An evaluation of heart rate as a measure of dailymetabolism in pigeons (Columba livia)

0300-9629~79~0801-051

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AN EVALUATION OF HEART RATE AS A MEASURE OF DAILY METABOLISM IN PIGEONS (COLUMB.4 LWIA) ROBERT K. FLYNN and JAMES A. GESSAMAN Department of Biology, Utah State University, Logan, UT 84322, U.S.A. (Receioed

9 October

1978)

Abstrict-1. A positive, linear relationship of heart rate (HR) to metabolic rate, as measured by O2 consumption (V,,), was demonstrated in 7 pigeons. 2. Heart rate-O* consumption regressions measured within a l- or 2-week period on 7 pigeons did not differ significantly. However, the slopes of the regressions increased significantly in all birds over the next 6 weeks. 3. Vo,-T, data extrapolated to a body temperature of 407°C at zero metabolism and thermal conductance was - 0.23 cal/hr g “C. 4. The individual regression equations were used in conjunction with average 24-hr heart rate to predict the existence metabolism (EM) of these same pigeons measured in each of three food consumption trials. Predicted EM values averaged 41.7 + 7.1% higher than measured values. The data suggest that the HR-Vo, relationship of a solitary bird changes in the presence of social interactions.

INTRODUCTION

The use of heart rate as an indirect measure of metabolic rate in free-living animals has been examined by several authors in a variety of homeothermic vertebrates (Webster, 1967; Brockway & M&wan, 1969; Owen, 1969; Morhardt & Morhardt, 1971). Johnson & Gessaman (1973) reviewed the literature on this subject and examined the strengths and weaknesses of heart rate as an indicator of metabolism. They concluded that “heart rate can be a fair to good index of the average hourly metabolism” in some individual animals that (a) are at rest or exercizing moderately, (b) demonstrate strong linear correlation between resting metabolic rate and resting heart rate, and (c) are maintained in an emotional state of minimal stimulation during experimentation. More recently, Wooley & Owen (1977) demonstrated a positive, linear relationship of heart rate to metabolic rate in 19 wild, adult black ducks (Anas rubripes). Data were pooled by sex to yield two linear equations with r* values of 0.45 and 0.57 for males and females, respectively. The authors concluded that heart rate can be used to monitor energy expenditure of free-living ducks, but that care should be taken in evaluating the impact of the radiotransmitter and the influence of psychological stimuli on heart rates. Holter er al. (1976) examined the metabolism-heart rate relationship in 6 adult white-tailed deer (Odocoileus virginianus). Their results demonstrated statistical differences in metabolic rate among individual animals as well as seasonal effects. The authors presented general, predictive equations for each season and concluded that the technique would be useful for studying deer in their natural environment. Holmes et al. (1976) examined the heart rate-heat production relationship (HR-HP) in 3 Jersey calves under both laboratory and field conditions. They measured heart rate and CO2 production (HP) simultaneously in a climatic chamber under a variety of temperature (alternating between 4 and 20°C). mois-

ture, and air movement conditions. After 1 or 2 days of accommodation to the experimental procedure, significant correlation was observed for the HR-HP relationship. Field measurements of heart rate were obtained by radiotelemetry while each calf experienced a variety of sun, wind, rain and snow conditions over an ambient temperature (T,) range of - 2 to + 15°C. Immediately after the heart rate measurements in the field had been completed, each calf was returned to the climatic chamber for 24-36 hr of simultaneous HR-I-fP measurements. The metabolic rates measured in the climatic chamber corresponded closely with those predicted from the HR-HP relationship that had been determined after the field measurements. The authors concluded that measurement of heart rate can provide useful information regarding the energy metabolism of free-ranging animals, provided that the HR-HP relationship is measured at regular intervals under conditions similar to those encountered in the field. In summary, the potential of HR as a measure of metabolism in homeotherms has been established. However, no one has previously evaluated the accuracy of this method. That is, no one has compared metabolism estimated from HR with metabolism measured concurrently by a totally independent method, under free-ranging or partially free-ranging conditions. In the study described here we assessed the accuracy of the heart rate method on homing pigeons. The food consumption method and the doublylabelled water (D,‘aO) method (Mullen, 1973) are the only alternatives available for measuring the metabolism of a bird either penned outdoors or ranging freely in the field. Based on 3 separate studies of: (1) American kestrels (F&o spmverius) by the second author of this paper, (2) white-crowned sparrows (Zonotrichia leucophrys) by James R. King (personal communication) and (3) Laysan albatross (Diomedea immutnbilis) by Eugene LeFebvre (personal communi-

511

512

ROBERT K. F’L.YNNand JAMES A. C&SSAMAN

cation). the i&‘sO method was judged unreliable. The food consumption method was, therefore, chosen for this study. We elected to study homing pigeons for this study because their daily food consumption could be measured accurately. The pigeons ranged freely outside their coop for 1 to 1.5 hr each day, then voluntarily returned to feed and remained in the coop for the duration

of that

particular

24-hr

period.

the caloric value of the collected guano was subtracted from the total (Cday) GE1 to determine a measure of existence metabolism (EM. kcal!day). In both Parts I and II, heart rates were detected bk electrodes implanted in each bird’s sternum (Sawby & Gebsaman, 1974) and telemetered via an electrocardiogram transmitter (Narco Biosystems Inc Mode1 E-3. &ight 6.7 g). Impulses were recorded on a \trtp chart physmgraph during the 15-set samples taken ebery IOmin for all sampling intervals.

