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Bioenergetics of growth in the Pigeon Guillemot, Cepphus columba Koelink, Anthony Francis 1972

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c-1 BIOENERGETICS OF GROWTH IN THE PIGEON GUILLEMOT, Cepphus columba by ANTHONY FRANCIS KOELINK B.Sc, Notre Dame University, 19 68 A THESIS SUBMITTED IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE i n the Department of Zoology We accept th i s thesis as conforming to the required standard THE UNIVERSITY OF BRITISH COLUMBIA September, 1972 In p r e s e n t i n g t h i s t h e s i s i n p a r t i a l f u l f i l m e n t o f the requirements f o r an advanced degree a t the U n i v e r s i t y o f B r i t i s h Columbia. I agree t h a t the L i b r a r y s h a l l make i t f r e e l y a v a i l a b l e f o r r e f e r e n c e and study. I f u r t h e r agree t h a t p e r m i s s i o n f o r e x t e n s i v e copying of t h i s t h e s i s f o r s c h o l a r l y purposes may be granted by the Head of my Department o r by h i s r e p r e s e n t a t i v e . I t i s under-stood t h a t copying or p u b l i c a t i o n o f t h i s t h e s i s f o r f i n a n c i a l g a i n s h a l l not be allowed w i t h o u t my w r i t t e n p e r m i s s i o n . Department o f Zoology The U n i v e r s i t y o f B r i t i s h Columbia Vancouver 8, B.C., Canada Date: /*t* /?, /ff£ ABSTRACT The e n e r g e t i c s o f growth and f e e d i n g of the c h i c k s and t h e i r r e l a t i o n to the problem of e v o l u t i o n o f brood s i z e were i n v e s t i g a t e d i n the a l c i d Cepphus columba, the Pigeon G u i l l e m o t , a c o l o n i a l s p e c i e s n e s t i n g a t Mandarte I s l a n d , B r i t i s h Columbia. The study i n v o l v e d the n a t u r a l l y o c c u r r i n g broods o f one and two c h i c k s , b u t to e l u c i d a t e i n f o r m a t i o n on the e v o l u t i o n of b r o o d - s i z e , e x p e r i m e n t a l l y induced broods of t h r e e were c r e a t e d . F o l l o w i n g the technique of Royama [1966], f i l m r e c o r d s show an "optimal working c a p a c i t y " f o r the p a r e n t Pigeon G u i l l e m o t s a t Mandarte I s l a n d of a t o t a l d a i l y f i s h r a t i o n o f 200 grams. In no case were parents observed t o b r i n g more than t h i s amount when means were computed over 5-day p e r i o d s . The r e s u l t i n g l i m i t a t i o n expresses i t s e l f i n a depressed growth r a t e i n a r t i f i c i a l l y induced t h r e e - c h i c k broods i n a l l seasons, and i n twin broods i n c e r t a i n y e a r s . The p a r e n t does not endanger i t s own s u r v i v a l i n f a v o u r of i t s brood, but m a i n t a i n s body weight i n a l l c i r c u m s t a n c e s . Each p a r e n t r e q u i r e s f o r i t s e l f 90 grams of food d a i l y or 20% of i t s own weight. The "optimal working c a p a c i t y " of each p a r e n t i s about 100 grams o f food d e l i v e r e d to the n e s t or 22% of the p a r e n t a l body weight. Subsequently i i i when f e e d i n g the n e s t l i n g s the p a r e n t doubles the r a t e o f f i s h i n g . A procedure f o r whole c a r c a s s a n a l y s i s on 27 Pigeon G u i l l e m o t c h i c k s and 2 a d u l t s i s d e s c r i b e d to determine; c o o l i n g r a t e f o r c a l c u l a t i o n o f heat p r o d u c t i o n , s u r f a c e area to c a l c u l a t e thermal conductance, gross f a t , ash, m o i s t u r e , crude f a t and heat of combustion. The l e a n d r y f e a t h e r l e s s biomass o f 8 n e s t l i n g s o f v a r i o u s ages had an average energy c o n t e n t o f 4.75 K c a l . / g r . , and u s i n g t h i s f i g u r e as w e l l as assuming a combustion v a l u e o f 9 K c a l . / g r . f o r f a t and 5 K c a l . / g r . f o r plumage, the average c a l o r i c v a l u e f o r l i v e weight was c a l c u l a t e d a t 1.92 Kcal/gr. w i t h a range o f 1.34 K c a l . / g r . a t h a t c h i n g to 2.6 5 K c a l . / g r . a t the time o f f l e d g i n g . The a d u l t Pigeon G u i l l e m o t had an average c a l o r i c d e n s i t y o f 2.56 K c a l . / g r . l i v e weight. The change i n the l i v e weight c a l o r i c d e n s i t y i s r e l a t e d to the d e p o s i t i o n o f f a t which o c c u r s between the 11th and 21st day f o l l o w i n g h a t c h i n g and a t f l e d g i n g i s i n excess o f the f a t depot found i n a d u l t s . Growth i n body weight, i . e . i n a b s o l u t e terms as d a i l y increment i n grams, reaches a maximum between the 8th and 15th f o l l o w i n g h a t c h i n g , whereas the r e l a t i v e r a t e o f growth, i . e . the d a i l y increment w i t h r e s p e c t to the n e s t -l i n g s weight, reaches a maximum about the 4th day f o l l o w i n g h a t c h i n g . i v The c o n v e r s i o n r a t e f o r the e n t i r e f l e d g i n g p e r i o d of c h i c k s i n the f i e l d i s 2400 grams of f i s h per c h i c k f o r an increment o f 375 grams i n body weight or 2800 K c a l . f o r an increment of 1001 K c a l . body weight g a i n (=35%). Consumption o f f i s h f o r the two c h i c k s h a n d - r a i s e d s u c c e s s f u l l y a t camp i s 3400 grams f o r a c o n v e r s i o n r a t e of 25%, and compares w e l l w i t h r e s u l t s of s i m i l a r experiments by o t h e r i n v e s t i g a t o r s . The maintenance c o s t s of the c h i c k a r e kept low by keeping energy l o s s e s to a minimum so t h a t a l a r g e share o f the energy i n p u t i s allowed f o r growth, a p r o c e s s o f o v e r -r i d i n g importance i n the Pigeon G u i l l e m o t c h i c k ( F i g u r e 19). The f i n d i n g s on f l e d g i n g success i n the Pigeon G u i l l e m o t (summarized i n Table 3b) are c o n s i s t e n t w i t h Lack's h y p o t h e s i s on the e v o l u t i o n of b r o o d - s i z e i n t h a t two-chick broods r e p r e s e n t the l i m i t t h a t the parents can r a i s e s u c c e s s f u l l y . O v e r a l l success i n the a r t i f i c i a l l y induced t h r e e -c h i c k broods i s poor compared w i t h the normal two-chick broods i n t h a t they f l e d g e a t an o l d e r age (37.3 to 33.9) , t h e i r weight a t f l e d g i n g i s lower (385 to 407 grams) which may i m p a i r t h e i r p o s t - f l e d g i n g s u r v i v a l , and the average number o f c h i c k s produced from t r i p l e t broods i s o n l y m a r g i n a l l y g r e a t e r than from twin broods (1.9 to 1.8 c h i c k s per n e s t ) . TABLE OF CONTENTS PAGE LIST OF TABLES v i i LIST OF FIGURES v i i i ACKNOWLEDGEMENTS x i CHAPTER 1. INTRODUCTION 1 2. GROWTH AND FEEDING OF THE CHICK 6 A. Methods and Materials 6 B. Results 12 1. Growth of the Chick 12 2. Parental Care During the Fledging Period 17 (a) Daily pattern 18 (b) Seasonal pattern 22 (i) feeding frequencies 22 ( i i ) t o t a l d a i l y f i s h weight frequencies 24 3 . ENERGETICS 28 A. Methods and Materials 28 1. Thermoregulation and Basal Metabolism 28 2. Carcass Analysis 30 (a) Cooling rate determination 31 (b) Surface area determination 32 v i CHAPTER PAGE (c) Gross f a t d e t e r m i n a t i o n 33 (d) Ash, mo i s t u r e , crude f a t and heat of combustion 34 3 . C o n t r o l l e d Feeding of Chicks , 3 4 B. R e s u l t s 35 1 . Thermoregulation and B a s a l Metabolism . 35 2 . C a r c a s s Composition 40 3 . C o n t r o l l e d Feeding of Ch i c k s 44 4 . SYNTHESIS 49 A. The Growth Process 49 B. Development o f Temperature R e g u l a t i o n . . . . 60 C. The Problem of B r o o d - s i z e 61 D. Summary 67 LITERATURE CITED 69 LIST OF TABLES TABLE PAGE 1. Types of Food Brought to 6 Nests d u r i n g the 1969 and 1970 Seasons 25 2. Instantaneous R e l a t i v e Growth i n the Pigeon G u i l l e m o t , Wood Sto r k , and Glaucous-winged G u l l 51 3a. F l e d g i n g Age and Weight as a F u n c t i o n o f B r o o d - s i z e 64 3b. F l e d g i n g Success of the Pigeon G u i l l e m o t as a F u n c t i o n o f B r o o d - s i z e 64 LIST OF FIGURES FIGURE 1. Automatic camera r e c o r d i n g u n i t i n o p e r a t i o n . . . . 2. Growth i n body weight i n the Pigeon G u i l l e m o t , as a f u n c t i o n of brood-s i z e 3. Mean d a i l y weight increments f o r the d a t a p r e s e n t e d i n F i g u r e 2 4. Growth i n wing l e n g t h (=radio-ulnar l e n g t h ) , as a f u n c t i o n o f b r o o d - s i z e ( a ) ; growth i n primary l e n g t h as a f u n c t i o n of b r o o d - s i z e (b); growth i n f o o t l e n g t h (= t a r s o - p e d a l l e n g t h ) , as a f u n c t i o n of b r o o d - s i z e ( c ) ; growth i n b i l l l e n g t h (= g r e a t e s t l e n g t h ) , as a f u n c t i o n o f b r o o d - s i z e (d) 5. D a i l y f e e d i n g p a t t e r n , based on frequency of food d e l i v e r i e s , as a f u n c t i o n of b r o o d - s i z e . The h i s t o g r a m shows h o u r l y i n t e r v a l s , and a summary i s g i v e n a t the r i g h t i n 2-hourly p e r i o d s , where the r a t e between 0700 and 0900 hours was taken as 100% 6. F i r s t and l a s t p a r e n t a l food d e l i v e r i e s p l o t t e d i n r e l a t i o n to P.D.S.T. i n n e s t S-5, 1969 ( a ) ; the times o f n e s t d e p a r t u r e (P.D. S.T.) o f c h i c k s from 8 n e s t s f o r the 1969, 1970 and 1971 seasons [ A i t c h i s o n i n c l . ] ( b ) 7. Mean blenny weight as a f u n c t i o n of n e s t l i n g age a t t h r e e g u i l l e m o t n e s t s (chronology: n e s t S-5, 1969, day 10 = 27 J u l y n e s t B, 1970, day 10 = 5 August n e s t B, 1971, day 10 = 27 J u l y ) 8. D a i l y food r a t i o n (grams of f i s h d e l i v e r e d per c h i c k per day), as a f u n c t i o n of brood s i z e f o r G u i l l e m o t n e s t l i n g s (Means f o r one t r i p l e t [ A i t c h i s o n , 1972], 5 double broods, and 5 s i n g l e broods) i x FIGURE PAGE 9. B a s a l m e t a b o l i c r a t e i n the Pigeon G u i l l e m o t n e s t l i n g , w i t h two a d u l t s p l o t t e d f o r com-p a r i s o n ( A d u l t s ) . Values are p l o t t e d a c c o r d i n g to body weight on a double l o g a r i t h m i c s c a l e on which the Brody - P r o c t o r p r e d i c t i o n f o r me t a b o l i c r a t e o f homeiotherms i s a s t r a i g h t l i n e ; the 50% and 150% l i n e s have a l s o been ente r e d 37 10. B a s a l m e t a b o l i c r a t e per square meter o f body s u r f a c e as a f u n c t i o n o f age i n the Pigeon G u i l l e m o t 38 11. Thermal conductance ( K c a l . l o s t per degree c e n t i g r a d e g r a d i e n t per square meter o f body s u r f a c e per hour) as a f u n c t i o n o f age i n the Pigeon G u i l l e m o t 39 12. Plumage weight ( i n grams) as a f u n c t i o n o f age f o r the c a r c a s s Pigeon G u i l l e m o t a n a l y s i s ( b i r d s s a c r i f i c e d a t v a r i o u s ages) 41 13. Su r f a c e volume r a t i o (square c e n t i m e t e r s per ml. body volume) as a f u n c t i o n o f age i n the Pigeon G u i l l e m o t 45 14. M e t a b o l i c i n t e n s i t y ( K c a l . per day per gram o f l i v e weight) as a f u n c t i o n o f age i n the Pigeon G u i l l e m o t 42 15. Water c o n t e n t o f n e s t l i n g Pigeon G u i l l e m o t ( t o p ) , p l o t t e d as a percentage of l i v e weight, and f a t c o n t e n t o f the same b i r d s (bottom), p l o t t e d as a percentage o f l e a n d r y weight 43 16. Rate of c o n v e r t i n g food i n t o body t i s s u e , p l o t t e d as grams o f f i s h r e q u i r e d to b u i l d one gram o f b i r d v e r s u s the age of the n e s t -l i n g Pigeon G u i l l e m o t 46 17. Mean o v e r n i g h t weight l o s s (expressed as grams per hour) f o r the h a n d - r a i s e d c h i c k s , as a f u n c t i o n o f age 48 18. Instantaneous r e l a t i v e growth r a t e (a); t o t a l body weight increments on a d a i l y b a s i s (b); and plumage weight increments on a d a i l y b a s i s (c) f o r the Pigeon G u i l l e m o t n e s t l i n g . . . 