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Metabolic adaptation of the beaver (Castor canadensis Kuhl) to the Arctic energy regime Aleksiuk, Michael 1968

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THE METABOLIC ADAPTATION OF THE BEAVER (CASTOR CANADENSIS KUHL) TO THE ARCTIC ENERGY REGIME by MICHAEL ALEKSIUK B.Sc, University of Alberta, 1965 A THESIS SUBMITTED IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in the Department of ZOOLOGY We accept t h i s thesis as conforming to the required standard THE UNIVERSITY OF BRITISH COLUMBIA July, 1968 In presenting t h i s thesis in p a r t i a l f u l f i l m e n t of the requirements for an advanced degree at the University of B r i t i s h Columbia, I agree that the Library s h a l l make i t f r e e l y available for reference and study. I further agree that permission for extensive copying of t h i s thesis for scholarly purposes may be granted by the Head of my Department or by h i s representative. It i s understood that copying or publication of t h i s thesis for f i n a n c i a l gain s h a l l not be allowed without my written permission. Department of Zoology The University of B r i t i s h Columbia Vancouver 8, B.C. Canada. Date : July, 1968 Chairman: Professor Ian McTaggart Cowan ABSTRACT The beaver (Castor canadensis Kuhl) i s subjected to a widely fl u c t u a t i n g energy regime i n the northern portion of i t s d i s t r i b u t i o n . During the summer the animal has free access to an abundant food supply i n the form of growing plant material, while during the winter the food supply i s lim i t e d to a store of cached saplings. The working hypothesis of this study was that seasonal s h i f t s occur i n energy expenditure such that i t i s highest during the summer when an abundant food supply i s r e a d i l y available. In the Mackenzie Delta, Northwest T e r r i t o r i e s , growth was found to be rapid i n the summer and absent i n the winter. A winter weight loss characterized immature animals. Fat was deposited i n the autumn, maintained during the winter and mobilized i n the spring. Animals were lean during the summer. Thyroid gland weights were high i n the summer and low i n the winter. It was concluded from these data that metabolic energy expenditure i s high during the summer and low during the winter. A consideration of possible e x t r i n s i c causes of this annual pattern and the finding that the beaver ceases to grow during the winter when on a constant ration made available ad libitum led to the conclusion that the pattern i s an inherent property of the beaver at northern l a t i t u d e s . The thyroid gland was hypothesized as the major effector of the annual pattern within the organism. Light i n t e n s i t y was hypothesized as the environmental factor that times the l e v e l of energy expenditure to environmental conditions. No major seasonal changes i n thyroid a c t i v i t y , food intake or growth were observed i n C a l i f o r n i a beavers maintained under Vancouver climatic conditions and a constant r a t i o n made available ad libitum, but A r c t i c beavers maintained under the same conditions showed a growth cessation, a 40% reduction i n food intake and a depression i n thyroid a c t i v i t y during the winter. This i s consistent with the conclusion that the annual metaboli pattern observed i n northern beavers i n the f i e l d i s an inherent a t t r i b u t e . Manipulation of l i g h t conditions had no detectable e f f e c t s on C a l i f o r n i a beavers, but.exposure of A r c t i c beavers to constant darkness resulted i n a reduction of food intake to zero after 17 and 22 days, a weight loss and a complete muscular paralysis of unknown nature. No body temperature drop occurred. Exposure to constant incandescent l i g h t after 24 days of darkness returned thes e f f e c t s to normal. The thyroid hypothesis was questioned because food intake dropped to zero rather than to a low basal l e v e l during the depression. It was hypothesized that the muscular paralysis represents a peripheral control of a c t i v i t y that reduces winter a c t i v i t y to a minimum. Continued exposure of the A r c t i c beavers to l i g h t during the winter resulted in rapid growth and high food intake during that period. It was concluded that i n nature decreasing l i g h t i n t e n s i t y i n the autumn induces a metabolic depression in the northern beaver and increasing l i g h t i n t e n s i t y in the spring dispels i t . TABLE OF CONTENTS i v Page ABSTRACT i TABLE OF CONTENTS i v LIST OF TABLES v i LIST OF FIGURES v i i ACKNOWLEDGEMENTS x GENERAL INTRODUCTION 1 PART I. SEASONAL ENERGY EXPENDITURE IN RELATION TO ENVIRONMENTAL ENERGY AVAILABILITY 4 I n t r o d u c t i o n 4 H a b i t a t and C l i m a t i c C o n d i t i o n s 7 Methods 10 R e s u l t s 17 S e a s o n a l Food C o n s i d e r a t i o n s 17 Growth Dynamics 22 F a t D e p o s i t i o n and M o b i l i z a t i o n 34 T h y r o i d A c t i v i t y 41 D i s c u s s i o n 49 PART I I . AN EXPERIMENTAL ANALYSIS OF THE WINTER METABOLIC DEPRESSION 67 I n t r o d u c t i o n 67 Methods 7 0 R e s u l t s 7 5 V Seasonal Changes in the Metabolic A c t i v i t i e s of Northern and Southern Beavers in Captivity 75 Growth 75 Food Intake 80 T a i l Fat Changes 82 -^Thyroid A c t i v i t y 82 E f f e c t of Light on Food Intake, Body Weight, T a i l Fat Content and Muscular A c t i v i t y 84 ^ Discussion 94 SUMMARY AND CONCLUSIONS 110 LITERATURE CITED 115 v i L IST OF TABLES Tab l e Page I C o m p o s i t i o n o f beaver f o o d caches. Caches #1 and #2 were a n a l y z e d on 30 August 1965; the remainder were a n a l y z e d i n e a r l y September, 1966. The f i g u r e s r e f e r t o t h e number o f stems i n a g i v e n cache. 18 I I M o i s t u r e c o n t e n t , p r o t e i n c o n t e n t , c a l o r i c d e n s i t y and p r o t e i n t o c a l o r i e r a t i o s o f p l a n t s used as f o o d by t h e b e a v e r . W.B. = Wet B a s i s ; D.B. = Dry B a s i s . 20 I I I Comparison o f average a b s o l u t e growth r a t e s o f Mackenzie D e l t a and Saskatchewan b e a v e r s . Growth r a t e s a r e e x p r e s s e d i n k i l o g r a m s p e r day. Growth r a t e s o f Saskatchewan b e a v e r s were c a l c u l a t e d from d a t a p r e s e n t e d by Pearson (1960). 28 IV C o m p o s i t i o n o f U.B.C. R a t i o n 42-57 on w h i c h t h e e x p e r i m e n t a l a n i m a l s were m a i n t a i n e d . 7 2 V R e c t a l t e m p e r a t u r e s i n °C o f b e a v e r s i n d e p r e s s e d s t a t e s and b e a v e r s i n n o r m a l p h y s i o l o g i c a l s t a t e s . Ambient t e m p e r a t u r e s i n a l l c a s e s were 21-22°C. 90 v i i LIST OF FIGURES Figure Page 1 Summary of temperature and p r e c i p i t a t i o n conditions at Aklavik, Northwest T e r r i t o r i e s . After Mackay, 1963. 8 2 Relationship of t o t a l length to age in dead-collected specimens. 11 3 Total weight growth curve to s e n i l i t y . .23 4 Skeletal (total length) growth curve to s e n i l i t y . 24 5 Heart growth to maturity. 25 6 Right kidney growth to maturity. 26 7 Quantitative changes in fat depots in r e l a t i o n to season in immature individuals. 30 8 Seasonal' changes in percent f a t in t a i l tissue of immature individuals. 32 9 Relationship between percent fat and percent water in t a i l tissue of the beaver. 33 10 Seasonal changes in t a i l volume r e l a t i v e to heart weight in immature individuals. 36 11 Relationship between percent t a i l f a t and t a i l volume. 37 12 Relationship between percent t a i l f a t and subcutaneous f a t . 39 13 Relationship between splenic f a t and subcutaneous f a t . 40 v i i i 14 Changes i n r e l a t i v e thyroid weight with time to s e n i l i t y . 43 15 Seasonal changes i n r e l a t i v e thyroid weight i n yearlings. 45 16 A model depicting annual patterns of energy expenditure i n the beaver at d i f f e r e n t l a t i t u d e s . Portions of b and c below a represent winter expenditure; portions above a represent summer expenditure. 59 17 A schematic representation of an hypothesis which attempts to explain the winter metabolic depression i n the beaver. 65 18 Total weight growth of A r c t i c beavers i n c a p t i v i t y , 1966 and 1967. 76 19 Total weight growth of C a l i f o r n i a beavers i n c a p t i v i t y , 1966 and 1967. A l l animals were exposed to Vancouver l i g h t conditions except i n d i v i d u a l s o and x, which were exposed to constant darkness from 18 October to 18 January. 77 20 Relative food intake of A r c t i c beavers, 1966 and 1967. Each point on the graph represents a four day average. 78 21 Relative food intake of C a l i f o r n i a beavers, 1966 and 1967. Each point on the graph represents a four day average. 79 ix 22 Seasonal changes in percent t a i l fat content of A r c t i c and C a l i f o r n i a beavers. 81 131 23 Seasonal changes in PBI conversion r a t i o s of A r c t i c and C a l i f o r n i a beavers. 83 24 Eff e c t of l i g h t r e s t r i c t i o n and constant l i g h t on t o t a l weight growth and r e l a t i v e food intake of 2 A r c t i c beavers. 86 25 Percent t a i l f a t content of 2 A r c t i c beavers subjected to a r t i f i c i a l l i g h t conditions. 92 26 Summary of temperature and p r e c i p i t a t i o n conditions at Quincy, Plumas County, C a l i f o r n i a during 1966. (U.S. Climatological Data, 1966). 100 X ACKNOWLEDGEMENTS This study was financed by the Canadian W i l d l i f e Service, the National Research Council of Canada through grants made to Dr. I.McT. Cowan, the A r c t i c and Alpine Committee of the University of B r i t i s h Columbia and the A r c t i c I n s t i t u t e of North America. The completion of this study owes a great deal to the ever ready assistance, suggestions and encouragement offered by Dr. I.McT. Cowan, who was my major advisor. Working under his guidance was an i n s p i r a t i o n and a pleasure, and to him I of f e r my sincere thanks. Drs. I.E. Efford, H.D. Fisher, H.C. Nordan and J.M. Taylor c r i t i c a l l y read the thesis and offered many useful suggestions. Dr. H.C. Nordan provided laboratory space, designed the beaver pens and generally provided invaluable ai d i n the care of l i v e beavers. The f i e l d portion of t h i s study was done while I served as Student Assistant to Vernon D. Hawley, Research S c i e n t i s t , Canadian W i l d l i f e Service. I am gr a t e f u l to him f i r s t l y for generously permitting me to conduct the study while i n his employ, and secondly for doing everything he could to ensure the c o l l e c t i o n of the necessary data. The warm h o s p i t a l i t y of Mr. and Mrs. V.D. Hawley and Dr. and Mrs. T.W. Barry made my stay on the Mackenzie Delta a pleasant one. x i Dennis King and Ernie Moore assisted me i n portions of the f i e l d work. Raylor Addison helped procure the northern beavers used i n the experiments. The southern beavers were obtained through the complete cooperation of the C a l i f o r n i a Department of F i s h and Game. The Inuvik Research Laboratory provided me with laboratory space and various f i e l d equipment during the f i e l d portion of the study. Mrs. B. March, Department of Poultry Science, Dr. D. Middaugh, Faculty of Dentistry, Dr. J. Birkbeck, Faculty of Medicine and P h i l i p Whitehead, Canadian W i l d l i f e Service allowed me the use of their laboratory space and equipment at the University of B r i t i s h Columbia. Funds for my personal maintenance were made available through three National Research Council scholarships, one Canadian W i l d l i f e Service scholarship and a Teaching Assistantship. Also, I would l i k e to acknowledge the various people who helped make my stay at the University of B r i t i s h Columbia a pleasant one. 1 GENERAL INTRODUCTION A problem of importance encountered by a l l animals i s the procurement of energy necessary for the maintenance of l i f e . A large portion of an animal's a c t i v i t y i s directed to that end, and i f i t i s not attained, the normal r e s u l t i s death. Short-term energy r e s t r i c t i o n s have undoubtedly occurred throughout the evolutionary history of vertebrates. An universal adaptation to short-term r e s t r i c t i o n s among vertebrates i s the a b i l i t y to store energy in the form of neutral t r i g l y c e r i d e s during periods of high a v a i l a b i l i t y . The t r i g l y c e r i d e s are then u t i l i z e d as a source of energy when food i s not r e a d i l y available in the environment, thus permitting the organism to maintain homeostasis and function normally during such periods. The winter of the northern hemisphere r e s u l t s in a prolonged energy r e s t r i c t i o n of regular occurrence to herbivorous mammals inhabiting that region, as discussed in d e t a i l by Formozov (1946). Food plants are usually covered by snow, and their n u t r i t i o n a l value may be reduced owing to the i r dormant state. Formozov describes some of the behavioural and morphological adaptations that have resulted in mammals apparently as a consequence of thi s reduction in energy a v a i l a b i l i t y . A s t r i k i n g example of metabolic adaptation i s seasonal hibernation in certain species of rodents (Folk, 1966, p.206; Kalabukhov, 1960). 2 Hibernators deposit a variable quantity of depot fat in the autumn, and maintain a reduced body temperature throughout most of the winter (Lyman and Chatfield, 1955). The reduction in body temperature and concomitant reduction in metabolism substantially reduce energy expenditure in the body, and the animal i s able to pass the winter subsist-ing largely on i t s f a t reserves. Research in the f i e l d of metabolic adaptation of mammals to adverse energy conditions has centred largely around natural hypothermia. There has been a widespread search for mammals with a l a b i l e body temperature, and an intensive study of the physiology and biochemistry of hibernation and temperature regulation. The study of natural hypothermia has been in vogue for the past two decades, probably owing to the spectacular nature of the phenomenon. L i t t l e attention has been given the p o s s i b i l i t y that mechanisms other than hypothermia might serve to reduce energy expenditure during periods of low energy a v a i l a b i l i t y . This study i s an examination of that p o s s i b i l i t y . The beaver (Castor canadensis Kuhl), a non-hibernating rodent, ranges from Mexico in the south to the Mackenzie Delta, Northwest T e r r i t o r i e s , in the north (Hall and Kelson, 1959). In the northern portion of i t s d i s t r i b u t i o n i t i s subjected to a long winter. It spends the winter in a micro-environment which consists of a lodge and a small area of a c t i v i t y in front of the lodge beneath the ice of the lake 3 or stream on which the lodge i s situated. The animal i s e f f e c t i v e l y separated from the remainder of i t s habitat by a thick layer of ice and frozen s o i l . It apparently depends e n t i r e l y on food stored in the water in front of the lodge for i t s nourishment (Novakowski, 1967), and thus the quantity of available energy i s limited to that present in the food store. During the summer the energy l i m i t a t i o n does not e x i s t . The animal i s able to range widely and has free access to an abundant food supply in the form of growing plant material. Those two d i s t i n c t periods l a s t eight months and four months respectively on the Mackenzie Delta. Conceivably there i s s u f f i c i e n t energy in the food store to permit the beaver to maintain i t s metabolic a c t i v i t i e s at the same rate during the winter as that maintained during the summer. The preliminary work of Stephenson (1956) and Pearson (1960), which indicated a winter growth depression in the species, suggests that there i s not. The purpose of t h i s study i s to examine the metabolic r e l a t i o n s h i p of the beaver to i t s seasonally f l u c t u a t i n g energy regime in the extreme northern portion of i t s d i s t r i b u t i o n . The f i r s t portion of the study i s an examination of seasonal energy expenditure in r e l a t i o n to environmental food a v a i l a b i l i t y . The second portion i s an experimental analysis of an apparent metabolic adaptation to the r e s t r i c t e d energy regime of winter. 