ISSN 00963925, Moscow University Biological Sciences Bulletin, 2014, Vol. 69, No. 4, pp. 184–188. © Allerton Press, Inc., 2014. Original Russian Text © V.V. Gavrilov, G.V. Morgunova, 2014, published in Vestnik Moskovskogo Universiteta. Biologiya, 2014, No. 4, pp. 46–50.
FAUNA AND FLORA
Diurnal Rhythms of Standard Metabolic Rate and Respiratory Quotient in the Coal Tit (Periparus Ater, Aves) during the Autumn–Winter Period V. V. Gavrilov and G. V. Morgunova Skadovskii Zvenigorod Biological Station, Department of Biology, Moscow State University, Moscow, 119899 Russia email:
[email protected] Received March 11, 2013
Abstract—Standard metabolic rate of birds has been measured by flowthrough respirometry based on their standard O2 consumption and CO2 release during the day and nighttimes in a darkened chamber at a con stant temperature of 25°C. The research was carried out in October–March 2009–2013, in the western part of Moscow region. The standard metabolic rate and respiratory quotient of coal tits have wellpronounced diurnal rhythms reaching their minimum in the nighttime (from 2:00 a.m. to 5:00 a.m.) and maximum in the daytime (from 11:00 a.m. to 2:00 p.m.). A significant linear dependence has been found between an increase in the standard metabolic rate and that in the respiratory quotient. The maximum difference between values of the standard metabolic rate during the day and nighttimes is 55%. It may be concluded that the main ele ments oxidized at night are fat reserves, whereas proteins, as well as a mixture of proteins, fats, and carbohy drates, are oxidized during the daytime. Keywords: coal tit, diurnal rhythms, standard metabolic rate, RMR, RQ, respiratory quotient. DOI: 10.3103/S009639251404004X
INTRODUCTION The metabolic rate (MR) of birds has been covered in many works since the 19th century. Nevertheless, the view has emerged that all data on this issue should be revised [1–3]. It is shown that the difference between the standard MR during the day and nighttimes is 25–40% [4] or 20% [5, 6]. In addition, a diurnal rhythm in the stan dard MR was found. This rhythm remains stable under permanent conditions [6–12]. It was also revealed that variations in MR depend on season, mode of life, hab itat types being used, etc. [13–16]. The amount of these variations, their stability during the day, diurnal rhythms, and relationship with other physiological and ecological characteristics are still not understood. During the oxidation of various substrates, differ ent amounts of CO2 are released [17]. The ratio between CO2, which forms during the process of metabolism, and O2, which is consumed, is defined as the respiratory quotient (RQ). This parameter plays an important role in the physiology of metabolism. To accurately estimate the metabolic costs of birds under different conditions and feeding, it is necessary to simultaneously measure O2 consumption and CO2 release [18]. The aim of this work is to measure, during different daytimes, the standard MR and RQ in coal tits (Peri parus ater, Aves) dwelling in the Moscow region during
the autumn–winter period taken directly from nature after passing the autumn molt and before the onset of nuptial period in the thermoneutral zone under stan dard conditions. MATERIALS AND METHODS The studies were performed in 2009–2013 in the period from October to March on the territory of the Zvenigorod Biological Station (Department of Biol ogy, Moscow State University) in the western part of Moscow region. Wild birds were caught by mistnets and enclosure traps. After the standard measurements, they are placed in a gas analyzer chamber, where their standard MR was measured by the method of indirect calorimetry. O2 consumption and CO2 release of birds were determined using a FoxBoxC flowthrough respirometer (Sable Systems, United States). Simulta neously, the rate of air passage through the chamber, temperature in the chamber, as well as concentrations of CO2 and O2, were measured. O2 consumption and CO2 release rates were determined by the method of flowthrough respirometry [19]. Outdoor air in the thermostat was divided into two equal flows. The first flow came into the hermetic respiration chamber with the bird. The second flow was blown into a similar empty (control) chamber. An incessant flow of air was allowed through the chambers by autonomous pumps (flow rate 600–850 mL/min, chamber volume
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Standard metabolic rate and respiratory quotient of coal tits during different day and night hours Time, hour
Number of experiments
Standard metabolic rate, kJ/(day g)
Respiratory quotient
11:00 p.m.–2:00 a.m. 2:00 a.m.–5:00 a.m. 5:00 a.m.–8:00 a.m. 8:00 a.m.–11:00 a.m. 11:00 a.m.–2:00 p.m. 2:00 p.m.–5:00 p.m. 5:00 p.m.–8:00 p.m. 8:00 p.m.–11:00 p.m.