50 FIGURE x PAGE 19 Five-day increments i n f i s h r a t i o n (from camera u n i t s ) , energy stored i n body ( d i f f e r e n t i a t e d are plumage (c) , lean body weight (b) and f a t (a)) as taken from carcass a n a l y s i s , and minimal maintenance costs (taken from basal metabolic ra te i n respirometer t r i a l s ) ' 5 7 20 Growth as a funct ion of brood-s ize i n the Pigeon Gui l l emot . P lo t ted are the means for a l l data from 1969 and 1970: s i n g l e -tons are compared with the fas te s t and slowest-growing i n d i v i d u a l s of the twin broods, and the fa s t e s t and slowest-growing i n d i v i d u a l s of the t r i p l e t broods 62 ACKNOWLEDGEMENTS I wish to extend my deepest g r a t i t u d e to my r e a s e a r c h a d v i s o r , Dr. R.H. Drent, who suggested t h i s p r o j e c t to me. His i n v a l u a b l e a d v i c e and a s s i s t a n c e both i n the f i e l d and i n the p r e p a r a t i o n of t h i s manuscript warrants my indebtedness. I b e n e f i t t e d from Mrs. B.E. March's g r a c i o u s a d v i c e on c a r c a s s a n a l y s i s and a p p r e c i a t e d her p e r m i s s i o n to use the equipment i n the P o u l t r y S c i e n c e l a b o r a t o r y . Dr. T.G. Northcote and Dr. H.C. Nordan c r i t i c a l l y read the manuscript and suggested a number of improvements. I am t h a n k f u l to the owners o f Mandarte I s l a n d , the n a t i v e peoples of the Tsawout and Tseycum bands, f o r a l l o w i n g me to l i v e and work on the i s l a n d . Throughout the course o f my f i e l d w o r k I was g r e a t l y helped by oth e r members o f the "Mandarte Team"; I . Robertson, J.O. Anvik, J.C. Ward, and the Hendersons. N. A i t c h i s o n generously allowed the use o f r e s u l t s on h i s f o l l o w - u p study on the Pigeon G u i l l e m o t d u r i n g the 1971 summer. My w i f e , Susan K o e l i n k , d e v o t e d l y took c a r e of the experiment c o n s i s t i n g o f h a n d - r a i s i n g Pigeon G u i l l e m o t c h i c k s . W. Braeuer c o n s t r u c t e d the e l e c t r o n i c camera u n i t s , and I am g r a t e f u l e x p e c i a l l y f o r h i s w i l l i n g n e s s to make a l t e r a t i o n s and r e p a i r s d u r i n g the course o f the i n v e s t i g a t i o n . I am a p p r e c i a t i v e o f C a p t a i n J . Drent who t r a n s p o r t e d my equipment to and from the i s l a n d each summer. x i i The warm h o s p i t a l i t y of Mrs. R. Mathew contributed to making my stay on the i s l a n d a pleasant one. Fi n a n c i a l support for thi s study came from the Univer-s i t y of B r i t i s h Columbia and the National Research Council of Canada grant to Dr. R.H. Drent f o r the purchase of equipment. I CHAPTER 1 INTRODUCTION E c o l o g i c a l work on the b r e e d i n g b i o l o g y o f b i r d s has i n the p a s t decade or so d i v e r g e d i n t o two w e l l - d e f i n e d streams. On the one hand, the d i r e c t i o n of e v o l u t i o n a r y  e c o l o g y , s t i m u l a t e d p a r t i c u l a r l y by the w r i t i n g s of LACK (1954, 1966 and 1968 f o r summaries), i s concerned w i t h f i n d i n g r e a s o n a b l e e x p l a n a t i o n s f o r the a d a p t i v e s i g n i f i c a n c e o f the present-day p a t t e r n s and modes i n b i r d s . For example, why do some s p e c i e s h a b i t u a l l y l a y v e r y l a r g e c l u t c h e s , whereas o t h e r s may o n l y produce one o r two eggs a n n u a l l y ? Lack has championed the view t h a t c l u t c h s i z e , one o f the determinants of r e p r o d u c t i v e r a t e , i s the r e s u l t of n a t u r a l s e l e c t i o n . The genotype of the p a r e n t r a i s i n g the maximum number o f young f o r e v e n t u a l r e c r u i t m e n t to the b r e e d i n g p o p u l a t i o n w i l l e v e n t u a l l y dominate the p o p u l a t i o n . Where p a r e n t a l f e e d i n g of the brood has evolv e d , c l u t c h s i z e , a c c o r d i n g to t h i s h y p o t h e s i s , r e f l e c t s the maximum brood s i z e t h a t the pa r e n t s are capable o f r a i s i n g s u c c e s s f u l l y . The s p e c i a l case o f the much s m a l l e r c l a s s of s p e c i e s where the pa r e n t s do not feed t h e i r young w i l l not f u r t h e r concern us here. Other f e a t u r e s o f the b r e e d i n g arrangements of b i r d s a re a l s o under i n v e s t i g a t i o n by t h i s s c h o o l along much the same l i n e s ; one can speak of e v o l u t i o n a r y s t r a t e g i e s of bree d i n g 2 impinging on such features as length and timing of the breed-ing season, number of broods, type of nesting s i t e , pattern of parental care, or ontogenetic pattern of ne s t l i n g s . A second major stream can be designated as energetics, and has received i t s impetus l a r g e l y through the writings of ODUM [1959 and subsequent editions] and KENDEIGH. This d i r e c t i o n focusses i t s attention on measuring the energy flow throughout the l i v i n g world, and i n the spec i a l case of breed-ing biology attempts to measure how much energy i s involved i n the reproductive e f f o r t of the parents (e.g. c a l o r i c cost of egg production, of incubation, and of ne s t l i n g care), the t o t a l energy content of the food c o l l e c t e d by the parents while r a i s i n g the young, the e f f i c i e n c y of conversion of thi s energy into the growing body of the ne s t l i n g , and the estimation of the quantitative importance of the various avenues into which t h i s energy i s diverted ( l o s t i n faeces, basal metabol-ism, cost of temperature regulation, retention i n body tissues, external work). Due to the formidable d i f f i c u l t i e s that must be overcome before these parameters can be estimated, l e t alone accurately measured, i n the f i e l d , t h i s i s s t i l l a very new area, with l e s s than h a l f a dozen studies conducted to date. In a very thought-provoking paper, ROYAMA [1966] has sought to combine these two approaches i n h i s f i e l d study of the breeding of the Great T i t , Parus major. The philosophy behind h i s study was that the energetics of brood-raising 3 must be i n v e s t i g a t e d i f the q u e s t i o n of the e v o l u t i o n o f b r o o d - s i z e i s to be approached; although h i s t o r i c a l l y d i s t i n c t l i n e s o f thought, the two d i r e c t i o n s i n f a c t can complement one another. ROYAMA r e a l i z e d t h a t unaided o b s e r v a t i o n a t the n e s t c o u l d never supply the r e q u i s i t e data, and t h e r e f o r e d e v i s e d an automatic n e s t - v i s i t r e c o r d e r l i n k e d w i t h a c i n e -camera, y i e l d i n g a n e g a t i v e o f each p a r e n t a l v i s i t . S i nce i n t h i s s p e c i e s food items are brought one a t the time, and are c a r r i e d i n f u l l view i n the b i l l , t h i s method gave complete i n s i g h t i n t o the food brought to the n e s t l i n g s . Growth and d e f a e c a t i o n r a t e o f the n e s t l i n g s was a l s o measured, and an est i m a t e d energy budget c o n s t r u c t e d . The i n t r o d u c t i o n o f the f i l m r e c o r d i n e f f e c t r e p l a c e d a team o f o b s e r v e r s such as had been employed by TINBERGEN [1960] i n h i s now c l a s s i c r e s e a r c h on t h i s s p e c i e s , and was the e s s e n t i a l s t e p i n p u t t i n g t h i s type o f study w i t h i n the reach o f a s i n g l e i n v e s t i g a t o r . My own study was envisaged as an a p p l i c a t i o n and a m p l i f i c a t i o n o f ROYAMA*s approach to e l u c i d a t e the e v o l u t i o n o f b r o o d - s i z e i n the c o l o n i a l l y n e s t i n g a l c i d Cepphus columba, the Pigeon G u i l l e m o t . B a s i c a l l y , the thought was to d e v i s e an automatic camera u n i t to moniter a l l f e e d i n g t r i p s , s i n c e i n t h i s s p e c i e s as i n the T i t the food items are brought i n d i v i d u a l l y and are c a r r i e d i n f u l l view d a n g l i n g from the pa r e n t ' s b i l l , and to i n c o r p o r a t e i n the u n i t a balance so 4 t h a t the weight of the food items c o u l d be determined from the n e g a t i v e . Where ROYAMA's approach was to be extended, i n v o l v e d the c o n t r o l o b s e r v a t i o n s on n e s t l i n g s r a i s e d by hand on known r a t i o n s o f f i s h , f o l l o w i n g the methods employed by KAHL [196 2] on the Wood S t o r k , M y c t e r i a americana. A second i n n o v a t i o n concerned the use o f an o p e n - c i r c u i t metabolism apparatus f o r measuring the response o f the growing n e s t l i n g s to a l t e r a t i o n s i n a i r temperature, as a means of e s t i m a t i n g the c o s t o f temperature r e g u l a t i o n a l o n g the l i n e s o f KENDEIGH's [1939] p i o n e e r study. In o r d e r t o make the f i n d i n g s d i r e c t l y r e l e v a n t to the problem of the e v o l u t i o n o f b r o o d - s i z e , my i n t e n t i o n was to apply these methods not o n l y to the n a t u r a l l y o c c u r r i n g broods of one and two c h i c k s , b ut i n a d d i t i o n to e x p e r i m e n t a l l y induced broods o f thr e e ( " t r i p l e t s " ) . Q u i t e a p a r t from the framework i n which these r e s u l t s are pre s e n t e d , namely the e v o l u t i o n o f brood s i z e i n b i r d s , the da t a have i m p l i c a t i o n s f o r the ways i n which the parents respond q u a n t i t a t i v e l y to the needs of t h e i r c h i c k s , and might a l s o be a p p l i e d i n the study o f the p a r e n t g u i l l e m o t as a p r e d a t o r of f i s h . My main ta s k , however, has been to o b t a i n an energy budget f o r the d e v e l o p i n g c h i c k s , v a l i d f o r f i e l d c o n d i t i o n s , and t h i s t a s k has p r e c l u d e d g i v i n g adequate a t t e n t i o n to the s i d e l i n e s mentioned. Some of these p o i n t s were i n v e s t i g a t e d by AITCHISON [197 2] . 5 My c h o i c e o f the Pigeon G u i l l e m o t as an o b j e c t of study deserves comment. Camera m o n i t e r i n g was c o n s i d e r e d p r e r e q u i s i t e , and i n i t s s i m p l e s t form t h i s l i m i t s the c h o i c e to a h o l e - n e s t i n g s p e c i e s t o l e r a n t enough to accept m o d i f i -c a t i o n s o f i t s n a t u r a l home. Secondly, i t was e s s e n t i a l t h a t my n e s t s be a v a i l a b l e f o r simultaneous study, so i t seemed re a s o n a b l e to c o n s i d e r p r i m a r i l y c o l o n i a l l y - n e s t i n g s p e c i e s . F i n a l l y , i t was important to choose a s p e c i e s where the b a s i c p a t t e r n s of b r e e d i n g had a l r e a d y been worked out [DRENT, 1965, 1964], so t h a t one c o u l d a t the o u t s e t s t a r t t o pose more s o p h i s t i c a t e d q u e s t i o n s w i t h f u l l knowledge o f the normal p a t t e r n . The Pigeon G u i l l e m o t i s a h o l e - n e s t i n g c o l o n i a l b i r d , r e l a t i v e l y t o l e r a n t o f d i s t u r b a n c e , and the b a s i c f e a t u r e s of i t s b r e e d i n g b i o l o g y have been d e s c r i b e d [ S t o r e r , 1952; Thoreson and Booth, 1958; Drent, 1965]. 6 CHAPTER 2 GROWTH AND FEEDING OF THE CHICK A. Methods and M a t e r i a l s F i e l d work was conducted a t Mandarte I s l a n d d u r i n g the s p r i n g and summer o f 1969 and 1970. Mandarte I s l a n d i s l o c a t e d i n the G u l f I s l a n d area o f B r i t i s h Columbia; f o r a d e t a i l e d d e s c r i p t i o n see Drent e t a l ^ . , 1964 . Pigeon G u i l l e m o t s a t Mandarte I s l a n d re-use the n e s t -burrows of the p r e v i o u s season and when my study began the g r e a t m a j o r i t y of the n e s t s were s t i l l used and marked from p r e v i o u s work by Drent [1965]. A c c e s s i b l e n e s t s were checked d a i l y f o r c l u t c h commencement and h a t c h i n g . In the 1969 season the growth of the c h i c k s o f b o t h c o n t r o l and e x p e r i -mental broods was checked d a i l y b ut i n the 197 0 season, i n o r d e r to minimize d i s t u r b a n c e , the c o n t r o l broods were checked every a l t e r n a t e day. The Pigeon G u i l l e m o t normally l a y s a maximum o f two eggs. One-chick broods, however, occur r e g u l a r l y as a r e s u l t o f the f o l l o w i n g f a c t o r s : (1) o n l y one egg l a i d , (2) one o f the two eggs l a i d became a d d l e d . T h i s f a c t o r i s the most common cause o f one-chick broods. (3) death of one of the two c h i c k s . 