ISSN 10623590, Biology Bulletin, 2013, Vol. 40, No. 8, pp. 678–683. © Pleiades Publishing, Inc., 2013. Original Russian Text © V.V. Gavrilov, E.O. Veselovskaya, V.M. Gavrilov, M.Ya. Goretskaya, G.V. Morgunova, 2013, published in Zoologicheskii Zhurnal, 2013, vol. 92, No. 1, pp. 50–56.
Diurnal Rhythms of Locomotor Activity, Changes in Body Mass and Fat Reserves, Standard Metabolic Rate, and Respiratory Quotient in the FreeLiving Coal Tit (Parus ater) in the Autumn–Winter Period V. V. Gavrilov, E. O. Veselovskaya, V. M. Gavrilov, M. Ya. Goretskaya, and G. V. Morgunova Faculty of Biology, Moscow State University, Moscow, 119992 Russia email:
[email protected] Received January 12, 2012
Abstract—These studies were conducted in 1999–2010 on the territory of the Zvenigorod Biological Station of Moscow State University (western Moscow suburbs, 55o44′ N, 36o51′ E). Birds (Parus ater) were caught by mistnets. All the birds were banded and weighed, and their fat reserves were determined; then, the birds were released. A total of 85 individuals were caught. The standard metabolic rate and respiratory quotient (by the method of indirect calorimetry) were measured in 46 experiments with 16 birds. Two peaks were distin guished in the daily locomotor activity: a strongly pronounced daily peak (from 6 a.m. to 4 p.m.) and a weak evening peak (from 6 to 10 p.m.). The body mass did not change during the day. However, some trend for an increase in the mean body mass toward the middle and end of the day was noted. The fat reserves drastically changed during the day. The metabolic rate and respiratory quotient had a wellpronounced diurnal rhythm with minimal values at night (from 12 p.m. to 4 a.m.) and maximum values in the afternoon (from 12 a.m. to 4 p.m.). The total energy budget of Parus ater in the autumn–winter period, energy balance, and the main tenance of constant flying weight along with the dynamics of fat reserves are discussed. Keywords: coal tit, diurnal rhythms, locomotor activity, body mass, fat reserves, energy metabolism, respira tory coefficient DOI: 10.1134/S1062359013080062
The rhythm of general life activity and of specific characteristics is peculiar to all animals. The basis for all rhythms is the specifics of biochemical and physio logical reactions taking place in a living body. Func tioning of the whole body is based on the integration of individual rhythms and their agreement with environ mental changes. The rhythms of biological processes correspond to diurnal and seasonal dynamics of eco logical conditions. In birds, diurnal and seasonal peri odicities are defined. As a whole, birds combine their various biological seasonal phenomena with periods most favorable for their execution (Aschoff, 1966; Dol’nik, 1974, 1975; Gwinner, 1975; Daan and Aschoff, 1975; Berthold, 1980; Farmer, 1980; Gwin ner, 1984; Shilov, 1985; Brandstatter, 2002; Wikelski et al., 2008). Most locomotor activity of birds in the autumn– winter period corresponds to their feeding behavior. The dynamics of locomotor activity as a whole describes the search for food by birds in nature. The results of the search for food may be judged from the dynamics of body mass and fat reserves of birds. If the body mass and fat reserves of birds increase, it means
that the search for food was successful. If the body mass and fat reserves decrease, this corresponds to starvation, and it means that the food found was insuf ficient. The energy characteristics demonstrate energy possibilities and expenditures of the body, and some of them even give an idea of the substrate (food) used by an animal. The connection between animals and the environ ment is exercised through energy transfer and trans formation. Animals receive energy mainly from oxida tion of nutrients; therefore, oxygen consumption can serve as a measure of energy metabolism. There are almost no papers on the study of relations between specific features of behavior of birds in nature and their physiological characteristics. It seems important to study diurnal rhythms of various indices of the life activity of birds providing their existence in nature. Locomotor activity of birds, body mass and fat reserves of birds, and energy characteristics of birds have been considered. The object of this study is coal tits (Parus ater) dwelling in Moscow suburbs in the autumn–winter
