Singing is not energetically demanding for pied flycatchers, Ficedula ...

Behavioral Ecology Vol. 15 No. 3: 477–484 DOI: 10.1093/beheco/arh038

Singing is not energetically demanding for pied flycatchers, Ficedula hypoleuca Sally Ward,a Helene M. Lampe,b and Peter J. B. Slatera School of Biology, Bute Medical Buildings, University of St. Andrews, St. Andrews, Fife, KY16 9TS, UK; bDepartment of Biology, Division of Zoology, University of Oslo, P.O. Box 1050, Blindern, N-0316 Oslo, Norway

a

ost theoretical analyses of sexually selected displays predict that such displays should be costly (Fisher, 1930; Grafen, 1990a,b; Lande, 1981; Zahavi, 1975). Passerine bird song is a classic example of a display that is used in mate attraction by males and in mate choice by females (Andersson, 1994; Searcy, 1992; Searcy and Yasukawa, 1996). Female birds can use male song to select mates on the basis of high song rate (see Alatalo et al., 1990), large repertoire size (see Catchpole et al., 1986) or particular song phrases (see Vallet and Kreutzer, 1995). The importance of female choice in reproductive strategies has been reinforced by studies of paternity using DNA fingerprinting, because even paired males have the potential to obtain additional mates and extrapair matings, or to be cuckolded (Møller and Birkhead, 1991). Male song thus has clear fitness benefits to the singer. However, there are few empirical data regarding whether vocalization is energetically costly for birds, and the interpretation of some studies has been controversial (Eberhardt, 1994; Franz and Goller 2003; Gaunt et al., 1996; McCarty, 1996; Oberweger and Goller, 2001; Verhulst and Wiersma, 1997; Ward et al., 2003; Weathers et al., 1997). It has often been suggested that passerine bird song is an energetically costly display (see Baptista and Kroodsma, 2001; Catchpole and Slater, 1995; Lambrechts, 1996). This idea is intuitively attractive as bird song is often a protracted series of rather loud sounds produced by a comparatively small animal. Song production clearly involves some metabolic cost to a bird because energy is transmitted to the surroundings in the form of sound pressure waves. The muscles involved in the control of respiration, the syrinx, and movements of the beak are used during song (Larsen and Goller, 2002; Suthers et al., 1999), and all muscular activity requires energy. Field data also suggest that passerine bird song has an energetic cost that may be great enough to influence daily energy budgets. The overnight rate

M

Address correspondence to S. Ward. E-mail: [email protected]. Received 14 April 2003; revised 11 August 2003; accepted 13 August 2003.

of mass loss by nightingales, Luscinia megarhynchos, has been found to increase with the duration of nocturnal song (Thomas, 2002). These data suggest that singing requires more energy than does roosting, although rates of mass loss are difficult to quantify in terms of energy use (Kvist et al., 1998). Gottlander (1987) showed that pied flycatchers, Ficedula hypoleuca, decreased their song rates in cold weather when thermoregulatory costs are greater (Calder and King, 1974), and foraging rates are likely to be reduced owing to lower insect activity (Benton et al., 2002). The song rates of pied flycatchers were increased by provision of supplementary food during cold weather but not during warm weather, suggesting that shortage of energy on cold days led to the reduction in song rate (Alatalo et al., 1990, Gottlander, 1987). Field data from other passerine species also imply that singing has an energetic cost because song rate increased when birds were in good body condition or were provided with supplementary food and decreased after cold nights and after activity, or when the ectoparasite load was experimentally increased (for review, see Lambrechts, 1996). However, it can be difficult to separate the effects of the energetic cost of sound production from changes in food intake owing to trade-offs in time budgets between singing and foraging. Thomas et al. (2003) found that diurnal rates of mass gain by European robins, Erithacus rubecula, were reduced when birds sang more, but considered that this was likely to be owing to reduction in the time spent feeding rather than to the energetic cost of singing. There have been only two previous studies of the energetic cost of singing in wild-caught birds, and these have reached contradictory conclusions regarding whether singing is energetically costly. Eberhardt (1994) found that singing was energetically costly in Carolina wrens, Thryothorus ludovicianus (3.9 6 1.4 3 basal metabolic rate [BMR]), whereas Oberweger and Goller (2001) concluded that sing was not energetically costly for European starlings, Sturnus vulgaris (2.1 6 0.2 3 BMR). Study of additional species is required to determine which conclusion is likely to be applicable to most passerine birds. The three studies of captive strains of canaries, Serinus canaria, and zebra finches, Taeniopygia guttata, found that

Behavioral Ecology vol. 15 no. 3 International Society for Behavioral Ecology 2004; all rights reserved.