7 Experimental ly induced three-chick broods or s o - c a l l e d "supernormal" broods were created by adding another chick to a two-chick brood. Care was taken i n choosing a chick of s i m i l a r age and weight to i t s new s i b l i n g s to al low for equal competit ion for food among each o ther . C ontro l broods r e f e r to one- , two- and three-chick broods of which only growth data was obtained, whereas e x p e r i -mental broods had i n a d d i t i o n to the measuring of growth, the automatic camera recording u n i t placed i n f ront of the nest . Chicks i n the two-chick and three-chick broods were marked i n d i v i d u a l l y to d i s t i n g u i s h between them i n c o l l e c t i n g growth, age and f l edg ing d a t a . Each chick was weighed us ing "Pesola" spr ing balances with ranges from 0 to 100 and 0 to 500 grams. The accuracy of each scale was w i t h i n one percent . Along with the weighings, the lengths of the fo l lowing body parts were measured with a s p e c i a l l y constructed r u l e r : 1. "wing" or r a d i o - u l n a r l ength , measured between outer perimeters or condyles , 2. tarso-peda l length measured from the superior condyle to the t i p of the n a i l on the middle toe . The length was measured with the b i r d i n a t y p i c a l p lant igrade p o s i t i o n with the tarsus and foot f la t tened against the r u l e r . 8 3. outermost primary f e a t h e r l e n g t h measured from the t i p to the i n s e r t i o n i n t o the s k i n . 4. b i l l l e n g t h measured l a t e r a l l y as the g r e a t e s t l e n g t h between the t i p and the i n s e r t i o n i n t o the s k i n . An automatic camera r e c o r d i n g u n i t was c o n s t r u c t e d f o l l o w i n g the technique of ROYAMA [1966] w i t h c e r t a i n m o d i f i -c a t i o n s f o r t h i s p r o j e c t ; (1) a 35 mm., h a l f - f r a m e (1/2 x 24 x 36 mm.) camera was used i n s t e a d o f a 16 mm. c i n e camera, (2) i n the hope o f o b t a i n i n g weights of the incoming and o u t -going p a r e n t s , a weighing s c a l e , w i t h a s c a l e range of 500 grams, a c c u r a t e to w i t h i n 1 gram, was added to the r e c o r d i n g u n i t . The s c a l e was equipped w i t h an o i l damper. I t was hoped t h a t t h i s damper would pr e v e n t o s c i l l a t i o n of the weighing pan caused by the waddling motion o f the p a r e n t . The camera u n i t was p l a c e d along w i t h the weighing s c a l e i n a wooden box and p l a c e d i n f r o n t of a n e s t burrow. (F i g u r e 1 ) . To minimize p o s s i b l e d e s e r t i o n or d i s t u r b a n c e to the r e g u l a r b r o o d i n g and f e e d i n g p a t t e r n o f the p a r e n t s , the f o l l o w i n g p r e c a u t i o n s were taken: (1) two to t h r e e weeks p r i o r to a c t u a l o p e r a t i o n , the empty wooden box was p l a c e d i n the v i c i n i t y of the n e s t to a l l o w the parents to become accustomed to the box, (2) d u r i n g the l a s t t hree days the complete u n i t was moved g r a d u a l l y from a l o c a t i o n s e v e r a l meters away from the n e s t to a p o s i t i o n i n f r o n t of the 9 FIGURE 1 Automatic camera recording unit in operation 1. Lead storage battery 2 . Electronic flash control unit 3 . Half-frame 35 mm. camera 4. Plexiglass window 5 . Pocket watch 6. Weighing scale 7. Photoelectric 'eye' 8. Approach ramp to nest-burrow 10 nest , (3) i n order to camouflage the set -up, the box was painted a s la te -grey to blend with the t e r r a i n . A t y p i c a l sequence of events during the d e l i v e r y of a food item i s as fo l lows: 1. one of the parents lands on the approach ramp with a food item hanging from i t s b i l l . The approach ramp i s attached to the h o r i z o n t a l sec t ion i n the box and functions as both a runway to the entrance of the nest-burrow where the chick awaits i t s meal, and a weighing plat form attached to the scale pan, which r e s u l t s i n a needle d e f l e c t i o n on the scale face . The speed by which the parents d e l i v e r the food i s i n the order of four to f i v e seconds and was found to be too f a s t to allow the weighing scale to reach the c o r r e c t va lue . Subsequently, i n the 1970 season the approach ramp was s lanted to reduce the speed of food d e l i v e r y . The Pigeon Gui l lemot walks on i t s t a r s i as we l l as feet (plantigrade) and as a r e s u l t has to waddle e s p e c i a l l y when walking up an i n c l i n i n g s lope . This modi f i ca t ion of the runway was r e l a t i v e l y successful i n curbing the speed of food d e l i v e r y . 2. halfway across the h o r i z o n t a l sec t ion of the r u n -way, the parent walks through a p h o t o - e l e c t r i c l i g h t beam which i s connected with the automatic 11 camera u n i t . When the l i g h t beam i s broken by the b i r d i t t r i ggers o f f the camera u n i t and e l e c t r o n i c f l a s h and a p i c t u r e i s taken (see F igure 1 ) . 3 . the parent proceeds to d e l i v e r the food item to the c h i c k s , turns around and waddles out . Another p i c t u r e i s taken as i n (2), t h i s time without the food item which r e s u l t s i n a lower scale weight. 4 . the parent walks halfway down the approach ramp and immediately f l i e s o f f . Camera and f i l m checks were made twice a day depending on the age and number of feedings , When necessary, the f i l m was replaced and the exposed f i l m developed w i t h i n the next two days. The negatives were immediately examined under a d i s s e c t i o n scope to check for f a u l t y equipment or developing technique. F i n a l t r a n s c r i p t i o n of data from a t o t a l o f approximately 15,000 negatives took place i n the fo l lowing f a l l and winter . By examination of the negatives i t was hoped that a complete record of a l l food items d e l i v e r e d to the nest could be obtained and i d e n t i f i e d at l e a s t to f a m i l y . By subtrac t ing the outgoing from the incoming weight, weight of i n d i v i d u a l food items should be c o l l e c t e d . Since the female parent i s l i g h t e r i n weight than the male by approximately 30 grams, i t was hoped that the outgoing weights would 12 d i f f e r e n t i a t e between sexes, assuming l i t t l e change i n body weight of the parents throughout the course of the day. B. Results 1. Growth of the Chick Mean growth i n body weight and mean d a i l y weight i n c r e -ment of chicks i n broods of one, two and three are shown i n Figure 2 and 3 r e s p e c t i v e l y . No s i g n i f i c a n t d i f f e r e n c e was found between the two seasons and thus the r e s u l t s have been combined. S i m i l a r l y no diff e r e n c e i n growth was apparent between broods i n nest-burrows with a camera u n i t and t h e i r c o n t r o l counterparts. In general, the curve described by the growth data i s t y p i c a l l y sigmoidal and thus can be divided into 3 phases. The f i r s t phase represents the f i r s t 8 days a f t e r hatching and shows a rapid increase i n body weight but not as f a s t as the next phase. No apparent difference e x i s t s between the three brood-sizes i n t h i s early phase, and i s c l e a r l y shown i n Figure 2. The second or middle phase represents the s t r a i g h t l i n e portion by eye of the growth curve and i s thus the period of arithmetic growth. I t l i e s between 8 and 18 days of age. As expected, the d a i l y weight gained (Figure 3) i s greatest during t h i s i n t e r v a l f o r a l l brood-sizes with means of 17.4 grams per day per chick, from single broods, 17.0 grams per day for double broods, and 13.4 grams per day 13 50Ch e — a broods of one, 13 chicks 0...—.0 broods of two, 3 6 chicks A — * broods of three, 18 chicks 10 20 30 Days after hatching 4 0 Figure 2 Growth in body weight in the Pigeon Guillemot, as a function of brood-size Figure 3 Mean daily weight increments for the data presented in Figure 2 15 f o r t r i p l e t broods. Combining s i n g l e s and doubles g i v e s a mean growth r a t e f o r no r m a l - s i z e d broods, which d i f f e r s i g n i f i c a n t l y (P < 0.05) from the r a t e f o r t r i p l e t s . C l e a r l y , c h i c k s i n broods of th r e e s u f f e r a depressed growth r a t e compared t o c h i c k s i n one- and two-chick broods. The e f f e c t o f b r o o d s i z e i s most n o t i c e a b l e i n the t h i r d phase. The weight g a i n per day i s l e a s t depressed i n the s i n g l e c h i c k brood and most depressed i n the th r e e c h i c k brood w i t h the two-chick brood f a l l i n g i n between. S i m i l a r l y , the d a i l y weight increment f a l l s o f f w i t h an i n c r e a s e i n b r o o d - s i z e . Mean wing l e n g t h d u r i n g the f i r s t day a f t e r h a t c h i n g , age z e r o , i s 20.5 mm. and the growth t h e r e a f t e r f o l l o w s a s i g m o i d a l curve i d e n t i c a l to the growth i n body weight ( F i g u r e 4a) w i t h the second phase o r p e r i o d o f a r i t h m e t i c growth f a l l i n g between 8 and 18 days of age f o r a l l t h r e e b r o o d - s i z e s . No c l e a r d i f f e r e n c e i n growth c o u l d be found between the th r e e b r o o d - s i z e s as the g r e a t e r wing growth i n the one-chick brood between 30 and 38 days o f age may be a r e f l e c t i o n o f a s m a l l sample s i z e o f 2 and 3 c h i c k s . The outermost primary f e a t h e r d i d not break through the s k i n and s t a r t to develop u n t i l approximately 5 days o f age, (F i g u r e 4b). The slowest p e r i o d of growth f a l l s between ages 5 and 15 days (1.1 mm. per day) f o l l o w e d by a r a p i d i n c r e a s e to twice the f o r e g o i n g r a t e (2.3 mm. per day) and c o n t i n u e s to grow a t a d i m i n i s h e d r a t e a t the time of f l e d g i n g . The r a t e of growth i s s i m i l a r f o r a l l three b r o o d - s i z e s . 90n tO 20 3 0 tO 0 10 20 3 0 4 0 Days after hatching Days after hatching ure 4 Growth i n wing length (=radio-ulnar length) , as a function of brood-size (a); growth i n primary length as a function of brood-s ize (b); growth i n foot length (=tarso-pedal l ength) , as a funct ion of brood-size (c); growth i n b i l l length (=groatest length) , as a function of brood-s ize (d) 17 T a r s o - p e d a l l e n g t h a t zero day of age i s 43 mm. (Figure 4 c ) , and immediately s t a r t e d to develop a t i t s h i g h e s t r a t e (2.3 mm. per day) t i l l 12 days of age. A t 20 days the t a r s u s and f o o t had almost reached t h e i r f u l l l e n g t h . Again, no d i f f e r e n c e i n the growth r a t e c o u l d be found between the th r e e b r o o d - s i z e s . A b i l l l e n g t h o f 21 mm. was recor d e d d u r i n g the f i r s t day a f t e r h a t c h i n g and s i m i l a r t o the growth r a t e o f the t a r s u s and f o o t i t immediately developed a t a maximum o f 0,9 mm. per day t i l l a p p roximately 13 days o f age then grad-u a l l y d e c r e a s i n g c u r v i l i n e a r l y , s t i l l growing when the c h i c k s f l e d g e d . The growth r a t e appeared to be s i m i l a r f o r a l l b r o o d - s i z e s . ( F i g u r e 4d) 2. P a r e n t a l Care During the F l e d g i n g P e r i o d D u r i n g the 19 69 season s e v e r a l attempts were made to form t h r e e - c h i c k broods, 3 experimental w i t h the camera u n i t and 2 c o n t r o l w i t h o u t the r e c o r d e r . Only one of the c o n t r o l t r i p l e t s was s u c c e s s f u l and no e x p l a n a t i o n can be g i v e n why the o t h e r s f a i l e d . V a r i o u s f a c t o r s may be r e s p o n s i b l e . Even though the added c h i c k was o f s i m i l a r age and weight as i t s new s i b l i n g s i t may have been too young o r not capable o f a d a p t i n g to the new n e s t o r f o r some reason c o u l d not compete f o r food s u c c e s s f u l l y w i t h i t s new s i b l i n g s ; the pa r e n t s d i d not respond to the i n c r e a s e d demand f o r food 18 o r c o u l d not e f f e c t i v e l y i n c r e a s e the food d e l i v e r i e s due to the l o c a t i o n