefficients in some birds have been shown to substantially increase as a result of cold acclima- tion (Gelineo, 1955; Hart, 1957; Veghte, 1964), with the highest values usually recorded during the coldest times of the year (Hart, 1962; Lustick and Adams, 1977). Yet, opposite results have also been found in other avian species acclimated or acclimatized to cold thermal con- ditions (Dontcheff and Kayser, 1934; Riddle, §t_al,, 1934; Scholander, l., 1950b; Wallgren, 1954; King and Farner, 1964). This enhanced gt thermogenic capability does not appear to have a non-shivering basis (Hart, 1962; Chaffee, §t_al,, 1963; West, 1965; Rautenberg, 1969). Insulative and metabolic alterations may account for the downward shift in lower critical temperature demonstrated in cold acclimated and acclimatized birds (Scholander, §t_§l,, 1950a; Wallgren, 1954; Gelineo, 1955; Dawson, 1958; Gelineo, 1964; Hart, 1964; Irving, 1964; Veghte, 1964; West, 1972a). Yet, other investigations have found no such change (Irving, §t_gl,, 1955; Hart, 1957; Irving, 1960; Hart, 1962; Rautenberg, 1969) or have demonstrated a reversal in summer (Riddle, gt_pl,, 1934). Whether the underlying causes are related to insulative or metabolic alterations, it has been clearly established that cold tolerance in avian species is significantly increased following cold 32 thermal conditioning (Gelineo, 1955) and especially during the fall and winter months (Kendeigh, 1934, 1949; Seibert,_1949; Davis, 1955; Hart, 1962; Gelineo, 1964; Veghte and Herreid, 1965; Barnett, 1970; Kendeigh and Blem, 1974). However, there has been no indication that the lower lethal temperature of birds is reduced by residence in such cold thermal conditions (Dawson and Hudson, 1970). It should be emphasized that, when induced by cold acclimation or during natural acclimatization, these metabolic and insulative alterations in adult birds require at least one week of exposure to become detectable and approximately one month before the ultimate levels of adaptation are fully established (Gelineo, 1934, 1955) and probably as long in immature birds as well (Aulie, 1977). Acclimation and acclimatization to cold environmental temperatures has been shown to effectuate additional changes related to avian thermo- regulation. A significant increase in the weight of feathers has been noted in cold acclimated and acclimatized birds (Fisher, gt_gl., 1965; Berthold and Berthold, 1971) and in the fall plumage (Kendeigh, 1934; Wallgren, 1954; Irving, 1960; West, 1962; Hart, 1964; Barnett, 1970; Palokangas, Nuuja, and Koivusaari, 1975). Increases in body weight (Baldwin and Kendeigh, 1938; Nice, 1938; Kontogiannis, 1968; Blackmore, 1969; Cain, 1973; March and Sadlier, 1975; Dare, 1977) and in the thick- ness of the subcutaneous fat layer (Barnett, 1970) of birds exposed to cold thermal conditions have also been documented. These alterations may be related to the significant rise in feeding activity and food intake demonstrated in many avian species subjected to low environmental temperatures (Barott and Pringle, 1947, 1949; Seibert, 1949; Barott and Pringle, 1950; Davis, 1955; Steen, 1957; West, 1960; Hart, 1962; Prince, 33 .gp__l., 1965; Brooks, 1968; Kontogiannis, 1968; Kendeigh, gt_§l,, 1969; Rautenberg, 1969), although a U—shaped curve has been shown for neonate chicks (Kleiber and Dougherty, 1934) and Rautenberg (1957) found no difference in food consumption between adult summer and winter birds. Increases in the plasma lipid (Fisher, gt _l,, 1965; Freeman, 1967; Davison, 1973) and catecholamine (Lin and Sturkie, 1968) concentrations have been ascertained in some cold-acclimated birds. The significance of the later observation remains questionable however, since injection of these substances does not result in the substantial increases in metabolic rates noted in acclimated birds duringcold stress (Chaffee, gt p1,, 1963; Hart, 1964; Freeman, 1966; Wittke, 1967; Hissa and Palo- kangas, 1970). This may be related to the absence of non-shivering thermogenesis in adult birds (Freeman, 1967; Hissa and Palokangas, 1970) or suggests a hormonal stimulant different from that utilized by mammalian species (Smith and Horwitz, 1969). Although the effects of cold environments on avian thermoregulation have been studied in greater detail, some information is available which indicates that extended exposure to warm temperature conditions can influence the maintenance of thermal balance in birds during temperature stress. It is difficult at this time to draw specific conclusions con- cerning these effects however, since various and sometimes opposing results of exposing birds to warm thermal conditions have been found. Some birds have shown a decrease in insulation resulting from warm acclimation (Fisher, §t_al,, 1965; Greenwald, gt_al,, 1967) and during late spring or summer (Wetmore, 1936; Brooks, 1968). Moreover, birds from southern latitudes tend to have less insulation than their northern counterparts (Blem, 1974). Alterations in the characteristics and 34 motility of the plumage as well as vasomotor responses (Hillerman and Wilson, 1955) may contribute to this lowered insulation, but their relative inputs remain to be ascertained. Alternatively, no changes in insulative indices have been found in some birds under warm thermal conditions (Davis, 1955), while other avian species have shown increased insulation when exposed to high ambient temperatures (Irving, pt 91-: 1955) which could retard heat influx under these warm thermal regimes. Enhanced capacities for evaporative cooling have been demonstrated in many birds native or acclimated to warm environments (Hudson and Kimzey, 1966; Lasiewski, Acosta, and Bernstein, 1966; Calder and Schmidt- Nielsen, 1967; Rising, 1969) and during summer (Weiss and Borbely, 1957). The respiratory effort necessary to maintain thermal balance under heat stress has been shown to be lower in warm, as compared to cold, acclimated (Weiss, Frankel, and Hollands, 1963) and acclimatized birds (Hillerman and Wilson, 1955). Lowered rates of basal metabolism in warm acclimated and acclimatized birds have been repeatedly recorded (Dontcheff and Kayser, 1934; Winchester, 1940; Enger, 1957; Huston, Cotton, and Cameron, 1962; King and Farner, 1964; Hudson and Kimzey, 1966; Harrison and Biellier, 1969; Rising, 1969; Weathers, 1977), although some species apparently do not undergo such alterations (Wallgren, 1954; Rautenberg, 1957; Dawson, 1958). These lower metabolic levels may-have resulted from depressed thyroid activity associated with the removal of cold stimulation rather than as a direct result of ex- tended exposure to warm thermal conditions (Miller, 1939; Hoffman and Shaffner, 1950; Huston, Edwards, and Williams, 1962; Rising and Hudson, 1974). These decreases in the rate of basal metabolism require sus- tained exposure to warm environments, since similar results have not 35 been demonstrated in birds subjected to temperatures which fluctuate between the warm and cold range (Wallgren, 1954). However, repeated short exposures to warm thermal conditions have been shown to improve avian heat tolerance (Hillerman and Wilson, 1955). Moreover, warm acclimated and acclimatized birds have routinely exhibited enhanced tolerance of warm and hot temperatures (Hutchinson and Sykes, 1953; Hudson and Kimzey, 1966; Rising, 1969; Siegel, 1969) indicating their superiority in maintaining thermal balance under these extreme thermal conditions. Birds acclimated to warm temperatures develop hyperthermia more slowly (Weiss and Borbely, 1957; Siegel, 1969) and show lower rates of heat production (Weiss, 1959; Weiss, §t_al,, 1963), as well as have longer survival times during heat exposure (Weiss, 1959), when exposed to warm thermal conditions than non-conditioned subjects. Increases in the upper critical temperatures of warm acclimated and acclimatized birds have been demonstrated (Gelineo, 1934; Wallgren, 1954; Gelineo, 1955; Dawson, 1958; Greenwald, gt gig, 1967) which reflect alterations in insulative, evaporative, and/or metabolic responses. There has been no indication however that the upper lethal temperature of avian species is increased by extended exposure to warm or hot conditions since birds succumb to similarly high body temperatures at all times of the year (Weiss and Borbely, 1957). Changes in the insulative, evaporative, and metabolic responses of adult birds resulting from acclimation and accli- matization to warm thermal conditions become established over a time period of from one to f0ur weeks (Gelineo, 1955; Whittow, gt_gl., 1966; Harrison and Biellier, 1969). Alterations in other factors related to avian thermoregulation which result from extended exposure of birds to warm thermal conditions 36 have also been demonstrated. A number of studies have ascertained decreases in the body weights of warm acclimated birds (Fisher, pp 11., I965; Kontogiannis, 1968; Blackmore, 1969). The weights of feathers of birds reared under warm thermal conditions have been shown to be lighter than in cold-reared individuals (Fisher, gt_al,, 1965), while the summer plumage tends to be less dense than during the colder times of the year (Irving, 1960; Hart, 1964). Feeding activity and food intake appear to be reduced in many avian species subjected to warm environmental temper- atures (Wilson and Edwards, 1952; Cox, 1961; Prince, gt_gl,, 1965; Brooks, 1968; Rautenberg, 1969). Significant increases in the comb weights of warm-acclimated fowl have also been shown (Lamoreux, 1943). All of these changes undoubtedly enhance the capability of birds to maintain thermal balance during heat stress. Ontogeny gf_Temperature Regulation jg Birds There has been increasing interest in the past few years concerning the ontogeny of temperature regulation in birds. Although it has long been appreciated that birds hatch at different stages of overall relative development (Edwards, 1839; Pembrey, Gordon, and Warren, 1895) and that the variable thermoregulatory capabilities found in young chicks are closely related to these different developmental states (Leichtentritt, 1919; Baldwin and Kendeigh, 1932), it is only recently that a comprehensive understanding of the factors underlying avian thermoregulatory ontogeny has been achieved. King and Farner (1961) identified some of the events contributing to improved control over thermolysis and increased thermogenesis that occur during the develop— ment of a bird which could be potentially important in the attainment 37 of adult thermoregulatory capabilities. Even though relevant data has become available for some birds (g,g,, Dawson, gt_gl,, 1972; Bernstein, 1973), quantification of these parameters remains to be accomplished for most avian species. The responses of young birds to imposed thermal stress have been examined in some detail. The greater tolerance of extreme cold as well as warm temperatures in young birds as compared to older individuals and adults of the same species has been well established (Boni, 1942; Randall, 1943; Koskimies, 1950; Westerkov, 1956; Dawson, gt p1,, 1972). The ability to withstand severe thermal stress would appear to be adap- tive since young birds normally may be subjected to such temperature conditions when these animals are capable of little or no thermoregula— tory control (Baldwin and Kendeigh, 1932; Kendeigh, 1952). Decreases in thermal tolerance limits have been found during development in young birds, encompassing both increases in the lower lethal tempera- tures (Baldwin and Kendeigh, 1932; Randall, 1943) as well as decreases in the upper lethal temperatures (Moreng and Shaffner, 1951), so that older birds are able to survive only less dramatic changes in body temperature. A depression as well as restriction of the zone of thermo- neutrality has also been described (Palokangas and Hissa, 1971) which coincides with these developmental changes. However, the ability to maintain thermal balance has repeatedly been shown to improve with age in many birds (Baldwin and Kendeigh, 1932; Dawson and Evans, 1957, 1960; Ricklefs and Hainsworth, 1968a; Seel, 1969; Borchelt and Ringer, 1973; Neal, 1973; O'Connor, 1975; Dunn, 1976a). The rate of thermoregulatory ontogeny has been found to vary considerably among avian species, with precocial birds usually showing early attainment of complete temperature 38 control (Rolnik, 1948; Farner and Serventy, 1959; Caldwell, 1973), while slower rates of development have been described in altricial species (Baldwin and Kendeigh, 1932; Boni, 1942; Dawson and Evans, 1957, 1960; Dunn, 1975). Numerous studies have established that the body tempera- tures maintained in birds rise to within the normal adult range during development (Card, 1921; Randall, 1943; King, 1956; Dawson and Evans, 1957, 1960; Poczopko, 1967b; Morton and Carey, 1971; Gotie and Kroll, 1973; Austin and Ricklefs, 1977) concomitant with the overall improve— ment