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period after passingthe autumn molt and before the onset of the nuptial period. MATERIALS AND METHODS Field studies were performed in 1999–2010 in the period from October to March at Zvenigorod Biologi cal Station of the Biological Faculty of Moscow State University (Moscow oblast, 55o44′ N, 36o51′ E). Birds were caught by stationary mistnets. Nets 5 to 15 m long and 2 to 3 m high with a standard mesh of 14 mm were placed in the floodplain of the Moscow River and at the boundary of the floodplain and the first above floodplain terrace, at a site with an area of approxi mately 2.75 ha among trees and shrubs. In the periods of capture, 14 to 60 nets were used round the clock. The time of capture of birds was determined with an accuracy to 0.5–1 h. The rhythms of locomotor activ ity were determined from the number of birds caught in 1 h. The caught birds were banded, measured, and weighed, the presence of fat reserves was determined in them, and then they were released. Some birds were captured several times. The total caught was 85 indi viduals. Subcutaneous fat reserves in birds vary in propor tion to the fat content in the body cavity and tissues, always comprising a half of the total fat reserves (Blu mental’ and Dol’nik, 1962; Vinogradov et al., 1976). The subcutaneous fat of the fat depot is visible through the skin and in small birds is seen during puffingup of feathers. Methods of intravital assessment of fatness of birds are based on it. The semiquantitative method of fat determination—assessment of visible subcutane ous fat reserves in scores—was used (Blumental’ and Dol’nik, 1962; Vinogradova et al., 1976; Gavrilov et al., 2004). Since fatness in birds increases nonlin early, individuals with fatness score “much” were assigned coefficient 9 (Blumental’, 1967). From October 2009 to March 2010, some caught birds were placed into a gas analyzer chamber where standard energy metabolism was measured using the method of indirect calorimetry, which is based on measurement of gas exchange in an animal. Oxygen consumption and carbonic gas exhalation by the bird were measured using a flowthrough respirometer FoxBox of Sable Systems Inc. Simultaneously the rate of air passage through the chamber, temperature in the chamber, and the concentration of carbonic gas and oxygen were recorded. The intensity of ventilation of the respirometer chamber (passage rate) was set within 600–850 mL/min. The rate of oxygen consumption and carbonic gas exhalation was determined by the method of flowthrough respirometry. Through the hermetic respiration chamber in which the bird was located, air was blown in an incessant flow. The rate of oxygen consumption and carbonic gas exhalation was calculated on the basis of measuring the difference between the concentration of these gases at the output BIOLOGY BULLETIN
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Number of catches 20 18 16 14 12 10 8 6 4 2 0 06:30 08:30 10:30 12:30 14:30 16:30 18:30 20:30 Time of the day, h Fig. 1. Diurnal activity in the autumn–winter period.
of the respiration chamber with the bird and at the output of an empty similar chamber. The rate of oxy gen consumption and carbonic gas exhalation was equal to the difference between these concentrations multiplied by the rate of air passage through the cham ber. The concentration of carbonic gas and oxygen after respiration chamber with the bird and a similar empty 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. Measurements were performed in the daytime during 2.5–3.2 h and at night (8–10 h) in a darkened cham ber at a continuous temperature of 25°C that corre sponds to a thermoneutral zone. The time from the moment of catching the bird to placing it in the cham ber was 20–40 min. Experiments were started at dif ferent times of the day. The respiratory coefficient was determined during the experiment. For analysis, min imal values of the respiratory coefficient obtained dur ing the experiment were used. Energy metabolism in birds was calculated incessantly on the basis of the cal culated values of the respiratory coefficient at the given moment of time. For analysis, minimal values of the energy metabolism of the bird in the experiment were used. They were usually recorded 1.0–1.5 h from the beginning of the experiment or later when the gas trointestinal tract of the bird was empty. After termina tion of the experiment, the bird was released. Some birds were caught and measured several times. A total of 49 experiments with 16 birds were performed. RESULTS Locomotor Activity in the Autumn–Winter Period In the locomotor activity of coal tits, one can dis tinguish two periods: a clearly defined morning time daily from 6 a.m. to 4 p.m. (maximum from 10 a.m. to 11 a.m.) and a weakly pronounced evening one from 6 to 7 p.m. (Fig. 1). It is considered that all diurnal rhythms are based on circadian rhythms, and the usual rhythm of loco motor activity of small Passeriformes has a twopeak
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Body mass, g 10.2 10.0 9.8 9.6 9.4 9.2 9.0 8.8 8.6 8.4 06:30 08:30 10:30 12:30 14:30 16:30 18:30 20:30 Time of the day, h Fig. 2. Diurnal dynamics of body mass in the autumn– winter period.