o f the n e s t i n or near the t e r r i t o r i e s or perch s i t e s of a g r e s s i v e Glaucous-winged g u l l s Larus glaucescens and B l a c k O y s t e r - c a t c h e r s Haematopus bachmani and p o s s i b l y o t h e r s p e c i e s of b i r d s r e s i d i n g or n e s t i n g on the i s l a n d [see Drent e t a l ^ . , 1964] . A shortage of c h i c k s d u r i n g the 1969 season p r e c l u d e d f u r t h e r t r i a l s . During the 1970 season no attempts were made to form experimental t r i p l e t s and of the attempted 8 c o n t r o l t r i p l e t s 2 were completely s u c c e s s -f u l and the remaining 6 p a r t i a l l y so. To o b t a i n some i n f o r m a t i o n on the d a i l y frequency o f food d e l i v e r i e s i n the s u c c e s s f u l t r i p l e t of the 1969 season, o b s e r v a t i o n s from a b l i n d were c a r r i e d out and the times o f d e l i v e r i e s between s u n r i s e and sunset r e c o r d e d . (a) D a i l y p a t t e r n F i g u r e 5 shows the e f f e c t o f brood s i z e on the d a i l y f e e d i n g p a t t e r n f o r the e n t i r e f l e d g i n g p e r i o d . The combined d a t a from both seasons f o r the one- and two-chick broods were o b t a i n e d from the automatic camera r e c o r d s ; data f o r the t h r e e - c h i c k brood i n c l u d e b o t h d i r e c t o b s e r v a t i o n s i n 1969 and A i t c h i s o n ' s camera r e c o r d from 1971. For the one- and two-chick broods the h i g h e s t f r e -q uencies of food d e l i v e r i e s o c c u r r e d i n the e a r l y morning between 06 00 and 1000 h r s . ( T h i r t y - s e v e n p e r c e n t o f the d a i l y t o t a l f o r both brood s i z e s ) , and then g r a d u a l l y de-19 6 12 18 6 12 18 Time (PDST) Time (PDST) Figure 5 D a i l y feeding pattern, based on frequency of food d e l i v e r i e s , as a f u n c t i o n of brood-size. The histogram shows hourly i n t e r v a l s , and a summary i s given a t the r i g h t i n 2-hourly p e r i o d s , where the r a t e between 0700 and 0900 hours was taken as 100% creased to a f i n a l low number between 2000 and 2100 hrs. The rate of decrease i s f a s t e s t and continuous through the day i n the one-chick brood, whereas i n the two-chick brood the l a t e morning decrease i s only temporary and i s followed by an increase i n the afternoon, between 1300 and 1800 hrs., a f t e r which feeding frequency drops o f f to cease at dusk. Most noticable i s the frequency plateau i n the three-chick brood where no decrease i s evident u n t i l the evening, past 1800 hrs. C l e a r l y a constant frequency l e v e l i s maintained throughout the day. When the mean for every two hours i s taken and 100% i s assigned to the peak d a i l y frequencies 0700 - 0900 hrs. for a l l brood-sizes, the above described d a i l y frequency pattern are more c l e a r l y d i f f e r e n t i a t e d (Figure 5, right-hand s i d e ) . The Pigeon Guillemot feed t h e i r chicks only during the d a y l i g h t hours, leaving the chicks f o r the night, except for the i n i t i a l brooding period when one of the parents broods the chick overnight [Drent, 1965] . From personal observations from a b l i n d and the conclusive record of times for the f i r s t food d e l i v e r y from the recording u n i t s , the f i r s t feeding of the day takes place approximately 1 1/2 -2 hours a f t e r sunrise and becomes l a t e r as the season progresses and the number of daylight hours decrease (Figure 6a). This timespace i s l i k e l y due to time required by the parent for f i s h i n g a c t i v i t i e s , including i t s own needs, and to f l y from the f i s h i n g grounds to the nest. S i m i l a r l y a 21 1<H P o 7 E h 6H l a s t f o o d d e l i v e r y c i v i l t w i l i g h t —o- o , —-o— "O ... s u n s e t f i r s t f o o d d e l i v e r y —o s u n r i s e c i v i l t w i l i g h t j2 6 1 o O 4 . <D E z 19 Figure 6 —[——1 1 1 r~ 2 0 21 2 2 Time ( P D S T ) F i r s t and l a s t parenta l food d e l i v e r i e s p l o t t e d i n r e l a t i o n to P . D . S . T . i n nest S-5, 1969 (a); the times of nest departure ( P . D . S . T . ) of chicks from 8 nests for the 1969, 1970 and 1971 seasons [Ai tch i son i n c l . ] (b) 22 the l a s t feeding f o r the day occurs approximately 1 1/2 - 2 h r s . a f ter sunset and becomes e a r l i e r along with the time the sun sets as the season progresses . The parent makes i t s l a s t f i s h i n g t r i p probably jus t p r i o r to sunset and subsequently cannot make the d e l i v e r y to the chicks u n t i l a f t e r sunset, r e q u i r i n g the same timespace p r i o r to the f i r s t food d e l i v e r y . F igure 6b shows a s t r i c t d a i l y rhythm i n the time of nest departure . (b) Seasonal pat tern (i) feeding frequencies Data on feeding frequencies have often been used as an i n d i c a t i o n of the quant i ty of food brought, and the o r i g i n a l i n t e n t i o n i n th i s study was to use feeding frequencies as a measure of food q u a n t i t y . However, ana lys i s of the f i l m records soon revealed c o n f l i c t i n g trends i n the s i ze of the food item at the various nests , making comparisons on th i s bas i s mis l ead ing . As an example, nest S-5 [1969] shows an increase i n the mean s i ze of blenny with age, nest B i n 1970 shows f i r s t a dec l ine and l a t e r an increase , and the same nest i n the 1971 season [Aitchison 197 2] a continuous dec l ine i n mean blenny s i ze (Figure 7 ) . C l e a r l y , frequencies are not a r e l i a b l e bas is for comparison (note that mean blenny weight v a r i e s by a fac tor of two i n the example shown i n the f i g u r e ) , 8 n 3 1 0 15 2 0 2 5 3 0 3 5 4 0 Days after hatching Figure 7 Mean blenny weight as a f u n c t i o n of n e s t l i n g age a t three guillemot nests (chronology: nest S-5, 1969, day 10 = 27 July nest B, 1970, day 10 = 5 August nest B, 1971, day 10 = 27 July) 24 and hence f u r t h e r a n a l y s i s w i l l be based on the computed d a i l y t o t a l f i s h weight brought to the n e s t . ( i i ) t o t a l d a i l y f i s h weight f r e q u e n c i e s A more meaningful comparison on p a r e n t a l f e e d i n g between b r o o d - s i z e s i s the t o t a l f i s h weight d e l i v e r e d by the p a r e n t s per day as a f u n c t i o n o f c h i c k age ( F i g u r e 8 ) . One of the purposes o f the weighing s c a l e i n the automatic camera u n i t was to a l l o w computation of the f i s h weights by s u b t r a c t i n g the p a r e n t ' s o u t g o i n g weight from the parent's incoming weight. Upon c l o s e examination of the r e s u l t s from the p h o t o g r a p h i c n e g a t i v e s i t was d i s c o v e r e d t h a t the weights o f the food items d e l i v e r e d v a r i e d too much i n r e l a t i o n t o the s i z e of the f i s h to be m e a n i n g f u l . Causes f o r t h i s v a r i a t i o n c o u l d l i e w i t h the poor damping of the o s c i l l a t i o n due t o e i t h e r the waddling motion o f the p a r e n t o r the e f f e c t s o f the wind on the runway o r b o t h . Subsequently, i t was d e c i d e d to measure the l e n g t h o f the f i s h w i t h a d i s s e c t i o n -scope equipped w i t h a t r a v e l l i n g v e r n i e r s c a l e and to c o n v e r t the v e r n i e r l e n g t h to a c t u a l l e n g t h (120 v e r n i e r d i v i s i o n s = 180 mm. a c t u a l l e n g t h ) . In agreement w i t h Drent [1965], a t l e a s t 75% of the f i s h d e l i v e r e d c o n s i s t e d o f b l e n n i e s and s c u l p i n s and d i e t c o m p o s i t i o n v a r i e d g r e a t l y between n e s t s (Table I ) . 25 TABLE I Types o f Food Brought to 6 Nests d u r i n g the 1969 and 1970 Seasons .Number Percentage 1. B l e n n i e s X i p h i s t e r i d a e P h o l i d a e S t i c h a e i d a e Lumpenidae 1173 63.8 2. S c u l p i n s C o t t i d a e 242 13.2 3. P a c i f i c h e r r i n g C l u p e i d a e Clupea p a l l a s i i 36 2.0 4. Sandlance Ammodytidae 101 5.5 5. Shrimp M a l a c o s t r a c a 12 0.7 6. F l a t f i s h B othidae P l e u r o n e c t i d a e 47 2.6 7. Poachers Agonidae 32 1.7 8. R i v e r Lampreys Petromyzontidae Lampetra a y r e s i 14 0.8 9. U n i d e n t i f i e d spp. 184 10.0 1841 100 .0 26 Since i t was not always poss ib le to key the f i s h on the negatives to species , i t was decided to i d e n t i f y the food items only to fami ly , ass igning both the fami l i e s Pholidae and St ichaeidae to the common category of b l e n n i e s . A length versus weight graph was constructed for blennies and sculp ins from samples c o l l e c t e d i n the f i e l d and from f i s h found i n the nest-burrows of the Pigeon Gui l l emot . By p l o t t i n g the converted vern ier length of the "negative" f i s h on the l e n g t h / weight graph constructed for that category of f i s h , the mean weight can be read o f f the absc i s sa . Any e r r o r caused as a r e s u l t of t h i s method would be at random. The weights for the small number o f other food items brought i n by the parents which inc lude poachers, f l a t f i s h , lampreys, sandlances and shrimps were approximated from a small number of samples found i n the nest-burrows of the Pigeon Gui l l emot . The f ishweights c a l c u l a t e d by t h i s method form the source of Figure 8; t o t a l f i s h weight i n grams per chick per day for the three brood- s i ze s . The graph c l e a r l y demon-s trates that with an increase i n brood-s ize there i s a p r o p o r t i o n a l decrease i n the amount of food d e l i v e r e d to each chick for the e n t i r e n e s t l i n g p e r i o d . I t i s evident that a long plateau of t o t a l food weight de l ivered by the parents i s maintained between approximately 11 and 30 days of age for a l l the brood-s izes with a dec l ine i n food input therea f t er . The sudden increase i n t o t a l food weight jus t p r i o r to f l edg ing i n the one-chick brood may be a r e f l e c t i o n of a small sample s i ze of only 2 nests . 1 4 0 n 9 1 2 0 - A E 4 0 " o — © broods of one • o o broods of two 2 0 - * A broods of three , 1 1 1 r- 1 1 i O 1 0 2 0 3 0 4 0 Days after hatching F i g u r e 8 D a i l y f o o d r a t i o n (grams o f f i s h d e l i v e r e d p e r ^ c h i c k per d a y ) , as a f u n c t i o n o f b r o o d s i z e f o r G u i l l e m o t n e s t l i n g s (Means f o r one t r i p l e t [ A i t c h i s o n , 1972], 5 d o u b l e b r o o d s , and 5 s i n g l e broods) CHAPTER 3 ENERGETICS A. Methods and M a t e r i a l s 1. T hermoregulation and B a s a l Metabolism A l a b o r a t o r y was b u i l t to h o l d equipment ne c e s s a r y f o r c o n d u c t i n g experiments on t h e r m o r e g u l a t i o n and b a s a l metabolism of the Pigeon G u i l l e m o t . I t was d e c i d e d to employ an o p e n - c i r c u i t g r a v i m e t r i c method of measuring Carbon D i o x i d e p r o d u c t i o n . T h i s method was d e v i s e d by Haldane [Brody 1942: 324] m o d i f i e d f o r t h i s purpose, and i s simple t o o p e r a t e e s p e c i a l l y i f the R.Q. i s not r e q u i r e d . The Pigeon G u i l l e m o t c h i c k s and a d u l t s are a d i u r n a l s p e c i e s , r e s t i n g a t n i g h t t i m e . In order to o b t a i n t r u e b a s a l c o n d i t i o n s and the l e a s t v a r i a b i l i t y i n r e a d i n g s , A s c h o f f and Pohl [1970] suggest t h a t measurements of b a s a l metabolism should be c a r r i e d out on animals i n a p o s t - a b s o r p t i v e s t a t e , i n the thermoneutral zone and w i t h o u t p h y s i c a l movement, a t a g i v e n l i g h t i n t e n s i t y , and a t a s p e c i f i e d stage of the d i u r n a l c y c l e . In o r d e r to f i t these s p e c i f i c a t i o n s , measurements were taken a t n i g h t t i m e . Although t r u e " b a s a l " o r "standard" c o n d i t i o n s are not met u n t i l a f t e r 24 hours f o l l o w i n g 29 cessation of food, the R.Q. values approximate the f a s t i n g metabolic rate within 3 hours following the onset of darkness [Romijn and Lokhorst, 1966]. The bird's R.Q. i s assumed at approximately 0.70 for f a t combustion. Lusk's tables f o r an R.Q. of 0.70 gives a constant thermal equivalent of 3.41 