in temperature regulation capabilities. The ontogeny of avian thermoregulatory control reflects develop- mental changes related to both thermolysis and thermogenesis. Insula— tive indices measured in most avian species have indicated progressive improvement in the ability of the young bird to control heat gain and heat loss (Kendeigh, 1939; Dyer, 1968; Freeman, 1970a, b; Untergasser and Hayward, 1972; Bernstein, 1973; McNabb and McNabb, 1977). These insulative alterations have been linked to the growth and development of more effective plumage (Breitenbach and Baskett, 1967; Jehl, 1968; Morton and Carey, 1971), as well as to enhanced tissue insulation related to the increased thickness of subcutaneous fat layers (Brenner, 1964). Changes in ptilomotor responses have generally not been empha- sized in earlier studies perhaps because these mechanisms appear to be fully developed in many birds at or soon after hatching (Baldwin and Kendeigh, 1932), although more recent evidence suggests that such responses may be ontogenetically important in the thermoregulatory development of some species (Aulie and Moen, 1975). However, improved control over the arrangement of more highly-insulative feathers may be important in the attainment of adult thermoregulatory capabilities 39 (McFarland and Budgell, 1970). Peripheral vasomotor responses also appear to become fully mature at relatively early stages of development. Although such alterations have not been subjected to close scrutiny following an ontogenetic approach, changes in peripheral blood flow have been suggested in some studies (e,g,, Yarbrough, 1970; Bernstein, 1973) which, when coupled with purported adjustments in plumage, may contribute to the improved thermolytic control measured in developing birds. The overall growth of the young bird has been repeatedly sug- gested as being important in the ontogeny of avian thermoregulation since the ratio of thermolytic surface area to thermogenic body mass decreases with age in birds (Kendeigh and Baldwin, 1928; Freeman, 1965; Dunn, 1975), even though the relative input of such changes has been questioned (Wekstein and Zolman, 1971). Measurements of the rates of evaporation have indicated that cutaneous water loss decreases during avian development (Bernstein, 1971a). Although panting and gular flutter responses are present in young birds at hatching, control over respiratory evaporative cooling has been shown to improve during devel- opment in young birds (Bernstein, 1973), in some cases showing rapid rates of maturation (Dawson, gt_al,, 1972; Hudson, Dawson, and Hill, 1974). Developmental changes in thermogenic capabilities have been found in many young birds. The rate of basal metabolism has often been shown to increase with age in most species of birds (Riddle, Nussmann, and Benedict, 1932; Barott, Byerly, and Pringle, 1936; Kendeigh, 1939; Romijn, 1954; Beattie and Freeman, 1962; Freeman, 1964; Diehl and Myrcha, 1973; Hudson, gt_gl,, 1975) and may underlie the rise in body temperature level and overall improvement in thermoregulatory control 40 noted during avian development. However, the progressive increases in temperature coefficients which have been documented (Gelineo, 1954; Freeman, 1963; Dyer, 1968; Wekstein and Zolman, 1969; Freeman, 1970a, b) probably provide a better indication of the improving ability of the young chick to maintain thermal balance, especially during cold stress. Non-shivering thermogenesis has been suggested as the source of such enhanced heat production capabilities in some species (Freeman, 1966), although the validity of this conclusion has been questioned (Allen, Garg, and Marley, 1970; Calder and King, 1974). However, non-shivering thermogenesis probably does not persist throughout early avian develop- ment and is often subsequently replaced by muscular heat production (Odum, 1942). Most investigations have indicated that cold-induced increases in heat production result from enhanced muscular responses in the young bird, especially shivering activity, which generally im- proves with age (Kendeigh, 1939; Morton and Carey, 1971; Aulie, 1976; Dawson, Bennett, and Hudson, 1976). Basal metabolic rates, temperature coefficients, and levels of shivering activity have been found to decline in some birds later during development when the insulative capacities of the animal have improved (Odum, 1942; Barott and Pringle, 1946). Alternatively, other studies have shown no such remission in thermogenic levels coincident with plumage development (Kendeigh, 1939). Feather development itself may not be of critical importance however, since fairly effective thermoregulation has been found in some young birds before sufficient plumage insulation has become fully established (Ginglinger and Kayser, 1929; Baldwin and Kendeigh, 1932; Kendeigh, 1939; Dawson and Evans, 1957, 1960) and has been shown to develop, albeit more slowly, even in depilated chicks (Wekstein and Zolman, 1971) 41 Previous investigations concerning the ontogeny of avian thermo— regulation have generally emphasized the changing endothermic capabili- ties of the young chick (Dawson and Hudson, 1970), while comparatively little work has been done on the development of ectothermic responses in young birds. However, since the thermoregulatory capabilities of many avian species are relatively limited during early developmental stages, behavioral responses could assume critical importance in the maintenance of thermal balance in the young bird before the ontogeny of endothermic regulation of body temperature has been completed. Young altricial birds would appear to be particularly susceptible to imposed thermal stress due to their comparatively slow rates of overall and thermoregulatory development coupled with their relative helpless- ness during the early stages of the nesting period (Nice, 1943; Dawson and Evans, 1957, 1960). Although altricial young have been shown to be quite tolerant of extreme temperature conditions (Boni, 1942; Westerkov, 1956), equable thermal conditions have been found to be most conducive to optimal rates of chick development and fledging success (Stoner, 1935; Baumgartner, 1938; Banks, 1959; Whittow, 1965b). Since these young birds are incapable of extensive behavioral control of body temperature at early stages of development, the activities of their parents could assume an important role in the maintenance of ther- mal balance in altricial nestlings. The significance of parental behavior in assisting thermoregulation of their young offspring has been repeatedly demonstrated (Hafez, 1964). Responses such as shelter— ing and shading of young nestlings by the parents have been described (Bartholomew and Dawson, 1953; Spellerberg, 1969; Morton and Carey, 1971; LeCroy and Collins, 1972) which reduce heat flux to the young 42 from hot thermal environments, particularly where the incidence of solar radiation is intense. Parental brooding of young birds and modifications of nest location and construction have also been docu- mented in environments where the nestlings are exposed to adverse thermal conditions (Baldwin and Kendeigh, 1932; Irving and Krog, 1956; Ricklefs and Hainsworth, 1968b; Bateman and Balda, 1973; Gotie and Kroll, 1973). A rather elaborate developmental sequence has been described with respect to the close relationship between parental at- tentiveness towards nestlings and stages of thermoregulatory ontogeny in young altricial birds (Kendeigh, 1952; Howell and Dawson, 1959; King and Farner, 1961; Austin and Ricklefs, 1977) indicating the rela- tively high level of parental input early in development which later subsides as the young become more thermally independent of the parents. Concomitant with the ontogeny of avian endothermic control, the behav— ioral capabilities of the nestlings have also been shown to improve during development so that ectothermic activities of the young birds begin to assume a role in their thermoregulation at later stages of the nesting period. Responses such as seeking and utilizing protected areas outside the confines of the nest and huddling with siblings have been described in older altricial nestlings, which represent important contributions to temperature regulation in these animals under adverse thermal conditions (Koskimies, 1950; Lohrl, 1955; Howell, 1959; Howell and Bartholomew, 1961b; Howell, 1964; Morton and Carey, 1971; LeCroy and Collins, 1972). Although precocial avian species have been found to attain endo- thermic control of body temperature relatively earlier in life than their altricial counterparts (King and Farner, 1961), including some 43 suggestions that this developmental process may actually begin prior to hatching (Romanoff, 1941; Bartholomew and Dawson, 1952; Aulie and Moen, 1975), these young birds are still liable to thermal stress during the early portions of life before their endothermic ontogeny has been completed. The problems of maintaining thermal balance in precocial young may be even more intense since the behavior of the parents appears to play a less significant thermoregulatory role than has been found in altricial species (Kendeigh, 1952; Boggs, Norris, and Steen, 1977). Investigations into the ontogeny of avian tempera- ture regulation in precocial species have suggested that ectothermic responses contribute to thermoregulation during development. Huddling behavior has been shown in young precocial chicks subjected to cold environmental conditions (Kleiber and Winchester, 1933). Movement of these young animals to more favorable microclimates has also been docu- mented (Bartholomew and Dawson, 1954b; Howell, 1959; Dunn, 1976b). Utilization of water for drinking and bathing has been described in young birds exposed to severe heat loads (Bartholomew, et_gl., 1953). Laboratory studies of the ectothermic responses of young precocial species have indicated that newly-hatched chicks tend to locate them- selves at warmer positions in a thermal gradient chamber than do older individuals (Poczopko, 1967a; Ogilvie, 1970). These responses have been assumed to contribute to the maintenance of thermal balance in these young birds during the early stages of development when their endothermic capabilities have been shown to be ineffective (Wekstein and Zolman, 1967, 1969). Moreover, ectothermic activities appear to persist in mature birds even after endothermic control has been fully established (Hafez, 1964; Budgell, 1971). 44 Investigations into the ontogeny of avian temperature regulation have virtually ignored the effects of acclimation and acclimatization as being potential factors in the thermoregulatory development of birds. This would appear to be an important oversight since many studies have shown significant effects of environmental thermal conditions on a number of thermoregulatory parameters in adult birds, particularly their endothermic responses (Hart, 1957; Chaffee and Roberts, 1971). Since the ontogeny of body temperature control in young birds is closely related to the development of endothermic capabilities (Kendeigh, 1939; Dawson and Evans, 1957, 1960; Freeman, 1964, 1970a; Wekstein and Zolman, 1971), it would seem likely that thermal conditions prevalent during the early life of a bird could directly influence the rate of avian thermoregulatory development. Moreover, if prior thermal conditions would indeed affect endothermic ontogeny, one might expect to find compensatory modifications in the ectothermic responses of young birds maintained under different thermal environments during their early development. Although some earlier studies have indicated that thermoregulatory development was either retarded (Ryser and Morrison, 1954) or apparently not influenced (Aulie and Steen, 1976) in young birds previously exposed to cold thermal conditions, most investigations concerning the ontogeny of avian temperature regulation have to date not directly examined the effects of prior thermal exposure on the rate of thermoregulatory development in young birds. The studies of either Koskimies and Lahti (1964) or Dawson and Evans (1957, 1960) characterize the attention that has been placed on the effects of temperature conditions during develop- ment on the ontogeny of thermoregulation in young birds. Koskimies and 45 Lahti (1964) examined the body temperature control capabilities in various species of widely-distributed ducks and found that the rates of thermoregulatory ontogeny in the ducklings were inversely related to the temperature conditions prevailing during development. Northern species attained complete body temperature control earlier than resi- dents of the warmer southern environments, but the contributions ascribable to species differences could not be differentiated from the effects of diverse temperature conditions. Dawson and Evans (1957, 1960) studied the development of temperature regulation in sparrows and found species differences