S4ATERIAL.S AND METHODS RESCILTS 4UD DIS(‘lW3ON Seven pigeons (Cnl~rmhu Iwiu) were randomly selected from a flock of 13 birds for this experiment. ,411 birds were housed outdoors in a coop that was roofed. screened on two sides (facing north and west) and solid paneled on the other sides. This experiment was divided into two parts. Heart rate (HR) was measured concurrently with oxygen consumption iv;,,) in Part 1. and with existence metabolism (EM) in Part II. Part I (trial 1) was performed prior to Part II and then repeated (as trial 2) after the completion of Part II, approximately 6 weeks later. One linear regression equation was derived from each of the two trials of Part I. These equations were then used to predict two values of average daily metabolic rate from average 24-hr heart rate (HR2.J recorded during each food consumption trial of Part II. In Part I, each bird was enclosed in a darkened metabolism chamber and exposed to an average of 10 air temperatures (- 10 to + 25°C) to vary the animal’s rate of oxidative metabolism. VU, was measured by a Beckman 0, Analyzer (Model G-2) in an open circuit systep (flow rate = about 2.0l/min. Measurements of HR and V’, were made simultaneously for 2 hr at each chamber temperature. The birds were allowed to adjust to each new temperature for at least 30,min before measurements were started. The majority of Voz measurements were made during the daylight hours and all values were corrected to standard temperature and pressure conditions. The birds under study were fasted for at least 12 hr prior to any measurements and a respiratory quotient of 0.72 was assumed (King & Farner. 1961). The chamber temperature was measured by thermocouple. In Part II. existence metabolism was determined by a modification of the food consumpti~~n technique (Kendeigh. 1949. 19753. The flock was released daily from the coop just after the seven experimental birds had been weighed to the nearest 0.1 g. They usually flew within the vicinity of the coop for 5 IOmin. then returned to rest near the coop for another 60 90 min. At the end of the release period, a dish of food (Purina Pigeon Racing Mix) was placed in the coop. Subsequently. the pigeons entered a one-way door to the coop and ate for about 20min. they then were again weighed to the nearest 0.1 g. Water and grit were provided an l&irrml except during this 20-min period. The birds remained m the coop until this procedure was repeated the next day. about 22 hr later. We assumed that weight gained during the ?-hr period equalled the weight of food confumed for the entire 24-hr period. since the birds did not have access to food in the other 22 hr. Three 7-day feeding trials were carried out with each bird. Since the net change In body weight during a feeding trial was less than 2”,, of the body weight. daily metabolism measured by the food consumption method was regarded as existence metabolism. The product of the daily food consumption and its caloric equivalent (4.15 kcal’gm) equalled the gross energy intake (GEl. kcaliday). The EM for each trial was computed as rhe product of GEI and the average assimilation efficiency (EM!GEI) for a given bird. The EM!GEI was determined from two 4-day feeding trials during which each bird was housed in a separate cage. For each trial.

