Temperature regulation in hatchling puffins (Fratercula arctica)

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163 j. Orn. 128, 1987: S. 163-170

Temperature Regulation in Hatchling Puffins (Fratercula arctica) By Claus Bech, Frode J. Aarvik and Dag Vongraven The developmental pattern in birds ranges from an altricial pattern, with the chicks being totally dependent on parental care, to a precocial pattern characterized by a high degree of independence of the chicks. In addition are several intermediate patterns (semi-altricity and semi-precociality) recognized. The pattern of development is usually reflected in the thermoregulatory capacity of the newly hatched chicks: precocial chicks being thermoregulatory superior to altricial chicks. However, even within a family having the same developmental pattern, thermoregulatory adaptions to the environment can be found. Thus, in the Anatidae, in which development are precocial, newly hatched chicks from species breeding at higher latitudes are more coldresistant than chicks from species breeding in warmer areas (KoSKIMIES& LAHTI1964). The pattern of development in birds is evolutionary conservative, i.« there is usually a uniform developmental pattern within each family (NIcE 1962, RICKLErS 1983). Actually, Alcidae is the only family split between developmental types. Four species of murrelets are precocial, with the chicks leaving for sea within 2--4 days after hatching, while the majority of the other species within the Alcidae are semi-precocial, the chicks being brooded for a longer time and departure occurring only after attaining near adult body weight (SEAI_¥1973). In addition a few species (the Razorbill, Alca torda, and the Murres, Uria) have an intermediate developmental pattern between precociality and semi-precociality. In these species, the chicks leave the nest when at approximately one-fifth of adult body weight (SEAI~Y1973). The first thorough study on chick thermoregulation in a precocial alcid was provided by EPPLEY(1984). He studied the Xantus' Murrelet, Synthliboramphys hypoleucus, and found a high metabolic capacity in hatchlings, resembling that found in the highly precocial diving ducks (KosKIMIES& LAHTI1964). Although semi-precociality is the most common type of development within the Alcidae, only fragmentary data on the thermoregulation in semi-precocial alcid chicks have been published (DRENT 1965, JOHNSON & WEST 1975, TZCHANZ1979, BARI~TT 1984). In the present study we describe the thermoregulatory capacity of newly hatched Common Puffins, Fratercula arctica, a semi-precocial alcid (S~ALY1973), and compare the results with similar data obtained from other species within the Alcida« The aim of the study is to investigate if the different developmental patterns are reflected in the thermoregulatory capacity of the newly hatched chicks.

Material and Methods The study was carried out during June and July 1984 on the island of Sklinna on the central

164

C. BECH,E AARVIK& D. VONGRAVEN

[ J" 128Orn"

west coast of Norway (65.12 N 11.0 E). The puffin colony on the island numbers about 2250 pairs (ROV 1982). In the middle of June puffin eggs were collected and placed in an artificial incubator, in which the temperature and relative humidity was held at 37 °C and 60--70 % relative humidity respectively. After hatching the chicks were allowed to dry before we used them in experiments. They were used within 48 hours after hatching and were not allowed to feed before the experiments. The mean body weight of the chicks was 41.9 (S. D. = 3.3; 36.2--53.0; n = 25) g.

The oxygen consumption ({tO2) was measured by a two-chambered manometric respirometer, The chicks were placed in one of the chambers in which a 25 % NaOH-solution acted as a CO2-absorber. The two chambers were connected by a water-filled V-shaped tube Constant pressure was assured in the chambers by injecting pure oxygen from a graduated syringe into the chamber holding the chick. The amount of oxygen injected equalled the oxygen consumed. All values of ~O2 are given in STPD-conditions. The metabolic rate (MR) was calculated from the oxygen consumption using a conversion-factor of 1 ml 02 (8TPD) g-1 h-1 equal to 5.582 W kg-1. During experiments, the body temperature (Th) was measured continuously using an insulated copper-constantan thermocouple placed in the rectum of the chick. The thermocouple extended out through a sealed hole in the top of the bird-compartment and was connected to a Fluke digital thermometer (accuracy 0.2°C). The respiratory mbvements of the chicks produced small fluctuations of the water-column between the two compartments, enabling us to record the respiratory frequency (f). The time for 10-20 breaths was measured using a stop-watch and the frequency was expressed as number of breaths per minute Usually 10 measurements were taken during one experimental trial at a certain ambient temperature, the mean value being used. In addition to obtaining the respiratory frequency during the oxygen-consumption measurements, we also measured f independently at several levels of Th. Experiments were run at ambient temperatures (Ta) between 20 °C and 38.5 °C. The respirometers were submerged in a thermostat-controlled water-bath, in which the watet temperatute could be varied by adjusting the thermostat (Grant, type FC 15). Data were obtained after two hours exposure to the experimental temperature. During periods of stabilization, the birdcompartment of the respirometer was flushed with atmospheric air at a rate of 100 ml min -1 in order to prevent hypoxia.