4 PART I. SEASONAL ENERGY EXPENDITURE IN RELATION TO ENVIRONMENTAL ENERGY AVAILABILITY Introduction An i n t e g r a l part of the ecology of any species i s the method by which i t successfully u t i l i z e s an energy source. The Mackenzie Delta harbours a substantial beaver population which i s apparently stable from year to year and thus the species i s successful there (Aleksiuk, in press). This suggests that the animal i s adapted to i t s t o t a l environment in that area. The singular feature of the beaver's energy environment in the northern portion of i t s d i s t r i b u t i o n i s that food a v a i l a b i l i t y fluctuates seasonally in a regular and extreme manner. One might expect that the animal would be poorly adapted at the peripheral portions of i t s d i s t r i b u t i o n , e s p e c i a l l y insofar as the energy supply d i f f e r s r a d i c a l l y along the north-south axis of i t s d i s t r i b u t i o n , but such does not appear to be the case. The purpose of t h i s section i s to examine metabolic aspects of seasonal energy expenditure in the beaver on the Mackenzie Delta, and thus to learn how the species successfully u t i l i z e s i t s energy source at northern l a t i t u d e s . The working hypothesis i s that seasonal s h i f t s occur in energy expenditure such that i t i s highest during the summer. The major energy-expending processes of homeotherms are mechanical work, osmotic work, synthesis of new material 5 and maintenance of a constant body temperature. Although growth represents only part of the t o t a l energy expenditure, i t was chosen as the measure most useful for t h i s study. As well as being easy to measure under f i e l d conditions, i t i s most sensitive to changes in energy conditions. Given a r e s t r i c t i o n in energy intake, growth i s l o g i c a l l y the f i r s t energy-demanding process that w i l l respond with a reduction in rate. This i s the case because a cessation of growth i s compatible with the functioning of a homeotherm whereas a cessation of mechanical work, osmotic work or thermoregulation i s not. These l a t t e r three processes are a l l included in maintenance, and are necessary to maintain the i n t e g r i t y of the organism. Gain in t o t a l weight, s k e l e t a l growth and organ growth were measured. Two other parameters chosen to gain information on seasonal energy expenditure are body f a t content and thyroid a c t i v i t y . The body f a t content of a mammal, although subject to numerous influencing factors, r e f l e c t s accurately the balance between energy intake and energy expenditure. It was necessary to measure indices of body f a t content rather than t o t a l body fat per se due to the i m p r a c t i c a l i t y of extracting the t o t a l f a t from an animal with the body size of a beaver. The d i r e c t c o r r e l a t i o n between thyroid a c t i v i t y and general body metabolism i s well known. The l e v e l of thyroid a c t i v i t y provides a crude but very useful measure of the 6 l e v e l of general body metabolism and thus provides further information on metabolic energy expenditure. It would be most useful to determine the entire energy budget on a seasonal basis during the course of one year. Theoretically, t h i s could be done through the use of the somewhat over-simplified model put fort h by McNab(1963), which describes energy expenditure as a function of time, environmental temperature and rate of metabolism. Also, i t could be determined more r e a l i s t i c a l l y through the measurement of the four important variables concerned in t h i s balance, v i z . , food, stored energy, work and heat production, as suggested by Brobeck (1948). However, both methods are impossible to implement in nature where the animal i s f r e e -ranging. This study w i l l not y i e l d information on the quantitative aspects of energy expenditure in absolute terms, but i t w i l l indicate whether seasonal s h i f t s in energy expenditure occur. The f i e l d work was done on the Mackenzie Delta, Northwest T e r r i t o r i e s , Canada, at approximately 133°59' W, 67°55'N. "Freeze-up" and "break-up" dates at Aklavik, near the study area, averaged over nine years are October 9 and June 1 respectively (Mackay, 1963). Therefore the beaver population at those lati t u d e s i s r e s t r i c t e d to the under-ice environment from October to May i n c l u s i v e and free-ranging from June to September i n c l u s i v e . 7 Habitat and Climatic Conditions The southern portion of the Mackenzie Delta i s considered subarctic, while the northern portion i s a r c t i c (Mackay, o p . c i t . ) . The beaver population under study i s in the subarctic portion, very near the t r a n s i t i o n a l zone, although scattered colonies are found in the a r c t i c portion. The climate i s t y p i c a l l y severe subarctic, with long, cold winters and short, cool summers; p r e c i p i t a t i o n i s l i g h t ( F i g . l ) . The study area i s in t y p i c a l d e l t a i c t e r r a i n and f a l l s in the extreme northern portion of the boreal forest. More accurately, the vegetation type might be termed a r c t i c taiga, in that the area i s part of the t r a n s i t i o n a l zone between the boreal forest and a r c t i c tundra. The study area i s 28 square miles in area. It contains one small r i v e r channel, a number of small streams entering the channel from the east and a large number of lakes. Most of the lakes cover less than one square mile and average about 2 to 3 metres in depth. Shoreline development i s f a i r l y high. During years of high floods the majority of the area i s covered with s i l t - l a d e n water, causing the lakes to be f i l l e d with t h i s water and a layer of s i l t to be deposited over the entire region. The t e r r e s t r i a l portion of the habitat on the study area consists of spruce climax forest, willow-alder fringe, willow-poplar-alder islands and willow f l a t s . The spruce (Picea glauca) climax forest has an understory of alder 8 Figure 1. Summary of temperature and p r e c i p i t a t i o n conditions at Aklavik, Northwest T e r r i t o r i e s . After Mackay, 1963. 9 (Alnus crispa) and i s usually found on well-drained ground. The ground cover i s largely Pyrola spp., Hedysarum alpinum, Rosa bourgeauiana, Equisetum arvense and various mosses. A number of other species occur in lesser numbers. Lakes and streams are bordered by a fringe of deciduous trees. The fringe may be willow (Salix spp.), alder or a combination of the two. Small poplar (Populus  balsamifera) trees are often found in t h i s fringe. The degree of openness of the fringe varies greatly. A closed fringe has very l i t t l e ground cover, with Rosa bourgeauiana and Equisetum arvense being most common forms. An open fringe, on the other hand, has an extensive ground cover. Willow-poplar-alder "islands" occur commonly on well-drained areas. The r e l a t i v e proportions of the tree species in the islands varies greatly. Where these islands occur near lakes or streams the poplar has been largely removed by beavers. Ground cover consists of Pyrola spp., Hedysarum  alpinum, assorted other forbs, Rosa bourgeauiana and various grasses. Willow f l a t s are found on poorly-drained areas which spruce, poplar and alder apparently cannot invade. Such areas are consistently dense and uniform in composition. Equisetum arvense, grasses and sedges predominate in the ground cover. 10 Methods The May to September periods of 1964-66 inclusive were spent in the f i e l d obtaining data on growth, fat content and thyroid a c t i v i t y . Two methods, l i v e trapping and dead c o l l e c t i o n , were employed in procuring specimens for study. Beavers were l i v e trapped during the open-water season with Hancock and Bailey traps, primarily for growth data. Upon capture each beaver was weighed and then anaesthetized by i n j e c t i n g thamylal sodium ( S u r i t a l : Parke-Davis) i n t r a p e r i t o n e a l l y at a dosage of 18.3 milligrams per kilogram body weight. The animal was removed from the trap, weighed to the nearest f i f t h of a kilogram, measured for t o t a l length to the nearest h a l f centimetre, examined for sex and tagged in each ear with a f i s h tag. It was returned to the trap,held u n t i l i t had recovered from the anaesthetic and then released. It was possible to determine the age of animals up to approximately 24 months of age from a t o t a l weight versus age co r r e l a t i o n curve prepared with data from dead specimens (Fig.2). Thirty-one individuals less than 24 months of age were captured a t o t a l of 63 times in t h i s manner. Recaptures were very useful in y i e l d i n g data on weight changes of given individuals. Data obtained by l i v e trapping are limited to late spring, summer and early autumn. 1 1 F i g u r e 2 . R e l a t i o n s h i p o f t o t a l l e n g t h t o a g e i n d e a d - c o l l e c t e d s p e c i m e n s . \ 12 Ninety-one dead specimens were procured by trapping with the Conibear trap and shooting with a .22 c a l i b r e r i f l e . Dead trapping through the i c e was used to obtain specimens during the autumn, winter and spring. Forty-three specimens were obtained i n this manner by a l o c a l resident and made availa b l e to me through the courtesy of the Inuvik Research Laboratory, where they were stored i n the freezer f a c i l i t i e s . A l l specimens were aged by the dental development method of van Nostrand and Stephenson (1964). Each animal was weighed to the nearest f i f t h of a kilogram and measured for length to the nearest half centimetre. The sex was recorded. The heart and kidneys were weighed to the nearest gram. The splenic and peri r e n a l f a t depots were removed with sharp scissors and sca l p e l , and weighed to the nearest tenth of a gram. An attempt was made to obtain an objective subcutaneous f a t index by taking a skin plus f a t plug with a sharp cork borer and measuring the thickness of the f a t layer. This proved unsuccessful l a r g e l y due to the compressibility of the f a t layer and the d i f f i c u l t y encountered i n severing p r e c i s e l y the f a t from the under-l y i n g muscle. Instead subcutaneous f a t was subjectively l a b e l l e d as absent, rare, moderate, abundant or extremely abundant. I t i s important to note that the index i s subjective, and the gradations between the various labels are not necessarily uniform. For example, the difference 1 3 between "absent" and "rare" i s probably very much smaller than that between "abundant" and "extremely abundant". During preliminary observations i t was noted that there was an apparent correlation between the fat content of the animal and the appearance of the t a i l . The t a i l of lean individuals appeared s l i g h t l y shrunken and wrinkled on the surface, while that of obese individuals was smooth in appearance. These observations led to the hypothesis that the t a i l serves as a fat depot. It was decided to test the hypothesis by searching for seasonal fluctuations in t a i l volume and percentage t a i l f a t content which might be correlated with weight fluctuations of known f a t depots. T a i l volume was measured to the nearest cubic centimetre by a water displacement method. Percentage fat content in the t a i l was determined as follows. A c y l i n d r i c a l plug was removed from the t a i l by means of a sharp cork borer and the skin layer on each end s l i c e d o f f . Caution was exercised to ensure that the sample did not contain muscle ti s s u e which i s found in proximal and saggital portions of the t a i l . If i t did, the sample was discarded and another obtained. The sample was weighed on an Ohaus "505" balance scale to the nearest one hundreth of a gram and preserved in 95% ethanol. Percentage fat determinations were performed by Coast Eldridge Engineers and Chemists Ltd. Vancouver. 14 The height of the columnar c e l l s in the f o l l i c u l a r epithelium of the thyroid gland i s the standard index used in assessing thyroid a c t i v i t y in f r e s h l y - k i l l e d mammals. However, in the present study i t was often impossible to process specimens u n t i l they had been dead for several hours. The resultant breakdown of c e l l structure precluded the use of h i s t o l o g i c a l techniques in assessing thyroid a c t i v i t y . Instead, thyroid gland weight was used as an index of thyroid a c t i v i t y . The method i s rather insensitive, but there i s a very good cor r e l a t i o n between gland weight, height of f o l l i c u l a r epithelium and thyroidal uptake and release of radio-active iodine (Greer, 1959; Hoffman and Kirkpatrick, 1960; Hoffman and Robinson, 1966; Keating et a l . , 1945; Schockaert, 1932). The thyroid gland of each specimen was excised and weighed to the nearest tenth of a gram. The indices of body fat and thyroid a c t i v i t y used in t h i s study are dependent on weights of fat depots and the thyroid gland respectively. This necessitated the standardization of weights to permit comparisons between animals d i f f e r i n g in body weight. The usual method of standardizing t h i s type of data i s to express the measure-ments r e l a t i v e to body weight. However, i t was found that body weight could not be used for this purpose due to the extremely variable body fat content. The weight of the heart varies a maximum of 3% with extreme changes in body 15 fat content (Kleiber, 1961), and presumably bears a simple r e l a t i o n s h i p to lean body mass. It was decided to standardize f a t depot and thyroid weights by expressing them in units per unit heart weight. The graphs of seasonal changes in growth, fat content and thyroid weight are composite in nature in that each point on a given graph represents a d i f f e r e n t animal. This presents a problem, esp e c i a l l y in the case of the growth curves. There i s considerable v a r i a t i o n in the growth of individuals within a population due to both genetic and environmental factors. It i s the magnitude of the variation that determines the degree of confidence that can be placed in a composite curve. The v a r i a t i o n in t o t a l body weight and t o t a l body length i s small to three years of age. Total weight v a r i a t i o n increases beyond that point but t o t a l length v a r i a t i o n remains small. V i s c e r a l organ weight data are p a r t i c u l a r l y variable, with only the f i r s t two years of growth s u f f i c i e n t l y uniform to project a recognizable pattern. The graphs of f a t content and thyroid weight are constructed on the basis of indices which r e f l e c t only physiological states in the organism, and thus are not precise quantitative measures. As a r e s u l t less v a r i a t i o n i s expected within samples, and such i s found to be the case. Plant samples col l e c t e d for proximate analysis and bomb calorimetry were weighed, a i r - d r i e d and weighed again. The loss of moisture was recorded and the samples were sealed 16 in p l a s t i c bags. In the laboratory they were dried in an oven for two hours at 95°C, and thus their t o t a l moisture content was determined. Nitrogen content was determined by the macro-Keljdahl technique and the crude protein calculated by multiplying the nitrogen figure by 6.25. The c a l o r i c content of plant samples was determined with a Gallenkamp automatic adiabatic bomb calorimeter (A. Gallenkamp & Co. Ltd., Christopher St., London, E.C.2). The methods used were those of the Association of O f f i c i a l A g r i c u l t u r a l Chemists (1965). A l l curves were f i t t e d to the data by hand, with one exception. A l i n e was f i t t e d to the data in Figure 13 by a stepwise regression analysis. 