Kcal./mg. C0 2 produced [Brody 1942: 310]. Chicks of various ages and adults were c o l l e c t e d from the f i e l d j u s t p r i o r to sunset and subjected to tests on thermoregulation and measurements of basal metabolism during the night. A single b i r d was put i n a metal container, appropriate for the size of the b i r d , and as a whole were placed i n a cabinet i n which the temperature was thermostatic-a l l y c o n t r o l l e d within 1-2 °C of the desired temperature. Dried a i r was pumped through the container at a cont r o l l e d rate of 60 l t r s . / h r . Body temperatures were measured by i n s e r t i n g a f l e x i b l e thermocouple about 10 mm. into the rectum, and secured with a c l i p to feathers around the cloaca. The birds were able to move f r e e l y but generally s e t t l e d down a f t e r a few minutes of being placed i n the temperature cabinet. Steady l e v e l s of CC>2 production and body temperature were reached a f t e r 1-2 hrs. The set-up and procedure have been tested and succe s s f u l l y used by Drent [1971] . The n i g h t l y tests extended over 8 to 12 hrs. during which the temperature i n the cabinet was raised and lowered gradually i n stages of 2-3 °C, within an extreme range of -5 to +32 °C. Tests usually began at ambient temperature and 30 proceeded toward one extreme and then towards the o ther . CG*2 product ion was measured over 20 minute i n t e r v a l s and dupl i ca ted for each temperature s e t t ing i f the r e s u l t s were i n agreement, otherwise more runs were c a r r i e d out . To measure CC^ product ion , a i r from the drum was l ed i n succession through two U-tubes of " d r i e r i t e " and two of "ascar i t e ," which r e s p e c t i v e l y absorbed water and CC^; amounts of CC»2 were determined by weighing the A s c a r i t e tubes on a M e t t l e r balance before and a f ter each 20 minute r u n . Heat product ion was c a l c u l a t e d by m u l t i p l y i n g the weight of CC>2 captured with the thermal equivalent of CC»2 • The e r r o r introduced by neglect ing u r i n a r y N loss i s l e s s then 0.2% [Romijn and Lokhorst , 1966] . 2. Carcass Ana lys i s The above procedure was used i n measuring basa l metabolism and d e f i n i n g thermoneutral zone. Further estimates on heat product ion were obtained from coo l ing rates of Pigeon Gui l lemot carcasses . Chicks of various ages were c o l l e c t e d from the f i e l d during the 1970 season and s a c r i f i c e d and put i n a deep freezer for l a t e r determination of surface area and volume, thermal conductance, gross f a t , ash, moisture and heat of combustion. This work was c a r r i e d out on campus of the U n i v e r s i t y of B r i t i s h Columbia during the f a l l and winter of 1970. 31 (a) Cool ing Rate Determination The frozen carcass was thawed overnight and placed i n an oven set at 40 °C t i l l the core temperature of the carcass had reached ambient oven temperature. The carcass was then suspended by the b i l l i n a large p l a s t i c box ins ide a temperature cab inet , set at 0 ° C , to prevent uneven c o o l -ing due to co ld fan-dr iven a i r current s , which c i r c u l a t e through the cabinet*. A f l e x i b l e YSI thermal probe was inser ted through the b i l l down the oesophagus in to the proventr i cu lus or as f a r as p o s s i b l e , and a YSI needle probe stuck into the v i s c e r a l c a v i t y with the point of the needle located i n the core r e g i o n . Care was taken not to d i s t u r b the plumage. Needle, p r o v e n t r i c u l a r and ambient temperature readings were taken every 5 minutes for at l e a s t one hour, on a YSI 5-channel temperature meter, accurate to w i th in 0.1 ° C , and corrected for meter d e v i a t i o n s . The average ambient temperature was subtracted from each corrected needle and p r e v e n t r i c u l a r read ing . The drop i n temperature over a given time i n t e r v a l as w e l l as the i n d i v i d u a l readings of the v i s c e r a l c a v i t y and p r o v e n t r i c u l a r were checked to be equa l . The carcass was then removed and weighed on a M e t t l e r balance , accurate to w i th in 0.5 gram, and the coo l ing rate of the carcass determined as a drop per °C gradient per hour. The c o o l i n g rate i s used i n c a l c u l a t i n g the rate of heat l e ss for the whole carcass ( K c a l . / ° C x h r . ) by employing the s p e c i f i c heat of b i r d tissue, 0.83 Kcal./°C x gm. [Misch, 1960] and body weight. The t h e o r e t i c a l value for heat production i s then computed by multiplying the rate of heat loss by the gradient, i . e . the lower c r i t i c a l temperature of a Pigeon Guillemot of s i m i l a r age and weight minus the ambient temper-ature at that L.C.T.), (Kcal./°C x hr. x °C gradient). (b) Surface Area Determination Following the procedure i n (a), the same carcass was plucked c a r e f u l l y and as thorough as possible, c o l l e c t i n g and weighing the feathers i n a p l a s t i c bag of known weight. The denuded b i r d was again suspended by the b i l l and the body surface covered with s i l i c o n e sealant except for the feet, b i l l and wings. As such i t was allowed to dry for 1 day and before removing the coating the contours of a l l 4 sides of the wings traced on paper. The coating was then divided into equal segments, pressed and pinned firmly on paper and the outlin e s traced. The surface area of the b i r d below the feathers was then determined with a planimeter. After removal of the coating the b i r d was weighed again on a Mettler balance and then suspended i n water i n a large graduated c y l i n d e r . The d i f f e r e n c e i n waterlevel before and a f t e r the suspension represents the volume and should approximate the weight of that carcass ( s p e c i f i c weight of b i r d tissue i s 1.) The surface area obtained as such was used i n c a l c u l a t i n g 2 thermal conductance = Kcal./cm. x hr. x °C, 33 (cooling rate) (body weight) ( s p e c i f i c heat)  2 " ' surface area x hr. (c) Gross Fat Determination Following the surface-area determination, the carcass and feathers are freeze-dried to constant weight, and weighed accurately to one decimal on a Mettler balance before and a f t e r freeze drying to give moisture content. The dried feathers are placed i n an a i r - t i g h t p l a s t i c bag and stored i n a freezer. Rather than following the methods employed by B r i s b i n [19 68] i n taking aliquots of the ground-up carcass the Pigeon Guillemot chicks and adults are small enough (maximum 500 grams) to allow whole-carcass a n a l y s i s . Subse-quently the frozen-dried carcass i s placed i n a large b o t t l e containing petroleum-ether, and allowed to stand for 1 week. The ether i s then removed and the carcass washed twice with fresh ether. A l l the ether i s c o l l e c t e d and f i l t e r e d by suction into a large 1 l t r . round f l a s k followed by d i s t i l l a -t i o n over a hot-water bath to r e t a i n the crude f a t . The f a t i s transferred to a smaller f l a s k of known weight and i s placed i n an oven set at 35 °C, to remove any traces of water. The smaller f l a s k was weighed to constant weight over 3 to 7 days. From l a t e r determination of any remaining crude f a t (see d) i t was calculated that t h i s " u n o f f i c i a l " method r e -moves at l e a s t 98% of a l l the f a t or ether extract. The f a t l e s s carcass was freeze-dried again for 1 day to remove any traces of ether and moisture and then the whole 34 carcass and feathers were immediately ground up i n a 1 quarter volume t r i p l e blade rotary grinder using a 2 mm. mash. The ground material was c o l l e c t e d and mixed i n a b o t t l e with a t i g h t l i d and stored i n a freezer for the following; (d) Ash, moisture, crude f a t or ether extract (Soxhlet extraction apparatus) and heat of combustion (Parr adiabetic Oxygen bomb calorimeter) determinations, adhering to the O f f i c i a l Methods as l a i d down i n the Manual 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 [A.O.A.C. Manual, 10th E d i c t i o n , 1965]. 3. Controlled Feeding of Chicks Control observations on the growth of chicks were car r i e d out at camp during the 1970 season, by r a i s i n g chicks on a d i e t of f i s h of known weight. Attempts were made to feed the chicks a d i e t c l o s e l y to the natural one i n the f i e l d , supplemented, with portions of commercially caught flounders, herring and rock-cod. Chicks of various ages were c o l l e c t e d from the f i e l d the majority (13 of 20) of ages from 5 to 8 days, j u s t past being brooded. They were colour banded for i d e n t i f i c a t i o n and housed i n burrow-like nests, constructed from d r i f t wood, the s i z e and volume being s i m i l a r to the nests i n the f i e l d . P r i o r to the f i r s t feeding, usually at 07:00 hours, the chick were weighed followed by feedings at a rate depend-ing on the age and weight of each chick but usually at 4 5 35 minutes i n t e r v a l s . Care was taken to maintain the weight of each chick proper for i t s age. One hour a f t e r the l a s t feeding (21:00 hrs . ) , they were weighed again, the various body parts (see section A) measured and returned to t h e i r a r t i f i c i a l nests. Of the 20 chicks c o l l e c t e d and raised only 2 chicks fledged successfully at a weight and age s i m i l a r to f i e l d r e s u l t s . The r e s t died at various ages of unknown causes. The average l i f e span at camp was 18 days (one half the natural n e s t l i n g period). Only those portions of the records where growth was s i m i l a r to the growth rate i n the f i e l d were used. Consequently, r e s u l t s on energy retension, i . e . gram food intake to gain one gram gross body weight, compare favourably with s i m i l a r r e s u l t s from the f i e l d . (Figure 16). B. Results 1. Thermoregulation and .Basal Metabolism The basal metabolic rate of Pigeon Guillemot chicks increases c u r v i l i n e a r l y with increase i n body weight with the maximum rate of increase (50%) occurring between hatching and 100 grm. body weight or 6 days of age. Calculations of basal metabolism based on cooling rates appear to be lower i n chicks of 300 grams and over, than on measurements based on r e s p i r a -tory C0 2 production, which may be a r e f l e c t i o n of f a u l t y measuring techniques or i n c o r r e c t assumptions (R.Q.). Figure 9 indicates a rapid increase i n basal metabolism the f i r s t few days following hatching, intercept the Brody-Proctor 100% l e v e l and remain higher than and p a r a l l e l to that l e v e l u n t i l the chicks reach a weight of 200 grams (12 days o l d ) , then gradually l e v e l s o f f to eventually intercept the 100% l e v e l again at the predicted adult value. Data from Drent [1965] has been included (open dots Figure 9) and show good agreement with basal metabolic rates calculated from cooling rates of carcasses for the i n i t i a l phase. 2 Basal metabolism as a function of surface area (m ) versus age (Figure 10) shows a s i m i l a r d r a s t i c increase during the i n i t i a l 6 days a f t e r hatching, and then gradually decreases to adult l e v e l . The graph i s based on values obtained from cooling rates of carcasses and i s thus i n d i c a t i v e of heat conduction and r a d i a t i o n . I t neglects the a b i l i t y of the l i v i n g b i r d to control body temperature by evaporation (convection), posture, degree of f l u f f i n g of the feathers and e f f e c t i v e c i r c u l a t o r y control to d i s t a n t parts of the body. However, any discrepancy that may e x i s t i s a consistent one since the methods used are simple and s i m i l a r for a l l values obtained. The same argument applies to thermal 2 conductance of Pigeon Guillemot carcasses (Kcal./m x °C x hr.) as a function of age (Figure 11). The graph shows a d r a s t i c decrease i n the rate of heat conduction between core and feather surface during the f i r s t 8 to 10 days following hatching. This improvement coincides, with a period of con-37 • r e s p i r o m e t r y 1 1 1 1 1—i— i— |—| 1 1 1 1 1 1— i— i— r— | 100 1000 body weight in grams Figure 9 Basal metabolic rate i n the Pigeon Guillemot n e s t l i n g , with two adults p l o t t e d f o r comparison (A). Values are pl o t t e d according to body weight on a double logarithmic scale on which the Brody-Proctor p r e d i c t i o n for metabolic r a t e of homeio-therms i s a s t r a i g h t l i n e ; the 50% and 150% l i n e s have also been entered. 