Fatness, score 5.0 4.5 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0 06:30 08:30 10:30 12:30 14:30 16:30 18:30 20:30 Time of the day, h Fig. 3. Diurnal dynamics of fat reserves in the autumn– winter period.
Energy metabolism, kJ/24 h g 3.0 2.5 2.0 1.5 1.0 0.5 0
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Fig. 4. Diurnal dynamics of energy metabolism at rest in the autumn–winter period.
pattern: the first peak is in the morning and the sec ond, in the evening (Dol’nik,1974, 1975; Daan and Aschoff, 1975; Gwinner, 1975; Brandstatter, 2002; Wikelski et al., 2008). Our studies of other bird species demonstrated that their locomotor activity varies dur ing the day; activity peaks can shift to various hours of the day (Gavrilov et al., 2003, 2008). Dynamics of the Body Mass and Fat Reserves in the Autumn–Winter Period The diurnal dynamics of the body mass of coal tits in the autumn–winter period is shown in Fig. 2. The
body mass of birds during the day is almost constant. Only a tendency for an increase in the average body mass in the middle and end of the day immediately after passing a peak of locomotor activity was recorded (Figs. 1, 2). The diurnal dynamics of fat reserves in the autumn–winter period differs from the dynamics of body mass (Fig. 3). During the day, considerable fluc tuations of fat reserves were revealed: maximum differ ences comprised 4 scores. Fat reserves from 12 a.m. to 7 p.m. are higher than at other times. The obtained differences are significant (p < 0.001, H = 11, N = 82 according to the Kruskal–Wallis rank test). An increase in fat reserves also follows the peak of loco motor activity of birds. Energy Characteristics in the Autumn–Winter Period Since experiments for determination of energy characteristics of birds continued for more than 3 h, the time of the day was divided into fourhour periods, for which the average values of minimal metabolism of rest and the minimal respiratory coefficient were obtained. Energy metabolism of rest in coal tits has a clearly defined diurnal rhythm, with the minimal value in the night hours (from 12 a.m. to 4 a.m.) and one peak in the day hours (from 12 p.m. to 4 p.m.) (Fig. 4). Energy metabolism during night hours significantly differs— rank test. The maximum values of energy metabolism of rest fall on the period of 12 to 4 p.m. However, these values differ insignificantly from values obtained from 8 a.m. to 12 p.m., and together these values differ sig nificantly from values obtained from 4 to 8 p.m. The values of energy metabolism of rest obtained for the dark time of the day (from 4 a.m. to 8 a.m. and from 8 p.m. to 12 a.m.) do not differ and are not distin guished from values obtained in the evening, but rela tively light time of the day (from 4 to 8 p.m.). The minimal values of energy metabolism of rest for coal tits were obtained in the night hours from mid night to 4 a.m. (Fig. 4). This value corresponds to basal metabolism of birds (BMR) and is comparable to those obtained in other studies, BMR = 1.72 ± 0.99 kJ/day g (n = 8, where n is the number of experi ments). The maximum of daily energy metabolism of rest is 2.81 ± 0.35 kJ/24 h g (n = 6). In the literature there is only one value of the basal metabolism of coal tits in the autumn–winter period obtained for birds kept in captivity in Kaliningrad oblast. BMR at night is 2.13, and in the daytime it is 2.52 kJ/24 h g (Gavrilov et al., 1981). The values obtained in the given study for freeliving birds in Moscow suburbs differ from the published data, values of night measurements of energy metabolism of rest are smaller, and those of daily ones, greater. On the basis of a single comparison, one cannot conclude whether these differences are related to population BIOLOGY BULLETIN
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specific features of the studied birds or to different methods of study. The maximum differences between the values of energy metabolism of rest in the daytime and at night are 40%, which corresponds to the conclusions of Aschoff and Paul (1970). The differences in values obtained in other periods of the day are considerably smaller, for instance, metabolism of rest in the daytime (from 4 to 8 p.m.) is higher than minimal metabolism at night by only 17%, which corresponds to the con clusions of other authors (Kendeigh et al., 1977; Gavrilov, 1981). The values of energy metabolism of rest obtained in the dark time of the day in early morn ing and evening (from 4 to 8 a.m. and from 8 p.m. to 12 a.m.) do not differ significantly from the values obtained in