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

in the Department

of

Zoology

We accept this thesis as conforming to the

required standard

THE UNIVERSITY OF BRITISH COLUMBIA

September, 1972 In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia. I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the Head of my Department or by his representative. It is under• stood that copying or publication of this thesis for financial gain shall not be allowed without my written permission.

Department of Zoology

The University of British Columbia

Vancouver 8, B.C., Canada

Date: /*t* /?, /ff£ ABSTRACT

The energetics of growth and feeding of the chicks

and their relation to the problem of evolution of brood

size were investigated in the alcid Cepphus columba, the

Pigeon Guillemot, a colonial species nesting at Mandarte

Island, British Columbia. The study involved the naturally

occurring broods of one and two chicks, but to elucidate

information on the evolution of brood-size, experimentally

induced broods of three were created.

Following the technique of Royama [1966], film records

show an "optimal working capacity" for the parent Pigeon

Guillemots at Mandarte Island of a total daily fish ration

of 200 grams. In no case were parents observed to bring more

than this amount when means were computed over 5-day periods.

The resulting limitation expresses itself in a depressed

growth rate in artificially induced three-chick broods in all

seasons, and in twin broods in certain years. The parent

does not endanger its own survival in favour of its brood, but maintains body weight in all circumstances.

Each parent requires for itself 90 grams of food

daily or 20% of its own weight. The "optimal working

capacity" of each parent is about 100 grams of food delivered

to the nest or 22% of the parental body weight. Subsequently iii when feeding the nestlings the parent doubles the rate of fishing.

A procedure for whole carcass analysis on 27 Pigeon

Guillemot chicks and 2 adults is described to determine; cooling rate for calculation of heat production, surface area to calculate thermal conductance, gross fat, ash, moisture, crude fat and heat of combustion. The lean dry featherless biomass of 8 nestlings of various ages had an average energy content of 4.75 Kcal./gr., and using this figure as well as assuming a combustion value of 9 Kcal./gr. for fat and 5

Kcal./gr. for plumage, the average caloric value for live weight was calculated at 1.92 Kcal/gr. with a range of 1.34

Kcal./gr. at hatching to 2.6 5 Kcal./gr. at the time of fledging. The adult Pigeon Guillemot had an average caloric density of 2.56 Kcal./gr. live weight. The change in the live weight caloric density is related to the deposition of fat which occurs between the 11th and 21st day following hatching and at fledging is in excess of the fat depot found in adults.

Growth in body weight, i.e. in absolute terms as daily increment in grams, reaches a maximum between the 8th and 15th following hatching, whereas the relative rate of growth, i.e. the daily increment with respect to the nest• lings weight, reaches a maximum about the 4th day following hatching. iv

The conversion rate for the entire fledging period of chicks in the field is 2400 grams of fish per chick for an

increment of 375 grams in body weight or 2800 Kcal. for an

increment of 1001 Kcal. body weight gain (=35%). Consumption of fish for the two chicks hand-raised successfully at camp

is 3400 grams for a conversion rate of 25%, and compares well with results of similar experiments by other

investigators.

The maintenance costs of the chick are kept low by keeping energy losses to a minimum so that a large share of

the energy input is allowed for growth, a process of over• riding importance in the Pigeon Guillemot chick (Figure 19).

The findings on fledging success in the Pigeon

Guillemot (summarized in Table 3b) are consistent with Lack's hypothesis on the evolution of brood-size in that two-chick broods represent the limit that the parents can raise

successfully.

Overall success in the artificially induced three- chick broods is poor compared with the normal two-chick broods

in that they fledge at an older age (37.3 to 33.9) , their weight at fledging is lower (385 to 407 grams) which may

impair their post-fledging survival, and the average number of chicks produced from triplet broods is only marginally greater than from twin broods (1.9 to 1.8 chicks per nest). TABLE OF CONTENTS

PAGE

LIST OF TABLES vii

LIST OF FIGURES viii

ACKNOWLEDGEMENTS xi

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

(ii) total daily fish 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 vi

CHAPTER PAGE

(c) Gross fat determination 33

(d) Ash, moisture, crude fat and heat

of combustion 34

3. Controlled Feeding of Chicks ,34

B. Results 35

1. Thermoregulation and Basal

Metabolism . 35

2. Carcass Composition 40

3. Controlled Feeding of Chicks 44

4. SYNTHESIS 49

A. The Growth Process 49

B. Development of Temperature Regulation .... 60

C. The Problem of Brood-size 61

D. Summary 67 LITERATURE CITED 69 LIST OF TABLES

TABLE PAGE

1. Types of Food Brought to 6 Nests during the 1969 and 1970 Seasons 25

2. Instantaneous Relative Growth in the Pigeon Guillemot, Wood Stork, and Glaucous-winged Gull 51

3a. Fledging Age and Weight as a Function of Brood-size 64

3b. Fledging Success of the Pigeon Guillemot as a Function of Brood-size 64 LIST OF FIGURES

FIGURE

1. Automatic camera recording unit in operation ....

2. Growth in body weight in the Pigeon Guillemot, as a function of brood- size

3. Mean daily weight increments for the data presented in Figure 2

4. Growth in wing length (=radio-ulnar length), as a function of brood-size(a); growth in primary length as a function of brood-size (b); growth in foot length (= tarso-pedal length), as a function of brood-size (c); growth in bill length (= greatest length), as a function of brood-size (d)

5. Daily feeding pattern, based on frequency of food deliveries, as a function of brood-size. The histogram shows hourly intervals, and a summary is given at the right in 2-hourly periods, where the rate between 0700 and 0900 hours was taken as 100%

6. First and last parental food deliveries plotted in relation to P.D.S.T. in 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 [Aitchison incl.](b)

7. Mean blenny weight as a function of nestling age at 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)

8. Daily food ration (grams of fish delivered per chick per day), as a function of brood size for Guillemot nestlings (Means for one triplet [Aitchison, 1972], 5 double broods, and 5 single broods) ix

FIGURE PAGE

9. Basal metabolic rate in the Pigeon Guillemot nestling, with two adults plotted for com• parison (Adults). Values are plotted according to body weight on a double logarithmic scale on which the Brody-Proctor prediction for metabolic rate of homeiotherms is a straight line; the 50% and 150% lines have also been entered 37

10. Basal metabolic rate per square meter of body surface as a function of age in the Pigeon Guillemot 38

11. Thermal conductance (Kcal. lost per degree centigrade gradient per square meter of body surface per hour) as a function of age in the Pigeon Guillemot 39

12. Plumage weight (in grams) as a function of age for the carcass Pigeon Guillemot analysis (birds sacrificed at various ages) 41

13. Surface volume ratio (square centimeters per ml. body volume) as a function of age in the Pigeon Guillemot 45

14. Metabolic intensity (Kcal. per day per gram of live weight) as a function of age in the Pigeon Guillemot 42

15. Water content of nestling Pigeon Guillemot (top), plotted as a percentage of live weight, and fat content of the same birds (bottom), plotted as a percentage of lean dry weight 43

16. Rate of converting food into body tissue, plotted as grams of fish required to build one gram of bird versus the age of the nest• ling Pigeon Guillemot 46

17. Mean overnight weight loss (expressed as grams per hour) for the hand-raised chicks, as a function of age 48

18. Instantaneous relative growth rate (a); total body weight increments on a daily basis (b); and plumage weight increments on a daily basis (c) for the Pigeon Guillemot nestling ... 50 x FIGURE PAGE

19 Five-day increments in fish ration (from camera units), energy stored in body (differentiated are plumage (c), lean body weight (b) and fat (a)) as taken from carcass analysis, and minimal maintenance costs (taken from basal metabolic rate in respirometer trials) '57

20 Growth as a function of brood-size in the Pigeon Guillemot. Plotted are the means for all data from 1969 and 1970: single• tons are compared with the fastest and slowest-growing individuals of the twin broods, and the fastest and slowest-growing individuals of the triplet broods 62 ACKNOWLEDGEMENTS

I wish to extend my deepest gratitude to my reasearch advisor, Dr. R.H. Drent, who suggested this project to me.