1 7 Results Seasonal Food Considerations This study i s based on the premise that food a v a i l a b i l i t y i s limited from October to May inclusive, and e s s e n t i a l l y unlimited from June to September inclusive. It i s v i r t u a l l y impossible to obtain a d i r e c t quantitative measure of environmental food a v a i l a b i l i t y . Observations or evidence of feeding a c t i v i t y were recorded to provide at least limited information about food u t i l i z a t i o n in r e l a t i o n to a v a i l a b i l i t y . Upon f i r s t emerging from winter confinement the beaver feeds largely on the bark of willow (Salix spp.,) and to a lesser extent on that of poplar (Populus balsamifera) and alder (Alnus c r i s p a ) . With the onset of plant growth in the t h i r d week of June there i s a major s h i f t in food habits. U t i l i z a t i o n of bark ceases, and the animals consume primarily the leaves and the succulent apical portions of willows and to some extent poplar. Young-of-the-year observed in c a p t i v i t y use the leaves exclusively. This continues u n t i l late August when bark i s reverted to as the major food material. The use of herbaceous plants on the Mackenzie Delta appears to be ne g l i g i b l e , although a number of scattered instances were observed. Food-storing a c t i v i t i e s commence in the second week of August and continue into September. Willow, poplar and 18 TABLE I. Composition of beaver food caches. Caches #1 and #2 were analyzed on 30 August 1965; the remainder were analyzed in early September, 1966 The figures refer to the number of stems in a given cache. Diameter Willow Poplar Alder (inches) 0-1 1-2 2 -3 0-1 1 -2 2-3 3 -4 0-1 1 -2 Cache #1 80 46 6 7 7 1 1 13 8 Cache #2 53 45 0 2 2 1 1 5 6 Cache #3 348 101 3 150 71 6 6 63 15 Cache #4 428 157 18 2 2 0 0 56 16 Cache #5 256 83 0 29 1 0 0 15 15 Total Stems 1624 288 212 Mean per Cache 325 58 42 19 alder saplings are cut and stored in a discrete food cache below the surface of the water in front of the lodge. Table I gives the r e s u l t s of the analysis of the species composition of f i v e food caches. Willow i s the predominant plant used. The bark of the stored saplings i s consumed from freeze-up to break-up. Novakowski (1965) states that stems less than two inches in diameter are consumed e n t i r e l y . In the present study careful examination of the area in front of the lodge suggested that t h i s i s not the case on the Mackenzie Delta. Numerous stems as small as one-quarter inch in diameter with the bark chewed o f f were found on lake and stream bottoms around lodges. This was es p e c i a l l y evident in cases where water le v e l s had receded due to drainage, thus exposing the lake or stream bottom. In late A p r i l or early May, one month before break-up, there i s a second food-gathering period. Approximately h a l f of the colonies emerge at that time through holes chewed in the ice and cut saplings which are removed beneath the ice. This behaviour pattern p e r s i s t s for approximately one week. The beavers then retreat below the ice once more and presumably consume the bark of the newly-cut saplings u n t i l break-up. The occurrence of spring food-gathering a c t i v i t y suggests that some of the colonies deplete th e i r food caches prior to break-up. 20 TABLE II. Moisture content, protein content, c a l o r i c density and protein to c a l o r i e r a t i o s of plants used as food by the beaver. W.B. = Wet Basis; D.B. = Dry Basis. % Moisture % Protein Caloric Density P:C Ratio (Calories/Gram) (mgm/Cal.) Poplar W.B. D.B. W.B. D.B. Leaves 65.6 4.5 13. 2 1.614 4.693 28. 1 Twigs 56. 2 2.6 6. 0 2. 265 5. 172 11.5 Bark 49.4 1.9 3.8 2.521 4. 983 7.6 Willow Leaves 66.1 5.3 18.4 1. 364 4.579 40. 0 Twigs 56. 7 2.1 4. 9 2. 141 4. 944 10.0 Bark 51.3 1. 9 3.8 2. 399 4. 925 7.8 Alder Leaves 70.5 7.5 19.5 1.414 4. 793 40. 6 Twigs 59.1 4.0 9. 7 2.132 5. 212 18. 7 Bark 50.0 4.6 8.6 2. 930 5.436 15. 9 As well as d i f f e r i n g in a v a i l a b i l i t y between winter and summer, food may change in qual i t y with season due to the change in food habits. It has been demonstrated that the protein to c a l o r i e r a t i o in the diet of mammals and birds i s an important q u a l i t a t i v e factor. Mackenzie(1964) showed that a decreased r a t i o causes reduced growth and increased f at deposition in the rat, and Pastro(1965) found that a decreased r a t i o r e s u l t s in reduced growth and reduced thyroid a c t i v i t y in the chick. Therefore the protein to c a l o r i e r a t i o in the die t i s espe c i a l l y pertinent to thi s study since the three major parameters in use are growth, body f a t content and thyroid a c t i v i t y . Proximate analysis and bomb calorimetry were performed on the major winter and summer foods (Table I I ) . The major summer foods, willow and poplar leaves, have r a t i o s of 40.0 milligrams protein per Calorie and 28.1 mgm./Cal., while the major winter foods willow and alder bark, have r a t i o s of 7.8 mgm./Cal. and 15.9 mgm./Cal. Summer r a t i o s are approximately three times as large as winter r a t i o s . The willow leaf, the predominant summer food of immature beavers, has a r a t i o that i s f i v e times larger than that of willow bark, the predominant winter food. Thes seasonal differences may or may not have an eff e c t on the metabolism of the beaver, but i t i s important to be aware of them when considering seasonal changes in growth, fat content and thyroid a c t i v i t y . 22 Growth Dynamics Figs. 3 and 4 depict the t o t a l weight and skel e t a l growth curves of the Mackenzie Delta beaver. In both cases the curve r i s e s r a p i d l y to 40 months of age and then very slowly to s e n i l i t y . Growth occurs throughout l i f e and no asymptote i s apparent. Forty months, the point at which the sharp break occurs in the curve, can be considered the age at which the beaver reaches mature body weight and size. No sexual dimorphism was evident in growth, and therefore data from males and females can be pooled. The growth curves of heart and kidney to maturity are presented in Figs. 5 and 6. Pronounced seasonal o s c i l l a t i o n s are present in a l l cases, growth being rapid during the summer and absent during the winter. Growth begins in June and ceases in October. There i s a considerable drop in body weight between December and May. This seasonal type of growth has been observed in the beaver in Alaska (Buckley and Libby, 1955), Saskatchewan (Pearson, 1960), New York (Buckley and Libby, o p . c i t . ) , Maine (Hodgdon and Hunt, 1953) and Alberta (Novakowski, 1967) . Buckley and Libby (op.cit.) indicate that winter growth does occur in Alaska, but at a much slower rate than summer growth. Novakowski (op.cit.) suggests that one and two-year-olds grow throughout the winter, whereas older individuals do not. Data from the extreme southern portion of the species 23 Figure 3. Total weight growth curve to s e n i l i t y . T O T A L WEIGHT IN KILOGRAMS O 24 Figure 4. Skeletal (total length) growth curve to s e n i l i t y . 25 Figure 5. Heart growth to maturity. 26 Figure 6. Right kidney growth to maturity. 27 d i s t r i b u t i o n are not available; a l l populations for which data are available experience a winter of ice and snow cover. Pearson (op.cit.) reported that in what he considered high-q u a l i t y habitat beavers in Saskatchewan grew throughout the winter, though slower than during the summer, while beavers in low-quality habitat l o s t weight during the winter. A close examination of h i s data revealed that he had i n s u f f i c i e n t data for the growth curve of beavers on high-quality habitat to support h i s hypothesis. Indeed, when he kept juvenile beavers in confinement and fed them a well-balanced d i e t ad  libitum, they ceased to grow in mid-winter. That finding appears to inva l i d a t e his statement regarding d i f f e r e n t i a l winter growth patterns in habitats of varying quality, and strongly suggests that the absence of winter growth i s an inherent a t t r i b u t e of the animal. When the t o t a l weight growth curve of the Mackenzie Delta beaver i s compared to that of the Saskatchewan beaver presented by Pearson (op.cit.), i t i s observed that the weights attained by a given age class at the end of each summer are very s i m i l a r . The period during which growth occurs, however, i s abbreviated on the Mackenzie Delta. The summer growth rate on the Mackenzie Delta i s approximately twice that obtained in Saskatchewan, while the winter weight loss i s only s l i g h t l y greater (Table I I I ) . Therefore the animals in the northern portion of the range grow more ra p i d l y TABLE III. Comparison of average absolute growth rates of Mackenzie Delta and Saskatchewan beavers. Growth rates are expressed in kilograms per day. Growth rates of Saskatchewan beavers were calculated from data presented by Pearson (1960). Mackenzie Delta Saskatchewan One-year-olds Summer Winter 0.076 -0.008 0.032 -0.006 Two-year-olds Summer Winter 0.055 -0.008 0.033 -0.007 29 in the summer but for a shorter period than do those in the central portion, r e s u l t i n g in approximately comparable adult dimensions. On a purely t h e o r e t i c a l basis one might expect that environmental conditions in the north would r e s u l t in a smaller body size, or in a prolonged period of immaturity. However, such i s not the case. The average body weight of mature individuals was found to be between 18 and 23 kilograms, which i s similar to that found in Alberta by Novakowski (op.cit.) and in Saskatchewan by Pearson (op.cit.), 21 kilograms and 18 to 23 kilograms respectively. Also, Novakowski found that beavers in Alberta attained mature body dimensions at four years of age, which i s similar to the si t u a t i o n on the Mackenzie Delta. Unfortunately, data are not available from the southern portion of the beaver's d i s t r i b u t i o n . A comparison of the data presented here with those presented by Novakowski i s not very meaningful since the winter energy r e s t r i c t i o n in northern Alberta i s similar to that on the Mackenzie Delta. The general finding that beavers in the p r a i r i e provinces and those on the Mackenzie Delta attain comparable weights at given ages, even though the length of the period when growth occurs varies between the two latitudes, can be explained as follows. Mammals are known to possess a great capacity for compensatory growth (Wilson and Osbourn, 1960). Given a r e s t r i c t i o n in growth in the juvenile stage, the retardation i s r e a d i l y compensated for by extraordinarily rapid growth when s u f f i c i e n t food i s made available (Osborne 30 Figure 7. Quantitative changes in fat depots in r e l a t i o n to season i n immature individuals. SPLENIC FAT WEIGHT PERIRENAL FAT WEIGHT IN MGM. PER IN MGM. PER SUBCUTANEOUS GM. HEART WEIGHT GM. HEART WEIGHT FAT INDEX 31 and Mendel, 1914; Jackson, 1937; Saxton and Silberberg, 1947). Osborne and Mendel (1915) state that even i f growth i s repressed for a long time the capacity to grow i s not necessarily l o s t at the end of the period at which growth o r d i n a r i l y ceases in any species. Stewart (1916) found that juvenile rats stunted by limited food intake were able on refeeding to overtake the f u l l - f e d controls before the end of the normal growth period. The beaver at northern l a t i t u d e s i s evidently able to compensate for the growth l o s t during the prolonged winter by growing very r a p i d l y during the summer and thus attains a body weight commensurate with that of southern animals of a comparable age at the end of the short growing season. The exact pattern of winter weight loss i s unknown due to a paucity of data from that period. The most l a b i l e component of the mammalian body i s the f a t content. Given a negative energy balance, depot f a t i s mobilized to meet the d e f i c i t . S i g n i f i c a n t losses in the n o n - l i p i d components occur only in cases of extreme and prolonged energy r e s t r i c t i o n s . It was observed that a limited amount of depot f a t was present in the spring, while abundant depot fat was present in the autumn. This strongly suggests that the winter weight loss was due to the mobilization of fat reserves. 32 Figure 8. Seasonal changes in percent f a t in t a i l t i ssue of immature individuals. 33 Figure 9. Relationship between percent f a t and percent water in t a i l tissue of the beaver. 34 Pat Deposition and Mobilization Fig. 7 depicts seasonal weight changes in splenic, pe r i r e n a l and subcutaneous f a t depots in immature beavers. A l l three patterns are b a s i c a l l y the same. Animals are lean during the summer, deposit f a t in the autumn, remain obese a l l winter and mobilize fat rapidly in the spring. Mammals deposit f a t as a neutral t r i g l y c e r i d e primarily in coelomic and subcutaneous fat depots. Therefore these curves represent the pattern of deposition and mobilization of the major portion of the storage f a t in the body of the beaver. The t a i l of the beaver was studied as a possible fa t depot. A pronounced seasonal pattern in t a i l f a t content emerges that correlates well with that of known fat depots (Fig. 8). The magnitude of the change in percentage t a i l f a t , 51.5% between spring and autumn, i s considerable. T a i l f a t content i s low in the la t e spring and summer, increases in the autumn, i s high during the winter and decreases at some point in the late winter or early spring. This annual cycle together with the magnitude of change between summer and winter f a t le v e l s i s good evidence that the t a i l functions as a fat depot. Hausberger (1965) presents data on the r e l a t i v e proportions of the water, l i p i d and residue components of the epididymal f a t depot of the laboratory r a t . The 35 percentage of these components in controls were 10%, 88% and 2.0% respectively, while in starved rats they were 78.9%, 3.5% and 17. 6% respectively. Comparable figures for the t a i l tissue of the beaver are 29.9%, 63.7% and 6.4% in the autumn, and 87.7%, 6.7% and 5.6% in the spring. The proportions of the components in obesity and the subsequent change with leanness agree clo s e l y with those in the epididymal f a t depot of the obese and lean r a t . Fi g . 9 depicts the re l a t i o n s h i p between percentage t a i l f a t and percentage t a i l water in the beaver. T a i l volume was measured during the various seasons (Fig. 10), as i t was thought that the t a i l might swell with obesity and shrink with leanness. A d e f i n i t e annual cycle with a pattern similar to that of percentage t a i l fat is obtained. The magnitude of change from summer to winter i s two-fold. Therefore, as well as changing substantially in percentage f a t content, the t a i l swells and shrinks seasonally. The r e l a t i o n s h i p between percentage t a i l f a t content and r e l a t i v e t a i l volume i s presented in Fig. 11. It suggests that the t a i l increases in volume only after the percentage fat content of the tissue has reached approximately 50%, a point near i t s maximum in immature animals, and thus that the t a i l swells to accommodate f a t after the tissue becomes saturated. L i e b e l t (1963) found that new fat c e l l s are added 36 Figure 10. Seasonal changes in t a i l volume r e l a t i v e to heart weight in immature ind i v i d u a l s . 37 Figure 11. Relationship between t a i l f a t and t a i l volume. o PERCENT TAIL FAT ro O CO O T o O T o O ro -> r m O a m > _ 2 z 1 c 5 « CP -$ n -m m O I Z! m H m on ro 38 to a f at depot only after a saturation l e v e l in f a t content for the c e l l s present at the onset of obesity has been reached. Indications are that t h i s occurs in the t a i l tissue of the beaver. Therefore in a l l aspects studied the t a i l of the beaver behaves l i k e a f a t depot. A close examination of the annual cycles of the d i f f e r e n t fat depots studied indicated temporal differences between them. The various fat indices were plotted against each other to determine whether p r i o r i t i e s for fat deposition exi s t among them. A d e f i n i t e pattern of p r i o r i t i e s became evident (Figs.12 and 13). The order of deposition i s t a i l fat, subcutaneous f a t and coelomic (splenic and perirenal) fa t . The order of mobilization i s the reverse of the order of deposition. Shafrir and Wertheimer (1965) state that generally intraperitoneal f a t depots are more active in response to adipokinetic agents, such as epinephrine and c o r t i c o t r o p i n , than are subcutaneous f a t depots. This order of mobilization would seemingly be adaptive in mammals at northern lat i t u d e s in view of the i n s u l a t i v e value of subcutaneous f a t . There i s a general paucity of data on annual fat cycles of non-hibernating rodents. The hibernators deposit depot fat in the l a t e summer and autumn, and are obese when they enter hibernation (Lyman and Chatfield, 1955). The fat 39 Figure 12. Relationship between percent t a i l f a t and subcutaneous f a t . 