15 i 1 1 1 1 1 1 1 i O 10 2 0 3 0 4 0 Days after hatching CO Figure 10 Basal metabolic rate per square meter of body surface as a function of age in the Pigeon Guillemot 40 a d u l t s . 0} 10 O 10 20 30 40 Days after hatching Figure 11 Thermal conductance (Kcal. lost per degree centigrade gradient per square meter of body surface per hour) as a function of age i n the Pigeon Guillemot s i s t e n t l y low values of i n s u l a t i v e properties such as plumage (feather weight Figure 12) and f a t content (Figure 15). The rate of heat conduction then gradually decreases c u r v i l i n e a r l y to reach adult values at approximately 30 days of age at which time plumage development i n terms of t o t a l feather weight i s almost completed (Figure 12). 2. Carcass Composition The mean c a l o r i c value of lean-dry carcasses of chicks and adults was determined by combustion at 4.7 5 Kcal. per gram (range 4.7 2 - 4.78 Kcal.) and the combustion value for f a t (ether extract) assumed at 9.00 Kcal. per gram. Figure 14 depicts the trend i n c a l o r i c value of one gram l i v e weight of Pigeon Guillemot chicks and adults with age, and Figure 15 the percentage f a t per lean-dry carcass weight and moisture content i n percentage per l i v e weight per b i r d as a function of age. The c a l o r i c value of l i v e chicks decreases during the i n i t i a l 8 days following hatching, which, as expected, r e s u l t s from a decrease i n f a t and increase i n moisture content. This decline i s then followed by a gradual generally l i n e a r increase i n energy content with correspond-ing increase i n the amount of f a t and decrease i n moisture. During the l a s t few days i n the nest the chicks possess a higher amount of f a t and le s s e r amount of moisture than the parents, which r e s u l t s i n a s l i g h t l y lower adult carcass energy value than chicks p r i o r to nest departure. 25n O 10 20 30 4 0 Days after hatching Figure 12 Plumage weight (in grams) as a function of age for the carcass Pigeon Guillemot analysis (birds sacrificed at various ages) Figure 14 Metabolic intensity (Kcal. per day per gram of l i v e weight) as a function of age i n the Pigeon Guillemot ro 9/ /o i Q C K (D O 0 r t r t ro r t K ro a o o 3 r t ro 3 r t o M l 3 fD o i r t H H* 3 (D H n ro (tO P ftl M l 01 ro r t P> V o ro *o MI ro oi h ro § ro p i ro 3 cr (u h tt ro 01 o >4 t. H i ro ~ 13 H- C H-«Q O H-vQ t r <t < o r t r t ro O § <• 3 »-»ro o H ft H o » ro «+ 3 r t O O ro 3 r t Pi a B> M i "rt ( S C O r f d fat (Lean dry weight) % water content (Live weight) O o o a Q <^ Q — h o z r Q O I T D ' IQ OJ. O 4\ o o I CD o 00 0) O O 2! a> o 00 00 e© 44 2 Values obtained for surface to volume r a t i o (cm. /ml.) versus age (Figure 13) show an increase during the f i r s t four days a f t e r hatching, r a p i d l y decreasing l i n e a r l y to approximately 22 days of age having reached close to adult values and then l e v e l o f f to fledge at a s l i g h t l y higher S:V r a t i o than the adult. 3. Controlled Feeding of Chicks One d i f f i c u l t y with the data on hand-raised birds i s that growth was at times retarded as compared to wild chicks, a r e s u l t due mainly to i n c o r r e c t estimates of the d a i l y r a t i o n required. I t was decided to use only those portions of the camp records where growth was s i m i l a r to the growth rates i n the f i e l d . In computing the weight of f i s h fed to each chick for every gram of body weight gain ("energy retention") f o r both the hand ra i s e d chicks and data from the camera un i t s , i t was discovered that the two sets of data agreed so well to j u s t i f y discussion of a composite curve (Figure 16). The graph indicates a constant rate of converting food into body tissue for approximately the f i r s t three weeks of n e s t l i n g l i f e , the e f f i c i e n c y d e c l i n i n g s t e a d i l y thereafter, r e f l e c t -ing the channeling of the food energy into other avenues. At the end of the n e s t l i n g period the rate of energy retention i n the body i s s i m i l a r to that i n the adult during periods of f a t deposition (one series of data extending over 3 days). O IO 20 30 Days after hatching 40 Figure 13 Surface volume ratio (square centimeters per ml. body volume) as a function of age i n the Pigeon Guillemot u JD M — o E D _^ CP 0 C o '5 - Q <L> _^ cr CO E • CP 3 0 ' 25-20-o 15-10-5-0 Acamp birds (captive chicks) ® field data (camera units) A w e • © A 8 * o A o A A * e © Figure 16 10 2 0 3 0 Days after hatching Rate of converting food into body tissue, plotted as grams of f i s h required to build one gram of bird versus the age of the nestling Pigeon' Guillemot 4 0 ON 47 Hand-raided chicks had to be force fed e s p e c i a l l y i f they were c o l l e c t e d from the f i e l d a t an o lder age, for example the two chicks that fledged success fu l ly a f t er being r a i s e d by hand were brought i n at only 7 days o f age. Furthermore i t was discovered that the l i f e span a t camp decreased inverse ly with increas ing age a t which they were c o l l e c t e d from the f i e l d . The rough handling during force feeding, e s p e c i a l l y o lder c h i c k s , may wel l be the cause of higher food demand. Overnight weight loss i n chicks from hand feeding a t camp (Figure 17) gradual ly increases to a maximum between 25 and 30 days of age (mean values for 5 day i n t e r v a l s ) then tapering o f f r a p i d l y to 40 days of age. n 1 1 1 1 1 1 10 20 30 40 Days after hatching Figure 17 Mean overnight weight loss (expressed as grams per hour) for the hand-raised chicks, as a function of age SYNTHESIS 1. The Growth Process Figure 18 presents i n summary form the time course of growth i n the Pigeon Guillemot. Growth i n body weight, when viewed i n absolute terms (daily increment i n grams) reaches a maximum from about the 8th to 15th day. When t h i s increment i s considered with respect to the ne s t l i n g weight each day, the r e l a t i v e rate of growth i s seen to reach a maximum much e a r l i e r , about the 4th day. The data shows a s i m i l a r onto-genetic pattern as i n two other semiprecocial b i r d species (Table 2); the Glaucous-winged Gull [Vermeer, 1963] and the Wood Stork [Kahl, 1962]. If these processes are r e f l e c t e d i n the food uptake, the implication i s that the quantity brought to the nest d a i l y should be maximal by about the 10th day, but that the e f f i c i e n c y of conversion of food to body mass may well be at peak values much e a r l i e r than t h i s . Follow-ing upon the period of rapid increase i n body weight i s the growth of the plumage, which i s p r a c t i c a l l y at a s t a n d s t i l l u n t i l about day 12, and v i r t u a l l y complete by day 28. My data are inadequate to pinpoint the period of maximal s k e l e t a l growth. Another major process at a peak between day 11 and 21, and tapering o f f l a t e i n n e s t l i n g l i f e , i s the deposition of f a t . When the ne s t l i n g leaves the colony i t has a f a t depot i n excess of that t y p i c a l for adults, and t h i s energy source i s undoubtedly adaptive i n helping to bridge the d i f f i -20-i 4 0 Days after hatching Figure 18 Instantaneous r e l a t i v e growth r a t e (a); t o t a l body weight increments on a d a i l y bas i s (b); and plumage weight increments on a d a i l y bas i s (c) for the Pigeon Gui l lemot n e s t l i n g TABLE 2 Instantaneous Relat ive Growth Rates Compared i n Percentages Species Pigeon Guil lemot, Cepphus columba Glaucous-winged G u l l Larus glaucescens Wood Stork Mycter ia americana Invest igator This study Vermeer, 1963 Kahl 1962 Weight at Hatching 44 grams 65 grams 62 grams Days ( intervals) af ter hatching 0 - 6 14.0 14 .0 21.9 7 - 1 2 11.1 15.7 14 .2 13 - 15 7.2 10.0 10 .6 16 - 20 4.6 4.4 9.0 21 - 26 2.8 4.7 4 .9 27 - 28 1.5 3.4 3.0 29 - 35 1.3 0.7 3 .0 Weight and age at f ledging 38 days 424 grams 45 days 913 grams 64 days 2350 grams U l c u l t t r i a l period of learning to f i s h . I t w i l l be remembered that the ne s t l i n g Pigeon Guillemot commences an independent l i f e from the moment i t leaves the nest f o r the f i r s t time. That t h i s nest exodus (followed at once by colony departure) almost always occurs i n the evening t w i l i g h t period i s reminiscent of the s i t u a t i o n i n other a l c i d s [Greenwood, 1964] and can be viewed as an antipredator device, i n the case of Mandarte f a c i l i t a t i n g escape from marauding Glaucous-winged G u l l s . Figure 19 presents i n condensed form the data f o r food intake. No f i l m records were obtained from the early stages when parental brooding i s s t i l l i n e f f e c t , and the only f i e l d data at t h i s age involve a 36 hour watch where a succession of observers occupied a hide b u i l t at the back of one nest, enabling observation of the feedings at close quarters (approximately 10 inches). V i s u a l estimates were made of the size of f i s h brought, and the type of f i s h noted, allowing subsequent conversion to weights. The agreement with the camp-raised birds i s reasonable. The d a i l y food r a t i o n reaches a plateau value at about the age when the d a i l y weight increment of the chicks reaches i t s maximum, i n agreement with the surmise stated above. As body growth declines, food uptake remains high, and thi s I i n t e r p r e t to mean that a major portion of the incoming energy i s now being channeled into growth of the plumage. In a sense growth i s made up of a succession of energy-demanding processes, regulated by a timetable of p r i o r i t i e s so as to minimize competition for the incoming energy. [cf Portmann, 1945], I t i s tempting to speculate that the plateau of food intake represents the p r a c t i c a l l i m i t of parental feeding i n t h i s species, what Royama [1966] has termed the optimal working capacity. In t h i s view, the pattern of growth found i n the Pigeon Guillemot has been evolved to shorten the ne s t l i n g period as much as possible given the l e v e l of intake that can f e a s i b l y be maintained; t h i s e n t a i l s a time budget of successive use of energy by the major energy demanding com-ponents of growth, rather than a simultaneous development of components. This suggestion i s not a new one, as Kahl [1962] stated the same hypothesis i n his study of the Wood Stork, but i n my case t h i s idea can be tested to a degree by consider-ing parental response to increased broods (see section 3 ) . In comparing the intake data for the Pigeon Guillemot with other studies, one point stands out s t r i k i n g l y . In the Great T i t [Royama, 1966], Wood Stork [Kahl, 1962], Herring G u l l [Spaans, 1972] and S t a r l i n g [Westerterp, 1972], food intake reaches an absolute maximum at or s l i g h t l y a f t e r the age of maximal d a i l y weight increment. This implies that energy demands for growth i n weight are of over-riding importance at thi s age, with the r e s u l t that i n order to balance the intake budget, maintenance costs must be kept low, i . e . to allow growth, the t o t a l energy input must be above and beyond the maintenance r a t i o n . The evolutionary 54 argument would be, given the optimal l e v e l of intake the parent can maintain, growth proceeds at a rate depending on the adaptations made to keep the energy losses at a minimum by (1) huddling, (2) a p p l i c a t i o n of heat by brooding parents, (3) maintaining burrow temperatures high and even and (4) reducing bodily movements, etc. Another way of viewing the intake data i s to compute the proportion of the incoming energy that i s incorporated i n the body t i s s u e s . Since we know the c a l o r i c value of the food f i s h (determinations gave 1.2 Kcal. per gram fresh weight for a sample of food blennies c o l l e c t e d from the nest, compar-ing favourably with values reported for other moderately f a t f i s h : Whiting, 1.02 [Kahl, 1964]; Fundulus, 