7 8 7 11 8 8 4 11
1.8 ± 0.08 1.76 ± 0.17 1.79 ± 0.09 2.7 ± 0.48 3.18 ± 0.76 2.13 ± 0.29 1.88 ± 0.26 1.83 ± 0.29
0.743 ± 0.041 0.729 ± 0.05 0.753 ± 0.034 0.779 ± 0.043 0.799 ± 0.04 0.751 ± 0.038 0.76 ± 0.015 0.745 ± 0.037
approximately 2 L). Moisture absorbers were not used. The rate of O2 consumption and CO2 release by the bird was calculated on the basis of measuring the dif ference between the concentration of these gases at the output of the respiration chamber with the bird and at the output of the empty similar chamber (determined as the difference between these concentrations multi plied by the rate of air passage through the chambers). The concentration of CO2 and O2 after the respiration chamber with the bird and the empty similar chamber was measured successively in one device over 24–30 and 6–10 min, respectively. The frequency of taking device readings was once per 10 s. All gas volumes were worked out to the standard conditions (STPD). Mea surements were performed in the day (2.5–3.2 h) and night (8–10 h) times in a darkened chamber at a tem perature of 25°C (thermoneutral zone). The time from the moment of catching the bird to placing it in the chamber was 20–40 min. Experiments were started at different times of the day. RQ was determined during the experiment. MR of birds was calculated inces santly on the basis of the calculated values of RQ at a given moment of time [19]. For analysis, minimal val ues of RQ obtained during the experiment were used. They were commonly registered 1–1.5 h after the beginning of the experiment. Data averaging was per formed in the MatLab program on the segment of at least 4 min (minimum value segment). The same cal culations were taken to determine RQ. After termina tion of the experiment, the bird was released. Some birds were caught and measured several times. A total of 64 experiments were performed. The average body weight of coal tits used in the experiments was 9.7 ± 0.6 g (n = 32), given as mean value ± standard deviation.
FMR = 2.02 m0.94. The significance of this equation is low (p > 0.05, R2 = 23%). To rule out further effects of the body weight on the standard MR of birds, only specified MR values (MR per unit of time/1 g of the body weight in the bird) are given for all energetic data. The body weight of birds was found to influence their RQ in both day and nighttime experiments. Each set of experiments on estimating MR of birds lasted 3 h. Thus, the day was divided into eight 3h intervals, for which the corresponding standard MR and the minimum RQ were calculated (see table). The standard MR of coal tits has a wellpro nounced diurnal rhythm reaching its minimum during the nighttime (from 2:00 a.m. to 5:00 a.m.) and one peak in the daytime (from 11:00 a.m. to 2:00 p.m.) (see table, Fig. 1). Although all measurements of the stan dard MR in coal tits were taken in a darkened cham ber, it is seen from Fig. 1 that MR of coal tits depends on light hours of their diurnal rhythm. During the Energy, kJ/day g 5.0 Median
25%75%
MinMax
4.5 4.0 3.5 3.0 2.5 2.0 1.5
RESULTS MR of birds during the nighttime was determined by their body weight, whereas that measured in the daytime did not show such dependence. For the stan dard MR at night (FMR, kJ/day), the degree of equa tion depending on body weight (m, g) was close to 1:
1.0
0:30 3:30 6:30 9:30 12:30 15:30 18:30 21:30 Time, hour
Fig. 1. Diurnal dynamics of the standard metabolic rate in coal tits during the autumn–winter period.