70 60 50 I— • 2 40 < h- 30 z l±J u cr LU 20 10 J— I I I L I 2 3 4 5 SUBCUTANEOUS FAT INDEX 40 Figure 13. Relationship between splenic f a t and subcutaneous f a t . I40r o LLl I20 or < LLl I IOO 5 CE LU CL 80 5 X LU < li_ 60 40 5 20| CL (J) I. I ! j_ _L SUBCUTANEOUS FAT 4 INDEX 41 i s used as the major source of energy during the hibernating period, and the animal i s lean when i t emerges in the spring. The annual f a t cycle of the beaver i s similar to that of hibernating rodents, with the difference that the beaver appears to maintain i t s fat reserves throughout the winter and then mobilizes them rather rapi d l y in the spring. Krebs (1965) found that lemmings (Lemmus  trimucronatus and Dicrostonyx groenlandicus) at Baker Lake contain less f a t during the summer than they do during the winter, but the difference between summer and winter lev e l s was not great. Indeed, the lemmings did not appear to be obese at any time. M i l l e r (pers. comm.) found that the red s q u i r r e l (Tamiasciurus hudsonicus) in B r i t i s h Columbia likewise does not store a substantial amount of fat, and that there i s no apparent difference between summer and winter l e v e l s . Didow (pers. comm.) found only a s l i g h t increase in the white adipose tissue mass of Microtus during the winter months in Alberta. In contrast with these other species of non-hibernating rodents the beaver i s characterized by a pronounced seasonal pattern of fat content. Thyroid A c t i v i t y Thyroid a c t i v i t y as r e f l e c t e d by r e l a t i v e thyroid weight i s very high in the young-of-the-year, decreases steadily to maturity and thenceforth remains at a A 2 c o n s i s t e n t l y low l e v e l (Fig. 14). Sexual differences were not evident i n the data. This age-related pattern of thyroid a c t i v i t y i n the beaver conforms with the pattern generally displayed by mammals. Gorbman et a l . (1952), using various measures,- found that the thyroid a c t i v i t y of the near-term bovine fetus far exceeded that of the pregnant cow from which i t was obtained. Thyroxine secretion rates per unit body weight are higher i n juveniles than i n adults i n mice (Hurst and Turner, 1947), laboratory rats (Grad and Hoffman, 1955; Kumausan and Turner, 1967; Narang and Turner, 1966) and the opossum (Didelphis marsupialis) (Bauman and Turner, 1966) . Bauman et a l . (1965) found that the b i o l o g i c a l h a l f - l i f e of L-thyroxine to be shorter i n the juvenile raccoon (Procyon lotor) than i n the adult. Haensley et a l . (1964), working with dogs, found that r e l a t i v e thyroid weights decreased with age to one year and then stayed at a low l e v e l to s e n i l i t y . The general decrease i n thyroid a c t i v i t y with age to maturity i s undoubtedly associated with growth and maturational processes. There i s an extreme seasonal pattern of thyroid a c t i v i t y superimposed on the age-related pattern i n young beavers. The exact pattern of change i n a c t i v i t y i s d i f f i c u l t to ascertain due to the composite nature of \ the graph, but i t i s evident that a c t i v i t y i s low i n the 43 Figure 14. Changes in r e l a t i v e thyroid weight with time to s e n i l i t y . THYROID WEIGHT IN MGM. PER GM. HEART WEIGHT 44 early spring, high during the summer and on the decrease i n the autumn. I t i s assumed that a c t i v i t y i s low throughout the winter i n view of the low values found i n the late autumn and early spring. The pattern becomes more obvious when a single age group i s chosen and th e i r r e l a t i v e thyroid weights plotted against an expanded time scale (Fig. 15). Each spring the r e l a t i v e thyroid weights of immature indi v i d u a l s are approximately those of adults (Fig. 14), while each summer they decrease progressively to maturity. The apparent decrease i n the autumn and the low value (approximately the adult value) i n the spring i n the f i r s t three years of l i f e indicates a return to some constant state during the winter. It suggests that during the winter there i s an i n h i b i t i o n which blocks the expression of a l e v e l of a c t i v i t y c h a r a c t e r i s t i c of a given age. The i n h i b i t i o n apparently does not e x i s t during the summer and the c h a r a c t e r i s t i c l e v e l of a c t i v i t y for a given age i s expressed. The question arises at this point as to whether the observed vernal increase i n thyroid weight i s a manifestation of a goitrogenic state i n the animal. I t i s t h e o r e t i c a l l y possible that a change i n food habits i n the spring i s accompanied by a greatly reduced iodine intake by the beaver. However, thyroidal hyperplasia begins p r i o r to the change i n food habits, which precludes such a p o s s i b i l i t y . Secondly, i f the hyperplasia were 45 Figure 15. Seasonal changes in r e l a t i v e thyroid weight in yearlings. 46 due to a decreased iodine intake, i t should occur i n adults as well as i n immature i n d i v i d u a l s . I t does not (Fig. 14). Therefore i t i s extremely u n l i k e l y that the observed vernal hyperplasia of the thyroid i s due to a goitrogenic state. Thyroid a c t i v i t y i n the non-hibernating rodents investigated by others i s high during the winter r e l a t i v e to that during the summer (Berstein, 1941; Hoffman and Kirkpatrick, 1960; El e f t h e r i o n and zarrow, 1962; Hoffman and zarrow, 1958). The increased thyroid a c t i v i t y during the winter i s presumably linked with increased thermoregulatory demands with the advent of the cold season. The metabolic response of mammals to cold i s not controlled by the thyroid, as i t p e r s i s t s a f t e r thyroidectomy (Leblond and Gross, 1943; Sahovic and Popovic, 1953, ref e r r e d to i n Popovic, I960), but the thyroid plays a r o l e i n the maintenance and e f f i c i e n c y of the response (Boatman, 1959; Ershoff, 1948; Woods and Carlson, 1956; Ring, 1942; S e l l e r s , 1957; S e l l e r s and You, 1950). Hibernators display an annual pattern of thyroid a c t i v i t y which i s the reverse of that i n non-hibernators, a c t i v i t y during the summer being high r e l a t i v e to that during the winter (Hoffman and zarrow, 1958; Vidovic and Popovic, 1954). The beaver, a non-hibernator, possesses the hibernator pattern of 47 thyroid a c t i v i t y . A r t i f i c i a l cold exposure causes a hypertrophy of the thyroid gland in non-hibernators (Stevens et a l . , 1955; Rand et a l . , 1952; Deane and Lyman, 1954), but not in hibernators (Hoffman and Zarrow, op c i t . ; Foster et a l . , 1939). In fact, Knigge (1957) found that with cold exposure f o l l i c u l a r c e l l height of the thyroid decreased in the golden hamster (Mesocricetus auratus), a hibernator. Recently, Tashima (1965) showed that although cold exposure does not increase f o l l i c u l a r c e l l height in the hamster, i t does increase the uptake of I^"*" 131 by the thyroid, the PBI conversion r a t i o and the rate 131 of disappearance of the injected thyroxine-I . Tashima's r e s u l t s question the previously generally accepted theory that the thyroid gland of active hibernators i s unresponsive to cold exposure. However, i t i s possible that the magnitude of the response i s much smaller than that in non-hibernators. That i s , the upper and lower l i m i t s of thyroxine secretion rates in warm and cold environments might be very narrow in active hibernators. Such a contention i s strongly supported by the general finding that c e l l u l a r hypertrophy in the thyroid i s not observed upon cold exposure. Perhaps some unknown factor overrides the e f f e c t of reduced . temperatures, which might be minimal. A comparison of thyroxine secretion rates in cold-exposed hibernators 48 and non-hibernators would help to c l a r i f y the s i t u a t i o n . The data obtained in t h i s study indicate that the beaver, l i k e the hibernating rodents, does not show a major increase in thyroid a c t i v i t y in response to the low temperatures of winter, and thus represents a departure from the c h a r a c t e r i s t i c response displayed by non-hibernating rodents. 49 Discussion This study i s based on the premise that the eight-month r e s t r i c t i o n to the under-ice environment i n the north has represented a period of low energy a v a i l a b i l i t y to the beaver during the course of i t s evolution, and that the remaining four months of open water represented a period of e s s e n t i a l l y unlimited energy a v a i l a b i l i t y . The working hypothesis about which the study i s oriented i s that there i s a s h i f t of metabolic energy expenditure from winter to summer i n the beaver at northern l a t i t u d e s . The data presented i n the r e s u l t s support this hypothesis e Growth i n immature animals was found to be rapid i n the summer and absent i n the winter. Winter thyroid a c t i v i t y i s low r e l a t i v e to summer thyroid a c t i v i t y . The absence of body f a t during the summer indicates that energy expenditure i s equal to energy intake at that time. The maintenance of large f a t reserves during the winter indicates that energy expenditure during that period i s less than or equal to energy intake. A low l e v e l of metabolic a c t i v i t y , as r e f l e c t e d by growth, thyroid a c t i v i t y and f a t content, obtains throughout the winter r e l a t i v e to that which occurs during the summer. Growth and thyroid a c t i v i t y are most revealing i n this respect. Growth i s a d i r e c t measure of synthetic a c t i v i t y i n the body; i t s cessation during the winter means thi s aspect of metabolism i s depressed. Thyroid a c t i v i t y i s an i n d i r e c t 50 but excellent indication of the l e v e l of general body metabolism. The observed winter depression in thyroid a c t i v i t y r e f l e c t s a depression in general body metabolism. Metabolic a c t i v i t i e s as r e f l e c t e d by these parameters are high during the summer. The available evidence indicates that the observed annual metabolic pattern i s an inherent property of the beaver rather than a n u t r i t i o n a l l y induced state. A growth depression can be n u t r i t i o n a l l y induced in mammals in two ways. F i r s t l y , i t can be a r e s u l t of a quantitative reduction in accessible energy. Reduction i n a c c e s s i b i l i t y r e s u l t s in a reduction in intake or in a greater expenditure of energy in obtaining food. In either case less energy i s available within the organism for b i o l o g i c a l processes other than maintenance. The growth of an animal can be reduced or terminated e n t i r e l y by experimental reduction in food intake. There are two reasons why t h i s i s not a possible explanation of the winter cessation of growth in the beaver. The food i s stored in a very discrete cache within easy reach of the animal and i s in fac t r e a d i l y accessible, yet the animal apparently reduces i t s food intake considerably in the autumn. Furthermore, the observed growth depression cannot be due d i r e c t l y to a lack of energy since there i s an abundant supply of energy in the form of f a t in the animal during the winter. 51 A second way in which a growth depression can be n u t r i t i o n a l l y induced i s by a reduction in food qua l i t y . The q u a l i t a t i v e factors of importance in t h i s respect are numerous. Vitamin d e f i c i e n c i e s , mineral d e f i c i e n c i e s , amino acid imbalance and low prote i n : c a l o r i e r a t i o s a l l have deleterious effects on growth. It was demonstrated that the pro t e i n : c a l o r i e r a t i o s in winter foods of the beaver are only 1/5th to l/3rd of those in summer foods. As well as having an e f f e c t on growth, a reduced protein: c a l o r i e r a t i o has been shown to decrease thyroid a c t i v i t y and produce a state of obesity (Pastro, 1965 and Mackenzie, 1964). Therefore, i t i s possible that the reduced r a t i o during the winter explains the. observed changes in growth, thyroid a c t i v i t y and body f a t content. However, upon examination of the time r e l a t i o n s between the observed e f f e c t and the possible cause i t becomes evident that such an explanation i s i n v a l i d . Body f a t i s mobilized long before the r a t i o increases in the spring, and thyroid a c t i v i t y also increases p r i o r to the change in the r a t i o . Furthermore, Stephenson (1956) and Pearson (1960) found that when they held juvenile beavers in c a p t i v i t y on a well-balanced d i e t fed ad libitum, growth ceased in October and January respectively. This argument strongly suggests that the observed seasonal changes are not n u t r i t i o n a l l y induced but are 52 instead inherent. A number of juvenile beavers from the study area must be studied under laboratory conditions and on a constant rat i o n before t h i s conclusion can be accepted with complete confidence. The l e v e l of metabolic a c t i v i t y and therefore metabolic energy expenditure p a r a l l e l s the l e v e l of environmental energy a v a i l a b i l i t y . Energy expenditure i s high during the summer when energy a v a i l a b i l i t y i s e s s e n t i a l l y unlimited and low during the winter when the amount of available energy i s limited to that in the food cache, an amount that must sustain the animals throughout the winter. This relat i o n s h i p , however, i s not a d i r e c t one in that environmental energy a v a i l a b i l i t y per se does not control the l e v e l of energy expenditure. Instead, an inherent physiological mechanism apparently exists in the beaver which controls energy expenditure in such a manner that i t coincides with the l e v e l of a v a i l a b i l i t y . Energy expenditure i s reduced in the autumn as i f in an t i c i p a t i o n of the reduced quantity of energy that i s available during the winter. The exact nature of the annual pattern of metabolic a c t i v i t y that can be deduced from the available data i s minimal. Only a general, and quite s u p e r f i c i a l , understanding of the annual sequence of events can be achieved at t h i s stage of the study. In the autumn there 53 i s an i n h i b i t i o n which r e s u l t s in a metabolic depression, examplified by the absence of growth and a low l e v e l of thyroid a c t i v i t y . Food intake i s low at t h i s time owing to the reduced energy expenditure which r e s u l t s from the metabolic depression. Those conditions p r e v a i l throughout the winter. The i n h i b i t i o n i s removed in the spring, allowing a l e v e l of metabolic a c t i v i t y to be expressed during the summer which i s at or near the genetic maximum of the animal. Growth i s rapid, thyroid a c t i v i t y i s high and food intake i s undoubtedly high. The functioning of the system i s analogous to that of seasonal hibernation. It i s not suggested that the beaver i s unique among non-hibernating rodents in t h i s type of adaptation, although i t might be. However, the data do suggest a high order of adaptation to seasonally f l u c t u a t i n g energy regimes that apparently has previously not been observed among non-hibernators. Reduction of growth in response to reduced food intake and subsequent ex t r a o r d i n a r i l y rapid growth with unlimited food a v a i l a b i l i t y i s a widespread phenomenon among homeotherms (Wilson and Osbourne, op. c i t . ) and might be considered an adaptation to changing energy conditions. The beaver has adapted further through the evolution of an inherent mechanism that controls energy expenditure in such a manner that 54 i t coincides with the l e v e l of energy a v a i l a b i l i t y . The normal sit u a t i o n in immature mammals i s that growth occurs i f s u f f i c i e n t food can be obtained on a d a i l y basis. If i t cannot, growth ceases at least temporarily. It i s evident that the beaver can obtain s u f f i c i e n t food from i t s cache to continue growing in the autumn, since the cache i s in close proximity to the lodge and r e a d i l y accessible. However, t h i s would possibly lead to the depletion of the cache early in the winter. The storage of a l i m i t e d quantity of food i s believed to be the c r i t i c a l factor in the evolution of a seasonal pattern of energy expenditure beyond the r e l a t i v e l y simple phenomenon of compensatory growth. The adaptive value of and selection for a seasonal pattern of energy expenditure at northern latitudes i s clear. The beaver stores a quantity of food in the autumn and depends exclusively on t h i s food store for i t s energy demands during the winter. No other source i s r e a d i l y available. If the store i s depleted p r i o r to spring, the most probable consequence i s death by starvation or freezing. Conceivably the animals could cut through the ice and c o l l e c t more food, as indeed some do in the spring, as discussed e a r l i e r . Such a behaviour pattern f i r s t l y exposes the animals to predation. Secondly, winter food-gathering a c t i v i t y would be bioenergetically 55 i n e f f i c i e n t due to a i r temperatures which are often as low as -45°Centigrade. The beaver i s seldom exposed to a i r temperatures below freezing. At a i r temperatures of -45°C, lodge temperatures are approximately -4°C i f the lodge i s abandoned and approximately +3°C i f i t i s occupied (Miller, 1966) . Exposure to a i r temperatures of -45°C would involve a great expenditure of energy for thermoregulation and would probably r e s u l t in the death of the animal. The feet and t a i l are largely devoid of hair, and thus are apparently subject to freezing. Furthermore, the beaver i s not adapted to locomotion through the soft deep snows of winter; at the time of the spring emergence the snow has become compacted by high temperatures and generally supports the weight of a beaver. Therefore winter emergence for the procurement of food could r e s u l t in a high mortality rate of such individuals and thus strong selection against them. The adaptive value of the reduction of energy expenditure during the winter i s one which increases the p r o b a b i l i t y that the food store w i l l sustain the colony throughout the winter. The higher s u r v i v a l rate of individuals that showed reduced winter energy requirements over those that did not would rapidly r e s u l t in a predominance of the former type of i n d i v i d u a l . Novakowski (op.cit.) studied the energetics of the beaver in r e l a t i o n to i t s winter food supply in northern Alberta. His calculations revealed that when the energy 56 in the stored food i s compared to the energy requirements of the colony, three of the f i v e colonies studied showed a d e f i c i t while the remaining two did not. When the energy stored in the form of f a t was taken into consideration, only one colony showed a d e f i c i t , and that colony was believed to forage during the winter. The findings of the present study indicate that the two basic assumptions on which Novakowski based his analysis may be in error. F i r s t l y , he assumed that stems less than two inches in diameter are consumed in their entirety. I found no evidence for t h i s on the Mackenzie Delta and question the v a l i d i t y of the assumption. Therefore, he may have vastly overestimated the portion of the energy in the cache which i s available to the colony. Secondly, he calculated the energy requirements of the beaver on the basis of the formula B.M.R. = 70 k c a l . per 3/4 power of the body weight in kilograms. This i s only a calculation of basal requirements and does not take into consideration energy expended through mechanical work and other variables. More important, indications in the present study are that energy requirements are very low during the winter and indeed basal requirements might not follow the above formula. An analysis of the type attempted by Novakowski i s extremely d i f f i c u l t , largely due to the wide margins of error which characterize the various measurements. 