Resuats

Altogether 39 measurements of oxygen uptake were obtained at ambient temperatures between 2 0 ° C and 38.5°C. The results indicates a narrow thermoneutral zone (TNZ) extending from 32 to 35 °C (Fig. 1). Within the T N Z the mean oxygen uptake was 1.31 ml 02 g-1 h-l, corresponding to a basal metabolic rate (BMR) of 7.31 W kg -1. Below the thermoneutral zone, the oxygen uptake increase linearily according to the formula VO2 -- 4.97 - - 0.11 Ta (n = 19, r 2 -- 0.84); the regression line intersects the abscissa at Tx of 44.0°C. Based on the measured VO2 at thermoneutrality and the m a x i m u m attainable VO2 reached at T~ of 20 °C, the thermogeneic capacity (TC) becomes 2.1 times BMR.

Heft 2 ] 1987

Temperature Regulation in Puffins

165

3.5 Fr«tercula

4: 3.0 o~ Co

2.5

0rcfica

00

2.0 II

o

1.5

•

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•

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eJ

o•

= o õ

1.0 0.5 I

20

2'5 3'0 3'5 Ambient femperefure {°C}

4'0

Fig. 1. Relationship b'etween ambient temperature (T~) and oxygen consumption in newly hatched pnffins. Values obtained after two hours exposure to each T~.

The body temperature of the chicks within the thermoneutral zone was 38.6 °C (n = 9, S. D. = 0.9). Below the TNZ, Tb showed a steady decrease (Fig. 2), even though VO2 increased simultaneously. Below Ta of 20°C, the lowest ambient temperature tested, the body temperature could not be maintained and would steadily decreas« At ambient temperatures above TNZ, the body temperature increased. 45 Frefercu[o

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25 30 35 Ambienf temperclture (°C)

I

l~0

Fig. 2. Relationship between ambient temperature (T~) and body temperature (Tl,) in newly hatched puffins. Values obtained after two hours exposure to each Ta. The diagonal line marks equal values of Ta and Th.

166

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C. BECH, E AARVIK& D. VONGRAVEN

J. Orn. 128

~.0

Fr«terculo arctkQ o O

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Ambienf femperafure (°C) Fig. 3. Thermal conductance as a function of ambient temperature in newly hatched puffins. All values obtained after two hours exposure to each T~.

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Fig. 4. Respiratory frequency in newly hatched puffins exposed to various ambient temperatures. The line is fitted using 5point moving averages.

Heft 2 ] 1987 J


167

The thermal conductance (C) was calculated as MR/(Tb -- Ta). Thus, C represents the overall ('wet') thermal conductance according to ASCHOFF(1981). The relationship between ambient temperature and thermal conductance is illustrated in Fig. 3. The relatively high values found in some of the experiments below TNZ, is due to wetting of the chicks and are therefore not representative The mean conductance found at Ta of 32°C and below (excluding the results from the wer chicks) is 1.22 mW g-1 oC-1. At high ambient temperatures the main avenue of heat loss is through respiration. Thus, at Ta above the TNZ, the thermal conductance increase sharply due to increased respiratory heat loss (Fig. 3). This is also evident from Fig. 4 showing a rise in respiratory frequency when Tb rises above the normal resting level. The highest respiratory frequency was recorded at Tb at about 41°C and amounted to 90 breaths per minute, which is 4.5 times the minimum value of 20 breaths min -I at Tb between 38 and 39.5°C. Discussion