in the rates of thermoregulatory ontogeny which were primarily related to variations in endothermic development. Prior thermal conditions were evidently not significant influencing factors underlying these endothermic differences however, since the species examined in these two investigations were both residents of the same geographic area with apparently equivalent prevailing temperatures. The results of these and other similar investigations in this area have demonstrated species differences in the rate of avian endothermic development. Yet there has been no clear determination of the specific effects of environmental thermal conditions during development on the ontogeny of endothermy in any one species of bird. Moreover, studies on the influence of prior temperature conditions on the development of avian ectothermic responses have been conspicuously absent, although there has been some suggestive evidence along this line. For example, a positive correlation has been found between the length of the nestling period and the prevailing ambient temperature, such that cold-exposed species apparently fledge earlier than those naturally reared under 46 warmer environmental conditions (Maher, 1964). These differences may be due to the earlier maturation of behavioral capabilities coincident with the faster rates of overall development in the young cold-exposed birds. Since relatively effective thermoregulatory control has been attained by these young birds at, or even before, the time of fledging, which may have resulted from these thermal influences on endothermic ontogeny, such differences would also suggest possible concomitant temperature effects on the development of behavioral thermoregulation in these animals. Whether such ectothermic variations are due to prior temperature conditions or are only reflective of species differences in overall behavioral development rates remains to be established. It should be apparent from the previous discussion that the rela- tionship between thermal rearing conditions and the development of avian temperature regulation has not been satisfactorily investigated to date. Therefore, the purpose of the present study was to determine the effects of acclimation temperature on the ontogeny of thermoregu- lation in the young chick (Gallus domesticus). Since temperature regulation involves both endothermic and ectothermic components, this problem was approached from somewhat different but nevertheless closely related viewpoints that were integrated into two series of experiments. In the first experimental series, groups of chicks were raised either under different specified thermal rearing conditions, or under specifically varied thermal rearing conditions, during early development and tested for their endothermic Capabilities. The hypothesis proposed in this series of experiments was that acclimation temperature during early development has a significant effect on the ontogeny of endothermy in the young chick. In the second experimental series, groups of chicks 47 were raised under different specified thermal rearing conditions during early development and tested for their ectothermic responses. The hypothesis proposed in this series of experiments was that acclimation temperature during early development has a significant effect on the behavioral regulation of body temperature in the young chick. These experiments were therefore designed to generate data that would permit specification of the relationship between acclimation temperature during early development and the ontogeny of thermoregulation in the young chick. GENERAL METHODS AND MATERIALS Animals The animals utilized as experimental subjects in this investiga- tion were young White Leghorn chicks (Gallus domesticus) from 1 to 12 days of age. The fertile eggs from which these chicks hatched were obtained from a commercial hatchery (Richard Hutting, Lansing, Michi- gan), whose flock of approximately 230 birds was comprised of about 200 laying hens and 28 cocks. Although the eggs were delivered to the lab within 24 hours after being laid, the batches that were supplied were composed of eggs which had been produced during the entire pre- vious day, so that the age variation of the embryos in the eggs, upon receipt, was a maximum of 24 hours. Prior to incubation, the eggs were refrigerated at 5°C for 48 hours, in order to achieve some reduc— tion in this variability of the ages of the embryos (Gottlieb, 1963). Incubation The incubation time required for hatching of these embryos was 21 days. The fertile eggs, in batches of 13 to 14 dozen, were incubated in a Jamesway single stage forced-draft incubator (Model 252B: James Mfg. Co.) for the first 20 days of development. During this time, the temperature in this incubator was maintained at 37.3 i O.2°C with the relative humidity between 85—90%, and the eggs were automatically turned every 6 hours. On day 20 of incubation, the eggs were 48 49 transferred to a smaller forced-draft incubator (Model 228.735; Sears, Roebuck, & Co.) where the chicks were allowed to hatch. The tempera- ture in this smaller incubator was maintained at 37.1 i 0.1°C with the relative humidity between 80-85%. This incubation procedure proved to be very successful and resulted in hatchability indices (j,g,, number of chicks hatched/number of fertile eggs incubated) of between 80-95%. The range of hatching times of these chicks was a maximum of 16 hours, with the majority of hatches occurring during the early morning of Day 0 (day of hatch). Maintenance At the end of Day 0, between 1600-1700 (1200 equals 12:00 noon), the newly-hatched chicks were removed from the smaller incubator and transferred to a 90 x 60 x 28 cm electric box brooder (Model No. 6401; Brower Mfg. Co.) where they remained overnight. External heat was provided by an electric bar heater located at one end of this communal brooder, where the ambient temperature was maintained at 35 i O.5°C. Most of the chicks stayed in this heated portion of the brooder during this time. Food (Purina Chick Startena ZO-V Medicated; Ralston Purina Co.) and water were available gg_lip,, even though the young animals of this age did little feeding or drinking. On the morning of Day 1 (between 0800-0900), the chicks were exam- ined, marked, and arbitrarily divided into the prescribed acclimation groups. Any chicks found upon inspection to have any obvious physical deficiencies (g,g,, unable to stand or walk) or defects in plumage were discarded. The remaining animals were then randomly divided into smal- ler groups of approximately equal number. The number of acclimation 50 groups (either two or three) was determined by the particular experi- mental series being conducted at that time. Next, each group of chicks was randomly assigned to one of the experimental treatment (j,g,, thermal acclimation) groups. The animals within any one experimental group were then marked either for individual identification by numbered wing bands (Zip Wing Bands, #895; National Band and Tag Co.) or for group identification by a small color patch placed on the head with a felt-tip marking pen. Finally, the groups of chicks were transferred to their respective communal rearing brooders. For the remainder of the time period under investigation, the chicks were reared in these communal brooders until used in an experi- ment. Each brooder was checked at least twice daily, during which time the 2g.11g, food and water supplies were replenished and dead chicks, if any, were removed. A 14L:IOD photoperiod (lights on at 0700) was maintained at all times in the rearing rooms. EXPERIMENTAL SERIES I The purpose of the first series of experiments was to determine the effects of acclimation temperature on the development of endothermic regulation of body temperature in the young chick. Groups of animals were raised either under different specified thermal rearing conditions, or under specifically varied thermal rearing conditions, during early development. These chicks were tested for their endothermic capabili- ties at various exposure temperatures for certain periods of time at various ages. Several pre-trial temperature conditioning procedures were used to further ascertain the thermal acclimation effects on the endothermic capabilities of these animals. The hypothesis tested in this experimental series was that acclimation temperature during early development has a significant effect on the ontogeny of endothermy in the young chick. Experimental Groups Five experimental groups were used in this series of investigations. Each group of chicks was reared in one of three separate but identical communal brooders under the same conditions of rations and photoperiod as previously described. The different thermal acclimation conditions were obtained by placing each brooder in one of two different rearing rooms in which the ambient temperature was varied. Two of the brooders were located in the cold acclimation rearing room in which the ambient 51 52 temperature was maintained at 20 i O.5°C from Day 1 through Day 12 (j,g,, the experimental period) of the chicks' early development. The two brooders in the cold acclimation rearing room housed Experimental Groups C and C/W. Since the brooder in which they were housed did not provide any external source of heat, the Group C chicks were reared under cold acclimation temperatures throughout the experimental period. The other brooder, which housed Group C/W, was outfitted with an elec— tric bar heater which maintained an ambient temperature level of 35 i O.5°C at one end of the brooder. The ambient temperature at the oppo- site end of this brooder was the same as that of the cold acclimation rearing room (20 i O.5°C). This arrangement provided a range of thermal conditions in the brooder such that the Group C/W chicks could locate themselves at any ambient temperature between 20-35°C during the experimental period. The third brooder, which housed Group W, was located in the warm acclimation rearing room, in which the ambient temperature was always maintained at 35 i O.5°C. The chicks in Group W were therefore reared under warm thermal acclimation conditions throughout the experimental period. Group C+W chicks were raised at 20 i O.5°C from Day 1 through Day 4 in the cold acclimation rearing brooder. Group W+C chicks were raised at 35 i O.5°C from Day 1 through Day 4 in the warm acclimation rearing brooder. 0n the morning of Day 5 (j,g,, between 0800-0900), C+W chicks were transferred to the warm acclimation rearing brooder and W+C chicks were transferred to the cold acclimation rearing brooder, where each group was respectively housed for the remainder of the acclimation period. The chicks in Group C+W were therefore reared under cold accli- mation conditions on the initial days, and under warm acclimation 53 conditions during the subsequent days, of their early development. The chicks in Group W+C were therefore reared under warm acclimation condi- tions for the first few days, and under cold acclimation conditions during the subsequent days, of their early development. The initial size of the acclimation groups was between 40-50 chicks per brooder. This number decreased over time as the animals were used only once in an experiment and then discarded. There was no differen- tial mortality between any of the five experimental groups reared under the different thermal acclimation paradigms. Apparatus A retaining apparatus was made in which the chicks were placed during the cold exposure trials. The outside of the apparatus was built from a wood and metal frame (46 x 46 x 23 cm), on the floor and sides of which pieces of 0.64 cm mesh chicken wire were fastened. Four 0.64 cm thick flat black fiber boards, 46 x 30 cm, with ten 0.64 cm holes per board, were used to construct an insert. These boards were cut in such a way that they fit together into two pair of interlocking slats, with each pair being at right angles to the other pair in a crisscrossed pattern. This insert, when placed inside the wired frame, subdivided this retaining apparatus into nine smaller compartments, each approxi- mately 15 x 15 cm. However, only the eight outer compartments were used to retain the chicks during the cold exposure trials, with one animal per compartment. The floor of the retaining apparatus was covered with newspaper which was replaced after every trial. The compartments per- mitted the chicks limited movement, yet provided enough space for them to assume any posture, from standing to laying, during the cold exposure 54 trials. Air movement in the compartments was provided for by the holes in the insert boards and the wire sides. This retaining apparatus was located on a lab table in the lighted cold exposure testing room, where the ambient temperature could be maintained to within i 1.0°C of the desired thermal level between 10-18°C. The body temperatures recorded in this investigation