Ox!:yun

~onsumpt

ion i77 ~/uf i0l1 r 0 llrtrrr ~~tr

The correlation between heart rate and po, was positive for each pigeon. The correlation coeficients (r) ranged from 0.72 to 0.97, with the exception of an I of 0.48 for pigeon 2, trial 1. Pigeon 2 was particularly excitable, but accommodation to experimentation and handling resulted in a correlation of 0.92 for this bird in trial 2. A comparable range of correlation coefficients was reported by Wooley & Owen (1977) for black ducks, with values ranging from 0.66 to 0.95 for males and 0.74 to 0.91 for females. In four cases, the HR--io, values recorded during the first 2 hr of experimentation (2 values) or during the regular feeding time, 1300 to 1500 hr (2 values), were poorly correlated with subsequently measured values. Holmes et nt. (1976) cited improvement in correlation between HR and HP with accommodation to experimentation. Wooley & Owen (1977) stated that “inadequate acclimation to test situations and the addition of unfamiliar stimuli, such as a radio transmitter, can elevate metabolism above true resting levels by considerable amounts”. We therefore eliminated these four values (4 out of 143 measurements) from the regression analysis. The variability of the HR-Gki relationship among individuals in this study was very low in contrast to the high individual variability reported elsewhere (Webster, 1967; Holmes, 1976; Wooley & Owen. 1977). Morhardt & Morhardt (1971) noted that the shapes and slopes of the HR-I;bi regression varied between individuals within 6 rodent species. and they anticipated that “slopes of regression lines from different individuals of any species would vary”. Halter er al. (1976) cited statjstica~ly significant differences in metabolic rates among individual white-tailed deer but excluded this main effect in their predictive model. As a result of the low variability among individual HR-V,, relationships in this study, the regression equations for each trial (except pigeon 2. trial 1) were combined to yield two generalized equations (Fig. 1). Analysis of covariance determined the statistical validity of these pooled equations with r values of 0.93 (F5.48 = 1.074) and 0.85 (F,,,, = 0.66) for trials 1 and 2, respectively. A shift in the HR-V,, relationship from trial 1 to trial 2 can be observed from the pooled equations in Fig. 1. The HR corresponding to a given Ijf)2 in trial 1 was consistently higher than that measured 6 weeks later in trial 2: i.e. the slopes of the regression lines became more positive with time. Holmes et trl. (1976) noted a shift in regression coefficient of the HR-HP relationship in one calf from 4.7 to 3.4 over a period of 14 days. Morhardt & Morhardt (1971) stated that the shapes and slopes of regression equa-

rate as a measure of daily metabolism

Heart

16.0-

N=59 14.0-

0 ./’

? 12.0.E E lO.O8 -r, 8.0g

513

of each bird in trials 1 and 2. The mean thermal conductance values for trials 1 and 2 were -U.21 and - 0.23, respectively. These values correspond very closely with Herreid & Kessel’s (1967) predicted values of -0.23 for birds of body weight = 282.?g. Furthermore, the line obtained by combining the Vo,-air temperature data for all birds in this study extrapolates to a body temperature approximation of 40.7”C at zero metabolism. From the above evidence; the pigeons in this study appear “normal” with respect to their ‘V,,-air temperature relationship.

#j’’

r = 0.93

in pigeons

6.0-

Average daily energy metabolism

4.02.0-

L, ,

I

50

100

I

I

150

200

Heart rate (bpm) Fig. I. Linear regression equations are shown for pooled data from trial 1 (solid line) and trial 2 (dotted line) of Part I. tions varied for the same individual on different days. The nature of the cardiovascular changes causing these shifts cannot be hypothesized since neither cardiac output or oxygen carrying capacity of the blood were measured.

O.x)~genconsumption in relation to air temperature A linear regression analysis of the vo, -air temperature data was used to describe the thermal conductance (defined as the slope of the f&-T, equation)

Metabolized energy. The measured values of average daily metabolized energy for each feeding trial are presented in column A of Table 1. Predictions based on the HR-V,, relationship. Average daily energy metabolism values predicted from HR,, and the HR-voZ relationships were consistently higher (41.7 + 7.1%) than those measured in concurrent food consumption trials (Table 1, columns B and C). The most probable explanation is that social interactions within the coop, disturbances from outside the coop, and possibly other factors elevated HRz.,, while energy expenditures remained low. The HRV,, relationship was measured on each individual while it rested alone in a chamber. The bird was then returned to the coop among 12 other pigeons. It is likely that the quantitative relationship between HR and V,, of a solitary bird changes in the presence of other pigeons. The effect of the emotional state of an animal on its heart rate has been thoroughly documented in the literature (Boas, 1932; Thompson, 1968). Holmes er

TABLE I. MEASURED AND PREDICTEDEXISTENCEMETABOLISMOF PIGEONS

Metabolic rate (kcal .day - ‘)

(4

(B)

(C)

Predicted from

Per cent of measured [(B-A)/A x IOO]

heart rate (HB,,)