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Respiratory quotient 0.88 0.86 0.84 0.82
Median
25%75%
MinMax
0.80 0.78 0.76 0.74 0.72 0.70 0.68 0.86
mal values of RQ are consistent with differences in the standard MR, but their significance is slightly lower (p < 0.05, Mann–Whitney Utest). Some differences were observed only for the time from 2:00 p.m. to 5:00 p.m. and from 5:00 p.m. to 8:00 p.m. It has been numerously emphasized in the previous studies that RQ of birds is lower during the nighttime than during the daytime [18, 20, 21]; the minimal val ues were observed during overnight starvation. During the day, RQ depends on the type of food and the dura tion of daytime starvation [18], as well as, possibly, on the activity of birds [22]. DISCUSSION
0:30 3:30 6:30 9:30 12:30 15:30 18:30 21:30 Time, hour
Fig. 2. Diurnal dynamics of the minimal respiratory quo tient in coal tits during the autumn–winter period.
autumn–winter period, day and night hours may be conditionally divided into: night (from 8:00 p.m. to 8:00 a.m.), day (from 8:00 a.m. to 5:00 p.m.), and twi light (from 5:00 p.m. to 8:00 p.m.). MR of coal tits is low during the entire nighttime. It is minimal in the middle of the night (from 2:00 a.m. to 5:00 a.m.). Dur ing the late daylight hours and twilight, MR gradually decreases from the level observed during the day to that reached in the nighttime (Fig. 1). MR of coal tits at rest is significantly different depending on the time of measurement (p < 0.001, Kruskal–Wallis test: H (7, N = 64) = 43.96). The minimal values of standard MR from 2:00 a.m. to 5:00 a.m. are significantly different from those obtained from 8:00 a.m. to 11:00 a.m., from 11:00 a.m. to 2:00 p.m., and from 2:00 p.m. to 5:00 p.m. (p < 0.01, Mann–Whitney Utest). The maximal values of standard MR obtained from 11:00 a.m. to 2:00 p.m. are significantly different from all values, except those observed from 8:00 a.m. to 11:00 a.m. (p < 0.01, Mann–Whitney Utest). Previously, when studying the standard MR rhythm of other bird species, two peaks of MR during the daytime (morning and evening hours) and one minimum (from 2:00 a.m. to 4:00 a.m.) were shown [6, 8, 10]. The minimal RQ of wild coal tits also has a well pronounced diurnal rhythm, which is minimal in the nighttime (from 2:00 a.m. to 5:00 a.m.) and has one peak in the daytime (from 11:00 a.m. to 2:00 p.m.) (see table, Fig. 2). The rhythm of RQ almost completely follows the rhythm of MR with one insignificant dif ference in the late day and twilight hours (Fig. 2). Sim ilarly to the standard MR, RQ is significantly different depending on the time of measurement, but the signif icance of differences is lower (p < 0.05, KruskalWallis test: H (7, N = 67) = 16.27). Differences in the mini
The minimal MR of coal tits at rest was obtained in the night hours: from 2:00 a.m. to 5:00 a.m. (see table, Fig. 1). These values correspond to all conditions of the basal (standard) metabolism in birds (BMR) and may be compared to the same ones obtained in other works. BMR = 1.76 ± 0.17 kJ/day g (n = 8). During the day, the maximal standard MR was 3.18 ± 0.76 kJ/day g (n = 8). The maximal difference between the standard MR during the day and nighttime was 55%, which corresponds to data [4] and even exceeds them. When comparing values obtained during other hours, let us emphasize that the differences were significantly lower. Thus, during the daylight hours (from 2:00 p.m. to 5:00 p.m.), the metabolism at rest was only 18% higher than the minimal one measured at night. The values of standard MR obtained in the dark time dur ing the early morning and evening hours differ signifi cantly (p > 0.05). In the literature, there is only one figure of basal metabolism obtained for coal tits that were kept in captivity during the autumn–winter period: 2.13 kJ/day g in the nighttime and 2.52 kJ/day g in the daytime [6]. In our study, the measurements of stan dard MR are lower in the nighttime and higher in the daytime. A single comparison is not enough to say whether these differences are related to specific fea tures characterizing populations of the studied birds or different methods of research. RQ allows us to judge about the main substrates used during oxidation: 0.7—fat metabolism prevails; 0.8—protein metabolism; 1—carbohydrate metabo lism [17]. Based on changes in RQ of coal tits, it may be concluded that fats are the main elements oxidized at night, whereas proteins or a mixture of substrates are oxidized during the daytime. It is known that the winter food of coal tits is lepidopterans (larvae of the light silverstriped piercer) (65%) and homopterans (15%). Other food objects are seeds, hymenopterans, beetles, and bugs [23]. These data follow the measure ments of RQ in coal tits. In coal tits, the diurnal rhythms of standard MR and minimal RQ are similar. In addition, there is a sig nificant linear dependence (p < 0.05), which associ
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metabolic rate and that in the respiratory quotient. The maximum difference between values of the stan dard metabolic rate during the day and nighttimes is 55%. MR of coal tits in Moscow region corresponds to MR of passerines. Nevertheless, the influence of dif ferent ecological and physiological factors on their level of MR demands further studying. Taking into account the rhythm of RQ, it may be concluded that the main elements oxidized at night are fat reserves, whereas proteins, as well as a mixture of proteins, are oxidized during the daytime.