His invaluable advice and assistance both in the field and in

the preparation of this manuscript warrants my indebtedness.

I benefitted from Mrs. B.E. March's gracious advice on carcass analysis and appreciated her permission to use the equipment in the Poultry Science laboratory. Dr. T.G. Northcote and

Dr. H.C. Nordan critically read the manuscript and suggested a number of improvements.

I am thankful to the owners of Mandarte Island, the native peoples of the Tsawout and Tseycum bands, for allowing me to live and work on the island. Throughout the course of my fieldwork I was greatly helped by other members of the

"Mandarte Team"; I. Robertson, J.O. Anvik, J.C. Ward, and the

Hendersons. N. Aitchison generously allowed the use of results on his follow-up study on the Pigeon Guillemot during

the 1971 summer. My wife, Susan Koelink, devotedly took care of the experiment consisting of hand-raising Pigeon

Guillemot chicks. W. Braeuer constructed the electronic camera units, and I am grateful expecially for his willingness

to make alterations and repairs during the course of the investigation. I am appreciative of Captain J. Drent who

transported my equipment to and from the island each summer. xii

The warm hospitality of Mrs. R. Mathew contributed to making my stay on the island a pleasant one.

Financial support for this study came from the Univer• sity of British Columbia and the National Research Council of Canada grant to Dr. R.H. Drent for the purchase of equipment. I

CHAPTER 1

INTRODUCTION

Ecological work on the breeding biology of birds has in the past decade or so diverged into two well-defined streams. On the one hand, the direction of evolutionary ecology, stimulated particularly by the writings of LACK

(1954, 1966 and 1968 for summaries), is concerned with finding reasonable explanations for the adaptive significance of the present-day patterns and modes in birds. For example, why do some species habitually lay very large clutches, whereas others may only produce one or two eggs annually? Lack has championed the view that clutch size, one of the determinants of reproductive rate, is the result of natural selection.

The genotype of the parent raising the maximum number of young for eventual recruitment to the breeding population will eventually dominate the population. Where parental feeding of the brood has evolved, clutch size, according to this hypothesis, reflects the maximum brood size that the parents are capable of raising successfully. The special case of the much smaller class of species where the parents do not feed their young will not further concern us here.

Other features of the breeding arrangements of birds are also under investigation by this school along much the same lines; one can speak of evolutionary strategies of breeding 2 impinging on such features as length and timing of the breed• ing season, number of broods, type of nesting site, pattern of parental care, or ontogenetic pattern of nestlings.

A second major stream can be designated as energetics, and has received its impetus largely through the writings of

ODUM [1959 and subsequent editions] and KENDEIGH. This direction focusses its attention on measuring the energy flow

throughout the living world, and in the special case of breed• ing biology attempts to measure how much energy is involved in the reproductive effort of the parents (e.g. caloric cost of egg production, of incubation, and of nestling care), the total energy content of the food collected by the parents while raising the young, the efficiency of conversion of this energy into the growing body of the nestling, and the estimation of the quantitative importance of the various avenues into which this energy is diverted (lost in faeces, basal metabol• ism, cost of temperature regulation, retention in body tissues, external work). Due to the formidable difficulties that must be overcome before these parameters can be estimated, let alone accurately measured, in the field, this is still a very new area, with less than half a dozen studies conducted to date.

In a very thought-provoking paper, ROYAMA [1966] has sought to combine these two approaches in his field study of the breeding of the Great Tit, Parus major. The philosophy behind his study was that the energetics of brood-raising 3 must be investigated if the question of the evolution of brood-size is to be approached; although historically distinct lines of thought, the two directions in fact can complement one another. ROYAMA realized that unaided observation at the nest could never supply the requisite data, and therefore devised an automatic nest-visit recorder linked with a cine• camera, yielding a negative of each parental visit. Since in this species food items are brought one at the time, and are carried in full view in the bill, this method gave complete insight into the food brought to the nestlings. Growth and defaecation rate of the nestlings was also measured, and an estimated energy budget constructed. The introduction of the film record in effect replaced a team of observers such as had been employed by TINBERGEN [1960] in his now classic research on this species, and was the essential step in putting this type of study within the reach of a single investigator.

My own study was envisaged as an application and amplification of ROYAMA*s approach to elucidate the evolution of brood-size in the colonially nesting alcid Cepphus columba, the Pigeon Guillemot. Basically, the thought was to devise an automatic camera unit to moniter all feeding trips, since in this species as in the Tit the food items are brought individually and are carried in full view dangling from the parent's bill, and to incorporate in the unit a balance so 4

that the weight of the food items could be determined from

the negative. Where ROYAMA's approach was to be extended,

involved the control observations on nestlings raised by hand on known rations of fish, following the methods employed by

KAHL [196 2] on the Wood Stork, Mycteria americana. A second

innovation concerned the use of an open-circuit metabolism

apparatus for measuring the response of the growing nestlings

to alterations in air temperature, as a means of estimating

the cost of temperature regulation along the lines of

KENDEIGH's [1939] pioneer study.

In order to make the findings directly relevant to

the problem of the evolution of brood-size, my intention was

to apply these methods not only to the naturally occurring broods of one and two chicks, but in addition to experimentally

induced broods of three ("triplets"). Quite apart from the

framework in which these results are presented, namely the

evolution of brood size in birds, the data have implications

for the ways in which the parents respond quantitatively to

the needs of their chicks, and might also be applied in the

study of the parent guillemot as a predator of fish. My

main task, however, has been to obtain an energy budget for

the developing chicks, valid for field conditions, and this

task has precluded giving adequate attention to the sidelines

mentioned. Some of these points were investigated by

AITCHISON [197 2] . 5

My choice of the Pigeon Guillemot as an object of study deserves comment. Camera monitering was considered prerequisite, and in its simplest form this limits the choice to a hole-nesting species tolerant enough to accept modifi• cations of its natural home. Secondly, it was essential that my nests be available for simultaneous study, so it seemed reasonable to consider primarily colonially-nesting species.

Finally, it was important to choose a species where the basic patterns of breeding had already been worked out [DRENT, 1965,

1964], so that one could at the outset start to pose more sophisticated questions with full knowledge of the normal pattern. The Pigeon Guillemot is a hole-nesting colonial bird, relatively tolerant of disturbance, and the basic features of its breeding biology have been described [Storer,

1952; Thoreson and Booth, 1958; Drent, 1965]. 6

CHAPTER 2

GROWTH AND FEEDING OF THE CHICK

A. Methods and Materials

Field work was conducted at Mandarte Island during the spring and summer of 1969 and 1970. Mandarte Island is located in the Gulf Island area of British Columbia; for a detailed description see Drent et al^., 1964 .

Pigeon Guillemots at Mandarte Island re-use the nest- burrows of the previous season and when my study began the great majority of the nests were still used and marked from previous work by Drent [1965]. Accessible nests were checked daily for clutch commencement and hatching. In the 1969 season the growth of the chicks of both control and experi• mental broods was checked daily but in the 197 0 season, in order to minimize disturbance, the control broods were checked every alternate day.

The Pigeon Guillemot normally lays a maximum of two eggs. One-chick broods, however, occur regularly as a result of the following factors: (1) only one egg laid, (2) one of the two eggs laid became addled. This factor is the most common cause of one-chick broods. (3) death of one of the two chicks. 7

Experimentally induced three-chick broods or so-called

"supernormal" broods were created by adding another chick to a two-chick brood. Care was taken in choosing a chick of similar age and weight to its new siblings to allow for equal competition for food among each other.