the evening, but still light time of the day (from 4 to 8 p.m.). The minimal values of the respiratory coefficient of freeliving coal tits also have a clearly defined diurnal rhythm, with the minimal value at night (from 12 a.m. to 4 a.m.) and one peak in the daytime (from 12 p.m. to 4 p.m.) (Fig. 5). Differences in values of the mini mal respiratory coefficient in various periods of the day and the significance of these differences com pletely correspond to the differences of energy metab olism at rest. In previous experiments it was repeatedly stated that the respiratory coefficient in birds at night is lower than in the daytime (Powers, 1991; Prinzinger et al., 1992; Walsberg and Wolf, 1995), and that minimal val ues are at night starvation. In the daytime, the respira tory coefficient depends on the type of food and dura tion of the periods of daily starvation (Walsberg and Wolf, 1995) and possibly on the activity pattern of birds (Suarez et al., 1990). At present only for the hummingbird has it been shown that an increase in the level of energy consumption is related to an increase in the values of the respiratory coefficient (Suarez et al., 1990). As a whole, the diurnal rhythms of the energy metabolism at rest and of the minimal respiratory coefficient coincide: peaks of both energy characteris tics followed the peak of locomotor activity of birds. DISCUSSION The flight weight of birds is under internal control. An increase in the body mass increases the load on the wing, and the power spent on flight increases. On the other hand, birds are characterized by a high rate of energy metabolism whose support under conditions of an uneven food supply is possible only in the presence of buffer reserves of nutrients. Storing up nutrients leads to an increase in the body mass. Thus, the body mass of a bird is exposed to two oppositely acting fac tors: control of flight weight and control of the weight of energy reserves (Dol’nik, 1975), which leads to a complex structure of diurnal and annual cycles of the change in the average weight of birds. It was shown BIOLOGY BULLETIN
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RQ 0.82 0.8 0.78 0.76 0.74 0.72 0.7 0.68 0.66
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Fig. 5. Diurnal dynamics of minimal values of the respira tory coefficient in the autumn–winter period.
that seasonal changes in the average weight of birds in the population are regular and are repeated from year to year with a high accuracy (Dol’nik, 1975). Thus, coal tits during the autumn–winter period strive to support their body mass at an approximately equal level. For this, birds require only one strongly pronounced peak of locomotor activity in the morning hours, after which a small increase in their body mass occurs. The subsequent maintenance of the body mass in a stable state requires a considerably smaller loco motor (search) activity. In nonmigratory periods, fat reserves serve as an energy source under unfavorable conditions. As a result of a high food activity in the morning hours, coal tits accumulate considerable fat reserves already towards the middle of the day and maintain them up to the end of the day. Apparently, precisely an increase in fat reserves leads to an increase in the body mass. As was repeatedly recorded previously, an increase in fat reserves does not always lead to an increase in the body mass of birds (Dol’nik, 1975). In coal tits, an increase in fat reserves of the body is compensated for by other components (possibly, water). A high level of locomotor activity falls on the time period with a high level of energy expenditures and indicates the energy readiness of the body to act pre cisely in this time period, i.e., the total energy expen ditures of coal tits are maximum in the period of max imum locomotor activity. Energy metabolism at rest demonstrates the rate of energy utilization by animal organs and tissues at com plete rest not stimulated by food digestion and assimi lation or low temperature; and energy expenditures on respiratory, cardiac, and other muscular and glandular activities essential for life support. As should be expected, the minimal values of energy metabolism at rest of coal tits were obtained in the daytime when it is necessary to provide muscular activity and utilize the obtained food. Note that proper digestion process according to experimental conditions was not consid ered during the analysis of energy metabolism at rest. Expenditures on food utilization (for storing up fat reserves) are higher than on provision of muscular activity.