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Male passerine bird song is a classic example of a sexually selected display. Theory predicts that such displays should be costly, but there are few empirical data on the potential costs of bird song. We measured the rate of oxygen consumption by male pied flycatchers, Ficedula hypoleuca, singing inside a respirometry chamber. Song is known to be important in mate choice by pied flycatchers, so we predicted that if passerine song is energetically costly, we should be able to measure the costs in this species. The metabolic rate of singing pied flycatchers (N ¼ 3) was 0.62 6 0.11 W, which was equivalent to 2.7 6 0.5 3 basal metabolic rate. Metabolism during singing did not differ significantly from that during standing. A power analysis of this test showed that the metabolic rate of singing birds was less than 1.12 6 0.04 times that of standing birds. Comparing the maximum cost of song production with daily energy expenditure (DEE) during nestling rearing, each hour of singing rather than standing would increase DEE by 0.4%. Thus, song production appears to be energetically cheap in the pied flycatcher in relation to the overall daily energy budget. However, because birds cannot sing and eat at the same time, there could be an energetic constraint to song duration owing to the need to spend sufficient time foraging. Key words: energy expenditure, Ficedula hypoleuca, pied flycatcher, song. [Behav Ecol 15:477–484 (2004)]

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METHODS Birds and experimental conditions The pied flycatcher is a small (12–13 g) Palearctic migrant passerine bird (Lundberg and Alatalo, 1992). Pied flycatchers were trapped at nest-boxes in woodland near Oslo, Norway, in May 2001 and May 2002. The birds were kept indoors at 20 C– 22 C in individual holding cages (23 3 40 3 35 cm) with a lighting regime of 18-h light/6-h dark. The birds were fed ad lib on mealworms, Tenebrio molitor; were provided with bathing water; and could see other male and female pied flycatchers. The data reported were collected after the birds had been in captivity for 2–3 weeks. The birds were released close to the sites at which they were captured after our experiments. The birds were caught under license from the Norwegian Directorate of Nature Management, and all experimental procedures were approved by the National Animal Research Authority of Norway. We tested 43 male pied flycatchers for willingness to sing in the respirometry chamber (ABS plastic, 17 cm long 3 12 cm high 3 15 cm wide; Briticent). Two birds were tested in both years of the study. One of these individuals sang inside the chamber in the second year. Only three of the birds sang inside the chamber. These birds did not differ in mass, wing length, tarsus length, or plumage color (Drost, 1936; Svensson, 1992) from the birds that did not sing (Mann-Whitney U tests, p ..2 in all cases). The chamber contained a wooden perch (1 cm diameter) 3 cm from the floor, upon which birds generally stood. The upper 9 cm of the chamber was translucent apart from a ‘‘window’’ at one end through which the bird inside the chamber could see a female flycatcher when we used this stimulus to encourage the bird inside the chamber to sing (see below). Mealworms were placed in the chamber for the bird to eat. The birds were in the chamber for 30–120 min for experiments during the day, and 7 h during overnight