Control broods refer to one-, two- and three-chick broods of which only growth data was obtained, whereas experi• mental broods had in addition to the measuring of growth, the automatic camera recording unit placed in front of the nest.

Chicks in the two-chick and three-chick broods were marked individually to distinguish between them in collecting growth, age and fledging data.

Each chick was weighed using "Pesola" spring balances with ranges from 0 to 100 and 0 to 500 grams. The accuracy of each scale was within one percent. Along with the weighings, the lengths of the following body parts were measured with a specially constructed ruler:

1. "wing" or radio-ulnar length, measured between

outer perimeters or condyles,

2. tarso-pedal length measured from the superior

condyle to the tip of the nail on the middle

toe. The length was measured with the bird in

a typical plantigrade position with the tarsus

and foot flattened against the ruler. 8

3. outermost primary featherlength measured from

the tip to the insertion into the skin.

4. bill length measured laterally as the greatest

length between the tip and the insertion into

the skin.

An automatic camera recording unit was constructed following the technique of ROYAMA [1966] with certain modifi- cations for this project; (1) a 35 mm., half-frame (1/2 x 24 x 36 mm.) camera was used instead of a 16 mm. cine camera,

(2) in the hope of obtaining weights of the incoming and out• going parents, a weighing scale, with a scale range of 500 grams, accurate to within 1 gram, was added to the recording unit. The scale was equipped with an oil damper. It was hoped that this damper would prevent oscillation of the weighing pan caused by the waddling motion of the parent.

The camera unit was placed along with the weighing scale in a wooden box and placed in front of a nest burrow.

(Figure 1). To minimize possible desertion or disturbance to the regular brooding and feeding pattern of the parents, the following precautions were taken: (1) two to three weeks prior to actual operation, the empty wooden box was placed in the vicinity of the nest to allow the parents to become accustomed to the box, (2) during the last three days the complete unit was moved gradually from a location several meters away from the nest to a position in front of the 9

FIGURE 1 Automatic camera recording unit in operation

1. Lead storage battery 5. Pocket watch 2. Electronic flash control 6. Weighing scale unit 7. Photoelectric 'eye' 3. Half-frame 35 mm. camera 8. Approach ramp to nest- 4. Plexiglass window burrow 10 nest, (3) in order to camouflage the set-up, the box was painted a slate-grey to blend with the terrain.

A typical sequence of events during the delivery of a food item is as follows:

1. one of the parents lands on the approach ramp

with a food item hanging from its bill. The

approach ramp is attached to the horizontal

section in the box and functions as both a runway

to the entrance of the nest-burrow where the

chick awaits its meal, and a weighing platform

attached to the scale pan, which results in a

needle deflection on the scale face.

The speed by which the parents deliver the

food is in the order of four to five seconds and

was found to be too fast to allow the weighing

scale to reach the correct value. Subsequently,

in the 1970 season the approach ramp was slanted

to reduce the speed of food delivery. The Pigeon

Guillemot walks on its tarsi as well as feet

(plantigrade) and as a result has to waddle

especially when walking up an inclining slope.

This modification of the runway was relatively

successful in curbing the speed of food delivery.

2. halfway across the horizontal section of the run•

way, the parent walks through a photo-electric

light beam which is connected with the automatic 11

camera unit. When the light beam is broken by

the bird it triggers off the camera unit and

electronic flash and a picture is taken (see

Figure 1).

3. the parent proceeds to deliver the food item to

the chicks, turns around and waddles out. Another

picture is taken as in (2), this time without the

food item which results in a lower scale weight.

4. the parent walks halfway down the approach ramp

and immediately flies off.

Camera and film checks were made twice a day depending on the age and number of feedings, When necessary, the film was replaced and the exposed film developed within the next

two days. The negatives were immediately examined under a dissection scope to check for faulty equipment or developing

technique. Final transcription of data from a total of

approximately 15,000 negatives took place in the following

fall and winter.

By examination of the negatives it was hoped that

a complete record of all food items delivered to the nest

could be obtained and identified at least to family. By

subtracting the outgoing from the incoming weight, weight of

individual food items should be collected. Since the female

parent is lighter in weight than the male by approximately

30 grams, it was hoped that the outgoing weights would 12 differentiate between sexes, assuming little change in body weight of the parents throughout the course of the day.

B. Results

1. Growth of the Chick

Mean growth in body weight and mean daily weight incre• ment of chicks in broods of one, two and three are shown in

Figure 2 and 3 respectively. No significant difference was

found between the two seasons and thus the results have been combined. Similarly no difference in growth was apparent between broods in nest-burrows with a camera unit and their control counterparts.

In general, the curve described by the growth data is

typically sigmoidal and thus can be divided into 3 phases.

The first phase represents the first 8 days after hatching and shows a rapid increase in body weight but not as fast as

the next phase. No apparent difference exists between the

three brood-sizes in this early phase, and is clearly shown

in Figure 2. The second or middle phase represents the

straight line portion by eye of the growth curve and is thus

the period of arithmetic growth. It lies between 8 and 18 days of age. As expected, the daily weight gained (Figure 3)

is greatest during this interval for all 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, 36 chicks A—* broods of three, 18 chicks

10 20 30 40 Days after hatching

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 for triplet broods. Combining singles and doubles gives a mean growth rate for normal-sized broods, which differ significantly (P < 0.05) from the rate for triplets. Clearly, chicks in broods of three suffer a depressed growth rate compared to chicks in one- and two-chick broods. The effect of broodsize is most noticeable in the third phase. The weight gain per day is least depressed in the single chick brood and most depressed in the three chick brood with the two-chick brood falling in between. Similarly, the daily weight increment falls off with an increase in brood-size.

Mean wing length during the first day after hatching, age zero, is 20.5 mm. and the growth thereafter follows a sigmoidal curve identical to the growth in body weight

(Figure 4a) with the second phase or period of arithmetic growth falling between 8 and 18 days of age for all three brood-sizes. No clear difference in growth could be found between the three brood-sizes as the greater wing growth in the one-chick brood between 30 and 38 days of age may be a reflection of a small sample size of 2 and 3 chicks.

The outermost primary feather did not break through the skin and start to develop until approximately 5 days of age, (Figure 4b). The slowest period of growth falls between ages 5 and 15 days (1.1 mm. per day) followed by a rapid increase to twice the foregoing rate (2.3 mm. per day) and continues to grow at a diminished rate at the time of fledging. The rate of growth is similar for all three brood-sizes. 90n

tO 20 30 tO 0 10 20 30 40 Days after hatching Days after hatching ure 4 Growth in wing length (=radio-ulnar length), as a function of brood-size (a); growth in primary length as a function of brood-size (b); growth in foot length (=tarso-pedal length), as a function of brood-size (c); growth in bill length (=groatest length), as a function of brood-size (d) 17 Tarso-pedal length at zero day of age is 43 mm. (Figure

4c), and immediately started to develop at its highest rate

(2.3 mm. per day) till 12 days of age. At 20 days the tarsus

and foot had almost reached their full length. Again, no difference in the growth rate could be found between the

three brood-sizes.