Bird

Trial

1

I 2 3

56.5 62.2 49.4

62.5 55.3 55.3

10.6 - Il.1 11.9

2

1 2

52.8 42.4

48.0 47.7

-9.1 12.5

3

1 2 3

45.1 33.9 56.0

60.3 62.9 68.8

33.7 85.5 22.9

4

1 2 3

41.9 45.4 41.9

11.0 69.1 88.2

60.8 53.5 110.5

5

1 2 3

39.9 39.5 41.3

56.3 55.8 69.3

41.1 41.3 67.8

6

1 2 3

50.4 42.0 45.0

59.3 68.1 19.4

17.7 62.1 76.4

I

1 2 3

49.2 38.6 40.2

62.5 62.5 62.9

21.0 61.9 56.5

Measured

Mean

k SE

41.7 + 7.1

ROBERTK. FLYNN and

514

~1. (1976) reported an increase in heart rate of 1.5 times resting levels within a 20-set period during which a calf observed a man and three dogs walking nearby. The calf did not stand up nor demonstrate obvious emotion at this or other stimuli. such as a tractor starting up or a door banging, both of which induced a similar response. In the present study, an HR increase that exceeded resting levels by 4 5 times was recorded during the first several minutes of each feeding period, even though the birds‘ activity levels increased only slightly. Social interactions and other psychological stimuli may have had a similar influence. Physical activity levels in the coop were consistently low. and even during their 2-hr release period the birds were at rest at least 95”,, of the time. Throughout the course of the food consumption trials, the birds were exposed to 7’;s near or within their thermoneuiral zone. Our data for two pigeons (1 and 2) seem to indicate that the error in predicting EM from the HR-Vo’,, relationship decreased as the actual level of EM increased. The feeding trials for these birds were conducted in early May while those for the remaining 5 birds were conducted from mid-July into August. During the May feeding trials the ambient temperatures averaged 1l.S3t which is below the lower critical temperature of 14 C for pigeons as reported by Steen (1957) and the measured EMS for these birds were higher than those measured in the summer. The difference between measured and predicted EM for pigeons 1 and 2 was 2.9 + 5.4”,. This suggests that if our entire experiment had been performed at lower ambient temperatures. the accuracy of predicting metabotism from heart rate may have been improved. In summary, this study has shown that a positive, linear correlation exists between heart rate and metabolic rate in individual hqming pigeons housed alone. The regressions of HR.-I/,, measured within a l- or 2-week period did not differ significantly among different individuals; however, the slopes of the regressions increased significantly in all birds over the next 6 weeks. We also noted that the average daily heart rate of a pigeon, used in conjunction with an HR--Vo, regression measured on that individual while in an isolation chamber, was a poor predictor of average daily metabolism when the bird was housed with other pige.ons in an outdoor coop. This suggests that the HR-Vo, relationship of a solitary bird changes in the presence of social interactions. Ackno,\~/edgemenr~-- This investigation was supported by NSF Grant Number GB 40109. We wish to thank Rav B. Owen, Jr, Keith L. Dixon and Lois Cox for review& an earlier copy of this manuscript. REFERENCES Boas E. P. (1932) The Heart Rate. Charles C. Thomas, Springfield, IL.

JAMESA.

GESSAMAN

BROCKWAY J. M. & M&WAN E. H (1969) Oxygen uptakr and cardiac performance in sheep. .I Phj,+)l. 202. 661-669.

HOLMFSC. W.. STEPHENS D. B. & ‘TONFRJ. N. (1976) Hearr rate as a possible indicator of the energy metabolism of calves kept out of doors I.if~rctcl&i Prod. SC?. 3. 33% 341. HOLTER J. B., URBAN W. E.. HAYI--?, H. H. X: SILVER13. (1976) Predicting metabolic rate from telemetered heart rate in white-tailed deer. J. Wild/. Mgmt 40. 626-629. JotgNx)N S. F. & GESSAMAN J. A. (1973) An evaluation of heart rate as an indirect monitor of free-living energy metabolism. In Ecoloyic~ul Eneryrric,s of Homeotherm.~~ .4 V&v Compntihle wsith Eco/ogic,u/ Modeling (Edited by GESSAMAN J .A.),pp. 44-54. Utah State University Press. Logan. KENDEIGH S. C. (1949) Ef%ect of temperature and season on the energy resources of the English sparrow. 4uh 66, 113-127. KENDE~GHS. C. (1975) Measurement of existence energy in granivorous birds, In .~ethods~~~ ~co~ogic~~ Bioenergerics. IBP Handbook No. 24 (Edited by GRODZINSKI W., KELKOWSKIR. Z. & DuIv(.A~: A.). pp. 341L345. Blackwell Scientific Publications, Oxford. KENDEIC;HS. C. (1977) Avian energetics. In Granirorcm\ Birds in Ecosystems, Vol. 12 (Edited by P~NOWSKIJ. B: KENDEI~;HS. C.), pp. 127-204. International Biological Programme. Cambridge University Press. KING;J. R. & FARNERD. S (1961) Energy metabolism thermoregulation and body temperature. In Bbloyy cm/ ~ornp~rufil!e Ph?;siology of Birds,Vol. 2 (Edited by MARSHALLA. J.), pp. 215-288. Academic Press. New York. MORHARDTJ. E. & MORHARDTS. S. (1971) Correlation between heart rate and oxygen consumption in rodents. Am J. Physiol. 221, 1580-1586. MULLEN R. K. (1973) ‘The D,“O method of measuring the energy metabolism of free-livmg animals. In Ecofo~~ic,ul Energerics of Homeorherms: A View Compurrhlts wirh Ecologiwl Modeling (Edited by GESSAMAI\J. A.). pp 3243. Utah State University. Logan. OWEN R. 6. JR (1969) Heart rate. a measure of metabolism Ph r‘sir1l 31. tn blue-winged teal. CT