measurements of BMR. The birds were weighed (to 0.5 g, 50g Pesola balance) before and after being placed in the chamber. The mean mass was taken to be the mass of the bird during each experiment. We encouraged the birds to sing inside the respirometry chamber by carrying out experiments at the time of day that pied flycatchers sing most intensely in the field (0600–1300 h). During the first year of the study (N ¼ 23 birds), we played pied flycatcher song (Sony CFM 140 II cassette player) or placed a female pied flycatcher in a cage outside the window in the respirometry chamber for durations of 2–10 min at 10- to 30min intervals on up to five occasions during each experiment if the bird inside the respirometry chamber had not sung during previous trials. In the second year of the study (N ¼ 22 birds), we performed our experiments in a room in which other pied flycatchers were housed so that the bird in the chamber could hear conspecifics singing. These birds continued to sing during the experiments. If the bird inside the chamber had not sung during previous trials, we placed a female pied flycatcher in a cage outside the window in the respirometry chamber for durations of 2–10 min at 10- to 30-min intervals on up to five occasions during each experiment. Respirometry We measured the rate of oxygen consumption of the pied flycatchers by open circuit respirometry. Gases were pumped through the chamber that contained the bird at 760–800 ml/ min STPD (Charles Austen pump, model DA1SE). Any changes in flow rate during experiments (which were always less than 0.5%) were included in the calculations. The gases from the chamber were dried (silica gel) before measurement of flow rate with a variable area flowmeter (Cole Parmer 150 mm correlated, maximum flow rate 2.3 l/min). The flowmeter was calibrated for the experimental temperature and pressure conditions by using a spirometer ( Jaeger Spiro Junior, accurate to 60.4%) to measure the amplitude of gas passed through the flowmeter in a given time. Repeat calibrations of the flowmeter against the spirometer showed that flowmeter accuracy was 61.5% at the flow rates used during our experiments. The oxygen content of a subsample (100 ml/min) of the gases from the chamber was measured with an oxygen analyser (Servomex 1100A). We used a custom made interface box connected to an analogue to digital conversion card and a computer running a customized program written for LabView to sample the analogue output from the oxygen analyser at 100 Hz. These data were averaged every second, and the mean value was stored every 5 s. Data from the oxygen analyser were collected for 15 min before and after each bird was placed in the chamber so that any drift in analyser response to ambient air during experiments could be taken into account. The span of the oxygen analyser was set by using ambient air at the start of each experiment. The zero point of the oxygen analyser was checked every 3–4 d using nitrogen gas (AGA). We calculated metabolic rate (W) from the reduction in oxygen content of the air leaving the chamber attributable to the presence of the bird multiplied by the air flow rate through the chamber (corrected to STPD) using an oxycalorific value 20.92 J ml1 O2 (Koteja, 1996; Speakman, 2000). To assess the washout characteristics of the chamber, we used nitrogen gas to reduce the oxygen content of the gases in the chamber to a level similar to that during experiments with the flycatchers. We then pumped ambient air through the chamber at flow rates within the range used during the experiments with the birds. These tests showed that the oxygen content of the gases leaving the chamber returned exponentially toward the level in ambient air. Ninety-five percent of the gas in the chamber was replaced in 6.5–6.8 min, depending on


singing was not energetically costly in these species (Franz and Goller, 2003; Oberweger and Goller, 2001; Ward et al., 2003). However, data from canaries and zebra finches may not be representative of the energetic cost of singing by wild birds because sexually selected displays may become less costly in domesticated breeds when reproductive success is determined mainly by artificial selection. The magnitude of the energetic cost of singing is controversial partly because Eberhardt’s (1994) pioneering study had technical problems that may have influenced the results and the conclusions drawn from them (Gaunt et al., 1996; Thomas, 2002; Ward et al., 2003). The present study overcomes these problems. Pied flycatchers are an interesting species in which to study the energetic cost of singing because song is important in mate choice (Alatalo et al., 1990; Gottlander, 1987; Lampe and Espmark, 2003; Lampe and Sætre, 1995). Thus, if male song has become energetically costly through sexual selection, we would expect to find evidence for this in pied flycatchers. We measured the rate of oxygen consumption of male pied flycatchers singing inside a respirometry chamber. Previous experience showed that some male pied flycatchers sing in captivity during the part of the breeding season when freeliving birds are pairing. Our data allow us to assess whether the relatively low energetic costs of singing by canaries, zebra finches, and starlings or the higher energetic cost of singing by Carolina wrens are likely to be representative of free-living passerine birds. We also calculate how much the energetic cost of singing would contribute to the daily energy expenditure (DEE) of a free-living pied flycatcher in order to place the energetic cost of the display in the context of the overall energy budget.

Ward et al.

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The energy cost of bird song

Bird behavior We recorded bird behavior during experiments with a video camera (Sony TR417E) linked to a video recorder. We recorded when the birds ate, and we categorized bird behavior as the following: sitting (on the perch with the legs and feet covered by the body feathers and the body in a relatively horizontal posture, with the eyes closed for part of the time), standing (on the perch with the tarsi exposed and the body held relatively vertically and the eyes open), or singing (during which birds stood between songs). The birds sometimes moved during bouts of standing or singing. Movement rate was calculated from the number of times that birds moved their feet (i.e., to hop between the perch and the chamber floor or to rotate by 180 upon the perch) divided by activity duration. We calculated song rate from the number of songs divided by the length of time between the start of the first song and the end of the final song in a bout of singing. Only data from bouts of behavior that were longer than the equilibration time of the chamber were included in analyses. Song amplitude We recorded pied flycatcher song inside the respirometry chamber on VHS video tape from the video camera microphone (Sony TR417E). The microphone did not have automatic gain control. We used the same equipment, placed at the same distance from the bird, to record song from one of the birds (bird 2) that sang inside the chamber when he was in a holding cage. The physical characteristics of respirometry chambers can alter the amplitude of recordings of the song of birds singing inside them (Ward et al., 2003). We therefore used the same equipment, placed in the same positions as during experiments with the birds, to record playback of pied flycatcher song (Sony TC-D5M cassette player, Creative SBS 15 speaker) from inside the respirometry chamber and in the holding cage. These songs were recorded in the field by using a Sony TC-D5M cassette recorder and a Telinga Pro II parabolic