A bill length of 21 mm. was recorded during the first

day after hatching and similar to the growth rate of the

tarsus and foot it immediately developed at a maximum of

0,9 mm. per day till approximately 13 days of age then grad• ually decreasing curvilinearly, still growing when the chicks

fledged. The growth rate appeared to be similar for all brood-sizes. (Figure 4d)

2. Parental Care During the Fledging Period

During the 19 69 season several attempts were made to

form three-chick broods, 3 experimental with the camera unit

and 2 control without the recorder. Only one of the control

triplets was successful and no explanation can be given why

the others failed. Various factors may be responsible. Even

though the added chick was of similar age and weight as its

new siblings it may have been too young or not capable of

adapting to the new nest or for some reason could not

compete for food successfully with its new siblings; the

parents did not respond to the increased demand for food 18 or could not effectively increase the food deliveries due to the location of the nest in or near the territories or perch sites of agressive Glaucous-winged gulls Larus glaucescens and Black Oyster-catchers Haematopus bachmani and possibly other species of birds residing or nesting on the island

[see Drent et al^., 1964] . A shortage of chicks during the

1969 season precluded further trials. During the 1970 season no attempts were made to form experimental triplets and of the attempted 8 control triplets 2 were completely success• ful and the remaining 6 partially so. To obtain some information on the daily frequency of food deliveries in the successful triplet of the 1969 season, observations from a blind were carried out and the times of deliveries between sunrise and sunset recorded.

(a) Daily pattern

Figure 5 shows the effect of brood size on the daily feeding pattern for the entire fledging period. The combined data from both seasons for the one- and two-chick broods were obtained from the automatic camera records; data for

the three-chick brood include both direct observations in 1969 and Aitchison's camera record from 1971.

For the one- and two-chick broods the highest fre• quencies of food deliveries occurred in the early morning between 06 00 and 1000 hrs. (Thirty-seven percent of the daily total for both brood sizes), and then gradually de- 19

6 12 18 6 12 18 Time (PDST) Time (PDST)

Figure 5 Daily feeding pattern, based on frequency of food deliveries, as a function of brood-size. The histogram shows hourly intervals, and a summary is given at the right in 2-hourly periods, where the rate between 0700 and 0900 hours was taken as 100% creased to a final low number between 2000 and 2100 hrs.

The rate of decrease is fastest and continuous through the day in the one-chick brood, whereas in the two-chick brood

the late morning decrease is only temporary and is followed by an increase in the afternoon, between 1300 and 1800 hrs., after which feeding frequency drops off to cease at dusk.

Most noticable is the frequency plateau in the three-chick brood where no decrease is evident until the evening, past

1800 hrs. Clearly a constant frequency level is maintained

throughout the day. When the mean for every two hours is

taken and 100% is assigned to the peak daily frequencies

0700 - 0900 hrs. for all brood-sizes, the above described daily frequency pattern are more clearly differentiated

(Figure 5, right-hand side).

The Pigeon Guillemot feed their chicks only during

the daylight hours, leaving the chicks for the night, except

for the initial brooding period when one of the parents broods the chick overnight [Drent, 1965] . From personal observations from a blind and the conclusive record of times

for the first food delivery from the recording units, the

first feeding of the day takes place approximately 1 1/2 -

2 hours after sunrise and becomes later as the season progresses and the number of daylight hours decrease (Figure

6a). This timespace is likely due to time required by the parent for fishing activities, including its own needs,

and to fly from the fishing grounds to the nest. Similarly a 21

last food delivery

civil twilight —o- o , —-o— "O ... sunset 1

first food delivery o7 E h 6H —o sunrise

civil twilight

j2 61 o

O 4.

E —[——1 1 1 r~ z 19 20 21 22 Time (PDST) Figure 6 First and last parental food deliveries plotted in relation to P.D.S.T. in 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 [Aitchison incl.] (b) 22 the last feeding for the day occurs approximately 1 1/2 - 2 hrs. after sunset and becomes earlier along with the time the sun sets as the season progresses. The parent makes its last fishing trip probably just prior to sunset and subsequently cannot make the delivery to the chicks until after sunset, requiring the same timespace prior to the first food delivery.

Figure 6b shows a strict daily rhythm in the time of nest departure.

(b) Seasonal pattern

(i) feeding frequencies

Data on feeding frequencies have often been used as an indication of the quantity of food brought, and the original intention in this study was to use feeding frequencies as a measure of food quantity. However, analysis of the film records soon revealed conflicting trends in the size of the food item at the various nests, making comparisons on this basis misleading. As an example, nest S-5 [1969] shows an increase in the mean size of blenny with age, nest B in 1970 shows first a decline and later an increase, and the same nest in the 1971 season [Aitchison 197 2] a continuous decline in mean blenny size (Figure 7). Clearly, frequencies are not a reliable basis for comparison (note that mean blenny weight varies by a factor of two in the example shown in the figure), 8n

310 15 20 25 30 35 40 Days after hatching

Figure 7 Mean blenny weight as a function of nestling age at 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 further analysis will be based on the computed daily total fish weight brought to the nest.

(ii) total daily fish weight frequencies

A more meaningful comparison on parental feeding between brood-sizes is the total fish weight delivered by the parents per day as a function of chick age (Figure 8).

One of the purposes of the weighing scale in the automatic camera unit was to allow computation of the fish weights by subtracting the parent's outgoing weight from the parent's incoming weight. Upon close examination of the results from the photographic negatives it was discovered that the weights of the food items delivered varied too much in relation to the size of the fish to be meaningful. Causes for this variation could lie with the poor damping of the oscillation due to either the waddling motion of the parent or the effects of the wind on the runway or both. Subsequently, it was decided to measure the length of the fish with a dissection- scope equipped with a travelling vernier scale and to convert the vernier length to actual length (120 vernier divisions

= 180 mm. actual length).

In agreement with Drent [1965], at least 75% of the fish delivered consisted of blennies and sculpins and diet composition varied greatly between nests (Table I). 25

TABLE I

Types of Food Brought to 6 Nests during the 1969 and 1970 Seasons

.Number Percentage

1. Blennies 1173 63.8 Xiphisteridae Pholidae Stichaeidae Lumpenidae

2. Sculpins 242 13.2 Cottidae

3. Pacific herring 36 2.0 Clupeidae Clupea pallasii

4. Sandlance 101 5.5 Ammodytidae

5. Shrimp 12 0.7 Malacostraca

6. Flatfish 47 2.6 Bothidae Pleuronectidae

7. Poachers 32 1.7 Agonidae

8. River Lampreys 14 0.8 Petromyzontidae Lampetra ayresi

9. Unidentified spp. 184 10.0

1841 100 .0 26

Since it was not always possible to key the fish on

the negatives to species, it was decided to identify the food items only to family, assigning both the families Pholidae and Stichaeidae to the common category of blennies. A length versus weight graph was constructed for blennies and sculpins

from samples collected in the field and from fish found in

the nest-burrows of the Pigeon Guillemot. By plotting the converted vernier length of the "negative" fish on the length/ weight graph constructed for that category of fish, the mean weight can be read off the abscissa. Any error caused as a result of this method would be at random. The weights for

the small number of other food items brought in by the parents which include poachers, flatfish, lampreys, sandlances and

shrimps were approximated from a small number of samples

found in the nest-burrows of the Pigeon Guillemot.

The fishweights calculated by this method form the

source of Figure 8; total fish weight in grams per chick per day for the three brood-sizes. The graph clearly demon•

strates that with an increase in brood-size there is a proportional decrease in the amount of food delivered to each

chick for the entire nestling period. It is evident that a

long plateau of total food weight delivered by the parents

is maintained between approximately 11 and 30 days of age for

all the brood-sizes with a decline in food input thereafter.