were all measured on a YSI Tele-Thermometer (Model 43TG) using a YSI Thermistor Temperature Probe (No. 423X), both manufactured by Yellow Springs Instrument Co., and were obtained in the following manner. The chick was picked up and held during the measurement. The probe was gently inserted into the animal's mouth and guided down the esophagus until the probe tip, which contained the thermistor, was at the level of the proventriculus. While the probe was held in this position, the tele- thermometer was then turned on and the meter was observed until the needle indicator had reached equilibrium (j,g,, did not move any more), at which time a reading was taken to the nearest 0.1°C and recorded. This particular probe had a time constant (j,§,, the time required for the probe to read 63% of a newly impressed temperature) of 1.4 seconds and since approximately five time constants were necessary for the probe to register 99% of the total temperature change, at least 7 seconds were required for the indicated reading to be at the actual temperature level. However, to insure the accuracy of the measurement, the probe was held in place for a minimum of 15 seconds before the' reading was taken. Thus, the total time required for taking one body temperature measurement, from the time the chick was initially picked up until the time it was returned to the compartment of the retaining apparatus, was no more than 25 seconds. As a means of providing a 55 reasonably good measure of the deep body, or "core", temperature of the chick, this procedure was maximally efficient in terms of accuracy of reading, consistency of probe placement, and speed of measurement, while causing minimal disturbance to the animal. Testing Procedures and Measurements The following procedures were utilized to test the chicks under exposure to cold temperatures. One to three trials were conducted between 1200 and 1500 on each testing day, in groups of eight animals per trial. The groups tested were composed of either two to three chicks randomly chosen from each of the C, C/W, and W acclimation groups or three to four chicks randomly selected from each of the C+W and W+C acclimation groups. The animals were removed from their respective rearing brooders and transferred in a cardboard box to the room outside the cold exposure testing room. The chicks were then randomly taken, one at a time, from the box and placed in the compartments of the re- taining apparatus at 30-second intervals. The compartments were arbitrarily numbered from 1 to 8 consecutively and the chicks were placed in the compartments following this sequential order (i,g,, the first animal was placed in compartment 1, the second animal in compart- ment 2, and so forth) until all animals in the trial group had been placed in the retaining apparatus. The body temperature was measured just prior to when each animal was placed in its respective compartment; this body temperature was designated as the initial body temperature (T0) at the start of the cold exposure trial. The body temperatures of the chicks were then measured again, at 30-second intervals, at specified times (as indicated by a stop-watch) in the same sequential 56 order in which the animals were initially placed in their respective compartments. The exposure times at which the body temperatures were measured were 5, 10, 15, 20, and 30 minutes and every 15 minutes there- after until the end of the trial. During these measurements on the animals from the C, C/W, and W acclimation groups, the legs and beak of the chick were felt by hand to determine the relative temperature of these structures to provide an indication of the presence or absence of peripheral vasoconstriction in these areas. The presence or absence of muscle tremors detectable while holding the animal for body tempera- ture measurement was also noted. Between the body temperature measure- ments, the posture of each chick in its respective compartment was recorded, as well as indications of locomotor activity, vocalization, and visible presence or absence of ptiloerection and shivering. Between the blocks of body temperature measurements, the retaining apparatus was rotated to insure equivalency of cold exposure of all the compartments. At the end of the trial, the chicks were weighed, to the nearest 0.1 gm, and the identification number or group color marking of each individual was recorded. The animals were then sacrificed and discarded, since each chick was used in only one trial. A diagram of the experimental manipulations and testing procedures used in this first series of experiments is presented in Figure 2. The standard cold exposure trial was a 60 minute test at 10 i 1.0°C. These trials were conducted at all ages from Day 1 through Day 12 on a total of 216, 208, and 234 chicks, respectively, from the C, C/W, and W accli- mation groups. Standard cold exposure trials were also conducted from Day 6 through Day 9 on a total of 40 chicks from both the C+W and the W+C acclimation groups. 57 ov viz .H meme Hmucmswcwaxm :H com: mmczumooca mchmwp wee meowomHschwE Hmpcwswcwaxm .N wczmHe oe oHuoHuwm”mmnwm ooHuvmnwm o :NTHV ANT: 0 m H NHIH :+ + :+ N H m m m m m m N H m m m 3‘ fl 2* o o o H z o H z o o o 3 3\u u H z oHuoHnNmnNmuNm V NNHm mgazHHHH> 0.05) in the C acclimation group, but was 82 Table 9. Analysis of Variance of Chick Body Temperatures (°C) at Start of 60 Minute Exposure to 10°C. Source DF MS 'F P Age 3 1.12 37.33 <<0.001 Acclimation Temperature 3 0.08 2.67 <0.05 Age x Acclimation Temperature 9 0.06 2.00 <0.05 Within 235 0.03 Total 250 Table 10. Duncan's Test on Mean Chick Body Temperatures (°C) at Start of 60 Minute Exposure to 10°C. Acclimation Group Agg_(days) C+W W+C C W 6 41.55 41.52 41.52 41.47 (0.07) (0.05) (0.04) (0.05) 7 41.62 41.61 41.63 41.59 (0.05) (0.05) (0.04) (0.03) 8 41.65 41.67 41.82 41.82 (0.04) (0.03) (0.03) (0.04) 9 41.66 41.75 41.87 41.83 (0.06) (0.04) (0.04) (0.03) Means subtended by the same line ( ) = 1 Standard error. do not differ at p = 0.05. 83 Table 11. Analysis of Variance of Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 10°C. Source DF MS ' F P Age 3 22.61 35.33 <<0.001 Acclimation Temperature 3 72.26 112.91 <<0.001 Age x Acclimation Temperature 9 2.63 4.11 <0.001 Within 235 0.64 Total 250 Table 12. Duncan's Test on Mean Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 10°C. Acclimation Group Agg_(days) C C+W W+C W 6 -1.04 -0.81 -2.38 -2.92 (0.17) (0.24) (0.30) (0.22) 7 -O.45. -O.14 -O.10 -3.03 (0.13) (0.05) (0.08) (0.25) 8 -O.18 -0.10 -O.23 -1.98 (0.05) (0.03) (0.06) (0.22) 9 0.002 -0.04 -O.35 -1.42 (0:06) (0.08) (0.09) (0.19) Means subtended by the same line do not differ at p = 0.05. ( ) = 1 Standard error. 84 Table 13. Analysis of Variance of Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 18°C (First Alternative Trial Procedure). Source DF MS F P Acclimation Temperature 1 7.04 352.00 <<0.001 Within 18 0.02 Total 19 Table 14. Mean Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 18°C (First Alternative Trial Procedure). Acclimation Group Mean Rate of C W Change of Chick Body Temperature 0.02 -1.16 (Standard error) (0.02) (0.06) 85 significantly different from zero in the W acclimation group (t= -20.59, df= 8, p << 0.001) as indicated in Table 14. Two-way analysis of variance procedures, using the parameters of trial procedure (standard or first alternative) and acclimation temper- ature (C or W) as the main effects variables, were used to further ascertain the effects of acclimation temperature on chick endothermic performance as tested under two different exposure temperatures. There were no significant differences either in body weights or T0 values between the standard and first alternative trial procedures or between the C and the W acclimation groups.- Body temperature slopes were signi- ficantly lower in the first alternative trial procedure (18°C exposure temperature) and in the C acclimation groups (Tables 15 and 16). The second alternative trial procedure involved the use of chicks, all six days of age, from both the C and the W acclimation groups in 180 minute cold exposure trials at 10 : 1.0°C. One-way analysis of variance procedures were utilized to examine the effects of acclimation temperature on chick endothermic performance using these longer exposure timgg, There was no significant difference between these two acclima- tion groups either in body weights or T0 values. However, body temper- atures measured in chicks from the C acclimation group were signifi- cantly higher after one hour (Tables 17 and 18) and after three hours (Tables 19 and 20) of cold exposure. Body temperature slopes during the first hour of cold exposure were significantly greater in the W acclimation group (Tables 21 and 22). The average body temperature slope was not significantly different from zero in the C acclimation group (t= -1.64, df= 8, p > 0.05), but was significantly different from zero in the W acclimation group (t= -7.85, df= 8, p << 0.001) as 86 Table 15. Analysis of Variance of Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 10°C (Standard Trials) and to 18°C (First Alternative Trial Procedure). Source DF MS F P Trial Procedure 1 26.83 41.28 <<0.001 Acclimation Temperature 1 42.75 65.77 <<0.001 Trial Procedure x Acclimation Temperature 1 - 1.66 2.55 NS Within 58 0.65 Total 61 Table 16. Mean Rates of Change of Chick Body Temperature (°C) during 60 Minute Exposure to 10°C (Standard Trials) and to 18°C (First Alternative Trial Procedure). Acclimation Group C Trial Means 10°C Exposure Temperature -1.04 (0.17) -2.92 (0.22) -1.98 (0.29) 18°C 0.02 (0.02) -1.16 (0.06) -0.57 (0.05) Group Means -0.69 (0.15) -2.36 (0.22) ( ) = 1 Standard error. 87 Table 17. Analysis of Variance of Chick Body Temperatures (°C) after One Hour of 180 Minute Exposure to 10 C (Second Alternative Trial Procedure). ' Source DF MS F P Acclimation Temperature 1 21.22 31.20 <<0.001 Within 18 0.68 Total 19 Table 18. Mean Chick Body Temperatures (°C) after One Hour of 180 Minute Exposure to 10°C (Second Alternative Trial Procedure). Acclimation Group C W Mean Body Temperature 41.15 39.09 (Standard error) (0.16) (0.33) 88 Table 19. Analysis of Variance of Chick Body Temperatures (°C) at End of 180 Minute Exposure to 10°C (Second Alternative Trial Procedure). Source DF MS F P Acclimation Temperature 1 80.80 10.15 <0.005 Within 18 7.96 Total 19 Table 20. Mean Chick Body Temperatures (°C) at End of 180 Minute Exposure to 10°C (Second Alternative Trial Procedure). Acclimation Group C W Mean Body Temperature 41.01 36.99 (Standard error) (0.21) (1.24) 89 Table 21. Analysis of Variance of Rates of Change of Chick Body, Temperature (°C) during First Hour of 180 Minute Exposure to 10°C (Second Alternative Trial Procedure). Source DF MS F P Acclimation Temperature 1 23.25 38.75 <<0.001 Within 18 0.60 Total 19 Table 22. Mean Rates of Change of Chick Body Temperature (°C) during First Hour of 180 Minute Exposure to 10°C (Second Alternative Trial Procedure). Acclimation Group Mean Rate of C W Change of Chick Body Temperature -0.26 -2.42 (Standard error) (0.16) (0.31) 90 indicated in Table 22. Discussion The results of Experimental Series I support the hypothesis that acclimation temperature during early development has a significant effect on the ontogeny of endothermy in the young chick. Continuous acclimation to cold thermal conditions clearly resulted in the fastest development of chick endothermic capabilities, while continuous accli- mation to warm thermal conditions resulted in the slowest rates of endothermic ontogeny in these animals (Table 7). Chicks that were able to determine their own acclimation temperature at or between these levels of cold and warm thermal conditions showed rates of endothermic development intermediate to those evident in the continuous cold and continuous warm thermally-acclimated chicks. Similar changes in both measures of endothermic performance (Tables 5 and 7) with inoreased age of chicks have been reported in numerous prior investigations (g,g,, Wekstein and Zolman, 1967, 1969, 1971), but never as a function of acclimation temperature. These findings contrast results from an earlier study (Ryser and Morrison, 1954) which showed that exposure of young ducks to cold thermal conditions retarded their thermoregulatory development. Cold thermal acclimation did not differentially influence the endothermic performances of these chicks at the end of early devel- opment (i,g,, Day 12) when all animals demonstrated effective thermo- regulatory capabilities (Tables 5 and 7). These results support the study by Aulie and Steen (1976) which showed that cold thermal accli- mation during the same stage of development had no effect on chick thermoregulatory performance. 