57 Although l i t t l e information i s available, the t o t a l quantity of energy expended in one year by the beaver .in the northern portion of the species d i s t r i b u t i o n i s thought to be very similar to that expended in one year by i t s counterpart in the southern portion. It was pointed out e a r l i e r that growing individuals of a given age class on the Mackenzie Delta and in Saskatchewan achieve comparable body weights at the end of the short growing season. This i s the r e s u l t of a shorter growing period and higher growth rates in the north. Energy expended in such basic p h y s i o l o g i c a l processes as osmotic work, c e l l u l a r replacement, reproduction, and thermoregulation are probably comparable throughout the species d i s t r i b u t i o n . It might be argued that more energy i s required in the north for thermoregulation, but the under-ice microenvironment in the north protects the animal from excessively low temperatures, and therefore seemingly such i s not the case. The major difference in energy expenditure between the two extremes i s that in the north certain energy-demanding processes are compacted into a short summer while in the south they are more evenly spaced throughout the year. This is most c l e a r l y borne out by growth, largely because growth lends i t s e l f to measurement under f i e l d conditions. Logic a l l y , energy expended through mechanical work i s greatest during the open-water period. During t h i s period the beaver ranges 58 widely over i t s home range, constructs dams and lodges, digs burrows and canals, cares for young, maintains a t e r r i t o r y and gathers a winter food supply. During the winter i t i s sedentary, and therefore l i t t l e energy i s expended through mechanical work. In the southernmost portion of the d i s t r i b u t i o n ponds remain open throughout the year and these various a c t i v i t i e s need not be compacted into the summer period. A model constructed to depict postulated annual patterns of energy expenditure i n northern and southern beavers i s presented i n F i g . 16. Curves a, b, and c represent annual patterns of southern, intermediate and northern beavers respectively. Portions of b and c below a represent winter energy expenditure, while portions above a represent summer expenditure. There are no data on which to base a. The curve i s drawn on the th e o r e t i c a l consideration that seasonal changes are not great at southern l a t i t u d e s , at least i n terms of food a v a i l a b i l i t y , and thus i s hypothetical. The area under each curve i s approximately the same, which means that the t o t a l annual energy expenditure along the north-south axis of the d i s t r i b u t i o n i s constant. Such a model cannot be e n t i r e l y accepted u n t i l more data are available, e s p e c i a l l y for southern animals. The question dealt with next i s that of the physio-l o g i c a l mechanism that controls metabolic energy expenditure 59 Figure 16. A model depicting annual patterns of energy-expenditure i n the beaver at d i f f e r e n t l a t i t u d e s . Portions of b and c below a represent winter expenditure; portions above a represent summer expenditure. a b c Southern Beavers Intermediate Beavers Northern Beavers Summer Winter TIME OF YEAR 60 to make i t p a r a l l e l environmental energy a v a i l a b i l i t y . Although the thyroid hormones have numerous actions i n the mammalian body, perhaps the most conspicuous and pronounced one i s th e i r e f f e c t on the l e v e l of general body metabolism. Approximately 3 5% of the normal r e s t i n g heat production of the body i s a t t r i b u t a b l e to the e f f e c t s of thyroid hormones (Bard, 1961; p.787). Furthermore, i t has been conclusively demonstrated that the thyroid gland has a d i r e c t influence on the production of growth hormone by the anterior hypophysis (Scow, et a l . , 1949; Koneoff et a l . , 1949). Normal thyroid function i s a prerequisite for the production of growth hormone (Russel and Wilhelmi, 1958). Growth ceases i n the thyroidectomized r a t and resumes upon the administration of thyroxine or growth hormone, or both. Thus, presumably through i t s action on the metabolism of the p i t u i t a r y , the thyroid gland has a profound influence on the growth of mammals. It was demonstrated that thyroid a c t i v i t y i n the beaver i s very low i n the winter when growth i s absent and high i n the summer when growth i s rapid. Furthermore, i t was observed that thyroid a c t i v i t y and body f a t content are negatively correlated. The mobilizing e f f e c t of thyroid hormones on depot f a t i s well known (Gorbman and Bern, 1962; p.168). Food intake i s p o s i t i v e l y correlated with thyroid a c t i v i t y (Warkentin, Warkentin and Ivy, 1943); this i s undoubtedly associated with the thyroid's e f f e c t on body metabolism. 61 On the basis of the f i e l d observations and the known actions of the thyroid hormones i n the body, i t i s hypothesized that the thyroid gland i s the major i n t r i n s i c e ffector i n the winter growth depression and the general metabolic depression which apparently occurs. In terms of t h i s hypothesis the f i e l d observations can be explained as follows. In the autumn there i s a drop i n thyroid a c t i v i t y , with a consequent drop i n body metabolism and growth hormone production. Reduced growth hormone production r e s u l t s i n a cessation of growth and t h i s , together with the general reduction i n body metabolism, reduces energy expenditure i n the organism. Fat i s deposited i n f a t depots, due to the reduction i n energy expenditure and the reduced l e v e l of c i r c u l a t i n g thyroid hormones. Food intake i s reduced due to reduced energy requirements. Those conditions of low energy expenditure and low food intake p r e v a i l throughout the winter. Thyroid a c t i v i t y i s increased i n the spring and there i s a general reversal of the reduction process that occurred i n the autumn. Growth hormone production i s reinstated, metabolic rate i s increased, f a t i s mobilized from f a t depots due to increased energy demands and growth resumes. Food intake increases to meet increased energy requirements. This high l e v e l of metabolic a c t i v i t y p r e v a i l s throughout the summer. 62 The maintenance of large energy reserves in the form of depot fat during the winter would appear to be highly advantageous to the animal and strongly selected for, rather than simply an incidental factor r e s u l t i n g from reduced energy expenditure and reduced thyroid a c t i v i t y in the autumn. F i r s t l y , subcutaneous fat has excellent i n s u l a t i v e q u a l i t i e s and i s important in reducing heat loss at the reduced temperatures of winter. Secondly, and probably more important, i t represents a large ready source of energy in the spring when metabolic a c t i v i t i e s are increasing but energy a v a i l a b i l i t y in the environment i s not. Indeed, energy a v a i l a b i l i t y i s at i t s lowest point in the spring, since the bulk of the food cache i s u t i l i z e d during the course of the winter and. many colonies must emerge through holes cut in the ice to procure additional food. The summer season when environmental conditions permit a high l e v e l of metabolic a c t i v i t i e s i s very short, and the ready source of energy in the form of f a t would seemingly be valuable to the animal, permitting a high l e v e l of metabolic a c t i v i t i e s to begin immediately. F i n a l l y , the fat reserves are available to correct short term energy d e f i c i t s which might occur during the course of the winter, in t h i s way serving as emergency energy depots. The proposed inherent system must have an environmental c o n t r o l l i n g factor which synchronizes the annual sequence of 63 events with seasonal energy a v a i l a b i l i t y . The system might be an e n t i r e l y self-contained endogenous rhythm independent of environmental cues but t h i s was considered u n l i k e l y . In pa r t i c u l a r , some environmental variable must trigger the onset of the metabolic depression in the autumn and i t s cessation in the spring. Presumably i t i s a variable that changes with r e g u l a r i t y and consistency during the course of the year. The most conspicuous variable that changes with r e g u l a r i t y between winter and summer in cold climates i s temperature. Summer temperatures at the latitudes of the study area are commonly as high as 27°C, while winter temperatures are often,as low as -45°C. However, the beaver i s not subjected to t h i s range of temperature change, largely due to the creation of a microenvironment by the bui l d i n g of a lodge and the use of burrows. Lodge temperatures during the winter are above freezing, as discussed e a r l i e r (Miller, op.cit. and Novakowski, o p . c i t . ) . Ice prevents the beavers from being subjected to a i r temperatures when the animals swim about in the water in front of the lodge. Although summer lodge temperatures are unavailable, they are undoubtedly prevented from approaching a i r temperatures outside by the insu l a t i v e walls. The beaver i s of course often exposed to a i r temperatures during the summer, but i t i s generally active at night when 64 temperatures are low. Furthermore, temperatures in the autumn and spring, when the animal is entering into and emerging from the depressed state respectively, are comparable. Therefore i t i s highly unlik e l y the temperature i s the c o n t r o l l i n g factor. A second seasonal variable at northern latitudes i s l i g h t . At the latitudes of the study area there i s an extreme difference between summer and winter l i g h t conditions,, The sun remains above the horizon for 24 hours a day for a short period in mid-summer, while i t remains below the horizon for 24 hours a day during the mid-winter. Furthermore, during the winter the beaver i s confined to the lodge and a small area of .activity in front of the lodge beneath a thick layer of ice and snow. This further reduces l i g h t intensity, although l i g h t i s able to pass through the ice. In t h i s connection an item of supporting evidence i s to be seen in an observation made by Hakala (1953), working in Alaska. He found that beavers occupying a spring-fed pond which remained open a l l winter grew throughout the winter, while those in frozen ponds did not. It may be assumed that the animals in the spring-fed pond were subjected to more l i g h t of a higher i n t e n s i t y than were those in the frozen ponds. Light i n t e n s i t y i s a variable that fluctuates in prec i s e l y the same manner from year to year, and therefore -65 Figure 17. A schematic representation of an hypothesis which attempts to explain the winter metabolic depression in the beaver. WINTER Increasing Light Intensity I Decreasing Light Intensity 6 6 can serve as a r e l i a b l e indicator of changing seasons. I t i s hypothesized that l i g h t i n t e n s i t y i s the environmental c o n t r o l l i n g factor of the winter metabolic depression i n the beaver. Light i n t e n s i t y rather than photoperiod i s hypothesized as the factor involved for the following reason. As i s true of most mammals, the beaver has a d i s t i n c t diurnal pattern of a c t i v i t y . The animal i s crepuscular and nocturnal, and spends most of the daylight hours i n the lodge where l i t t l e l i g h t reaches i t . Therefore the length of the daylight period i s information that does not reach the beaver. A schematic representation of the ent i r e hypothesis i s given i n F i g . 17. The next step i n this study i s to obtain juvenile beavers from the northern and southern extremes of the species d i s t r i b u t i o n and test various aspects of the hypothesis under controlled laboratory conditions. 67 PART II. AN EXPERIMENTAL ANALYSIS OF THE WINTER METABOLIC DEPRESSION Introduction The available evidence strongly suggests that the beaver does not hibernate. The animal is active throughout the winter, although r e s t r i c t e d to an under-ice environment, and there are no records of natural hypothermia in the species. Morrison (1960), in a th e o r e t i c a l analysis of hibernation function in r e l a t i o n to body weight, suggests that there i s no "need" for hibernation in the beaver in that i t s body weight i s of such a magnitude that f a t reserves could sustain the animal throughout the winter under basal conditions. However, the re s u l t s obtained in the f i r s t section of the present study indicate that there i s an inherent mechanism in the beaver which reduces metabolic energy expenditure during the winter. It was found that growth is rapid in the summer and absent in • the winter, summer thyroid a c t i v i t y i s high r e l a t i v e to winter thyroid a c t i v i t y , and f a t content i s low in the summer and high in the winter. The evidence indicated that t h i s annual pattern of metabolic a c t i v i t y is not a d i r e c t r e s u l t of seasonal changes in the die t of the animal but instead i s an inherent property of the beaver. The adaptive significance of that annual pattern' i s thought to be that energy expenditure i s timed to environmental 68 energy a v a i l a b i l i t y . A pronounced seasonal pattern of metabolic energy expenditure of the type observed in the beaver has not been previously observed. Seasonal growth o s c i l l a t i o n s have been observed in the racoon (Procyon lotor) (Mech et a l . , 1968) and the b l a c k t a i l deer (Odocoileus hemionus) (Wood, Cowan and Nordan, 1962). The winter cessation of growth in the racoon might be associated with energy conditions, but in the deer i t i s thought to be associated with reproduction (Wood, Cowan and Nordan, op. c i t ) . The method by which growth is controlled i s unknown in a l l these cases. A working hypothesis was established to explain the physiology of the mechanism involved in the beaver. It was hypothesized that an i n h i b i t i o n i s imposed on thyroid a c t i v i t y in the autumn, which in turn i n h i b i t s growth hormone production and thus growth. Low thyroid a c t i v i t y also r e s u l t s in a low l e v e l of general body metabolism, and t h i s , together with the reduction in growth, r e s u l t s in reduced food intake. This condition of low energy expenditure and low food intake pr e v a i l s throughout the winter. The i n h i b i t i o n is removed in the spring and the entire e f f e c t i s reversed, allowing the f u l l or n e a r - f u l l metabolic pot e n t i a l to be expressed during the summer. Light i n t e n s i t y was hypothesized as the environmental c o n t r o l l i n g f a c t o r : decreasing l i g h t i ntensity in the 69 autumn might serve to induce the state and increasing l i g h t i n t e n s i t y in the spring to d i s p e l i t . It i s possible that the pattern i s an expression of an endogenous physiological rhythm, as has been observed in the hibernating pattern of the golden-mantied ground s q u i r r e l (Spermophilus  l a t e r a l i s ) by Pengelley (1967), but t h i s was considered unlike l y . The objectives of t h i s section of the study are: (1) To determine the inherent differences in the seasonal changes in metabolic a c t i v i t i e s of beavers from the southern and northern portions of the species d i s t r i b u t i o n . (2) To examine the nature of the metabolic depression by testing various aspects of the hypothesis. (3) To determine whether l i g h t i ntensity i s the environmental c o n t r o l l i n g factor in the metabolic depression. 