The sudden increase in total food weight just prior to

fledging in the one-chick brood may be a reflection of a

small sample size of only 2 nests. 140 n

9 120- A

E 40 " o—© broods of one • o o broods of two 20 - * A broods of three

, 1 1 1 r- 1 1 i O 10 20 30 40 Days after hatching

Figure 8 Daily food ration (grams of fish delivered per ^ chick per day), as a function of brood size for Guillemot nestlings (Means for one triplet [Aitchison, 1972], 5 double broods, and 5 single broods) CHAPTER 3

ENERGETICS

A. Methods and Materials

1. Thermoregulation and Basal Metabolism

A laboratory was built to hold equipment necessary

for conducting experiments on thermoregulation and basal metabolism of the Pigeon Guillemot. It was decided to employ an open-circuit gravimetric method of measuring Carbon

Dioxide production. This method was devised by Haldane

[Brody 1942: 324] modified for this purpose, and is simple

to operate especially if the R.Q. is not required. The Pigeon

Guillemot chicks and adults are a diurnal species, resting at nighttime. In order to obtain true basal conditions and

the least variability in readings, Aschoff and Pohl [1970]

suggest that measurements of basal metabolism should be carried out on animals in a post-absorptive state, in the

thermoneutral zone and without physical movement, at a given

light intensity, and at a specified stage of the diurnal cycle. In order to fit these specifications, measurements were taken at nighttime. Although true "basal" or "standard" conditions are not met until after 24 hours following 29 cessation of food, the R.Q. values approximate the fasting metabolic rate within 3 hours following the onset of darkness

[Romijn and Lokhorst, 1966]. The bird's R.Q. is assumed at approximately 0.70 for fat combustion. Lusk's tables for an

R.Q. of 0.70 gives a constant thermal equivalent of 3.41

Kcal./mg. C02 produced [Brody 1942: 310].

Chicks of various ages and adults were collected

from the field just prior to sunset and subjected to tests on thermoregulation and measurements of basal metabolism during the night. A single bird was put in a metal container, appropriate for the size of the bird, and as a whole were placed in a cabinet in which the temperature was thermostatic• ally controlled within 1-2 °C of the desired temperature.

Dried air was pumped through the container at a controlled

rate of 60 ltrs./hr. Body temperatures were measured by

inserting a flexible thermocouple about 10 mm. into the

rectum, and secured with a clip to feathers around the cloaca.

The birds were able to move freely but generally settled down after a few minutes of being placed in the temperature

cabinet. Steady levels of CC>2 production and body temperature were reached after 1-2 hrs. The set-up and procedure have been tested and successfully used by Drent [1971] .

The nightly tests extended over 8 to 12 hrs. during which the temperature in the cabinet was raised and lowered

gradually in 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 other.

CG*2 production was measured over 20 minute intervals and duplicated for each temperature setting if the results were in agreement, otherwise more runs were carried out.

To measure CC^ production, air from the drum was led in succession through two U-tubes of "drierite" and two of

"ascarite," which respectively absorbed water and CC^; amounts of CC»2 were determined by weighing the Ascarite tubes on a Mettler balance before and after each 20 minute run. Heat production was calculated by multiplying the weight of CC>2 captured with the thermal equivalent of CC»2 • The error introduced by neglecting urinary N loss is less then 0.2%

[Romijn and Lokhorst, 1966] .

2. Carcass Analysis

The above procedure was used in measuring basal metabolism and defining thermoneutral zone. Further estimates on heat production were obtained from cooling rates of Pigeon

Guillemot carcasses. Chicks of various ages were collected from the field during the 1970 season and sacrificed and put in a deep freezer for later determination of surface area and volume, thermal conductance, gross fat, ash, moisture and heat of combustion. This work was carried out on campus of the University of British Columbia during the fall and winter of 1970. 31

(a) Cooling Rate Determination

The frozen carcass was thawed overnight and placed in an oven set at 40 °C till the core temperature of the carcass had reached ambient oven temperature. The carcass was then suspended by the bill in a large plastic box inside a temperature cabinet, set at 0 °C, to prevent uneven cool• ing due to cold fan-driven air currents, which circulate through the cabinet*. A flexible YSI thermal probe was inserted through the bill down the oesophagus into the proventriculus or as far as possible, and a YSI needle probe stuck into the visceral cavity with the point of the needle located in the core region. Care was taken not to disturb the plumage. Needle, proventricular and ambient temperature readings were taken every 5 minutes for at least one hour, on a YSI 5-channel temperature meter, accurate to within

0.1 °C, and corrected for meter deviations. The average ambient temperature was subtracted from each corrected needle and preventricular reading. The drop in temperature over a given time interval as well as the individual readings of the visceral cavity and proventricular were checked to be equal.

The carcass was then removed and weighed on a Mettler balance, accurate to within 0.5 gram, and the cooling rate of the carcass determined as a drop per °C gradient per hour.

The cooling rate is used in calculating the rate of heat less for the whole carcass (Kcal./°C x hr.) by employing the specific heat of bird tissue, 0.83 Kcal./°C x gm. [Misch, 1960] and body weight. The theoretical value for heat production is then computed by multiplying the rate of heat loss by the gradient, i.e. the lower critical temperature of a Pigeon

Guillemot of similar 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 in (a), the same carcass was plucked carefully and as thorough as possible, collecting and weighing the feathers in a plastic bag of known weight.

The denuded bird was again suspended by the bill and the body surface covered with silicone sealant except for the feet, bill and wings. As such it was allowed to dry for 1 day and before removing the coating the contours of all 4 sides of the wings traced on paper. The coating was then divided into equal segments, pressed and pinned firmly on paper and the outlines traced. The surface area of the bird below the feathers was then determined with a planimeter. After removal of the coating the bird was weighed again on a Mettler balance and then suspended in water in a large graduated cylinder.

The difference in waterlevel before and after the suspension represents the volume and should approximate the weight of that carcass (specific weight of bird tissue is 1.)

The surface area obtained as such was used in calculating 2 thermal conductance = Kcal./cm. x hr. x °C, 33 (cooling rate) (body weight) (specific 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 after freeze drying to give moisture content. The dried feathers are placed in an air-tight plastic bag and stored in a freezer. Rather than following the methods employed by

Brisbin [19 68] in taking aliquots of the ground-up carcass the Pigeon Guillemot chicks and adults are small enough

(maximum 500 grams) to allow whole-carcass analysis. Subse• quently the frozen-dried carcass is placed in a large bottle containing petroleum-ether, and allowed to stand for 1 week.

The ether is then removed and the carcass washed twice with fresh ether. All the ether is collected and filtered by suction into a large 1 ltr. round flask followed by distilla• tion over a hot-water bath to retain the crude fat. The fat is transferred to a smaller flask of known weight and is placed in an oven set at 35 °C, to remove any traces of water.

The smaller flask was weighed to constant weight over 3 to

7 days. From later determination of any remaining crude fat

(see d) it was calculated that this "unofficial" method re• moves at least 98% of all the fat or ether extract.

The fatless 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 in a 1 quarter volume triple blade rotary grinder using a 2 mm. mash. The

ground material was collected and mixed in a bottle with a

tight lid and stored in a freezer for the following;

(d) Ash, moisture, crude fat or ether extract (Soxhlet

extraction apparatus) and heat of combustion (Parr adiabetic

Oxygen bomb calorimeter) determinations, adhering to the

Official Methods as laid down in the Manual of the Association

of Official Agricultural Chemists [A.O.A.C. Manual, 10th

Ediction, 1965].

3. Controlled Feeding of Chicks

Control observations on the growth of chicks were

carried out at camp during the 1970 season, by raising chicks

on a diet of fish of known weight. Attempts were made to

feed the chicks a diet closely to the natural one in the field,

supplemented, with portions of commercially caught flounders,

herring and rock-cod. Chicks of various ages were collected

from the field the majority (13 of 20) of ages from 5 to 8

days, just past being brooded. They were colour banded for

identification and housed in burrow-like nests, constructed

from drift wood, the size and volume being similar to the

nests in the field.