Puffin chicks maintain a constant body temperature only within a very narrow thermoneutral zone extending flora 32 to 35 °C, below which the body temperature of the chicks are held at gradually lower levels (Fig. 2). It is remarkable that at ambient temperatures between the thermoneutral zone and approximately 20 °C, which is the lowest Ta at which Tb could be maintained relatively constant, the chicks maintain their metabolic rate at submaximal levels while their Tb is lowered below the thermoneutral level. Thus, it seems that the chicks instead of utilizing their metabolic capacity fully, choose to lower their body temperatur« A similar suggestion have been put foreward by JORGENSEN& BL~ (1985) for Willow Ptarmigan, Lagopus lagopus, chicks. Such a strategy will resuk in saving of energy and thus minimize the food &mand. However, the strategy is energetically most advantageous if the chicks are passively rewarmed by the patents and not have to spend energy on the rewarming process. As found in many other species of birds, the hatchling puffins have sub-adult body temperatures. Thus, the thermoneutral Tb is 38.6°C in newly hatched puffins, compared to 40.1 °C in adult birds (incubating birds, BARe,ETT 1984). Similar subadult body temperatures of hatchlings have been recorded in other alcid species (DRENT 1965, BARRETT1984, EPPLEY1984) as well as in many other species of birds (R~cKLEFS 1983, O'CONNOR 1984). The thermoneutral body temperature in the newly hatched chicks (38.6°C) is higher than Tb reported by BARRETT(1984) for 1 day old chicks immediately after removal from the nest (35.6°C) and even higher than Tb of 9 day old chicks measured by telemetry during natural behaviour in the nests (38.0 °, VONGRAVENet al. 1987). This indicates that during natural incubation, the newly hatched chicks exhibit a lower body temperature than measured at thermoneutrality during laboratory conditions, implicating that the mean operative temperature in the field is somewhat below the thermoneutral zone and that the chicks therefore have a body temperature and metabolic rate, which is lower and higher, respectively, than the thermoneutral levels (cf. Fig. 1 and 2).

168

C. BECH,E AARVlK84 D. VONGRAVEN

[ J' 128Orn"

It has been claimed that the low Tb found in newly hatched birds is a result of a low thermoregulatory set point (O'CoNNOR 1975, MYHRe & ST~EN 1979). An indication of such a lowered setpoint in the puffin chicks is the low temperature threshold for the increase in respiratory frequency. The threshold is 39.0°C (Fig. 4), i.« well below the adult body temperature of 40.1°C (BARRETT 1984). A similar result is found in the Black-legged Kittiwake, Rissa tridactyla (BECH et al. 1984). The low (sub-adült) body temperature in the puffin chicks is a resuk of a low basal metabolic rate in addition to a high thermal conductance The BMR is only 70 % of the predicted for an adult bird in the a-phase having similar body weight (AscHOFF & POHL 1970), and the thermal conductance is 40 % above the expected value for an adult bird of similar size (AscHOFF 1981; Tab.). It is evident that a low basal metabolic rate and a high thermal conductance (low insulation value) is a common trait of all newly hatched alcid chicks studied so far. The basal metabolic rate is highest in the precocial Xantus' Murrelet, while the semi-precocial species have the relatively lowest basal metabolic rate, that of the Puffin chicks being only 70 % of the expected value (Tab.). The thermal conductance seems to follow an unexpected trend: the precocial Xantus' Murrelet have the highest value (lowest plumage insulation), whereas the best insulation is found in the semiprecocial Common Puffin (Tab.). The thermogeneic capacity, i.e the factor by which the metabolic rate can be increased above the BMR, is much higher in the precocial species than in both the Brunnich's Guillemot and the Puffin (3.5 times vs. 1.6 and 2.1, respectively). Thus, the high thermogeneic capacity of the Xantus' Murrelet chick (EPPLEY1984) seems to be a main parameter characterizing the precocial type of development in contrast to both the intermediate and the semi-precocial type of development (Tab.). It is interesting that within the genus Larus the thermogeneic capacity seems to be the only parameter which is correlated with breeding distribution: the further north the species are breeding, the higher is the Thermoregulatory parameters in newly hatched chicks in the Alcidae. BW: body weight; Th: body temperature; TC: thermogeneic capacity; BMR: basal metabolic rate; C: thermal conductance; m: measured values. BW