70 METHODS Juvenile beavers were obtained from the Mackenzie Delta, Canada, and Plumas County, C a l i f o r n i a , representing the beaver populations at the northern and southern extremes of the species d i s t r i b u t i o n respectively. The two populations represent d i f f e r e n t subspecies, and, according to H a l l and Kelson (1959), are Castor canadensis canadensis and Castor canadensis subauratus respectively. One northern and two southern animals were obtained in the autumn of 1966, and were used largely for perfecting techniques to be used in the experiments. Four animals, two of each sex, were obtained from each area in the autumn of 1967. A l l were juveniles born the previous spring. The animals were housed i n d i v i d u a l l y in s p e c i a l l y designed pens in the Zoology Vivarium of the University of B r i t i s h Columbia. Each pen consisted of a livestock watering tank with a metal nest box at one end and a feeding platform, covered with a metal canopy, at the other. The ent i r e space between the nest box and the canopy was enclosed with heavy wire-mest screen to a height of two feet, which was the height of the nest box and the feeding canopy. The metal nest box contained a smaller wooden nest box and had a plunge hole in the f l o o r leading into the water. Wood excelsior was provided as nesting material. Tap water at a temperature of approximately 10°C was kept c i r c u l a t i n g 71 through the tank constantly by means of an i n l e t valve at one end and an outlet valve at the other. The pens were situated outdoors and thus the animals were subjected to Vancouver cli m a t i c conditions, unless otherwise sp e c i f i e d . An a r t i f i c i a l p elleted r a t i o n prepared by Buckerfields Ltd., Vancouver (U.B.C. Ration 42-57), was made available ad libitum (Table IV). Food intake was measured d a i l y by weighing a given amount of food into the feeding tray and weighing the remainder the following day. L i t t l e or no s p i l l a g e occurred. Each beaver was weighed at approximately two-week intervals to the nearest tenth of a kilogram. In the f i r s t portion of the study i t was demonstrated that the t a i l of the beaver functions as a fat depot. It was decided to obtain an _in vivo index of body f at content by sampling the t a i l tissue at interv a l s throughout the duration of the laboratory study. The animal was f i r s t immobilized by i n j e c t i n g succinylcholine chloride (Anectine: Parke-Davis) intramuscularly at a dosage of 0.367 milligrams per kilogram body weight. A c y l i n d r i c a l plug of tissue was then taken from the t a i l with a sharp cork borer, and the skin layer at each end s l i c e d o f f with a scalpel, leaving only i n t e r n a l t a i l tissue. The tissue was weighed and dried at 100°C for six hours. The sample was weighed again a f t e r cooling in a dessicator, and the weight loss reported TABLE IV. Composition of U.B.C. Ration 42-57 on which the experimental animals were maintained. Constituent A l f a l f a Vitagrass Cornmeal Ground Wheat Bran Mollasses S t a b i l i z e d Fat F i s h O i l Bone Meal Iodized S a l t Parts Per 2000 47 5 47 5 375 375 100 100 50 10 20 20 Total 2000 73 as a loss of moisture. The dried sample was ether-extracted i n a Soxlet extracting apparatus for sixteen hours, a i r - d r i e d for half an hour and then dried i n an oven at 13 5°C for two hours. The loss of weight by the dry sample during the ether extraction was reported as a loss of l i p i d s . This method complies with the o f f i c i a l method of the Association of O f f i c i a l A g r i c u l t u r a l chemists (1965). The f a t index was expressed as percentage f a t i n the undried sample. The t a i l f a t index i s not a d i r e c t index of body fa t content. The t a i l f a t depot has the highest p r i o r i t y of a l l depots for f a t deposition, as demonstrated e a r l i e r . The seasonal changes i n the f a t content of the t a i l are similar to those of other f a t depots, but f a t i s deposited f i r s t i n and mobilized l a s t from the t a i l . Therefore caution must be exercised i n the inte r p r e t a t i o n of the t a i l f a t index. 131 The protein-bound iodine conversion r a t i o was used as a measure of thyroid a c t i v i t y (Kaplowitz and Solomon, 1965; Clark et a l . , 1949). I o d i n e 1 3 1 (Radionics, Ltd., Montreal) was injected intramuscularly at a dosage of 1 microcurie per kilogram body weight. Approximately 8 m i l l i l i t e r s of blood were obtained at 48 hours aft e r 131 iodine i n j e c t i o n by f i r s t immobilizing the animal with succinylcholine chloride and then making a cut i n the t a i l . 74 The blood was allowed to d r i p d i r e c t l y from the cut into a test tube, allowed to coagulate and then centrifuged. 131 The PBI conversion r a t i o was determined on two 131 m i l l i l i t e r s of serum by means of the IORESIN PBI Conversion Ratio K i t (Abbott Laboratories, North Chicago, I l l i n o i s ) . Radioactivity in the samples was counted with a shielded well-type s c i n t i l l a t i o n counter. A multi-channel telethermometer (Yellow Springs Instrument Co., Inc.) was used to measure body temperature. The temperature probe was inserted into the rectum to a depth of two inches, and the temperature read two minutes after i n s e r t i n g the probe. Two pens were adapted for use in the l i g h t experiments. Each pen was enveloped with black polyethylene and a l l loose f i t t i n g s in the pen structure were caulked with burlap. Incandescent l i g h t bulbs were i n s t a l l e d within the polyethylene-covered pens. 75 Results Seasonal Changes In The Metabolic A c t i v i t i e s of Northern and Southern Beavers in Captivity Growth The growth curves of the northern beavers are depicted in Fig. 18. The 1966 i n d i v i d u a l grew throughout the autumn and early winter, and plateaued in February. Its weight stayed at approximately 8.8 kilograms u n t i l the l a t t e r part of May, when i t suffered a broken leg and had to be k i l l e d . The two 1967 individuals grew rap i d l y in the autumn and both plateaued in early December, at weights of 11.0 and 12.5 kilograms. The larger one showed an immediate weight loss. It was accidently k i l l e d by an overdose of succinylcholine chloride in January. The other in d i v i d u a l showed a s l i g h t weight loss between January and A p r i l , a loss of 1.0 kilogram, or 9.1% of i t s peak weight in the early winter. It began to grow again in A p r i l and continued for the duration of the experiment, which was terminated at the end of May. Unlike the northern individuals, the southern animals continued to grow throughout the winter (Fig. 19). The two 1966 individuals grew in a t y p i c a l sigmoid pattern, with no major breaks in the smooth curve. The three 1967 individuals, on the other hand, display a s l i g h t depression in their growth rate during the mid-winter, although growth does not cease. 76 Figure 18. Total weight growth of A r c t i c beavers in c a p t i v i t y , 1966 and 1967. T O T A L WEIGHT IN K I LOGRAMS ro ^ o CD O ro n 1 1 1 1 r 77 Figure 19. Total weight growth curve of C a l i f o r n i a beavers in c a p t i v i t y , 1966 and 1967. A l l animals were exposed to Vancouver l i g h t conditions except individuals o and x, which were exposed to constant darkness from 18 October to 18 January. 78 Figure 20. Relative food intake of A r c t i c beavers, 1966 and 1967. Each point on the graph represents a four day average. 79 Figure 21. Relative food intake of C a l i f o r n i a beavers, 1967. Each point on the graph represents a four day average. 80 Food Intake Food intake i s expressed r e l a t i v e to body weight rather than in absolute terms in order to permit comparisons between animals d i f f e r i n g in body weight. Also, i t permits temporal comparisons within a given i n d i v i d u a l . There i s a general decline in food intake with increasing age in a l l cases (Figs. 20 and 21) . In the southern animals food intake was between 50 and 70 grams per kilogram body weight per day in September and October, decreased gradually during November and December to a value of approximately 30 grams per kilogram in late December, and stayed at that value during the winter and spring. There i s some d a i l y and i n d i v i d u a l v a r i a t i o n . The winter values are generally between 25 and 35 grams per kilogram. The seasonal pattern of r e l a t i v e food intake in the northern animals i s b a s i c a l l y s i m i l a r to that in the southern ones, although there i s a temporal displacement in the 1966 in d i v i d u a l . The value was approximately 60 grams per kilogram in the 1966 in d i v i d u a l in November and early December, decreased during December, January and February to a value of approximately 20 grams per kilogram in March, and stayed at that l e v e l during A p r i l and May„ The two 1967 individuals had values of approximately 60 grams per kilogram in September. The value decreased gradually during October, November and December to approximately 20 in January, when one animal was accidently k i l l e d . The value 81 Figure 22. Seasonal changes in percent t a i l f a t content of A r c t i c and C a l i f o r n i a beavers. 82 in the other i n d i v i d u a l stayed at approximately between 15 and 20 during February and March, and began to increase in A p r i l . During mid-April i t plateaued at about 2 7, where i t stayed u n t i l the termination of the experiment in late May. T a i l Fat Changes The _in vivo t a i l f a t index used in t h i s study i s p a r t i c u l a r l y valuable because i t r e f l e c t s changes in body fat content in individuals with time. In vivo f a t indices are rare and very d i f f i c u l t to implement. Most fat indices require that the animal in question be k i l l e d and thus do not give data on f a t changes in a given i n d i v i d u a l over a period of time. Fig. 22 depicts temporal changes in t a i l f a t content. A great deal of si g n i f i c a n c e cannot be attributed to minor changes in f a t content, such as perhaps 10%, since t h i s probably r e f l e c t s only sample v a r i a t i o n within a given i n d i v i d u a l . The t a i l f a t content of a l l individuals increased in the autumn, to value of approximately 60-75% in l a t e November, and stayed at that l e v e l throughout the winter and spring. Thyroid A c t i v i t y Due to d i f f i c u l t i e s encountered in sampling techniques, the thyroid a c t i v i t y data are incomplete. The blood samples 83 Figure 23. Seasonal changes in PBI conversion r a t i o s of A r c t i c and C a l i f o r n i a beavers. 84 could not be obtained at the proper time in a number of cases, and consequently such tests were l o s t . The r e s u l t s of the thyroid a c t i v i t y tests are presented in F i g . 23. The conversion r a t i o r e f e r s to the percentage of the t o t a l radioactive iodine in the serum which i s bound to serum proteins. The radioactive iodine bound to serum proteins i s part of the thyroid hormones, and thus the conversion r a t i o indicates the percentage of the radioactive iodine in the serum which has been incorporated into thyroid hormones. A low conversion r a t i o indicates that l i t t l e of the injected radioactive iodine has been incorporated into thyroid hormones, and thus a low l e v e l of thyroid a c t i v i t y . A high conversion r a t i o , on the other hand, indicates a high l e v e l of thyroid a c t i v i t y . The conversion r a t i o was high in the northern beavers in September, decreased in November and December, was low in January and increased in March and A p r i l . The r a t i o in the southern animals was high in September, November and December, decreased s l i g h t l y in January and was high again in March and A p r i l . E f f e c t of Light on Food Intake, Body Weight, T a i l Fat Content and Muscular A c t i v i t y Two northern and two southern beavers, one of each sex in each case, were subjected to continuous darkness 85 commencing on 18 October 1967. This was done by enveloping their pens with black polyethylene, as was described in the methods section. The darkness was not absolute in that some l i g h t entered the feeding area during the d a i l y feeding procedure, although the animals were usually in the nest box at that time. Also, the animals were subjected to l i g h t during the weighings which took place at two-week int e r v a l s . The animals maintained under natural l i g h t conditions, described in the previous section, served as controls. There was no apparent response to the condition of darkness in the southern animals. No differences in food intake and body weight changes existed between the experimental animals and the controls, and the data from the experimentals was included in the previous section (Figs. 19 and 21). The polyethylene covers were removed from the pens housing the southern animals on 18 January 1968, three months after the condition of darkness was imposed. A spectacular response was obtained in the A r c t i c animals (Figs. 24, 18 and 20) . The condition of darkness resulted in reduced food intake and body weight in the experimental animals, while no similar changes were observed in the controls. Food intake began to drop immediately after the l i g h t r e s t r i c t i o n was imposed, and continued to 86 Figure 24. E f f e c t of l i g h t r e s t r i c t i o n and constant l i g h t on t o t a l weight growth and r e l a t i v e food intake of 2 A r c t i c beavers. T O T A L WEIGHT IN K ILOGRAMS drop u n t i l the animals stopped eating e n t i r e l y . Food intake reached zero 22 and 17 days after the beginning of the l i g h t r e s t r i c t i o n in individuals #3 and #4 respectively. Body weight dropped 1.0 and 1.2 kilograms (12.8% and 15.4%) in #3 and #4 respectively during the period when the animals were in darkness. Part of the weight loss was due to clearing of the alimentary canal, since the canal normally contains food and wastes which are excreted and not replaced by others during f a s t i n g . The remainder was presumably due to the mobilization of f a t reserves to meet energy requirements. An e f f e c t of the imposed darkness which was e n t i r e l y unexpected was that on muscular a c t i v i t y . A muscular par a l y s i s of unknown nature appeared in the experimental animals concomitantly with the reduction in food intake. Both animals showed great d i f f i c u l t y in using their locomotory and postural muscles. They were completely paralyzed by the time food intake had dropped to zero. They remained prostrate and were unable to walk or swim, but were able to wriggle t h e i r bodies and l i f t t h e i r heads. The central nervous system appeared to be functioning normally; the animals were mentally a l e r t and f u l l y aware of t h e i r surroundings. A state of relaxation normally prevailed, but when I approached to pick an animal up, i t made tremendous e f f o r t s to move away but was unable. This 88 supports t h e contention that the central nervous system was functioning normally, and suggests that the i n a b i l i t y to move was a peripheral e f f e c t . The entire e f f e c t was very similar to that produced by succinylcholine chloride. The drug i n h i b i t s the contraction of voluntary muscles by competing for receptor s i t e s in the neuromuscular junction (Grollman, 1965; p.425). It has no e f f e c t on the central nervous system, and while under i t s influence the animal often makes great attempts to move but i s unable. This further suggests that the i n a b i l i t y to move in the experi-mental animals was a peripheral e f f e c t . It appears to be a d e f i n i t e muscular block. There i s no reason to believe that the e f f e c t was due to a state of weakness in the animal. The two most apparent features of the state produced by darkness were the f a s t i n g and the pa r a l y s i s . It might be suggested that a cause and e f f e c t r e l a t i o n s h i p existed between them, in that possibly animals were unable to feed because