Prior to the first 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 intervals. Care was taken to maintain the weight of each chick proper for its age. One hour after the last feeding (21:00 hrs.), they were weighed again, the various body parts (see section A) measured and returned to their artificial nests.

Of the 20 chicks collected and raised only 2 chicks fledged successfully at a weight and age similar to field results. The rest died at various ages of unknown causes.

The average life span at camp was 18 days (one half the natural nestling period). Only those portions of the records where growth was similar to the growth rate in the field were used.

Consequently, results on energy retension, i.e. gram food intake to gain one gram gross body weight, compare favourably with similar results from the field. (Figure 16).

B. Results

1. Thermoregulation and .Basal Metabolism

The basal metabolic rate of Pigeon Guillemot chicks increases curvilinearly with increase in 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 in chicks of 300 grams and over, than on measurements based on respira•

tory C02 production, which may be a reflection of faulty measuring techniques or incorrect assumptions (R.Q.). Figure 9 indicates a rapid increase in basal metabolism the first few days following hatching, intercept the Brody-Proctor

100% level and remain higher than and parallel to that level until the chicks reach a weight of 200 grams (12 days old), then gradually levels off to eventually intercept the 100% level 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 initial phase. 2

Basal metabolism as a function of surface area (m ) versus age (Figure 10) shows a similar drastic increase during the initial 6 days after hatching, and then gradually decreases to adult level. The graph is based on values obtained from cooling rates of carcasses and is thus indicative of heat conduction and radiation. It neglects the ability of the living bird to control body temperature by evaporation

(convection), posture, degree of fluffing of the feathers and effective circulatory control to distant parts of the body. However, any discrepancy that may exist is a consistent one since the methods used are simple and similar for all 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 drastic decrease in the rate of heat conduction between core and feather surface during the first 8 to 10 days following hatching. This improvement coincides, with a period of con- 37

• respirometry

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 in the Pigeon Guillemot nestling, with two adults plotted for comparison (A). Values are plotted according to body weight on a double logarithmic scale on which the Brody- Proctor prediction for metabolic rate of homeio- therms is a straight line; the 50% and 150% lines have also been entered. 15

i 1 1 1 1 1 1 1 i O 10 20 30 40 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

adults . 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 in the Pigeon Guillemot sistently low values of insulative properties such as plumage

(feather weight Figure 12) and fat content (Figure 15). The rate of heat conduction then gradually decreases curvilinearly to reach adult values at approximately 30 days of age at which time plumage development in terms of total feather weight is almost completed (Figure 12).

2. Carcass Composition

The mean caloric 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 fat (ether extract) assumed at 9.00 Kcal. per gram.

Figure 14 depicts the trend in caloric value of one gram live weight of Pigeon Guillemot chicks and adults with age, and Figure 15 the percentage fat per lean-dry carcass weight and moisture content in percentage per live weight per bird as a function of age. The caloric value of live chicks decreases during the initial 8 days following hatching, which, as expected, results from a decrease in fat and increase in moisture content. This decline is then followed by a gradual generally linear increase in energy content with correspond• ing increase in the amount of fat and decrease in moisture.

During the last few days in the nest the chicks possess a higher amount of fat and lesser amount of moisture than the parents, which results in a slightly lower adult carcass energy value than chicks prior to nest departure. 25n

O 10 20 30 40 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 live weight) as a function of age in the ro Pigeon Guillemot 9//o fat % water content (Lean dry weight) (Live weight) CD 00 0) a> O o o O O 2! o I o

iQ C K (D

O 0 rt (D rt ro H n rort K ro a o o o (tO P 3 ftl Ml 01 rt

ro rt P> ro a o roV * o 3 Q MI ro oi h rt ^<

ro § ro o pi ro 3 Ml cr (u 3 Q fD oi —h h tt rort 01 >H4 o H* t. Hi ro ~ 313 o H- C H- «Q O H-vQ tr

B> Mi "rt (SCO OJ. rfd O

4\

00 o 00 e© 44 2 Values obtained for surface to volume ratio (cm. /ml.) versus age (Figure 13) show an increase during the first four days after hatching, rapidly decreasing linearly to approximately 22 days of age having reached close to adult values and then level off to fledge at a slightly higher S:V ratio than the adult.

3. Controlled Feeding of Chicks

One difficulty with the data on hand-raised birds is that growth was at times retarded as compared to wild chicks, a result due mainly to incorrect estimates of the daily ration required. It was decided to use only those portions of the camp records where growth was similar to the growth rates in the field. In computing the weight of fish fed to each chick for every gram of body weight gain ("energy retention") for both the hand raised chicks and data from the camera units, it was discovered that the two sets of data agreed so well to justify discussion of a composite curve (Figure 16). The graph indicates a constant rate of converting food into body tissue for approximately the first three weeks of nestling life, the efficiency declining steadily thereafter, reflect• ing the channeling of the food energy into other avenues.

At the end of the nestling period the rate of energy retention in the body is similar to that in the adult during periods of fat deposition (one series of data extending over 3 days). O IO 20 30 40 Days after hatching

Figure 13 Surface volume ratio (square centimeters per ml. body volume) as a function of age in the Pigeon Guillemot u 30' JD

M— o 25- DE^_ Acamp birds (captive chicks) CP ® field data (camera units) 0 C 20- o A

'5 -oQ 15- w e • © o A8 * cr 10- e

A * © 5- A CO A E • o CP 0 10 20 30 40 Days after hatching

ON

Figure 16 Rate of converting food into body tissue, plotted as grams of fish required to build one gram of bird versus the age of the nestling Pigeon' Guillemot 47

Hand-raided chicks had to be force fed especially if they were collected from the field at an older age, for example the two chicks that fledged successfully after being raised by hand were brought in at only 7 days of age.

Furthermore it was discovered that the life span at camp decreased inversely with increasing age at which they were collected from the field. The rough handling during force feeding, especially older chicks, may well be the cause of higher food demand.

Overnight weight loss in chicks from hand feeding at camp (Figure 17) gradually increases to a maximum between

25 and 30 days of age (mean values for 5 day intervals) then tapering off rapidly 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 in summary form the time course of growth in the Pigeon Guillemot. Growth in body weight, when viewed in absolute terms (daily increment in grams) reaches a maximum from about the 8th to 15th day. When this increment is considered with respect to the nestling weight each day, the relative rate of growth is seen to reach a maximum much earlier, about the 4th day. The data shows a similar onto• genetic pattern as in two other semiprecocial bird species

(Table 2); the Glaucous-winged Gull [Vermeer, 1963] and the

Wood Stork [Kahl, 1962]. If these processes are reflected in the food uptake, the implication is that the quantity brought to the nest daily should be maximal by about the 10th day, but that the efficiency of conversion of food to body mass may well be at peak values much earlier than this. Follow• ing upon the period of rapid increase in body weight is the growth of the plumage, which is practically at a standstill until about day 12, and virtually complete by day 28. My data are inadequate to pinpoint the period of maximal skeletal growth. Another major process at a peak between day 11 and

21, and tapering off late in nestling life, is the deposition of fat. When the nestling leaves the colony it has a fat depot in excess of that typical for adults, and this energy source is undoubtedly adaptive in helping to bridge the diffi- 20-i

40 Days after hatching

Figure 18 Instantaneous relative growth rate (a); total body weight increments on a daily basis (b); and plumage weight increments on a daily basis (c) for the Pigeon Guillemot nestling TABLE 2

Instantaneous Relative Growth Rates Compared in Percentages

Species Pigeon Guillemot, Glaucous-winged Gull Wood Stork Cepphus columba Larus glaucescens Mycteria americana

Investigator This study Vermeer, 1963 Kahl 1962

Weight at Hatching 44 grams 65 grams 62 grams

Days (intervals) after hatching

0-6 14.0 14 .0 21.9 7-12 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 38 days 45 days 64 days at fledging 424 grams 913 grams 2350 grams

Ul cult trial period of learning to fish. It will be remembered that the nestling Pigeon Guillemot commences an independent life from the moment it leaves the nest for the first time.