0.75 0.80 Respiratory quotient
0.85
0.90
Fig. 3. Dependence of the standard metabolic rate (E, kJ/day g) on the respiratory quotient (RQ) of coal tits during the winter–autumn period.
ACKNOWLEDGMENTS We thank S.Yu. Kleimenov for help during this research, V.M. Gavrilov for discussion of the results, and the reviewer for careful reading of the manuscript. The study was supported by the Russian Foundation for Basic Research, project no. 120401288a. REFERENCES
ates an increase in the standard MR (E, kJ/day g) with an increase in RQ (Fig. 3). The equation describing this dependence, which includes both night and day time data, is the following: E = 10.57 RQ—5.68; n = 39, R2 = 51% (p < 0.05). It follows from the equation that birds have low energy costs when resting at RQ, the values of which are close to 0.7 and those higher to 0.9. It may be assumed that this results from a simple concordance of two independent rhythms. To estimate this assump tion, we analyzed the relationship between RQ and MR for every time interval. A significant relationship remained between RQ and energy costs. In addition, this relationship was more reliable for the most signif icant periods of time. For the period from 2:00 a.m. to 5:00 a.m.—time of minimal values (p < 0.05, R2 = 50%, n = 8); from 8:00 a.m. to 11:00 a.m. (p < 0.05, R2 = 62%, n = 11); from 11:00 a.m. to 2:00 p.m.— time of maximal values (p < 0.05, R2 = 44%, n = 8); in other periods of time—p < 0.05, R2 = 17–40%. These results show that there is, in fact, a relationship between RQ and energy costs of coal tits. The lowest energy costs and, as may be suggested, a more calm state correspond to the process of fat oxidation, whereas higher energy costs and a more active state demand protein and carbohydrate oxidation. CONCLUSIONS Therefore, the standard MR and RQ of coal tits have diurnal rhythms reaching their minimum in the nighttime (from 2:00 a.m. to 5:00 a.m.) and one peak in the daytime (from 11:00 a.m. to 2:00 p.m.). These two rhythms coincide. A significant linear dependence has been found between an increase in the standard
1. McKechnie, A.E. and Wolf, B.O., The allometry of avian basal metabolic rate: good predictions need good data, Physiol. Biochem. Zool., 2004, vol. 77, no. 3, pp. 502–521. 2. Konarzewski, M. and Ksiazek, A., Determinants of intraspecific variation in basal metabolic rate, J. Comp. Physiol., B, 2012, vol. 183, pp. 27–41. 3. McKechnie, A.E., Phenotypic flexibility in basal meta bolic rate and the changing view of avian physiological diversity: a review, J. Comp. Physiol., B, 2008, vol. 178, no. 3, pp. 235–247. 4. Aschoff, J. and Pohl, H., Rhythmic variation in energy metabolism, Fed. Proc., 1970, vol. 29, no. 4, pp. 1541– 1552. 5. Kendeigh, S.C., Dolnik, V.R., and Gavrilov, V.M., Avian energetic, in Granivorous Birds in Ecosystem, Pinowski, J., and Kendeigh, S.C., Eds., Cambridge: Cambridge Univ. Press, 1977, pp. 78–107. 6. Gavrilov, V.M., Daily measurements of resting metabo lism in birds, Ornitologiya, 1981, vol. 16, no. 15, pp. 42– 50. 7. Pohl, H., Circadian rhythms of metabolism in cardue line finches as function of light intensity and season, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 1977, vol. 56, no. 2, pp. 145–153. 8. Gavrilov, V.M., Seasonal and circadian changes of ther moregulation in passerine and nonpasserine birds: which is more important?, in Acta XVIII Congressus Internationalis Ornithologici, Ilyichov, V.D. and Gavilov, V.M., Eds., Moscow: Nauka, 1985, pp. 1254– 1277. 9. Saarela, S., Klapper, B., and Heldmaier, G., Daily rhythm of oxygen consumption and thermoregulatory responses in some European winter or summeraccli matized finches at different ambient temperatures, J. Comp. Physiol., B, 1995, vol. 165, no. 5, pp. 366–376. 10. Gavrilov, V.M., Kerimov, A.B., Golubeva, T.B., Ivankina, E.V., Il’ina, T.A., Karelin, D.V., and Kol yaskin, V.V., Energetics, morphophysiological hetero
MOSCOW UNIVERSITY BIOLOGICAL SCIENCES BULLETIN
Vol. 69
No. 4
2014
188
11.