of an i n a b i l i t y to use the i r voluntary muscles, including those employed in mastication. This was not the case. When p e l l e t s of food were placed near the animals' heads, they picked up the p e l l e t s one by one w i t h t h e i r teeth and dropped them outside the cage. Therefore they had control over th e i r jaw muscles. Also, i t might be suggested that the pa r a l y s i s was a r e s u l t of dietary d e f i c i e n c i e s , since the animals were not eating. T h i s i s very u n l i k e l y . Starving animals are not known to d i s p l a y 89 p a r a l y s i s . There i s a s u f f i c i e n t store of v i t a l nutrients in the body to sustain an animal during s t r e s s f u l periods of food i n a v a i l a b i l i t y . Furthermore, the paralysis developed concomitantly with the reduction in food intake, rather than after the reduction. In general, the behaviour of the animals indicated that they were in a depressed metabolic state, which led to the p o s s i b i l i t y of hypothermia. Rectal temperatures were taken by means of a telethermometer, and are presented in Table V. The two experimental animals were not hypothermic while in the depressed state. Both animals were moved from th e i r outdoor cages to an indoor laboratory on 11 November 1967, 2 and 7 days after #3 and #4 respectively had stopped eating. Food and water was made available, and the beavers were subjected to continuous l i g h t from an incandescent l i g h t bulb at a strength of 16 foot candles. This resulted in a complete reversal of the e f f e c t s produced by continuous darkness (Fig. 24). Animal #3 began eating 3 days after exposure to l i g h t , and #4 began eating on day 6 after exposure. Food intake continued to increase u n t i l i t reached a maximum in mid-January, two months l a t e r . The maximum was at approximately the same l e v e l as the food intake had been at the beginning of the l i g h t experiment. Muscular a c t i v i t y began to return on day 4, when both animals 90 TABLE V. Rectal temperatures i n C of beavers i n depressed states and beavers i n normal ph y s i o l o g i c a l states. Ambient temperatures i n a l l cases were 21-22°C. Rectal Temperature Date #1 #2 #3 #4 #5 #6 #7 #8 20 Oct 37.1 37.0 37.2 35.6 36.3 36.3 37.0 3 N o v - - - 35.5* -3 Nov - - 36.0* 8 Nov - 37.1* 3 5.0* 11 Nov - - 36.0* 34.0* - - - -11 Nov - - 36.5* 36.8* - - - -13 Nov - - 35.9* 36.8* - - - -13 Nov - - 35.0* 35.2* 13 Nov - - 35.8* 34.8* -15 Nov - - 36.3* 35.9* -15 Nov - - 36.2* 35.6* -15 Nov - - 34.8* 34.7* -24 Nov 37.1 36.2 - 35.3 38.8 36.4 *beaver i n depressed metabolic state 91 frequently turned around in the i r cages, although they were s t i l l unable to support themselves on their legs. Number 4 was able to support i t s e l f on i t s legs on day 11, but #3 was not. Number 4 was able to walk when l e t out of i t s cage on day 18, but #3 was not, although #3 was able to stand on i t s legs. Grooming appeared at t h i s stage, and both animals spent a great deal of time at t h i s a c t i v i t y . Number 4 was normal in i t s muscular a c t i v i t y on day 31; #3 was normal on day 38. Both animals were returned to t h e i r outdoor pens on 31 December, after 50 days of exposure to constant l i g h t . Incandescent l i g h t bulbs i n s t a l l e d in the feeding area of t h e i r pens provided continuous l i g h t at a strength of approximately 20 foot-candles. The i n t e r i o r of the metal nest box was not illuminated. The body weight of both animals continued to drop after they were exposed to continuous l i g h t , reaching a minimum on day 32, 13 December 1967. Number 3 and #4 l o s t 2.0 and 2.4 kilograms respectively from the beginning of the l i g h t experiment to 13 December. This represented 25.6% and 30.8% of the i r o r i g i n a l weights respectively. Most of t h i s weight loss was undoubtedly due to the clearing of the alimentary canal and the mobilization of f a t from adipose tissue. T a i l f a t content increased in the autumn in the same manner as i t did in the controls (Fig. 25). Despite the 92 Figure 25. Percent t a i l f a t content of 2 A r c t i c beavers subjected to a r t i f i c i a l l i g h t conditions. I I I I I I I I Sept Oct Nov Dec Jan Feb Mar Apr DATE 93 period of fa s t i n g and low food intake, t a i l f a t reserves were high in late November. In January, however, the fat l e v e l s had dropped considerably, strongly indicating that other f a t depots had been depleted by t h i s time. This occurred during the period when food intake had increased markedly, and suggests that energy requirements and/or the endocrine a c t i v i t y of the body increased markedly as well. The t a i l f a t content of a l l other individuals remained high during the same period. Fat content in the experimentals increased gradually during the la t e winter and early spring. The two animals were kept in illuminated pens throughout the winter. Food intake stayed high and both animals continued growing throughout the winter, unlike the controls under Vancouver l i g h t conditions. The condition of darkness was imposed on the animals once again on A p r i l 28 to determine whether the metabolic depression could be induced in the spring. No response to the darkness was obtained. 94 Discussion It was t e n t a t i v e l y concluded in the f i e l d portion of the study that the winter growth depression i s an inherent property of the beaver in the northern portion of the species d i s t r i b u t i o n . The absence of winter growth in northern beavers maintained under Vancouver cli m a t i c conditions and a constant ration made available ad libitum, and the presence of winter growth in southern beavers maintained under pr e c i s e l y the same conditions, confirms that conclusion. The c h a r a c t e r i s t i c s of the winter depression in the captive beavers were i d e n t i c a l to those of the winter depression observed.in the f i e l d . In both cases the depression was characterized by an absence of growth, a state of obesity and low thyroid a c t i v i t y . It was impossible to measure food intake in the f i e l d , but i t i s assumed that i t i s r e l a t i v e l y low during the winter depression, as was observed in the captive animals. The re s u l t s of the l i g h t experiment demonstrate conclusively that l i g h t i s an environmental factor which can induce a depressed state in the autumn and can reverse t h i s state at least after a period of 24 days in the dark. Experimentally-imposed l i g h t changes had profound effects on northern beavers and no overt e f f e c t s on southern beavers. Constant darkness resulted in a cessation of growth and subsequent loss of weight, a reduction of food intake to 95 n i l and a muscular paralysis of unknown nature. This did not occur concomitantly in the controls under Vancouver l i g h t , nor did i t occur in the southern animals subjected to constant darkness. Like the controls, the experimental animals fattened during t h i s period. The subjection of the two experimental animals to constant l i g h t completely reversed the e f f e c t s induced by constant darkness. Muscular a c t i v i t y returned to normal, food intake returned to a high l e v e l , growth resumed and the t a i l f a t index dropped considerably in value. Two animals were subjected to constant l i g h t during the entire winter. The r e s u l t was high food intake and rapid growth throughout that period. During the same period the northern animals subjected to Vancouver l i g h t did not grow and had low food intake values. Evidently the condition of constant l i g h t prevented the experimental animals from entering the depression when the controls entered i t . These r e s u l t s strongly suggest that the depression in the two controls was induced by decreasing l i g h t i n t e n s i t y in the autumn. Wolfson (1964), in a review of photoperiodism in animals, recognizes three categories of photoperiodic phenomena. In the f i r s t category are the phenomena in which the r o l e of the environment i s only to serve as a Zeitgeber (timer). The annual rhythm i s endogenous in 96 the organism; changing l i g h t conditions serve only to keep periodic physiological events in phase with the seasons. In another category the environment controls the phasing and frequency of physiological events; again, the occurrence of the events are endogenous. The l a s t category includes those phenomena in which l i g h t conditions control the phasing, frequency and very existence of the rhythm. Such annual cycles disappear i f changes in l i g h t conditions are absent. It appears that the annual rhythm of metabolic a c t i v i t y in the beaver f a l l s in the t h i r d category. This i s suggested f i r s t by the exaggerated response produced by the extreme l i g h t r e s t r i c t i o n and secondly by the elimination of the metabolic depression during the winter through the subjection of the animals to constant high-intensity l i g h t . It w i l l be necessary to maintain a number of beavers under constant l i g h t conditions for the duration of one year before t h i s hypothesis can be accepted or rejected. The l i g h t regimes imposed on the two light-experiment animals were only crude approximations of the regimes which the animals are exposed to in nature. The l i g h t changes were abruptly imposed, and the changes in intensity were extreme, whereas in nature the l i g h t changes are gradual and minimal in magnitude. This might account for the exaggerated response obtained with the imposition of complete darkness. Food intake dropped to zero, while in nature the animals apparently feed throughout the winter. Secondly, 97 the animals became paralyzed to such an extent that they were unable to move, while i t i s known that they remain active throughout the winter in nature. Further experiments must be conducted implementing more r e a l i s t i c l i g h t changes. The preliminary experiments performed in t h i s study served only to demonstrate that l i g h t i n t e n s i t y i s indeed the most probable environmental factor which times growth and food intake to environmental food a v a i l a b i l i t y . If i t i s assumed that beavers in nature feed d a i l y during the winter, as was observed in c a p t i v i t y , then l i g h t i ntensity i s an excellent environmental cue for the observed system. The lodge i n t e r i o r , where the animals remain for most of the day, i s dark. Only a minute quantity of l i g h t might enter the lodge from the water by way of the plunge hole. When the animal swims out of the lodge beneath the ice to obtain food during the d a i l y feeding, i t i s subjected to the existent l i g h t conditions for a b r i e f period. The changing l i g h t i ntensity to which i t i s subjected i s an indication of changes occurring or about to occur in the environment. In e f f e c t , the animal i s "taking a check on l i g h t conditions" during the d a i l y feeding a c t i v i t y . Diminishing l i g h t intensity in the autumn induces the metabolic depression, thus conserving energy to meet the condition of limited food a v a i l a b i l i t y which characterizes the winter. Increasing l i g h t intensity 98 in the spring dispels the metabolic depression and prepares the animal for intensive metabolic a c t i v i t y during the summer when food a v a i l a b i l i t y i s e s s e n t i a l l y unlimited. The winter depression observed in northern beavers i s e n t i r e l y lacking in individuals from the southern portion of the species d i s t r i b u t i o n . Light changes had no e f f e c t on southern beavers and no seasonal changes in growth were observed in any of them. There was a . 131 s l i g h t depression in the PBI conversion r a t i o in January, but i t was minimal and the r a t i o s in November and March were both very high. The January r a t i o , although i t represented a s l i g h t drop from the previous value, was s t i l l i n d i c a t i v e of a hyperactive thyroid gland. Therefore, there appears to be no s i g n i f i c a n t winter drop in the thyroid a c t i v i t y of southern animals. The food intake data are more d i f f i c u l t to interpret. There was an autumnal drop in food intake in both northern and southern beavers when maintained under Vancouver l i g h t conditions outdoors. This drop i s in a l l l i k e l i h o o d due to the general drop in metabolism that occurs as mammals near maturity (Brody, 1945) . This in turn i s probably at least p a r t i a l l y due to a decreased heat loss with decreased surface to volume r a t i o s . The increased in s u l a t i v e value of the winter fur might also have contributed to the reduction in food intake in the beavers by reducing 99 heat loss. The drop in the two types, however, occurred to d i f f e r e n t l e v e l s . Food intake in the southern animals dropped to approximately 30 grams per kilogram body weight and stayed at that l e v e l throughout the winter, spring and early summer. In the northern animals, on the other hand, i t dropped to approximately 18 grams per kilogram body weight, where i t remained throughout the winter. In A p r i l i t began to increase gradually, and continued to increase u n t i l i t reached a l e v e l of approximately 27 grams per kilogram body weight, the approximate l e v e l maintained throughout the winter in the southern animals. Therefore i t i s concluded that there is no winter depression in the energetics of southern heavers. Beavers in the southern portion of the species d i s t r i b u t i o n do not experience a marked seasonal fluctuation in food a v a i l a b i l i t y , and hence one would not expect to fi n d a winter depression in the i r metabolism. Streams and lakes r a r e l y freeze, except at high al t i t u d e s , and the animal can obtain food f r e e l y during the winter. Figure 26 summarizes temperature and p r e c i p i t a t i o n conditions at Quincy, Plumas County, C a l i f o r n i a , where the experimental animals were procured (U.S. Climatological Data,. 1966). Snow was present on the ground for 11 days in 1966. The a l t i t u d e of the area i s 3400 feet above sea l e v e l . Since there i s no winter depression in the southern 100 Figure 26. Summary of temperature and p r e c i p i t a t i o n conditions at Quincy, Plumas County, C a l i f o r n i a during 1966. (U.S. Climatological Data). - l O h J F M A M J J A S O N D M O N T H S 101 beavers, t h e i r bioenergetics can serve as a baseline in the analysis of the depression in northern beavers. It provides a very simple and useful means of determining how much of the autumnal drop in the food intake of northern beavers was due to the metabolic depression. Thirty grams per kilogram body weight can be considered the food intake baseline. This i s the winter l e v e l of the southern animals, and, in t e r e s t i n g l y , i s approximately the l e v e l that the northern animal rose to in the spring, when growth had resumed. The winter food intake of the northern animals, 18 grams per kilogram body weight, thus represented a 40% drop from the baseline. Therefore, i t can be te n t a t i v e l y stated that the winter depression accounted for a 40% reduction in food intake. However, i t i s d i f f i c u l t to extrapolate t h i s figure to f i e l d conditions. The l i g h t r e s t r i c t i o n at the northern portion of the species range i s much greater than that at the 49th p a r a l l e l , where the experiment was performed, and therefore i t cannot be said that the depression observed under Vancouver l i g h t was of the same degree as that which occurs in the north. It i s d i f f i c u l t to ascertain the exact nature of the winter depression, and in what processes energy i s in fact conserved. At t h i s stage i t can only be stated that there i s an absolute cessation of growth and a 102 considerable reduction in thyroid a c t i v i t y . The p o s s i b i l i t y of hypothermia has been ruled out, at least under laboratory conditions. The reduction in thyroid a c t i v i t y can th e o r e t i c a l l y r e s u l t in a reduction in body metabolism to a maximum of 35% (Bard, 1961), which i s the reduction in metabolism which r e s u l t s after thyroidectomy. Therefore the reduction in thyroid a c t i v i t y could account for a reduction in food intake to a maximum of 35%, although i t i s probably not that high. The cessation of growth would r e s u l t in a reduction of food intake in the amount of that required for b u i l d i n g blocks plus that required to provide the energy necessary for synthetic work. As well as representing a reduction in food intake, the i n h i b i t i o n of growth might be advantageous in the following manner. The growth impulse in juvenile mammals is very high. Given the proper type of food in s u f f i c i e n t quantity, growth w i l l