1.01, Menidia, 1.15, Roccus 1.15 [Brisbin, 1965], as well as the c a l o r i c value of the nestlings body a curve of energy retention can be constructed. I prefer the term "energy rete n t i o n " to "eco-l o g i c a l growth e f f i c i e n c y " used by B r i s b i n and Kahl f o r t h i s concept, as i n the absence i f any data on a s s i m i l a t i o n rate, p a r t i t i o n of energy uses of the incoming food, we are i n f a c t not measuring e f f i c i e n c i e s as such. In the Pigeon Guillemot, a remarkably high proportion of the incoming energy i s channeled into body tissue early i n n e s t l i n g l i f e . As i n other birds where data i s a v a i l a b l e , the curve of energy retention p a r a l l e l s that of instantaneous r e l a t i v e growth, an expression of the f a c t that both measure the high p r i o r i t y of body weight gain at t h i s phase, at the expense of other energy uses. 55 That t h i s period of maximal conversion occurs during the phase of parental brooding deserves mention (in the Pigeon Guillemot one of the parents i s at the nest continuously by day u n t i l day 5, and by night u n t i l day 7). The chick i s maintained i n a warm and stable environment, obviously reducing the amount of energy l o s t to the surroundings as heat. Although parental brooding i s thus advantageous to the chick, t h i s cannot be prolonged i n d e f i n i t e l y as there must come a time when the food demands of the chicks cannot be met by the foraging of a single parent; the duration of the brooding phase must therefore represent a compromise between maximising growth e f f i c i e n c y and permitting the gathering of the r e q u i s i t e energy. The exact form of the curve for energy retention i s open to question. F i r s t , there are no data e a r l i e r than 4 days, and by analogy to other studies a lower retention rate i s to be expected at the outset of n e s t l i n g l i f e . A more serious objection concerns the method of computation. S t r i c t l y speaking, we are comparing the c a l o r i c value of the incoming food to the c a l o r i c value of the weight i n c r e -ment over that period. Since a l l body components are not growing at the same rate, i t cannot be expected that an over-a l l c a l o r i c value for the ent i r e carcass w i l l always be t r u l y representative of the c a l o r i c value of the portion of tissue l a i d down i n the period under consideration. If the increment i s predominantly f a t , for example, a much higher c a l o r i c equivalent per gram w i l l apply than for a protein increment. By considering the c a l o r i c values of the body components ( l e a n weight, f a t , and plumage) f o r n e s t l i n g s o f v a r i o u s ages e s t i m a t e s can be reached f o r the a c t u a l c a l o r i c i n c r e -ments (bomb c a l o r i m t e r y gave the e q u i v a l e n t s f o r l e a n weight, f a t was assumed to have a v a l u e o f 9 K c a l . per gram, and plumage 5 K c a l . per gram; these e q u i v a l e n t s c o u l d be m u l t i p l i e d by the weight o f each component to g i v e the t o t a l c a l o r i c c o n t e n t o f t h a t component). T h i s approach has been taken i n F i g u r e 19 (based on 8 n e s t l i n g s whose weight was normal f o r t h e i r age a t the time o f c o l l e c t i o n ) . The t o t a l c a l o r i c v a l u e of the increment r i s e s s h a r p l y over the f i r s t two weeks, i s a t a peak midway through the n e s t l i n g p e r i o d , and d e c l i n e s t h e r e a f t e r . R e t e n t i o n r a t e s computed from d a t a i n F i g u r e 19 g i v e an o v e r a l l r a t e o f 34% f o r the e n t i r e n e s t l i n g p e r i o d , a h i g h e r f i g u r e than t h a t o b t a i n e d from f i e l d e s t i m a t e s o f food i n t a k e per gram body weight g a i n (see F i g u r e 16) . An a l t e r n a t i v e way of computing t h i s o v e r a l l c o n v e r s i o n r a t e i s to take the t o t a l amount of f i s h r e q u i r e d to r a i s e a Pigeon G u i l l e m o t , and comparing t h i s w i t h the d i f f e r e n c e i n c a l o r i c v a l u e o f a n e s t l i n g and a f l e d g l i n g b i r d . From the f i e l d d a t a , approximately 2400 grams o f f i s h are d e l i v e r e d per c h i c k (= 2800 K c a l . ) , and the increment i n c a l o r i c v a l u e o f the n e s t l i n g s body i s approximately 1001 K c a l . (from comparison of c a r c a s s a n a l y s e s o f 1 day and 35 day o l d c h i c k s ) , f o r an o v e r a l l r a t e o f 35%. *1 iQ C l-l Q fu (U (tl H. 3 H -f t H - ^ O H - < o> 3 «-' rt rt> ft u » i 3 3 01 C » ti) »> g K O fu i Q 3 H -•O (D fD (5 H O 3 fD M 3 ~m O k ; G 3 tn n> r t 3 1 O r t o o til H i • O r t K •> r t Ul O 3 I ^ (B rt o PI n f t fu tu 3 H -H rt H 3 f • n n c H -fu 3 fu O 3 M l H " 01 Oi H-ci H I o i •< tr tn o tu £ a 3 3 (D •< K fu P - tu tr ~ r t fu » < 3* a H -to tn r t O fu (-•• H i 3 H 01 — H i - tr ra — g ~ H . H , fD fu (D h r t 3 tu 3 O tu a 3 r t 3 t r P- H -o 3 tu n H> H - H i r t O P - 3 fu (5 3 O H - r t to, O 3 K fu fu O Q ^< CO Q — h —+-CD ~\ LT Q r r D" I D o I 01 i O I I CD ro O i ro ro cn I ro 0 OJ O i w O O ro o o o o o o O Q JBMR body components j j intake • • O CT f ? CO a § -s O cn Q. fD ZT Q DD o Q. <^ O o 3 o D fD D I • ' II I . " BMR + body components 58 The two captive chicks raised s u c c e s s f u l l y at camp required approximately 34 00 grams of f i s h each to complete development, thus reaching only a 25% rate of energy ret e n t i o n . I t can be assumed that with the more frequent feedings i n the f i e l d , a more e f f i c i e n t use of the incoming energy could be attained, so that the true f i g u r e for the conversion r a t i o i n the Pigeon Guillemot i s probably closer to the f i e l d estimate of approximately one-third. How does th i s compare to other f i s h - e a t i n g birds? In no other study are f i e l d data a v a i l a b l e on food intake, but captive Herring Gulls have been raised by B r i s b i n [1965] and Spaans [1971] , Wood Storks by Kahl [1962], and a p a r t i a l record on Brunnich's Murre provided by Tuck and Squires [1955]. On a c a l o r i c basis B r i s b i n reports an o v e r a l l conversion rate of 26% f o r the Herring G u l l , and Kahl gives estimates f o r c a l o r i c equivalents enabling an approximation of 24% to be c a l c u l a t e d . These figures are astonishingly close to the value for the hand-raised guillemots. A comparison can also be made on the basis of grams of f i s h delivered per gram of gain i n body weight over the n e s t l i n g period: Cepphus columba 6.5(field) 9.1 (captive) [this paper] Mycteria americana 6.8 (captive) [Kahl, 1962] Larus argentatus 9.7 (captive) [Spaans, 1971] Uria lomvia 13.4 (captive) [Tuck and Squires, 1955] 59 The figure for Uria should be corrected downwards, since the records do not include the e a r l i e s t , and presumably most e f f i c i e n t , phase of growth. Considering the many uncertain-t i e s i n the o r i g i n a l data, the degree of agreement i s r e -markable, and suggests that the conversion of f i s h to body tissue i n growing birds goes on at a c e r t a i n rate (perhaps l i m i t e d by biochemical factors) regardless of the group of birds involved. A complete energy budget for the growing Pigeon Guillemot cannot yet be offered, since no attempt was made to assess faecal output or external work ( a c t i v i t y ) . Some idea of where the incoming energy goes can be given by taking the data from metabolic runs as an i n d i c a t i o n of minimal maintenance needs, data from carcass analysis to show c a l o r i c increments of the three body components (lean body = primarily muscle, f a t , and plumage), and data from the camera units for food intake. These data are assembled i n Figure 19, and show that the difference between intake and expenditure as represented by maintenance and growth i s of the order of 25% over the whole n e s t l i n g period. D i g e s t i b i l i t y of a f i s h r a t i o n by growing birds i s not known, but must obviously be high as a c t i v i t y must also be represented i n the remaining 25% as well as faecal l o s s . 60 2. Development of Temperature Regulation As reviewed by King and Farner [1961], a complex of factors are involved i n the establishment of functional temperature regulation: a changing surface/volume r a t i o , a r i s i n g metabolic rate, and growth of the plumage, may a l l be involved along with the establishment of r e q u i s i t e control mechanisms. In the case of the Pigeon Guillemot, the surest i n d i c a t i o n of e f f e c t i v e temperature regulation i s the cessation of brooding by the parent b i r d s . . The n e s t l i n g i s independent of a supplementary heat source by about day 5-7, so we can ask the question, which of the above contributory factors has made spectacular s t r i d e s i n the f i r s t week of n e s t l i n g l i f e . Comparison of the figures presented e a r l i e r make i t cle a r that growth of the plumage i s not involved at a l l , and that the dominant event i s the boosting of the metabolic rate, with a small contribution being made by a somewhat more favourable surface/volume r a t i o . The spec-tacular changes i n basal metabolic rate shown for the Pigeon Guillemot, with the n e s t l i n g r e s p i r i n g at rates i n excess of that expected of adult homoiotherms of s i m i l a r weight, show a pattern resembling that found i n the young of many other animals including man [for review, see Aschoff, 1970]. 61 3. The Problem of Brood Size Mean growth curves for the 1969 and 1970 seasons are presented i n Figure 20 to show the dependence of weight gain on brood s i z e . Singletons grew the most r a p i d l y and were noticeably heavier at fledging than twins (Table 3a) which were i n turn fa s t e r growers than t r i p l e t chicks. The comparison i n Figure 20 shows that the slower-growing chick of the p a i r i n the twin broods experienced a growth rate comparable to that of the fastest-growing chick of the t r i p l e t broods. The i n t e r p r e t a t i o n of these findings i s made e a r l i e r by looking f i r s t at growth records for the same nests i n other seasons. For some reason growth i n 1969 and 1970 i n p a r t i c u l a r was less rapid than i n eith e r 1959, 1960, or 1971 (mutually i n d i s t i n g u i s h a b l e ) . The s i g n i f i c a n t point i s that growth i n singleton broods i s equal i n a l l years, while growth i n twin broods i s indistinguishable from that i n singletons i n 1959, 1960 and 1971 (the "good" years) but lags behind as we have seen i n 1969 and 1970. The most pl a u s i b l e explanation would r e l a t e poor growth i n the l a t t e r years to a depressed a v a i l a b i l i t y of food items, since there does not seem to be an i n t r i n s i c reason why the parent Pigeon Guillemot cannot r a i s e two chicks as well as one [witness, 1959, 1960, and 1971]. Seasonal differences i n the growth rate of Glaucous-winged Gulls on the same i s l a n d have also been documented [Ward, i n preparation] but i n t e r e s t i n g l y the poor years do not correspond with the poor years for guillemots [1971 being 62 500 -1 i 1 1 1 1 1 1 1 o 10 20 3 0 4 0 Days after hatching Figure 20 Growth as a function of brood-size i n the Pigeon Guillemot. Plotted are the means f o r a l l data from 1969 and 1970: singletons are corcpared with the f a s t e s t and slowest-growiny i n d i v i d u a l s of the twin broods, and the f a s t e s t and slowest-growing i n d i v i d u a l s of the t r i p l e t broods the. a l l time low], making i t u n l i k e l y that some basic weather factors are involved. Although the young g u l l s are also raised predominantly on f i s h , the species involved d i f f e r considerably (herring, for instance, being a staple item although comprising less than 2% of the d i e t of n e s t l i n g guillemots). No quantitative information on f i s h stocks i s a v a i l a b l e to t e s t the idea of a l t e r a t i o n s i n the abundance of food f i s h from year to year. Table 3b shows the fledging success of the various brood-sizes on Mandarte Island. Even though as we have seen growth may be depressed i n c e r t a i n years, the success of