12.
13.
14.
15.
16.
17.
GAVRILOV, MORGUNOVA geneity of individuals, and population structure in birds. I. Energy, morphophysiological heterogeneity, and population structure of the great tits of Moscow, Ornitologiya, 1996, vol. 27, pp. 34–73. Woodin, M. and Stephenson, R., Circadian rhythms in diving behavior and ventilatory response to asphyxia in canvasback ducks, Am. J. Physiol. Regul. Integr. Comp. Physiol., 1998, vol. 274, pp. R686–R693. Arens, J.R. and Cooper, S.J., Seasonal and diurnal vari ation in metabolism and ventilation in house sparrows, Condor, 2005, vol. 107, no. 2, pp. 433–444. Swanson, D.L. and Liknes, E.T., A comparative analy sis of thermogenic capacity and cold tolerance in small birds, J. Exp. Biol., 2006, vol. 209, pp. 466–474. White, C.R., Blackburn, T.M., Martin, G.R., and But ler, P.J., Basal metabolic rate of birds is associated with habitat temperature and precipitation, not primary productivity, Proc. R. Soc. B, 2007, vol. 274, no. 1607, pp. 287–293. McNab, B.K., Ecological factors affect the level and scaling of avian BMR, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 2009, vol. 152, no. 1, pp. 22–45. Swanson, D.L., Seasonal metabolic variation in birds: functional and mechanistic correlates, Curr. Ornithol., 2010, vol. 17, pp. 75–129. SchmidtNielsen, K., Animal Physiology: Adaptation and Environment, Cambridge University Press, Cam bridge, 1980.
18. Walsberg, G.E. and Wolf, B.O., Variation in the respira tory quotient of birds and implications for indirect cal orimetry using measurements of carbon dioxide pro duction, J. Exp. Biol., 1995, vol. 198, pp. 213–219. 19. Lighton, J.R.B., Measuring Metabolic Rates. A Manual for Scientists, Oxford: Oxford Univ. Press, 2008. 20. Powers, D.R., Diurnal variation in mass, metabolic rate, and respiratory quotient in Anna’s and Costa’s hummingbirds, Physiol. Zool., 1991, vol. 64, no. 3, pp. 850–870. 21. Prinzinger, R., Schafer, T., and Schuchmann, K.L., Energy metabolism, respiratory quotient and breathing parameters in two convergent small bird species: the forktailed sunbird Aethopyga christinae (Nectarini idae) and the Chilean hummingbird Sephanoides seph anoides (Trohilidae), J. Therm. Biol., 1992, vol. 17, no. 2, pp. 71–79. 22. Suarez, R.K., B. Lington, J.R., Moyes, C.D., Brown, G.S., Gass, C.L., and Hochachka, P.W., Fuel selection in rufous hummingbirds: ecological implica tions of metabolic biochemistry, Proc. Natl. Acad. Sci. U.S.A., 1990, vol. 87, no. 23, pp. 9207–9210. 23. Ptushenko, E.S. and Inozemtsev, A.A., Biologiya i khozyaistvennoe znachenie ptits Moskovskoi oblasti i sopredel’nykh territorii (Biology and Economic Value of Birds of Moscow and Adjacent Areas), Moscow: Mosk. Gos. Univ., 1968.
Translated by A. Karmazina
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