91 Within the confines of the time and cold exposure parameters used in the present investigation, these different thermal acclimation para- digms neither prevented the development of endothermy, nor resulted in disparities between final levels of thermoregulatory capability attained, in these young chicks, but rather influenced the rates at which such functional capabilities were achieved by these animals. Comparisons of the measured T60 values (Table 5) and body temperature slopes (Table 7) with the normative age-specific values of comparable body temperature measurements in this study indicate that these chicks attained, on the average, effective thermoregulatory capabilities as operationally de- fined on Day 8 in the C acclimation group (Day 8 normal range = 41.81 i 0.18°C), Day 10 in the C/W acclimation group (Day 10 normal range = 42.01 H- 0.17°C), and Day 12 in the W acclimation group (Day 12 normal range 42.06 i 0.14°C). From Day 4 through Day 11, chicks which had experienced either continuous or intermittent cold thermal acclimation demonstrated superior endothermic performances than continuous warm thermally-acclimated animals (Table 7). These results demonstrate that cold acclimation enhanced endothermic performance even pgfgpg_effective endothermic capabilities had been attained in these chicks, again indi- cating that cold thermal acclimation affected rates of endothermic onto- geny. These results also show that cold thermal acclimation stimulated the endothermic responses in these young chicks within a much shorter time period (j,g,, approximately three days) than is apparently required to demonstrate comparable thermoregulatory effects in either adult birds (Gelineo, 1955; Siegel, 1969) or juvenile chicks (Aulie, 1977). Since thermolysis would be the same in chicks of the same body weight and body temperature, the hypothesis that differences in 92 endothermic performances between these groups of chicks (Tables 5 and 7) resulted from their diverse thermal acclimation conditions is further supported by the absence of between-groups differences in body weights (Table 1) and T0 values (Table 2) in these animals. The differences in endothermic performances between these groups of chicks also cannot be explained by variations in pre-trial temperature conditions (Tables 4 and 6). These results clearly demonstrate that the effects of'lggg; tgpm_thermal acclimation to both cold and warm temperatures predominate over the influences of short-term thermal exposure (i,g,, pretrial temperature conditioning) relative to their impact on the endothermic performances of chicks during the course of thermoregulatory ontogeny. Acclimation temperature therefore clearly had a significant effect on the endothermic performances of these chicks as assayed by the standard trials using one-hour exposures to 10 i 1.0°C. The question of whether similar results would also have been found using longer cold exposure trials will be addressed later in this discussion. The finding in this study of increased body temperatures in these chicks with increased age (Tables 2 and 3) was similar to results re- ported in many previous investigations (g,g,, Card, 1921; Randall, I943; Romijn, 1954; King, 1956; Dawson and Evans, 1957, 1960; Poczopko, 1967b; Morton and Carey, 1971; Gotie and Kroll, 1973; Austin and Ricklefs, 1977). Yet, the various thermal acclimation paradigms did not dif- ferentially influence these measured body temperature values between the three acclimation groups (Table 2). The thermal acclimation condi- tions employed in this study therefore did not alter either the norma- tive age-specific level of, or developmental rise in, the body tempera- ture "set point" in these young birds. There were no differences in 93 body temperature values between those measured in chicks at the start of the cold exposure trials (T0) and those measured at comparable times in the same animals housed in their respective thermal acclimation rear- ing brooders (age—specific determinations) as shown in Table 8. More- over, the three pretrial temperature conditioning procedures used in this study did not differentially influence T0 values (Table 2). Body temperature values in these young chicks therefore remained remarkably consistent over these varying conditions of measurement. In addition, the handling and transportation of these chicks associated with the conduct of the cold exposure trials did not result in aberant T0 values in relation to age-specific body temperatures. Chicks of all ages in each acclimation group consistently maintained their characteristic body temperatures when collectively housed in their respective rearing brooders. The question of whether individual chicks, especially in the C acclimation group, could also maintain normal body temperatures under these thermal rearing conditions will be addressed later in this discussion. Activities related to thermoregulation in these young chicks ob— served during this series of experiments were similar to those indicated in previous investigations, although there were some notable differen- ces, additions, and exceptions. The detected use of regional peripheral vasoconstriction in these young birds during cold exposure has been previously reported (Yarbrough, 1970; Bernstein, 1973). In the present study however, regional peripheral vasomotor responses apparently did not change concomitantly with endothermic ontogeny in relation to poorly insulated body surfaces (i,g,, legs and beaks of chicks) nor were they differentially affected by variations in acclimation temperature. These 94 results suggest that regional peripheral vasoconstriction under these body surface areas did not significantly influence endothermic ontogeny in these young chicks and that the differences in endothermic perfor- mances found between acclimation groups cannot be explained by differ- ences in vasomotor activity. Feather—covered body surface temperatures apparently were warmer in these chicks with increased age, which sug- gests that developmental modifications of regional peripheral vasomotor tonus under these surfaces accompanied endothermic ontogeny in these chicks. Feather-covered body surface temperatures were influenced by acclimation temperature, being warmest to coldest in the C, C/W, and W acclimation groups respectively, suggesting a developmental impact like that just described. Yet warmer body surface temperatures either with increased age or as influenced by thermal acclimation conditions would likely have resulted in increased thermolysis and therefore tended to impair thermoregulatory performance, rather than result in the observed improvement noted in all acclimation groups, especially the C and C/W group chicks, unless there were commensurate increases in insulation afforded by feathers or subcutaneous fat deposits. Assuming that insulative indices were the same in all three acclimation groups, these results indicate that chicks in the C/W and particularly the C acclima- tion groups produced sufficiently greater amounts of metabolic heat to compensate for their increased thermolysis during the cold exposure trials, since these chicks demonstrated superior endothermic perfor- mances than W group animals which presumably experienced lower rates of thermolysis. However, these increases in body surface temperatures cannot by themselves be distinguished from possible increased overall levels of thermogenesis just mentioned. Further quantitative studies 95 which would specify the levels of peripheral vasomotor activity and other thermolytic responses as well as the rates of thermogenesis are therefore suggested to resolve these questions. Muscle tremors detected in these chicks during the cold exposure trials were similar to those indicated in previous studies and also showed characteristic intensity decreases with increased age of the animals consistent with earlier reports (Kendeigh, 1939; Odum, 1942; Morton and Carey, 1971). Improvements in thermoregulation and the attainment of effective endothermic capabilities shown in these chicks were therefore accomplished without obvious utilization of muscular thermogenesis and suggests the importance of non-shivering thermogenesis during endothermic ontogeny as previously demonstrated (Freeman, 1966) in these animals. The lack of variation in these responses between the experimental groups implies that acclimation temperature had no effect on the intensity of muscle tremors in these chicks and could therefore not explain the observed differences in endothermic performance between the three acclimation groups. These few results however suggest that further quantitative studies be conducted on the relationship between acclimation temperature and muscle tremors in developing young chicks. The postures of chicks observed during the cold exposure trials in this investigation were similar to those described in earlier studies (g,g,, Hutchinson, 1952a; Hafez, 1964; Baldwin and Ingram, 1968). Previous reports (g,g,, Deighton and Hutchinson, 1940; Goldsmith and Sladen, 1961; Alder, 1963; Veghte and Herreid, 1965; Jones and Johansen, 1972) have indicated that differential heat losses occur in birds rela- tive to differences in assumed postures. The observed variations in postures adopted by these young chicks, and changes in postural 96 deployment with increased age consistent in all three acclimation groups, could therefore have evoked potential thermoregulatory effects on these animals. Assuming the results from these previous investiga- tions can be comparably applied to the findings of the present study, quantitative differences in thermolysis, from greater to lesser levels, probably accrued to the chicks which assumed the standing, crouching, sitting, and laying postures, respectively, during these cold exposure trials. Chicks at all ages may therefore have reduced total heat loss by assuming less standing and more crouching, sitting, and laying postures over the duration of these trials. The sequential changes in postures adopted by these chicks would also have resulted in progres- sively greater reductions in thermolysis. However, few chicks realized the maximal thermolytic reduction that would have been achieved by assumption of the laying posture for longer periods of time. Younger chicks in all three acclimation groups, with their relatively greater surface area to body mass ratios, were probably most adversely affected by not using the laying posture at greater frequencies. Older chicks gained greater thermolytic reductions by their postural deployment by assuming and maintaining crouching, sitting, and laying postures sooner, more frequently, and for longer periods of time in similar sequences than their younger counterparts. The observed improvements in endothermic performance in these chicks with increased age may therefore have resulted, at least in part, from concomitant developmental modifications in their assumed postures. These postural changes do not account for the observed differences in endothermic performances between the three acclimation groups however. The rela- tionship between postural deployment changes and endothermic ontogeny 97 would be particularly fertile for additional study. The observed changes in locomotor activity and vocalization of these chicks during the cold exposure trials may also have influenced their endothermic performances. Chicks of all ages moved slower and less frequently over the course of these trials, while older birds reduced activity sooner and were less active than younger animals. These findings contrast observations of increased activity in adult birds during cold exposure (Morrison, 1962). If increases in thermal conductance do attend these voluntary responses under such cold tem- perature conditions, as has been demonstrated by West and Hart (1966), reduction in chick movements may have also reduced thermolysis over the duration of these trials and particularly in the older animals. Since vocalizations of birds likely entail at least some amount of respiratory evaporative heat loss, the observed decreases in vocal activity would also have resulted in thermolytic reductions in these chicks similar to those described in birds exposed to comparably cold temperature condi- tions (Kendeigh, 1944; Lasiewski and Dawson, 1964; Bartholomew and Trost, 1970; Moldenhauer, 1970). Observed improvements in endothermic performances of these chicks with increased age may have partially resulted from parallel age-related decreases both in their movements and vocalization. Changes in these activities do not account for the observed differences in endothermic performance between chicks in the three acclimation groups. Since urohidrosis increases heat dissipation in birds (Wilson, t l., 1957; Kahl, 1963; Hatch, 1970), decreases in the frequency and amount of defecation/urination in these chicks over the course of the cold exposure trials and particularly in the older chicks likely 98 also reduced thermolysis in these animals. The demonstrated improvement in endothermic performance in these chicks