the Pigeon Guillemot i n r a i s i n g twins i s as high as that for singletons. A marked drop occurs when we consider the a r t i f i c i a l l y constituted t r i p l e t broods. Overall success i s poor, and only i n a single instance did two of the chicks a t t a i n weights comparable to the fledging weights of chicks from normal broods [1971 experiment]. There i s ample evidence for the view that an impaired fledging weight w i l l lessen the chances of s u r v i v a l a f t e r nest departure [Perrins, 1965; Robertson, 1971; Ward, i n prep.) so that i t i s safe to con-clude that the eventual recruitment from t r i p l e t broods would at best be only marginally greater than the recruitment from twin broods. In these circumstances there would be no s e l e c t i o n pressure for an increased brood s i z e . Examination of the records on food intake i n the various brood-sizes i s revealing. Twins receive a maximal 64 TABLE 3a Fledging Age and Weight as a Function of Brood-size Brood-size Age (days) Weight (grams) Number of Nests one chick 34.8 430.0 11 two chick 33.9 407.0 15 three chick 37.3 385.0 5 TABLE 3b Fledging Success of the Pigeon Guillemot as a Function of Brood-size ( A l l Years) Brood-size Sample Number Fledged Average per Nest one chick n=23 20 0.9 two chick n=60 103 1.8 three chick n=17 33 1.9 d a i l y t o t a l of approximately 200 grams of f i s h from day 10 to 30 according to the two complete camera records on broods of t h i s s i z e [one from 1970, and one from 1971] . The single t r i p l e t nest studied by Aitchison [1972] y i e l d s figures of s i m i l a r magnitude (15-day plateau gives a mean of 195 grams of f i s h per day). We can also compute the weight of f i s h that must have been delivered to the 1970 t r i p l e t s to obtain the observed growth increments (using the conversion rates i n Figure 21). In t h i s case the computed d a i l y f i s h t o t a l works out to 198 grams (plateau value over 20 days). I conclude from these figures that there i s no evidence that the parent Pigeon Guillemots brought more f i s h to the t r i p l e t nests d a i l y than they d i d to the normal twin broods. The reason why i n c e r t a i n cases t r i p l e t s could i n f a c t be ra i s e d , although at a slower rate of growth, i s that the plateau values were maintained for a longer period at these nets leading to a larger t o t a l f i s h input over the whole ne s t l i n g period. Differences i n the d a i l y feeding pattern between brood-sizes (Figure 5) might lead to the mistaken b e l i e f that more food i s delivered with an increase i n brood-size. However, these d a i l y feeding frequencies are nest s p e c i f i c (see Figure 7) as the mean s i z e , and thus weight, of the food items vary between nests. There i s ample evidence that the parent Pigeon Guillemot responds to the hunger needs of the chicks (experi-ments c i t e d i n Drent, 1965 and Aitchison, 1972] so that the i n a b i l i t y of the parents to bring more than the 200 gram d a i l y r a t i o n to the t r i p l e t nests must r e f l e c t d i f f i c u l t i e s i n food precurement, rather than i n communication between the chicks and the parents. The parent birds at the t r i p l e t nest d i d not experience a decline i n body weight during the n e s t l i n g period, i . e . there i s no evidence that they were i n a s i t u a t i o n of s t r a i n . Apparently the p r i o r i t y i n t h i s species i s for unimpaired s u r v i v a l of the parents, over-riding the requirements of the brood. This i s generally true f o r long-lived birds [Cave, 1968; Southern, 1970] where the adopted strategy ensures greatest p r o b a b i l i t y of renewed breeding i n the following season, rather than production under d i f f i c u l t conditions at possible r i s k to the adult. Bergman's [1971] findings are highly s i g n i f i c a n t i n t h i s regard. Bergman studied the Black Guillemot, Cepphus g r y l l e , the old-world counter-part of the Pigeon Guillemot (some authors have even considered the two forms conspecific) at the edge of i t s range i n Finland. In the study area the n e s t l i n g guillemots were fed almost e n t i r e l y on Zoarces v i v i p a r u s , and i n one season a s c a r c i t y of these f i s h led to a v i r t u a l l y complete withdrawal of the adult guillemots from the study area, and an almost t o t a l nesting f a i l u r e as a r e s u l t (eggs and chicks being abandoned by almost a l l parents between 13 July and 4 August). 67 D. Summary To summarize, the "optimal working capacity" of the parent Pigeon Guillemots at mandarte Island appears to be a t o t a l d a i l y f i s h r a t i o n of 200 grams. In no case were parents observed to bring more than t h i s amount when means were computed over 5-day periods, and the r e s u l t i n g l i m i -t a t i o n expresses i t s e l f i n a depressed growth rate i n t r i p l e t broods ( a r t i f i c i a l , super-normal broods) i n a l l seasons, and i n twin broods i n c e r t a i n years. I conclude that the parent guillemots are unable to r a i s e a t r i p l e t brood to reach normal fledging weights because they are already working at f u l l capacity when r a i s i n g a brood of two. The parent does not endanger i t s own su r v i v a l i n favour of i t s brood, but maintains body weight i n a l l circumstances (in extreme cases even abandoning the brood altogether as we know from Bergman's work). The "optimal working capacity" of the parent Pigeon Guillemot constitutes about 22% of the parental body weight, si m i l a r to the maximal d a i l y food r a t i o n that can be computed from Kahl's [1962, 1964] study of the Wood Stork: each parent brings 15-20% of i t s own weight to the nest d a i l y . Since f i s h - e a t i n g birds i n general require about one f i f t h to one-t h i r d of t h e i r body weight as a d a i l y adult food requirement [summary i n Spaans, 1971, to which can be added Skokowa, 1962, Jordon, 1967, Robertson, 1972, Kahl, 1964] we can state 68 that the parent Pigeon Guil lemot doubles the rate of f i s h i n g when feeding i t s nes t l ings (requirement for i t s e l f about 20% or 90 grams d a i l y , share i n n e s t l i n g food about 100 grams da i ly ) as does the Wood Stork . I t i s u n l i k e l y that t h i s w i l l turn out to be a general r u l e , however, s ince the a v a i l a b l e data for the Herring G u l l [Spaans, 1971] would i n d i c a t e a t r e b l i n g of parenta l f i s h i n g rate at the peak. LITERATURE CITED A i t c h i s o n , N.W. 1972. The Pigeon G u i l l e m o t , Cepphus columba: Breeding b i o l o g y and b r o o d - s i z e . B.Sc. T h e s i s , Univ. B r i t . C o l . A s c h o f f , J . and P o h l , H. 1970. Der Ruheumsatz von Vogeln a l s F u n k t i o n der T a g e s z e i t und der K o r p e r g r o s s e . J . Orn. 111:38-47. A s s o c i a t i o n of O f f i c i a l A g r i c u l t u r a l Chemists Manual, 10th e d i t i o n , 1965. Bergmann, G. 1971. G r y l l t e i s t e n Cepphus g r y l l e i n einem Randgebiet: Nahrung, B r u t r e s u l t a t , Tagesrhythmus und A n s i e d l u n g . Comment. B i o l . 42:26 pp. B r i s b i n , I . Lehr J r . 1965. A q u a n t i t a t i v e a n a l y s i s o f e c o l o g i c a l growth e f f i c i e n c y i n the H e r r i n g G u l l . M. Sc. T h e s i s , Univ. o f Geo r g i a , Athens, G e o r g i a . B r i s b i n , I . Lehr J r . 1968. A d e t e r m i n a t i o n o f the c a l o r i c d e n s i t y and major body components of l a r g e b i r d s . Ecology 49:792-794. Brody, S. 194 5. B i o e n e r g e t i c s and growth. New York. Cave, A . J . 1968. The b r e e d i n g o f the K e s t r e l , F a l c o t i n n u n - c u l u s L., i n the r e c l a i m e d a r e a O o s t e l i j k F l e v o l a n d . Neth. J . Z o o l . 18:313-407. Drent, R.H., G.F. van T e t s , F. Tompa, and K. Vermeer, 1964. The b r e e d i n g b i r d s o f Mandarte I s l a n d , B r i t i s h Columbia. Canad. F i e l d . Nat. 78:208-263. . 1965. Breeding b i o l o g y of the Pigeon G u i l l e m o t , Cepphus columba. Ardea 53:99-160. and B. Stonehouse, 1971. Thermoregulatory responses o f the P e r u v i a n Penguin, Speniscus humboldti. Comp. Biochem. P h y s i o l . 40:689-710. Greenwood, J . 1964. The f l e d g i n g o f the G u i l l e m o t U r i a a a l g e w i t h notes on the R a z o r b i l l A l c a t o r d a . I b i s . 106: 469-481. Jordan, R. 1967. The p r e d a t i o n of Guano b i r d s on the P e r u v i a n Anchovy ( E n g r a u l i s r i n g e n s J e n y n s ) . C a l . Coop. Oc. F i s h . I n v e s t . 11:105-109. 70 Kahl, M. P h i l i p , J r . 1962. Bioenergetics of growth i n nest l i n g Wood Storks. Condor 64:169-183. . 1964 . Food ecology of the Wood Stork (Mycteria americana) i n F l o r i d a . E c o l . Monogr. 34:97-117. Kendeigh, S.C. 1939. The r e l a t i o n of metabolism to the development of temperature regulation i n b i r d s . J . Exp. Zool. 82:419-438. King, J.R. and D.S. Farner. 1961. Energy metabolism, thermoregulation and body temperature, i n : A.J. Marshall (ed.), Biology and comparative physiology of b i r d s . I I . New York and London:215-288. Lack, D. 1954. The natural regulation of animal numbers Clarendon Press, Oxford. . 1966. Population studies of b i r d s . Univ. Press, Oxford. . 1968. Ec o l o g i c a l adaptations for breeding i n b i r d s . London, Methuen and Co. Ltd., Eng. Misch, M.S. 1960. Heat regulation i n the Northern Blue Jay, Cyanocitta c r i s t a t a bromia (Oberholser). P h y s i o l . Zool. 33:78-86. Odum, E.P. 1959. Fundamentals of ecology. Second Ed. (W.B. Saunders Co., P h i l a . ) . Perrins, CM. 1965. Population f l u c t u a t i o n s and c l u t c h -s i z e i n the Great T i t , Parus major L.J. Anim. Ec. 34 :601-647 . Portmann, A. 1945. Die postembryonale Entwicklung des Graureihers (Ardea cinerae L.) und ihre vergleichend-biologische Bedeutung. Schweiz. Arch, fur Ornith., 2:181-184. Robertson, I. 1971. The influence of brood-size on reproduc-t i v e success i n two species of Cormorant, Phalocrocorax  auritus & P. pelagicus, and i t s r e l a t i o n to the problem of c l u t c h - s i z e . M. Sc. Thesis, Univ. B r i t . C o l . Romijn, C. and W. Lokhorst. 1966. Heat regulation and energy metabolism i n the domestic fowl. In Physiology of the Domestic Fowl (Edited by Horton-Smith C. and E.C. Amoroso), pp. 211-227. O l i v e r & Boyd, Edinburgh. 71 Royama, T. 1966. Factors governing feeding rate, food require-ment and brood-size of the n e s t l i n g Great T i t s , Parus  major. I b i s , 108:313-347. Skokawa, A. 1962. On the n u t r i t i o n of piscivorous b i r d s . Ornitologia 4:288-296. Southern, H.N. 1970. The natural control of a population of Tawny Owls (Strix aluco). J . Zool., Lond. 162:197-285. Spaans, A.L. 1972. On the feeding ecology of the Herring G u l l , Larus argentatus pont., i n the northern part of the Netherlands. Ardea 59:73-188. Storer, R.W. 1952. A comparison of v a r i a t i o n , behavior and evolution i n the sea b i r d genera Uria and Cepphus. Univ. C a l i f . Publ. Zool. 52:121-222. Thoreson, A.C. and E.S. Booth, 1958. Breeding a c t i v i t i e s of the Pigeon Guillemot Cepphus columba columba ( P a l l a s ) . Walla Walla C o l l . Publ. B i o l . S c i . 23, 36pp. Tinbergen, L. 1960. The natural control of insects i n Pine-woods. Factors influencing the i n t e n s i t y of predation by songbirds. Arch. Neerl. Zool. 13:265-336. Tuck, L.M. and H.J. Squires. 1955. Food and feeding habits of the Brunnich's Murre (Uria lomvia lomvia) on Akpatok Island. J . F i s h . Res. Bd. Canada, 12:781-792. Vermeer, K. 1963. The breeding ecology of the Glaucous-winged G u l l , (Larus glaucescens) on Mandarte Island, B.C. Occ. Pap. B.C. Prov. Mus. 13, 104 pp. Ward, J.G. i n prep. Studies on the feeding ecology and breeding success of the Glaucous-winged G u l l (Larus  glaucescens) on Mandarte Island, B.C. Ph. D. Thesis, i n prep., Univ. B r i t . C o l . Westerterp, L. 1972. Verslag over het onderzoek naar de energiebalans van de Spreeuw (Sturnus v u l g a r i s L . ) , aan het I n s t i t u u t voor Oecologisch Onderzoek te Arnhem i n de broedseizoenen van 1968, 1969, en 1970. (English version to be submitted to Ardea). 

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