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According to the value of the respiratory coeffi cient, one can judge the main substrates used in oxy gen oxygenation. A value close to 0.7 indicates the domination of fat metabolism; 0.8, of protein metab olism; and values close to 1 indicate that carbohy drates are mainly used (ShmidtNielsen, 1982). From the changes in the values of the respiratory coefficient of coal tits (Fig. 5), it can be inferred that, during night hours, fats are predominantly oxygenated, and in the daytime protein food is mostly used. In winter, the food of coal tits by 65% consists of lepidopterans (cat erpillar of the cone tortricid moth (Laspeyresia stro bilella L.), by 15%, of homopterans, and the remain ing part is represented by small amounts of seeds, hymenopterans, beetles, and bugs (Ptushenko and Inozemtsev, 1968). These data agree with the values of the respiratory coefficient of coal tits. Since the body mass of coal tits during the autumn–winter period remains almost constant, and fat reserves regularly change during the day, we can conclude that in this period the energy balance is zero. This means that during the day birds receive from food as much energy as they spend per 24 h. Based on the data on energy metabolism at rest of coal tits at different times of the day, we can calculate the total energy consumption in the thermoneutral zone by hungry, inactive birds, staying in darkness for 24 h. The minimal energy expenditure by inactive, hungry coal tits for 24 h is 20.66 kJ/24 h, which corre sponds to 1.24 basal metabolisms (BMR). This is an energy level below which the energy diurnal expendi tures of coal tits cannot descend under any conditions. At the present moment we can assess the possible total diurnal energy expenditures of birds in nature. On the basis of data on diurnal energy expenditures by free living birds obtained by different methods, but mainly by labeled water, a generalizing equation of the depen dence of diurnal energy expenditures of birds on the body mass was calculated (Nagy, 2005). According to this equation, a bird with a body mass of 9.7 g will spend 49.33 kJ of energy per 24 h. The difference between the minimal level of energy expenditures of coal tits and their potentially possible level is 28.67 kJ or 1.72 BMR. This indicates that in the autumn–win ter period coal tits have a considerable reserve of pos sible energy that they can spend on the life activity and selfsupport. The presence of this energy is deter mined by presence and accessibility of food (mainly of insects and seeds). Since coal tits have a zero energy balance, every 24 h they should consume 49.33 kJ. If we take into consideration that the food assimilation coefficient is 0.7, every 24 h they should spend 70.47 kJ of energy. The average caloric content of insects is 8.78 kJ/g (Dol’nik et al., 1982). It is possible to calculate how many insects one coal tit consumes per 24 h—8.03 g of insects. The maximum fat reserves of the coal tit in the evening time, visually determined by the semiquanti
tative method of fat determination, are assessed as 4.5 scores. This for a bird with a mass of approximately 10 g comprises approximately 0.8 g of fat stored in the fat depots (Blumental’ and Dol’nik, 1962) or 31.2 kJ of energy. The calculations indicate that towards the evening coal tits store up as fat an energy amount that overlaps their minimal diurnal expenditures and cor responds to approximately 60% of energy spent during usual existence. We can suggest that the stored fat amount allows coal tits to live approximately 24 h without food with a minimal activity level. CONCLUSIONS In the autumn–winter period in coal tits, there is a complex dynamics of diurnal rhythms of various inter influencing characteristics. Coal tits maintain life activity in a stationary state: during the day they get as much energy as they spend in 24 h. During 24 h, coal tits maintain body mass on nearly the same level, and an insignificant increase in the average body mass was recorded in the middle and second half of the day. In the daytime coal tits receive energy feeding on various, mainly protein food; at night, in darkness, protein food is inaccessible, therefore, at night, energy is pro duced due to fat oxidation. In autumn and winter, the duration of the dark period at temperate latitudes is considerable; therefore, birds need to store up fat in noticeable amounts. However, creation of large fat reserves does not lead to a considerable increase in body mass. The fat reserve is formed in the daytime and is spent at night. The necessity to store up fat in this period is accompanied by increased energy expen ditures of birds at rest. Possibly precisely additional energy expenditures on food utilization and storage lead to a decrease in the activity level of birds in the second half of the day. Coal tits receive the total energy necessary for 24 h due to one peak of food activity that falls on the morning and daytime (maximum from 10 to 11 a.m.). Apparently, energy expenditures are also maximum in this period. The minimum of energy expenditures falls on the period from 12 to 4 a.m., when all energy is spent on respiratory, cardiac, and other muscular and glandular activities essential for life support and thermoregulation. Over 24 h towards the evening, the coal tits store up as fat an energy amount that overlaps their minimal diurnal expendi tures. We can suggest that the stored fat amount allows coal tits to live approximately 24 h without food at a minimal activity level. ACKNOWLEDGMENTS This study was supported by the Russian Founda tion for Basic Research (projects nos. 120401288a and 110400992a). BIOLOGY BULLETIN
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Translated by I. Pogosyants