with increased age may there- fore have been due, in part, to concomitant decreases in defecation/ urination activity, at least through Day 7. Decreases in urohidrosis do not however explain the observed differences between the three acclimation groups in chick endothermic performance. The lack of extensive utilization of either ptiloerection or shivering by any chicks during the cold exposure trials was not antici- pated. Numerous prior investigations have described the use and the thermoregulatory advantages of both ptiloerection (Kendeigh, 1939; Irving, 1960; McFarland and Baher, 1968; McFarland and Budgell, 1970) and shivering (Odum, 1942; Steen and Enger, 1957; West, 1965; Morton and Carey, 1971) in birds exposed to cold thermal conditions. The respective decrease in thermolysis and increase in thermogenesis resulting from ptiloerection and shivering responses would likely have contributed to the maintenance of body temperatures by these chicks, especially the younger and W group animals. Perhaps other chick responses producing similar thermoregulatory benefits obviated the necessity of ptiloerection and shivering for the maintenance of thermal stability in these chicks. Peripheral vasoconstriction discussed pre- viously may have provided sufficient thermolytic reductions without requiring ptiloerection. Chemical thermogenesis, demonstrated earlier in these animals (Freeman, 1966; Wekstein and Zolman, 1968), may have substituted for shivering activity. Utilization of non-muscular thermogenesis would be anticipated in C group chicks due to the effects of cold thermal acclimation on their basal metabolic rates (see Chaffee, gt_gl,, 1963 and El Halawani, gt_gl,, 1970), but would not be expected 99 in the W group animals (see Huston, gt_§l,, 1962). Detection of muscle tremors in these chicks during the cold exposure trials and observations of extensive ptiloerection and intense shivering in these animals upon their return to their respective rearing brooders shows that both responses were available to these chicks during the trials. Shivering and ptiloerection were clearly not used during the cold exposure trials at demonstrated post-trial levels. The decrease of post-trial shivering and ptiloerection shown in the chicks with increased age mirror results found in earlier studies which employed cold exposure trials (Odum, 1942; Barott and Pringle, 1946). Greater use of both shivering and ptiloerection by W group chicks during the cold exposure trials would be expected (Huston, gt gl., 1962), but the obvious shivering and ptilo- erection shown by these animals under the 35°C post-trial conditions remains enigmatic. The demonstrated improvements in endothermic per- formance of chicks with increased age are not explained by either exten- sive ptiloerection 0r shivering responses by these animals during the cold exposure trials. Differences in endothermic performance in chicks from the three acclimation groups are also not accounted for by dif- ferences in ptiloerection or shivering activities. Since ptilomotor and/or shivering responses may have been used by these animals at inten- sities below detectable levels in this investigation, further studies examining the possible occurrence and effects of lower levels of shi- vering and ptiloerection on chick endothermic ontogeny under comparable acclimation and cold exposure testing conditions are suggested. Chicks in the C and C/W groups were acclimated to thermal condi- tions different from the temperatures prevailing in the cold acclimation rearing room. The huddling responses, crouched postures, location at 100 warmer brooder positions, and limited movement noted in the 1 to 3-day- old C acclimation group chicks demonstrates that these animals were acclimated to temperature conditions within the thermal range (34-36°C) maintained in the warm acclimation rearing room. This would perhaps explain why few differences in endothermic performance were shown between these younger animals (j,g,, Day 1 through Day 3) in the C and the W acclimation groups (Table 7). Older C group chicks were more fully subjected to the prevailing 20 i O.5°C temperatures of the cold rearing room due to their changing activities (i,g,, less huddling, more exposed postures, more dispersed locations, and increased move- ment) in the rearing brooder. These realized cold thermal acclimation conditions may explain why the superior endothermic performances of the C group chicks were so clearly demonstrated during the middle and later stages (1,3,, Day 4 through Day 10) of early development (Table 7). Observed changes in fecal droppings patterns of C group chicks describe these same conditions of thermal acclimation in these animals. The actual thermal conditions to which C group chicks were acclimated were on many days warmer than the cold rearing room temperatures, but on most days were nevertheless colder than the thermal conditions to which both C/W and W group animals were acclimated. Therefore, even smaller differences in the acclimation temperatures between these groups of chicks than those previously cited are still sufficient to induce the modifications of chick endothermic ontogeny demonstrated in this study (Table 7). The C/W acclimation group_chicks acclimated themselves to a variety of thermal conditions within the range of temperatures (20-35 i O.5°C) available to these animals in their rearing brooder during the 101 acclimation period. The extensive use by these chicks of the heated portion of this brooder at all times during the first few days of acclimation may explain the few differences in endothermic performance demonstrated between the three acclimation groups on Day 1 through Day 3 (Table 7). The older C/W group chicks located themselves at increasingly colder brooder positions during the lights-on portion of the photoperiod, which would account for their superior endothermic performance as compared to W group chicks shown between Day 4 through Day 11. Although C/W group chicks assumed more exposed postures than their C group counterparts, the C/W animals were distributed at warmer locations in their brooder, especially when sleeping during the lights- off portion of the photoperiod. This would explain the endothermic superiority of the C group chicks demonstrated on Day 4 through Day 10 (Table 7) and the comparatively slower endothermic development of C/W group animals. These observations of chick locations, postures, and movements show that younger C/W group animals were acclimated to thermal conditions which were warmer than the 20 i O.5°C temperatures prevalent in the cold rearing room and that, with increased age, C/W group chicks were acclimated to progressively colder thermal conditions nearer the rearing room temperatures. The C/W group chicks therefore acclimated themselves to a range of temperatures intermediate to the thermal conditions experienced by the C and the W acclimation groups. The patterns of fecal deposition noted in the C/W group support the same description of thermal acclimation in these chicks. The activities of the W acclimation group chicks within their brooder did not significantly increase or decrease the thermal accli- mation conditions from those maintained in the warm rearing room. In 102 contrast to the C and the C/W groups, the observations of more exposed postures, limited huddling, even distribution in brooder, and greater movement in the W group chicks at all ages during the acclimation period shows that these animals were acclimated to thermal conditions within the 34-36°C range of this rearing room. The pattern of fecal deposition noted in W group animals indicates these same conditions of thermal acclimation. The W group chicks were therefore acclimated on most days of the experimental period to warmer temperatures than either the C or the C/W acclimation groups, which would account for the inferior endothermic performances of W group chicks during these stages of their early development. Results previously discussed have shown that continuous exposure to cold acclimation temperatures during early development increases the rate of endothermic ontogeny in the young chick (Group C), whereas exposure to continuous warm thermal rearing conditions during this time (Group W) does not produce the same effect on chick endothermic development. These results lead to the following questions: (1) Is continuous acclimation to cold thermal conditions during early develop- ment necessary to elicit a stimulatory effect on the endothermic onto- geny of the young chick, or are shorter cold exposure times sufficient to evoke a similar effect? (2) Does removal of a young chick from the stimulatory effects of cold thermal acclimation influence its subsequent endothermic ontogeny? The results of the Group C/W chicks provide a partial answer to the first of these questions. These C/W chicks acclimated themselves to early warm and later cold thermal conditions and demonstrated rates of endothermic ontogeny intermediate to the C and the W acclimation 103 groups. .These results suggest that, although continuous cold thermal acclimation induces the fastest rates of chick endothermic development, shorter periods of cold acclimation during only the middle and later stages of early development enhance the endothermic performances of animals on subsequent days. However, the Group C/W chicks continued to locate themselves at warm acclimation temperatures, particularly at night, even at later ages, so their results provide only an approxima- tion of the effects of early cold and later warm thermal acclimation on chick endothermic development. These effects are clearly demonstrated by Group W+C chicks, which were acclimated to imposed warm rearing con- ditions (35 i O.5°C) during the first four days of early development and then switched to cold acclimation temperatures (20 i O.5°C) and tested for their endothermic capabilities on subsequent days. Continuous acclimation to cold thermal conditions clearly is not necessary to stimulate endothermic ontogeny in these young chicks (Table 12). After only one day of cold acclimation, W+C group chicks demonstrated superior endothermic performances as compared to W group animals and similar differences were shown between these two groups on all subsequent testing days. The endothermic responses of these W+C group chicks mirror those previously described in the C/W animals which acclimated themselves to comparable thermal conditions (1,3,, early warm and later cold acclimation temperatures). Furthermore, after only two or three days of cold acclimation, W+C group chicks demon- strated endothermic capabilities equivalent to animals that had experi- enced four days of earlier cold acclimation (Group C+W), and either superior or equivalent to chicks which previously had been acclimated to seven or eight days of cold thermal conditions (Group C). Shorter 104 periods of cold acclimation (i,g,, one to three days) are therefore sufficient to stimulate endothermic ontogeny in these young chicks. These results also support the earlier finding in this study that cold thermal acclimation stimulated the endothermic responses in these young chicks within a much shorter time period than has been shown necessary to demonstrate comparable thermoregulatory effects either in adult birds (Gelineo, 1955; Siegel, 1969) or juvenile chicks (Aulie, 1977). There were no acclimation groups previously discussed which could provide even a partial answer to the second question posed above regarding the effects of early cold and later warm thermal acclimation conditions on endothermic ontogeny in these young chicks. However, the effects of removal of the stimulatory effects of cold thermal acclimation on chick endothermic development are demonstrated in the Group C+W animals which were acclimated to imposed cold thermal con- ditions (20 i O.5°C) during the first four days of early development and then switched to warm rearing conditions (35 i O.5°C) and tested for their endothermic capabilities on subsequent days. The increased rates of endothermic ontogeny in cold-acclimated chicks are not altered by removing the stimulatory effects of the cold thermal acclimation conditions (Table 12). The C+W group chicks, which had been acclimated to cold thermal conditions during gply the first four days of their early development, demonstrated endothermic capabil- ities that were on all testing days either equivalent or superior to the C group animals which had been acclimated to continuous cold thermal conditions throughout equivalent periods of their early development. Therefore, once the stimulation of endothermic development by cold thermal acclimation in the young chick has been established, 105 continuation of these faster rates of endothermic ontogeny does not require further acclimation to cold thermal conditions. These results also demonstrate, as was previously shown in this study, that continu- ous acclimation to cold thermal conditions is not necessary to stimu- late endothermic development in these young chicks. Several lines of further inquiry are suggested by the results of the W+C and the C+W groups of chicks. The endothermic capabilities of W+C animals were enhanced by just one day of cold thermal acclimation during the middle stage of early development. Future studies might examine the effects on chick endothermic ontogeny of such brief cold acclimation conditions applied during only the initial or only the later stages of early chick development. The W+C chicks did not clearly dem- onstrate improvements of their endothermic performances on all testing days, at least on Day 9 (Table 12). The increased rates of endothermic ontogeny in the C+W chicks were not abated by five days exposure to warm acclimation conditions (Table 12). Whether these same results would persist throughout the period of early chick development could be tested by continuation of the present experimental paradigm through Day 12. Finally, only chicks which had been reared under imposed alter- gtjgp§_of thermal acclimation conditions showed unexpected differences in T0 values (Table 10). Since all_other acclimation groups studied in this investigation did not demonstrate such differences, these results may only represent a Type I error (i,g,, rejection of a true null hypo- thesis). Yet the suggestion that imposed alteration of acclimation temperature pgy_§g_may have affected body temperature levels in the C+W and the W+C groups of chicks remains, perhaps to be verified and explained in further detail in future studies. 