Tb

(g)

(°C)

m

24.8

38.7

10.05

84

74.1

39.2

7.03

Cepphus columba 37.5 Fratercula arctica 41.9

38.6

8.26 7.31

Sp&ies

BMR (W kg-1)

TC

(% expl) (xBMR)

C (W kg-1 °C-1)

Reference

m

(%expb)

3.5

2.44

219

EewEY(1984)

79

1.6

1.21

183

AARvm& VoN~~VEN(unpubl.)

77 70

2.1

1.22

140

D~NT (1965) This study

Precocial: Synthliborarnphys hypoleucus

Intermediate: Uria lomvia

Semi-precocial:

a Basedon ASCHOFF& Po~L(1970) for adult non-passerine birds. -- b Basedon AscHorF(1981) for adult non-passerine birds in their a-phase

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169

thermogeneic capacity of the newly hatched chicks. Also, neither the insulation nor the BMR shows any relations to breeding distribution (DAwsoN & BEI,¢r~TT 1981). Thus, although the available data are limited, a tentative hypothesis concerning the significance of the different thermoregulatory parameters in the development of homeothermy, could be, that a high capacity for increasing the metabolic heat production have the main influence, insulation being of only minor significance There also seems to be a slight relationship between BMR and type of development (Tab.). The chicks of the Xantus' Murrelet requires parental brooding for only 2 - 4 days after hatching (EPeLEY1984), at which age the chicks have increased their insulation considerably, enabling them to be homeothermic when going to sea. So, the development of homeothermy in the chicks is not hampered by the low plumage insulation at hatching, as the insulatory property of the plumage is increased very rapidly within the first few days after hatching (EePLEYi984). The puffin chicks, in contrast, requires brooding behaviour for a much longer time Even though the puffin chicks hatch with a relatively good thermal insulation, their thermogeneic capacity is too limited to sustain homeothermy, which only is achieved at an age of 6 to 7 days, when the chicks have increased both the thermogeneic capacity and the plumage insulation (own unpubl, obs.). It thus seems that a prerequisite for a precocial type of development within the Alcidae is a high thermogeneic capacity at hatching. Therefore, the high value of TC (3.5 times BMR) found in the Xantus' Murrelet (EPPLEY1984) resembles that found in many newly hatched ducks ( K o s ~ s & LAHTI1964). In contrast is the low value in the puffin (2.1 x BMR) characteristic for many species developing semiprecocialy. We thank "SigvalBergesen d. y. og hustru Nanki's Almennyttige Stiftelse" for financial support, Lakseoppsynet for transportation and the Norwegian Lighthouse Authorities for the use of Sklinna Lighthouse facilities. Our thanks are also due to J. BARSETand N. Riäv for various assistanc« Summary Body temperature (Th), basal metabolic rate (BMR), thermal conductance and thermogeneic capacity was measured in newly hatched Common Puffin (Fratercula arctica) chicks. The thermoneutral zone extends from 32 to 35°C in which Tb was held at 38.6°C. The BMR (7.31 W kg-1) and thermal conductance (1.22 mW g-1 oC-1) was 70 % and 140 %, respectively, of the expected values for adult birds. The chicks were able to increase their metabolic rate by a factor of 2.1. A comparison with similar measurements for a precocial alcid species (the Xantus' Murrelet) suggests that the ability to increase the metabolic rate (i.e a high thermogeneic capacity) is a key factor for the precocial type of development within the Alcidae

Zusammenfassung T e m p e r a t u r r e g u l a t i o n bei frisch geschlüpften Papageitauchern

(Fratercula arctica) An frisch geschlüpften Papageitauchern (Nesthocker) wurden Körpertemperatur (Th), Basalstoffwechsel (BMR), der Wärmedurchgangswert und die Fähigkeit zur Wärmebildung

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C. BECH, E AARVIK& D. VONGRAVEN