That this nest exodus (followed at once by colony departure) almost always occurs in the evening twilight period is reminiscent of the situation in other alcids [Greenwood, 1964] and can be viewed as an antipredator device, in the case of

Mandarte facilitating escape from marauding Glaucous-winged

Gulls.

Figure 19 presents in condensed form the data for food intake. No film records were obtained from the early stages when parental brooding is still in effect, and the only field data at this age involve a 36 hour watch where a succession of observers occupied a hide built at the back of one nest, enabling observation of the feedings at close quarters (approximately 10 inches). Visual estimates were made of the size of fish brought, and the type of fish noted, allowing subsequent conversion to weights. The agreement with the camp-raised birds is reasonable. The daily food ration reaches a plateau value at about the age when the daily weight increment of the chicks reaches its maximum, in agreement with the surmise stated above. As body growth declines, food uptake remains high, and this I interpret to mean that a major portion of the incoming energy is now being channeled into growth of the plumage. In a sense growth is made up of a succession of energy-demanding processes, regulated by a timetable of priorities so as to minimize competition for the incoming energy. [cf Portmann, 1945],

It is tempting to speculate that the plateau of food intake represents the practical limit of parental feeding in this species, what Royama [1966] has termed the optimal working capacity. In this view, the pattern of growth found in the

Pigeon Guillemot has been evolved to shorten the nestling period as much as possible given the level of intake that can

feasibly be maintained; this entails 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 is not a new one, as Kahl [1962]

stated the same hypothesis in his study of the Wood Stork, but in my case this 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 strikingly. In the

Great Tit [Royama, 1966], Wood Stork [Kahl, 1962], Herring

Gull [Spaans, 1972] and Starling [Westerterp, 1972], food

intake reaches an absolute maximum at or slightly after the

age of maximal daily weight increment. This implies that

energy demands for growth in weight are of over-riding

importance at this age, with the result that in order to balance the intake budget, maintenance costs must be kept

low, i.e. to allow growth, the total energy input must be

above and beyond the maintenance ration. The evolutionary 54 argument would be, given the optimal level 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) application 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 is to compute the proportion of the incoming energy that is incorporated in the body tissues. Since we know the caloric value of the food fish (determinations gave 1.2 Kcal. per gram fresh weight for a sample of food blennies collected from the nest, compar• ing favourably with values reported for other moderately fat fish: Whiting, 1.02 [Kahl, 1964]; Fundulus, 1.01, Menidia,

1.15, Roccus 1.15 [Brisbin, 1965], as well as the caloric value of the nestlings body a curve of energy retention can be constructed. I prefer the term "energy retention" to "eco• logical growth efficiency" used by Brisbin and Kahl for this concept, as in the absence if any data on assimilation rate, partition of energy uses of the incoming food, we are in fact not measuring efficiencies as such. In the Pigeon Guillemot, a remarkably high proportion of the incoming energy is channeled into body tissue early in nestling life. As in other birds where data is available, the curve of energy retention parallels that of instantaneous relative growth, an expression of the fact that both measure the high priority of body weight gain at this phase, at the expense of other energy uses. 55

That this period of maximal conversion occurs during the phase of parental brooding deserves mention (in the Pigeon Guillemot one of the parents is at the nest continuously by day until day 5, and by night until day 7). The chick is maintained in a warm and stable environment, obviously reducing the amount of energy lost to the surroundings as heat. Although parental brooding is thus advantageous to the chick, this cannot be prolonged indefinitely 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 efficiency and permitting the gathering of the requisite energy.

The exact form of the curve for energy retention is open to question. First, there are no data earlier than 4 days, and by analogy to other studies a lower retention rate is to be expected at the outset of nestling life. A more serious objection concerns the method of computation.

Strictly speaking, we are comparing the caloric value of the incoming food to the caloric value of the weight incre• ment over that period. Since all body components are not growing at the same rate, it cannot be expected that an over• all caloric value for the entire carcass will always be truly representative of the caloric value of the portion of tissue laid down in the period under consideration. If the increment is predominantly fat, for example, a much higher caloric equivalent per gram will apply than for a protein increment.

By considering the caloric values of the body components (lean weight, fat, and plumage) for nestlings of various ages estimates can be reached for the actual caloric incre• ments (bomb calorimtery gave the equivalents for lean weight, fat was assumed to have a value of 9 Kcal. per gram, and plumage 5 Kcal. per gram; these equivalents could be multiplied by the weight of each component to give the total caloric content of that component). This approach has been taken in

Figure 19 (based on 8 nestlings whose weight was normal for their age at the time of collection). The total caloric value of the increment rises sharply over the first two weeks,

is at a peak midway through the nestling period, and declines

thereafter. Retention rates computed from data in Figure 19 give an overall rate of 34% for the entire nestling period, a higher figure than that obtained from field estimates of

food intake per gram body weight gain (see Figure 16). An

alternative way of computing this overall conversion rate is

to take the total amount of fish required to raise a Pigeon

Guillemot, and comparing this with the difference in caloric value of a nestling and a fledgling bird. From the field data, approximately 2400 grams of fish are delivered per

chick (= 2800 Kcal.), and the increment in caloric value of

the nestlings body is approximately 1001 Kcal. (from comparison of carcass analyses of 1 day and 35 day old chicks), for an

overall rate of 35%. ro O o o o O o o o O Q

DD o JBMR • • I O CT o body components Q. f? CO j j intake Q ^< a § O -s O o *1 01 3 iQ Q. C cn l-l i o Q D fD fD D ZT fu (U (tl H. 3 H- O ft H- ^ O H- < o> 3 «-' rt rt> O I ft u » i Q 3 3 01 C » ti) ^< »> g K CO O fu iQ 3 H- •O (D fD (5 fD M H o Q O o 3 O~ mk; G —h 3 til Hi • 3 —+- O rt K •> tn n> rt Ul O rt 3 CD I 3 I 1 O rt ~\ ^ (B LT CD rt o PI n ft fu tu 3 H- H rt H 3 Q f• n n c H- ro fu 3 fu O 3 Ml rr H" 01 Oi H- O ci HI oi •< tr tn i o tu £ a D" ro 3 3 (D •< K fu P- tu ID tr ~ rt fu »< 3* a H- to tn rt O fu (-•• Hi 3 H 01 — Hi ro - tr ra — cn g ~H. H, fD fu (D h I rt 3 tu 3 O tu a 3 rt 3 tr P- H- ro I • ' II I ." o 3 tu n 0 H> H- Hi rt O P-3 fu (5 3 O H- rt to, O 3 K OJ fu fu O i w

BMR + body components 58

The two captive chicks raised successfully at camp required approximately 34 00 grams of fish each to complete development, thus reaching only a 25% rate of energy retention. It can be assumed that with the more frequent feedings in the field, a more efficient use of the incoming energy could be attained, so that the true figure for the conversion ratio in the Pigeon Guillemot is probably closer to the field estimate of approximately one-third. How does this compare to other fish-eating birds? In no other study are field data available on food intake, but captive Herring

Gulls have been raised by Brisbin [1965] and Spaans [1971] ,

Wood Storks by Kahl [1962], and a partial record on Brunnich's

Murre provided by Tuck and Squires [1955]. On a caloric basis Brisbin reports an overall conversion rate of 26% for the Herring Gull, and Kahl gives estimates for caloric equivalents enabling an approximation of 24% to be calculated.