106 The stimulation of endothermic ontogeny in these young chicks by cold thermal acclimation was further demonstrated during the first alternative trial procedure (one-hour exposure to 18 i 1.0°C). Group C chicks showed superior endothermic capabilities as compared to W group .animals under these milder cold exposure conditions (Tables 13 and 14). These 6-day-old Group C chicks demonstrated effective endothermic per- formances during these trials, whereas W group animals did not maintain normal body temperatures even at these warmer exposure temperatures (Table 14). These differences in chick endothermic performance shown during the first alternative trial procedure are not explained by dif- n ferences in either body weights or T0 values between the two acclimation groups. Superior endothermic capabilities of cold acclimated chicks, also demonstrated previously in standard trials during one-hour expo- sures to 10 i 1.0°C (Table 7), therefore characterize chick endothermic performance over a broad range of environmental temperatures, rather than being limited only to extremely cold thermal conditions. Behavioral responses (ectothermy) may contribute to the maintenance of normal body temperatures in chicks even gftgp_the attainment of ef- fective endothermic capabilities. As previously discussed, C group chicks maintained age-characteristic body temperatures when collectively housed in the cold acclimation rearing brooder under 20 i O.5°C thermal conditions. Yet, C group animals clearly are capable of effective endo- thermic regulation of body temperature when tested individually under comparable thermal conditions (Table 14). Although endothermic responses alone would therefore have permitted normal body temperature control, the collectively-housed C group chicks nevertheless utilized ectothermic activities (i,g,, huddling) which have been shown to 107 facilitate thermoregulation in young birds under cold thermal condi- tions (Kleiber and Winchester, 1933; Dunn, 1976c). The relationship between behavior and chick thermoregulatory performance during the course of endothermic ontogeny will be examined in further detail in Experimental Series II. Chicks demonstrated different levels of endothermic performance under different cold exposure conditions. Chicks in the C and the W acclimation groups showed body temperature regulation respectively at or closer to normal levels during the first alternative as compared to the standard trial procedure (Tables 15 and 16). Since both groups of chicks demonstrated improved endothermic control under milder environ- mental temperatures, differences in thermoregulatory performance between these acclimation groups were due to different levels of chick endothermic development rather than solely a function of using a partic- ular set of cold exposure conditions. The endothermic superiority of cold-acclimated chicks is clearly shown by the fact that C group ani- mals exposed to 10 i 1.0°C conditions maintained their body tempera- tures at the same levels as did W group chicks exposed to 18 i 1.0°C conditions (Table 16). These differences in chick endothermic perfor- mance demonstrated during the first alternative trial procedure and standard trials were not due to differences either in body weights or T0 values between any of the C and the W groups of animals. In summary, the results of the first alternative trial procedure confirm and expand upon the finding of increased rates of endothermic ontogeny in cold- acclimated chicks previously demonstrated in standard trials by showing superior endothermic capabilities in C group animals under warmer exposure temperatures. 108 The stimulation of endothermic development in these young chicks was even more clearly demonstrated during the second alternative trial procedure (three-hour exposure to 10 i 1.0°C). Group C chicks showed superior endothermic capabilities as compared to W group animals during the first hour of these trials (Tables 17, 18, 21, and 22) similar to those previously demonstrated during standard trials (Tables 5 and 7). However, these 6-day-old Group C chicks continued to show superior endo- thermic capabilities for the duration of these three-hour trials, while 6-day-old Group W animals demonstrated continual declines in their body temperatures over the same cold exposure period (compare Tables 18 and 20). These differences in chick endothermic performance shown during the second alternative trial procedure were not due to differences in either body weights or T0 values between the C and the W groups of chicks. The use of the shorter one-hour exposure times during the standard trials understates the endothermic capabilities of C group chicks, while it clearly overstates the endothermic capabilities of W group animals. The use of these longer cold exposure times to demon- strate differences in endothermic capabilities in developing young chicks is therefore recommended in future studies. In summary, the results of the second alternative trial procedure confirm and expand upon the finding of increased rates of endothermic ontogeny previously demonstrated during standard trials by more clearly showing superior endothermic capabilities in C group animals during longer exposures to cold thermal conditions. EXPERIMENTAL SERIES II The first series of experiments has demonstrated both age- and thermal acclimation-related changes in the endothermic capabilities of the young chick during early development. Older chicks showed superior endothermic capabilities during cold exposure trials than younger chicks acclimated to the same thermal conditions. Chicks acclimated to either continuous or intermittent cold thermal conditions showed faster rates of endothermic ontogeny than chicks acclimated to warm thermal conditions throughout their early development. Although the younger and/or warm-acclimated chicks have less well- developed endothermic capabilities for body temperature control, these chicks certainly are not totally lacking in thermoregulatory defenses. Behavioral regulation of body temperature (ectothermy) provides an alternative method of thermoregulatory control in which the animal utilizes diverse temperature conditions in the environment that are conducive to the maintenance of thermal stability (j,g,, within the limitations of endothermic control). Ectothermic responses may be the gply_available means of thermoregulation in chicks with limited endo- thermic capabilities (g,g,, younger and/or warm-acclimated animals). Alternatively, ectothermic responses may not be important in chicks with well-developed endothermic capabilities (g,g,, older and/or cold-accli- mated animals). The first series of experiments has therefore examined only part of the total scheme of chick thermoregulatory development. 109 110 The purpose of the second series of experiments was to determine the effects of acclimation temperature on the ectothermic (behavioral) regulation of body temperature in the young chick. Groups of animals were raised under either warm or cold thermal rearing conditions during early development and tested for their ectothermic responses at various ages. The hypothesis tested in this experimental series was that acclimation temperature during early development has a significant effect on the behavioral regulation of body temperature in the young chick. Experimental Groups Two experimental groups were used in this series of investigations. Each group of chicks was reared in one of two communal brooders with gg_ 11p, food and water and a 14L:100 photoperiod under one of the following thermal acclimation conditions. A total of 114 chicks in Group C were raised throughout early development in the brooder which was located in the cold acclimation rearing room, in which the ambient temperature was always maintained at 20 i O.5°C. A total of 114 chicks in Group W were raised throughout early development in the other brooder which was located in the warm acclimation rearing room, in which the ambient temperature was always maintained at 35 i O.5°C. The initial size of the experimental groups was between 40-50 chicks per brooder. This number decreased over time as the animals were used only once in an experiment and then discarded. There was no differential mortality between the two experimental groups reared under these thermal accli- mation conditions. 111 Apparatus A multichambered thermal gradient apparatus was made in which the ectothermic responses of the chicks were tested. .This apparatus was comprised of several component parts which were constructed in the man- ner now described. The flat black, movable chamber unit was built from eight plywood slats (90 x 20 x 0.95 cm) and two boards (56 x 25 x 1.9 cm) which were used to make the side walls and ends, respectively, of the seven individual but contiguous 90 x 7 x 20 cm chambers. A diagram of one of these chambers is presented in Figure 3. The tops of the side walls of the chambers were marked with pencil lines at 7.5 cm intervals. These lines demarcated 12 consecutively numbered positions, along the long axis of the chambers, which were used as reference points to specify the locations of the chicks in the cham- bers. A 90 x 60 cm metal frame, which was covered with a single piece of 1.3 cm mesh chicken wire of the same dimensions, provided a floor on which the chamber unit was placed. This floor was held on top of a 90 x 60 x 90 cm angle iron rack. The heating elements were two 60 x 5 x 2.5 cm electric bar heaters, with adjustable controls, whose ends were bolted to the sides of the rack directly below the floor and perpendicular to the long axis of the chamber unit. One of these heating elements was located 19 cm, and the other heating element was placed 42 cm, from one end of the rack. As a control for the presence and positions of these heating elements, a "dummy heater", made from a 60 x 5 x 2.5 cm board, was similarly located beneath the floor 73 cm from the same end of the rack. A droppings pan, covered with news- paper, was located 20 cm below the floor of the chamber unit. The gradient of temperature conditions in the chambers was 112 .mHm_cp wcsnmooca 2O new OOO OOPLOO mmcspmcmgemp emnsmcu new mcoHpHmoa conemgo chumuHOcH mzpmcmaam pcmwcwcm Hoaxes» umcmnEmgoHszs to H56 ON x N x OOH Luggage 6:0 to 36H> no» to EchmHO .m mczmHe mHmwch mczumoocm duo OOHLOO HOOV mmcauwcmOEmH ceasesO OH OH OH OH OH OH OH OH OH OH OH OH meHcH mcznmooca 2O OOHLOO HOOV mmczpmcmasm» cmnEmSO OH OH OH OH OH ON Om ON ON ow ON OH Ht gt gt ya mm um m m .t m .t m am we me He he he NH HH OH O O N O m a m N H mcoHpHmoa smegmgo 113 obtained in the following manner. The entire thermal gradient apparatus was placed in the cold exposure testing room, where the ambient temper- ature was maintained at 10 i 1.0°C. The electric bar heaters were plugged into wall outlets. By setting the controls of these heating elements at different specified positions (as determined by preliminary studies), the output of each bar heater was regulated to provide a range of temperature conditions between 10°C and 40°C in the chambers above (see Figure 3). The temperature conditions on and 2.5 cm above the floor were measured, to the nearest 0.1°C, at each of the 12 positions in all 7 chambers. These