occur. If food i s scarce and of poor quality, or even of good quality, some growth may occur but the animal w i l l be in, for want of a better term, "poor condition". The growth impulse w i l l remain high but l i t t l e growth w i l l occur due to a lack of buil d i n g blocks or energy, or both. Due to the high p r i o r i t y of growth for available energy, fat deposition undoubtedly would not occur and the animal would remain lean. 103 The winter is a s t r e s s f u l period in terms of energy, and i t is highly advantageous to the animal to have energy reserves in the form of depot fa t . The i n h i b i t i o n of growth removes the growth impulse and allows fat deposition to occur, thus putting the animal into good n u t r i t i o n a l condition. Therefore, as well as reducing food intake, i t i s believed that the metabolic depression is advantageous to the beaver in that i t removes the growth impulse during a period when conditions are not conducive to growth and thereby allows f a t deposition to occur. The muscular paralysis that occurred in the northern beavers i s not understood. The behaviour of the animals during the paralysis strongly suggested that the central nervous system was functioning normally and that the i n a b i l i t y to move was a peripheral e f f e c t . It i s possible that the paralysis i s a peripheral method of c o n t r o l l i n g a c t i v i t y , up and above the normal central nervous system control, to reduce winter a c t i v i t y down to an absolute minimum. A large portion of the energy available within a mammal i s expended through a c t i v i t y ; indeed, the figure may be as high as 20% (McNab, 1963). A substantial reduction in a c t i v i t y would r e s u l t in a great saving of energy. Mammalian a c t i v i t y i s normally controlled by the central nervous system, and although there are 104 periods of i n a c t i v i t y , the mammal i s always capable of movement. Peripheral methods of c o n t r o l l i n g a c t i v i t y are unknown. Perhaps the strong s e l e c t i v e pressure for reduction in energy expenditure, coupled with l i t t l e need for a c t i v i t y during the winter, resulted in the evolution of such a method of c o n t r o l l i n g a c t i v i t y in the beaver. The beaver i s e n t i r e l y free of predators during the winter, which might be a c r i t i c a l factor in the evolution of such a control. Obviously a peripheral control of a c t i v i t y could not evolve in mammals that depend on a c t i v i t y for evading and escaping predators. The beaver's food supply i s cached in very close proximity to the lodge, and thus the food i s obtained with r e l a t i v e ease. The only apparent needs for a c t i v i t y are obtaining food and defecation in the water near the lodge. Therefore seemingly t h i s hypothesis of a peripheral control of a c t i v i t y i s a tenable one. Another possible explanation of the muscular paralysis observed in the experiment i s that i t was a side e f f e c t of the intense i n h i b i t i o n that apparently occurred in certain aspects of the animal's physiology, and thus represented an a r t i f a c t . The entire response was apparently greatly exaggerated over that which occurs in nature. Perhaps the pronounced response i n h i b i t e d muscular contraction by af f e c t i n g the peripheral nervous system or by the production 105 of unusual concentrations of metabolic wastes which in some way i n t e r f e r r e d with muscular a c t i v i t y . It i s impossible to understand the significance of the p a r a l y s i s on the basis of the data available at t h i s stage. The absence of any pathological conditions and the ease with which the p a r a l y s i s was reversed suggests that the e f f e c t was not merely an a r t i f a c t . It requires further investigation. The l i g h t experiment provides evidence against the hypothesis that the thyroid gland i s the major effector in the metabolic depression, and indicates that the mechanism involved in the depression i s much more complex than i n i t i a l l y suspected. Food intake dropped to zero; i f the drop were due wholly to. the e f f e c t s of reduced thyroid a c t i v i t y and lack of growth, i t should have dropped only to a low basal l e v e l . This eliminates decreased thyroid a c t i v i t y as the ultimate cause of reduced food intake during the depression and questions the previously-held notion that the drop in food intake i s simply and d i r e c t l y a r e s u l t of a reduction in energy expenditure. It suggests that food intake i s d i r e c t l y influenced by l i g h t intensity, presumably v i a the nervous system. This i s perplexing, as i t i s d i f f i c u l t to envision how food intake can be d i r e c t l y influenced by l i g h t and s t i l l meet exactly the energy requirements of the organism. I t . i s generally believed that energy expenditure i s c l o s e l y balanced by food intake 106 (Anand, 1961), but there are many exceptions to t h i s apparent general r u l e . Male deer of the genus Odocoileus cease feeding during the f a l l rut, even though food i s made re a d i l y available and energy expenditure remains high (Cowan, pers.comm.). Food intake increases far above energy expenditure in the White-crowned Sparrow (Zonotrichia leucophrys) in response to a long photoperiod (King, 1961) , which i s believed to be a mechanism of fat deposition. Certain salmonids do not feed during th e i r migration up fresh-water streams, despite the fact that energy expenditure i s high (Parker et a l . , 1959). Therefore the d i s p a r i t y between energy intake and energy expenditure observed in the beaver i s not an isolated example. Apparently mechanisms exis t that transcend the r e l a t i v e l y simple r e l a t i o n s h i p between energy intake and energy expenditure. Such a mechanism appears to come into play during the winter depression in the beaver. A great deal of further work i s necessary before an insight can be gained into the manner in which energy balance i s achieved during the metabolic depression in the beaver. The seasonal pattern of thyroid a c t i v i t y , i n i t i a l l y hypothesized to be the cause of the seasonal pattern in metabolic energy expenditure, i s in fact very probably one of the r e s u l t s of the pattern. That i s , due to the u t i l i z a t i o n of thyroid hormones in the metabolic a c t i v i t y . 107 of c e l l s i n peripheral tissues, the l e v e l of thyroid a c t i v i t y simply p a r a l l e l s the l e v e l of metabolic a c t i v i t y . This i s r e a d i l y comprehensible i n view of the negative feedback system that exists i n the t h y r o i d - p i t u i t a r y axis. A similar hypothesis was a r r i v e d at by Petrovic and Heroux (1967) i n r e l a t i o n to the r o l e of the thyroid i n the thermoregulatory response of the r a t to cold exposure. The exact p h y s i o l o g i c a l mechanism involved i n the metabolic depression remains unknown. However, the existence of the depression i s well established and i t s functioning as an energy-saving device i n r e l a t i o n to the beaver's seasonally-fluctuating energy regime i s understood. During the summer, when food i s r e a d i l y available, growth i s rapid, food intake i s high and body f a t content i s low. Decreasing l i g h t i n t e n s i t y i n the autumn induces a metabolic depression which i s characterized by an absence of growth, low food intake and, apparently, a low l e v e l of general body metabolism. A large store of energy reserves i n the form of depot f a t i s deposited at thi s time. The metabolic depression p e r s i s t s throughout the winter, and the f a t reserves apparently are not drawn upon. There i s some p o s s i b i l i t y that a peripheral control keeps a c t i v i t y , and thus energy expended through a c t i v i t y , to a minimum. In general, energy expenditure during the winter i s low. Increasing l i g h t i n t e n s i t y i n the spring reverses the 108 entire e f f e c t produced by low l i g h t i ntensity in the autumn. Depot f a t i s mobilized, growth resumes and food intake returns to a high l e v e l . In essence, t h i s pattern represents a s h i f t i n g of metabolic a c t i v i t y , e.g. growth, from the winter when the food supply i s limi t e d to the summer when food a v a i l a b i l i t y i s unlimited. Thus, energy expenditure i s timed to environmental energy a v a i l a b i l i t y . The ease with which the metabolic depression was induced in the autumn and the f a i l u r e to induce i t in the spring indicates that the beaver must be in a certain "prepared state" before entering the depression. This i s true in certain hibernators (Folk, 1966); indeed, some hibernators display an endogenous annual cycle of hibernation and a c t i v i t y which cannot be e a s i l y altered. There i s a d e f i n i t e annual cycle in the l i v e s of vertebrates in the northern hemisphere, consisting of mating, gestation, caring for young, molting, preparation for winter (migration, food storage, fat deposition, hibernation), et cetera. These events are i n t e r - r e l a t e d and often one sets the phy s i o l o g i c a l stage for another. The sequence of events i s c l o s e l y tuned to seasonal changes occurring in the environment. It appears that the winter metabolic depression i s deep-rooted in the annual ph y s i o l o g i c a l cycle in the beaver, rather than a metabolic i n h i b i t i o n which i s 109 largely independent of other processes occurring in the body. The winter metabolic depression in the beaver i s analogous to seasonal hibernation in certain rodents in that i t reduces energy expenditure during the winter. However, the mechanisms involved in the two depressions d i f f e r . The hibernators display a body temperature drop to a l e v e l just above ambient and an extreme depression in body metabolism. The beaver, on the other hand, maintains i t s body temperature at a normal l e v e l but reduces i t s metabolism to a low maintenance l e v e l . The question of why the beaver does not hibernate might r e l a t e to i t s body size. Morrison (op. c i t . ) states that a mammal with the body size of a beaver can ex i s t on i t s fat reserves for 200 days under basal conditions. Pearson (1960) speculates that the energy and time required to arouse a large mammal from a state of torpor might be pr o h i b i t i v e . The finding of the present study that the beaver does not display a temperature drop agrees with the predictions of these authors. Whatever the reason, i t is apparently more e f f i c i e n t for the beaver to maintain i t s body temperature, reduce i t s metabolism and remain active than to hibernate. 110 SUMMARY AND CONCLUSIONS The objective of t h i s study was to examine the metabolic r e l a t i o n s h i p of the beaver to i t s seasonally f l u c t u a t i n g energy regime in the northern portion of i t s d i s t r i b u t i o n . Seasonal energy expenditure was examined in r e l a t i o n to environmental food a v a i l a b i l i t y on the MacKenzie Delta, Northwest T e r r i t o r i e s . Total weight growth, s k e l e t a l growth and v i s c e r a l growth are rapid during the summer and absent during the winter. Depot f a t i s v i r t u a l l y absent during the summer, deposited in the autumn, maintained throughout the winter and mobilized r a p i d l y in the spring. The t a i l of the beaver was demonstrated to function as a fat depot. Thyroid a c t i v i t y i s high during the summer and low during the winter. This annual pattern of thyroid a c t i v i t y i s the reverse of the pattern present in other non-hibernating rodents. These observations led to the conclusion that metabolic energy expenditure i s high during the summer and low during the winter. Therefore the l e v e l of metabolic energy expenditure roughly p a r a l l e l s the apparent seasonal changes in environmental food a v a i l a b i l i t y . A consideration of possible n u t r i t i o n a l causes of the annual pattern, together with the finding of other investigators that I l l the beaver ceases to grow during the winter on a constant rati o n , led to the conclusion that the observed pattern i s an inherent a t t r i b u t e of the beaver at northern l a t i t u d e s . This was confirmed i n the laboratory portion of the study. 4. I t was therefore concluded that at northern latitudes the beaver possesses an i n t r i n s i c mechanism capable of equating energy demands with the l e v e l of environmental food a v a i l a b i l i t y . Energy expenditure i s reduced in the autumn "in a n t i c i p a t i o n of" the l i m i t e d quantity of food available during the winter. 5 . The thyroid gland was hypothesized as the major i n t r i n s i c e f fector of the annual pattern of metabolic a c t i v i t y . The hypothesis stated that a low l e v e l of thyroid a c t i v i t y during the winter i n h i b i t s growth hormone production, and thus growth, and reduces general body metabolism to a low l e v e l . A high l e v e l of thyroid a c t i v i t y during the summer removes the i n h i b i t i o n , causing a high l e v e l of body metabolism and r e s u l t i n g i n growth. Light i n t e n s i t y was hypothesized as the environmental factor that times the l e v e l of metabolic a c t i v i t y , and thus the l e v e l of metabolic energy expenditure, to environmental food conditions. 112 6. Five juvenile beavers were obtained from the MacKenzie Delta and s i x were obtained from C a l i f o r n i a to compare seasonal changes i n metabolic a c t i v i t i e s i n the two types and to examine the metabolic depression under controlled laboratory conditions. 7. Northern beavers displayed a winter depression i n food u t i l i z a t i o n and anabolic a c t i v i t y as expressed by growth under Vancouver c l i m a t i c conditions and a constant r a t i o n made available ad libitu m . The winter was characterized by a growth cessation. The winter depression i n food intake was calculated to be 40%; this figure needs confirmation. No s i g n i f i c a n t winter depression was observed i n southern beavers maintained under the same conditions; seasonal changes i n energy balance were absent. The f i e l d conclusion that the annual pattern of metabolic a c t i v i t y i s an inherent property of the beaver at northern latit u d e s was thus confirmed. 8. Constant darkness imposed i n the autumn resulted i n a reduction of food intake to zero, a weight loss and a muscular pa r a l y s i s i n the northern beavers, and had no e f f e c t on southern beavers. Exposure of the northern beavers to constant l i g h t r e s u l t e d i n a complete r e v e r s a l of the e f f e c t s observed under constant darkness. Continued exposure to constant l i g h t throughout the winter resulted 113 i n r a p i d growth and high food intake, while during the same period the northern animals exposed to Vancouver l i g h t conditions were i n a state of metabolic depression. I t was concluded that l i g h t i n t e n s i t y i s the environmental c o n t r o l l i n g factor i n the winter metabolic depression of northern beavers. 9. The subjection of northern beavers to constant darkness i n the spring r e s u l t e d i n no overt responses. I t appears that the winter metabolic depression i s an i n t r i n s i c , time-related part of the annual p h y s i o l o g i c a l cycle of the beaver, rather than simply a metabolic i n h i b i t i o n independent of other processes occurring i n the organism. 10. The important features of the metabolic depression are a cessation of growth and a reduction i n general body metabolism. The l a t t e r was deduced from the f a c t that a low l e v e l of thyroid a c t i v i t y p r e v a i l s during the winter. The adaptive s i g n i f i c a n c e of the metabolic depression i s believed to be the following. F i r s t l y , i t reduces food intake during the winter when t o t a l food a v a i l a b i l i t y i s low. Secondly, i t removes the growth impulse during a period when conditions are not conducive to growth, and allows ~fat deposition to occur. The sig n i f i c a n c e of the muscular pa r a l y s i s observed i n the l i g h t experiment i s unknown. I t was hypothesized that 114 i t represents a peripheral control of a c t i v i t y that reduces winter a c t i v i t y to a minimum, thus reducing energy expenditure due to a c t i v i t y . 11. The hypothesis that the thyroid gland i s the major effector of the annual pattern of metabolic a c t i v i t y was questioned on the basis of the observation that under constant darkness food intake dropped to zero rather than to a low basal l e v e l . I t was hypothesized that low thyroid a c t i v i t y i s a r e s u l t rather than a cause of the metabolic depression. 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