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 fish delivered per gram of gain in body weight over the nestling 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 earliest, and presumably most efficient, phase of growth. Considering the many uncertain• ties in the original data, the degree of agreement is re• markable, and suggests that the conversion of fish to body tissue in growing birds goes on at a certain rate (perhaps limited 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 (activity). Some idea of where the incoming energy goes can be given by taking the data from metabolic runs as an indication of minimal maintenance needs, data from carcass analysis to show caloric increments of the three body components (lean body = primarily muscle, fat, and plumage), and data from the camera units for food intake. These data are assembled in Figure 19, and show that the difference between intake and expenditure as represented by maintenance and growth is of the order of 25% over the whole nestling period. Digestibility of a fish ration by growing birds is not known, but must obviously be high as activity must also be represented in the remaining

25% as well as faecal loss. 60

2. Development of Temperature Regulation

As reviewed by King and Farner [1961], a complex of

factors are involved in the establishment of functional

temperature regulation: a changing surface/volume ratio, a rising metabolic rate, and growth of the plumage, may all be

involved along with the establishment of requisite control mechanisms. In the case of the Pigeon Guillemot, the surest

indication of effective temperature regulation is the

cessation of brooding by the parent birds. . The nestling is

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 strides in the first week of

nestling life. Comparison of the figures presented earlier make it clear that growth of the plumage is not involved at

all, and that the dominant event is the boosting of the

metabolic rate, with a small contribution being made by a

somewhat more favourable surface/volume ratio. The spec•

tacular changes in basal metabolic rate shown for the Pigeon

Guillemot, with the nestling respiring at rates in excess of

that expected of adult homoiotherms of similar weight, show

a pattern resembling that found in 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 in Figure 20 to show the dependence of weight

gain on brood size. Singletons grew the most rapidly and were noticeably heavier at fledging than twins (Table 3a)

which were in turn faster growers than triplet chicks. The

comparison in Figure 20 shows that the slower-growing chick

of the pair in the twin broods experienced a growth rate

comparable to that of the fastest-growing chick of the triplet

broods. The interpretation of these findings is made earlier

by looking first at growth records for the same nests in

other seasons. For some reason growth in 1969 and 1970 in

particular was less rapid than in either 1959, 1960, or 1971

(mutually indistinguishable). The significant point is that

growth in singleton broods is equal in all years, while growth

in twin broods is indistinguishable from that in singletons

in 1959, 1960 and 1971 (the "good" years) but lags behind as

we have seen in 1969 and 1970. The most plausible explanation

would relate poor growth in the latter years to a depressed

availability of food items, since there does not seem to be

an intrinsic reason why the parent Pigeon Guillemot cannot

raise two chicks as well as one [witness, 1959, 1960, and

1971]. Seasonal differences in the growth rate of Glaucous-

winged Gulls on the same island have also been documented

[Ward, in preparation] but interestingly 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 30 40 Days after hatching

Figure 20 Growth as a function of brood-size in the Pigeon Guillemot. Plotted are the means for all data from 1969 and 1970: singletons are corcpared with the fastest and slowest-growiny individuals of the twin broods, and the fastest and slowest- growing individuals of the triplet broods the. all time low], making it unlikely that some basic weather

factors are involved. Although the young gulls are also raised predominantly on fish, the species involved differ

considerably (herring, for instance, being a staple item

although comprising less than 2% of the diet of nestling guillemots). No quantitative information on fish stocks is

available to test the idea of alterations in the abundance of food fish 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 in certain years, the success of

the Pigeon Guillemot in raising twins is as high as that for

singletons. A marked drop occurs when we consider the

artificially constituted triplet broods. Overall success is

poor, and only in a single instance did two of the chicks

attain weights comparable to the fledging weights of chicks

from normal broods [1971 experiment]. There is ample evidence

for the view that an impaired fledging weight will lessen

the chances of survival after nest departure [Perrins, 1965;

Robertson, 1971; Ward, in prep.) so that it is safe to con•

clude that the eventual recruitment from triplet broods would

at best be only marginally greater than the recruitment from

twin broods. In these circumstances there would be no

selection pressure for an increased brood size.

Examination of the records on food intake in the

various brood-sizes is 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 (All 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 daily total of approximately 200 grams of fish from day 10 to 30 according to the two complete camera records on broods of this size [one from 1970, and one from 1971] . The single triplet nest studied by Aitchison [1972] yields figures of similar magnitude (15-day plateau gives a mean of 195 grams of fish per day). We can also compute the weight of fish that must have been delivered to the 1970 triplets to obtain the observed growth increments (using the conversion rates in Figure 21). In this case the computed daily fish total works out to 198 grams (plateau value over 20 days).

I conclude from these figures that there is no evidence that the parent Pigeon Guillemots brought more fish to the triplet nests daily than they did to the normal twin broods.

The reason why in certain cases triplets could in fact be raised, although at a slower rate of growth, is that the plateau values were maintained for a longer period at these nets leading to a larger total fish input over the whole nestling period.

Differences in the daily feeding pattern between brood-sizes (Figure 5) might lead to the mistaken belief that more food is delivered with an increase in brood-size.

However, these daily feeding frequencies are nest specific

(see Figure 7) as the mean size, and thus weight, of the food items vary between nests.

There is ample evidence that the parent Pigeon

Guillemot responds to the hunger needs of the chicks (experi- ments cited in Drent, 1965 and Aitchison, 1972] so that the inability of the parents to bring more than the 200 gram daily ration to the triplet nests must reflect difficulties in food precurement, rather than in communication between the chicks and the parents. The parent birds at the triplet nest did not experience a decline in body weight during the nestling period, i.e. there is no evidence that they were in a situation of strain. Apparently the priority in this species is for unimpaired survival of the parents, over-riding the requirements of the brood. This is generally true for long-lived birds [Cave, 1968; Southern, 1970] where the adopted strategy ensures greatest probability of renewed breeding in the following season, rather than production under difficult conditions at possible risk to the adult. Bergman's [1971] findings are highly significant in this regard. Bergman studied the Black Guillemot, Cepphus grylle, the old-world counter• part of the Pigeon Guillemot (some authors have even considered the two forms conspecific) at the edge of its range in Finland.

In the study area the nestling guillemots were fed almost entirely on Zoarces viviparus, and in one season a scarcity of these fish led to a virtually complete withdrawal of the adult guillemots from the study area, and an almost total nesting failure as a result (eggs and chicks being abandoned by almost all 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 total daily fish ration of 200 grams. In no case were parents observed to bring more than this amount when means were computed over 5-day periods, and the resulting limi• tation expresses itself in a depressed growth rate in triplet broods (artificial, super-normal broods) in all seasons, and in twin broods in certain years. I conclude that the parent guillemots are unable to raise a triplet brood to reach normal fledging weights because they are already working at full capacity when raising a brood of two. The parent does not endanger its own survival in favour of its brood, but maintains body weight in all 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, similar to the maximal daily food ration that can be computed from Kahl's [1962, 1964] study of the Wood Stork: each parent brings 15-20% of its own weight to the nest daily. Since fish-eating birds in general require about one fifth to one- third of their body weight as a daily adult food requirement

[summary in Spaans, 1971, to which can be added Skokowa,

1962, Jordon, 1967, Robertson, 1972, Kahl, 1964] we can state 68 that the parent Pigeon Guillemot doubles the rate of fishing when feeding its nestlings (requirement for itself about

20% or 90 grams daily, share in nestling food about 100 grams daily) as does the Wood Stork. It is unlikely that this will turn out to be a general rule, however, since the available data for the Herring Gull [Spaans, 1971] would indicate a trebling of parental fishing rate at the peak. LITERATURE CITED

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