[ J" 128Orn"

gemessen. Die Thermoneutralzone (konstante Körpertemperatur von ca. 38.6°C) liegt in einem Umgebungstemperaturbereich von 32 bis 35°C. Der BMR (7.31 W kg -l) und der Wärmedurchgangswert (1.22 mWg-1 °C-1) betrugen 70 % bzw. 140 % der zu erwartenden Adukwerte. Die Küken waren in der Lage, ihren Stoffwechsel um den Faktor 2.1 zu steigern. Ein Vergleich mit ähnlichen Messungen bei einer nestflüchtenden Alkenart (Synthliboramphys hypoleucus) legt nahe, daß die Fähigkeit, die Stoffwechselrate zu vergrößern (also hohe thermogenetische Kapazität) ein Schlüsselfaktor für den Typ des Nestflüchters bei den Alcidae darstellt. Literature

ASCHOFF, J. (1981): Thermal conductance in mammals and birds: its dependence on body size and circadian phase. Comp. Biochem. Physiol. 69A: 611--619 • ASCHOrr, J., & H. POHL(1970): Der Ruheumsatz von Vögeln als Funktion der Tageszeit und der Körpergröße. J. Orn. 111: 38-47. • B~ET~, R. T. (1984): Adult body temperatures and the development of endothermy in the Puffin Fraterculaarctica, Razorbill Alca torda and Guillemot Uria aalge. Cinclus 7: 119--123. • BECH, C., S. MARTINI,R. Bt~E~r& J. G. RaSMVSS~N(1984): Thermoregulation in newly hatched Black-legged Kittiwakes. Condor 86: 339--341. • Dr~vrr, R. H. (1965): Breeding biology of the Pigeon Guillemot, Cepphus columba. Ardea 53: 99--160. • DAWSON,W. R., & A. E BEr,~~TV(1981):Field and laboratory studies of the thermal relations of hatchling Western Gulls. Condor 74: 177--184. • EevrEY, Z. A. (1984): Development of thermoregulatory abilities in Xantus' Murrelet chicks Synthliboramphys hypoleucus. Physiol. Zool. 57: 307-317. • JOHNSON, S. R., & G. C. West (1975): Growth and development of heat regulation in nestlings, and metabolism of aduk Common and Thick-billed Murres. Ornis Scand. 6: 109--115. • JORGENSrN,E., & A. S. BLIX(1985): Is the rate of body cooling in cold exposed neonatal willow ptarmigan chicks a regulated process? Acta Physiol. Scand. 124, Suppl. 542:404 • KOSKIMIES,J., & L. LAHTI(1964): Cold-hardiness of the newly hatched young in relation to ecology and distribution in ten species of European ducks. Auk 81: 281--307. • MYHRE, K., & J. B. STEEN (1979): Body temperature and aspects of behavioural temperature regulation in some neonate subarctic and arctic species. Ornis Scand. 10: 1--9. • NIcE, M. M. (1962): Development of behaviour in precocial birds. Trans. Linn. Soc. N. Y. no. 8: 1--211. • O'CONNOR, R. J. (1975): Nestling thermolysis and developmental changes in body temperature. Comp. Biochem. Physiol. 52A: 419--422. • Ditto (1984): The growth and development of birds. John Wiley & Sons, Chichester. • POCKLEFS,R. E. (1983): Avian posmatal development. In: Avian Biology (FA~NrR, D. S., & J. R. KINGeds.) XII: 1--83; Academic Press, N. Y. • R~v, N. (1982): Sjofuglunders~kelser pä Sklinna 1980--81. Rep. Viltforskn. Trondheim. • SEALV,S. P. (1973): Adaptive significance of posthatching developmental patterns and growth rates in the Alcidae. Ornis Scand. 4: 113--121. • TSCHANZ,B. (1979): Zur Entwicklung von Papageitaucherküken Fratercula arctica in Freiland und Labor bei unzulänglichem und ausreichendem Futterangebot. Cinclus 2: 70--90. • VONCRAWN, D., E J. A~VIK & C. BrcH (1987): Body temperature of Puffin Fratercula arctica chicks. Ornis Scand. (in press). Authors' address: Department of Zoology, University of Trondheim, N-7055 Dragvoll, Norway.