measurements were made by a YSI Tele-Thermometer (Model 43TG) using a YSI Thermistor Temperature Probe (No. 423X), and by standard laboratory mercury thermometers, whose measurements were within O.2°C of those readings obtained by the tele-thermometer at the same chamber position(s). At least five temperature measurements were taken in each chamber at all 12 chamber positions; the mean of these measurements was designated as the representative temperature of that position. These temperature measurements showed that the gradient of thermal conditions along the longitudinal axis in the chambers was discontinuous, since the warmest temperatures were recorded directly above and on either side of the heating elements, while successively colder temperatures were recorded at further distances from these bar heaters (see Figure 3). Periodic re-measurement showed that these chamber temperatures remained consistent during the trials and over the time period in which these experiments were conducted. The chick body temperature measurements were made, to the nearest 0.1°C, by the YSI Tale-Thermometer using the YSI Thermistor Temperature 114 Probe employed above in the manner previously described for single body temperature determinations (see Apparatus section of Experimental Series 1). Testing Procedures and Measurements The following procedures were utilized to test the ectothermic responses of the young chicks in the thermal gradient apparatus. One to three trials were conducted between 1200 and 1500 on each testing day. Since preliminary studies, as well as earlier investigations (Ogilvie, 1970), indicated that similar results were obtained from the same chick when tested alone in any one chamber as well as when other animals were present in adjacent chambers, the chicks were tested in groups of seven animals per trial, with one chick in each of the seven chambers. The trial groups were composed of three or four chicks randomly chosen from each of the two acclimation groups. The trials were conducted in the following manner. The chicks were removed from their respective acclimation rearing brooders and transferred in a cardboard box to the room outside the cold exposure testing room. The chicks were then randomly taken, one at a time, from the box and placed in the chambers of the thermal gradient apparatus at 30-second intervals. The chicks were always initially placed at one of the following chamber positions: 1, 8, 9, 10, 11, or 12 (see Figure 3). The determination of which of these six chamber positions a chick was initially placed at was randomly made. The chambers were arbitrarily numbered from 1 to 7 consecutively and the chicks were placed in these chambers following this sequential order (1,3,, the first animal was placed in chamber 1, the second animal in chamber 2, and so forth) 115 until all animals in the trial group had been placed in the apparatus. The body temperature was measured just prior to when each chick was placed in its respective chamber; this body temperature was designated as the initial body temperature (T0) at the start of the trial. The body temperatures of each chick were again measured at the end of the trial. The locations of each chick in their respective chambers, relative to the 12 delimited positions (see Figure 3) were recorded, at 30-second intervals, at specified times (indicated by a stopwatch) during the trials, in the same sequential order in which the animals were initially placed in the thermal gradient apparatus. Between the trials, the chamber unit and its floor were rotated on the rack to control for possible position effects. At the end of the trial, the chicks were weighed, to the nearest 0.1 gm, and the identification number or group color marking of each animal was recorded. The animals were then sacrificed and discarded, since each chick was used in only one trial. A diagram of the experimental manipulations and testing procedures used in the second series of experiments is presented in Figure 4. Two different trial procedures were conducted at Ages 1, 3, 5, 7, and 9 days using several successive groups of chicks reared under the two thermal acclimation conditions. Since the electric bar heaters were not plugged into wall outlets during the OFF trial procedure, the temperatures at 31__chamber positions were the same as the cold exposure testing room (1,3,, 10 i 1.0°C). The positions of the chicks in their respective chambers were recorded every 30 seconds during these 20—minute OFF trials. Since the electric bar heaters were plugged into wall outlets during the ON trial procedure, the gradient of thermal conditions in 116 .HH mmwcwm Hmpcoewcqum OH vow: mwcsvmooca Ochmwp new meowpmHOOHceE Hmpcwswcwaxm .e OLOOHO mm mm mm mN MNHW msaz 0.05), but was significantly different from random during the ON procedure trials (G= 151.78, df= 2, p << 0.001). Chicks were located at chamber positions 3 and 6 at significantly higher frequen- cies during the ON procedure trials than during the OFF procedure trials (Tables 25 and 26). However, there was no significant differ- ence between the two acclimation groups in the distribution of chicks at chamber positions 3 and 6 during the ON procedure trials (G= 1.28, df= 1, p > 0.05). 119 Table 23. Analysis of Variance of Rates of Change of Chick Body Temperature (°C) during OFF and ON Procedure Trials. Source DF MS F P Trial Procedure 1 45.77 53.85 <<0.001 Acclimation Temperature 1 6.91 8.13 <0.005 Trial Procedure x Acclimation Temperature 1 6.07 7.14 <0.01 Within 224 0.85 Total 227 Table 24. Duncan's Test on Mean Rates of Change of Chick Body Temperature (°C) during OFF and ON Procedure Trials. Acclimation Group Trial Trial Procedure Procedure C W Means OFF -O.75 -1.71 -1.23 (0.26) (0.21) (0.26) ON 0.06 -O.23 -0.09 (0.03) (0.06) (0.03) Acclimation Group -O.12 -O.56 Means (0.07) (0.12) Means subtended by the same line do not differ at p = 0.05. ( ) = 1 Standard error. 120 Table 25. Distribution of Chicks in Thermal Gradient Chambers during OFF and ON Procedure Trials. Chamber Positions (Chamber Temperatures) Trial Procedure Acclimation Group .9 _w_ 1, 8-12 OFF 10 9 (<20°C) ON 12_ ‘13 29 24 2, 4, 5, 7 OFF 9 13 (20-29.9°C) ON 33 13 38 28 3, 6 OFF 6 3 (230°C) ON 1 33 4:14:- \1 on N 121 Table 26. Analysis of Independence of Chick Positions in Thermal Gradient Chambers during OFF and ON Procedure Trials. Hypothesis Tested DF ' G P Chamber Position x Trial Procedure 1 24.546 <0.001 independence Chamber Position x Acclimation Group 2 4.064 NS independence Trial Procedure x Acclimation Group 1 0.002 NS independence Chamber Position x Trial Procedure x 2 6.002 <0.05 Acclimation Group interaction Chamber Position x Trial Procedure * 1 17.856 <0.001 Chamber Position x Trial Procedure x 7 34.614 <<0.001 Acclimation Group independence * Single degree of freedom component Chamber Positions Qf£_ .gu 1, 8-12 19 34 3, 6 ._g 100 28 134' Chamber Temperatures <20°C 230°C 122 Discussion Chicks distributed themselves differently in the testing apparatus during the two trial procedures. During the OFF trials, chicks were randomly distributed amongst all chamber positions (Table 25). During the ON trials however, chicks were non-randomly distributed at the warmer chamber locations, especially positions 3 and 6 (Tables 25 and 26). These distributions of animals in the chambers resulted from chick movement, since these animals all began both trial procedures at non-random chamber positions (1,3,, chamber positions 1, 8-12). Therefore, when only uniform cold temperature conditions were present in the testing apparatus, chicks randomly distributed themselves throughout the chambers. However, when a range of thermal conditions between cold and warm temperatures was present in the testing appara- tus, chicks non-randomly distributed themselves at the warmer chamber positions. Movements of the animals in the thermal gradient chambers during the ON trials had a significant effect on chick body temperature regu- lation. During the OFF trials, neither group of chicks maintained normal body temperatures, although C group animals demonstrated superior thermoregulatory (1,3,, endothermic) capabilities under these uniform 10 i 1.0°C thermal conditions (Tables 23 and 24). During the ON trials however, 331p_groups of chicks maintained the 33m3_body temperature levels p11p1p_the normal range (Tables 23 and 24). These differences in thermoregulatory performance were not due to differences in either body weights or T0 values between these groups of chicks. Regulation of body temperature at normal levels in chicks during the ON trials resulted from movement by these animals to the warmer chamber 123 positions, since these chicks would not have been capable of such thermoregulatory performances had they remained at their initial (1,_,, 10 i 1.0°C) chamber positions. Earlier studies (3,g,, Poczopko, 1967a; Ogilvie, 1970) which showed that young chicks move to warmer positions in a thermal gradient chamber have only suggested that these responses assist thermoregulation in these animals. This investigation clearly demonstrates that these behavioral (ectothermic) responses were necessary for the effective thermoregulatory performances shown in these young chicks. Although the ectothermic responses of all chicks were similar during the ON trials, these responses did not have the same absolute effect on the thermoregulatory performances of the animals in both acclimation groups. Despite their less-developed endothermic capa- bilities, W group chicks demonstrated effective thermoregulatory performances, equivalent to C group animals, resulting from their movement to warmer chamber positions (Table 24). The W group chicks therefore gained significant thermoregulatory benefits from their ectothermic responses. The endothermically superior C group chicks also benefited from their comparable movements to warmer chamber positions, although the improvement in thermoregulatory performances of these animals was not the same magnitude as was shown in W group chicks (Table 24). Behavioral regulation of body temperature clearly contributed to the thermoregulatory performances of these young chicks regardless of developmental levels of their endothermic capabilities. Improvements in endothermic capabilities therefore do not necessarily reduce the role of ectothermic responses in the thermoregulatory performance of the young chick. SUMMARY 1. The hypothesis tested in this investigation was that acclima- tion temperature would influence the ontogeny of thermoregulation in the young chick (Gallus domesticus). 2. In Experimental Series 1, groups of chicks were reared under one of five different conditions of thermal acclimation. Changes in body temperatures measured during cold exposure trials were used to compare chick endothermic performances. Directly observed responses of chicks both during the trials and when housed in their respective acclimation brooders were also recorded. 3. Cold thermal acclimation stimulated endothermic ontogeny in these young chicks. Chicks acclimated to continuous cold thermal con- ditions demonstrated, with increased age, smaller decreases in body temperature during the trials than did continuous warm acclimated chicks. 4. Decreases in locomotor activity, vocalization, and defecation/ urination, as well as greater use of thermolytically advantageous pos- tures, during the trials in all chicks with increased age and over the course of the trials contributed to chick endothermic performances and their improvement during early development. Shivering, ptiloerection, and peripheral vasomotor responses did not influence chick endothermic ontogeny. Differences in chick endothermic performances between the acclimation groups were not explained by differences in these responses. 124 125 5. Continuous cold acclimation is not necessary to stimulate chick endothermic ontogeny. Chicks acclimated for only two or three days to cold thermal conditions demonstrated endothermic capabilities superior or equivalent, respectively, to chicks continuously acclimated for seven or eight days to the same cold thermal conditions. 6. Superior endothermic capabilities characterize cold acclimated chicks over a range of cold thermal conditions and during extended exposure to cold temperatures. 7. In Experimental Series 11, groups of chicks were acclimated to either cold or warm thermal conditions. Movements, distributions, and changes in body temperatures of chicks in a thermal gradient chamber apparatus during two different trial procedures were compared to deter- mine the influence of behavioral (ectothermic) responses on body temper- ature regulation in the young chick. 8. Movements of both warm and cold acclimated chicks to warmer positions resulted in the maintenance of normal chick body temperatures at levels not attainable by endothermic responses alone. 9. 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