microphone. We calculated the average amplitude of recordings of individual songs from the spectrogram window of Canary 1.2.4 software (Cornell Laboratory of Ornithology). Our amplitude data were not quantitative because we did not use a calibrated microphone to make the recordings. However, all the recordings were made with the same equipment when the source of the sound was the same distance from the microphone, allowing us to test for differences in amplitude between recordings. Preliminary analyses showed that the recordings of song from inside the chamber were quieter than those from the cage. This could have been because the sound was attenuated when it passed through the chamber walls, the bird sang more quietly when inside the chamber, or a combination of these reasons. To separate these potential causes, we compared the difference in amplitude between recordings of the bird singing inside the chamber and in the cage with the difference in amplitude between recordings of playback of song from the chamber and the cage. We used randomly selected examples of songs of the same type that were sung by the bird or played from the speaker in both the chamber and the cage. Song types differed between the bird and those played from the speaker and also differed among birds. To assess whether song amplitude inside the respirometry chamber varied among the three birds, we compared the amplitude of recordings of 25 randomly selected songs that each bird sang inside the chamber. Statistical analyses We used Kolmogorov-Smirnov normality tests to assess whether data sets were normally distributed before analysis with parametric statistics. Data sets that were not normally distributed were analyzed with nonparametric statistics. We used linear regression to assess whether metabolic rate increased with song rate or the rate at which birds moved inside the respirometry chamber. We used one-way ANOVA with bird as the factor to assess whether song amplitude inside the respirometry chamber differed between birds. We used Wilcoxon matched-pairs signed-rank tests to compare the amplitude of recordings of songs of the same type from inside the respirometry chamber with those from the holding cage. We used Mann-Whitney U tests to compare the difference in recordings of song amplitude between the respirometry chamber and the holding cage for a bird and the speaker, and to compare the metabolic rate of individual birds between different activities. The overall significance of tests across birds was assessed by using unweighted Z tests following the method of Rosenthal (1991). We used the 95% confidence interval of the difference between metabolic rate during singing and standing to calculate the difference in metabolism between these activities that we would have been able to detect given the variability of our data and our sample sizes (Colegrave and Ruxton, 2003). Our results apply, strictly, only to the three birds that we studied, because they were not a random sample of pied flycatchers. However, we believe that data from these birds were likely to be representative because their behavior appeared to be more normal than that of the birds that did not sing inside the respirometry chamber. Statistical analyses were performed by using Minitab 12.22 (Minitab Inc) following the methods of Zar (1996). All statistical tests were two tailed with values presented as mean 6 SD. RESULTS Metabolic rate Only one bird (bird 2) both sang and stood without moving for longer than the equilibration time of the chamber. The


the flow rate. We subsequently refer to this interval as the equilibration time of the chamber. We assumed that the oxygen content of the air leaving the chamber during experiments with the pied flycatchers would be representative of the metabolic rate of a bird performing a particular activity after that activity had been performed consistently for a period that was longer than the equilibration time of the chamber. We calculated the mean metabolic rate for each bout of activity that was performed consistently for longer than the equilibration time of the chamber from the mean oxygen content of the gases leaving the chamber between the end of the equilibration time of the chamber and the end of the activity. We calculated the rate of oxygen consumption in this way, rather than by using the instantaneous correction of Bartholemew et al. (1981), because such calculations can lead to inaccurate results (Frappell et al., 1989; Gaunt et al., 1996; Ortigues et al., 1997). There was a 20-s delay between gases leaving the chamber and reaching the oxygen analyser which we took into account when we matched data on the rate of oxygen consumption with bird activity. We measured BMR at night at 30 6 0.1 C (within the thermoneutral zone for a bird of this size; Calder and King, 1974). We controlled the air temperature inside the respirometry chamber by using a custom-made thermistor connected to a fan heater that periodically blew hot air into an insulated box that contained the respirometry chamber. We monitored air temperature inside the respirometry chamber using a Big Digit thermistor (Acu-rite). We calculated BMR from the minimum mean metabolic rate over 5 min.

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— 0.83 — — 1.11 1.12 6 0.04 (3) — 0.2 — — 1.5 6 0.8 (14) 2.3 6 1.3 (3) 0.21 0.39 6 0.01 (7) 0.49 6 0.06 (9) — — — 0.57 6 0.11 (13) 0.55 6 0.06 (14) 12.6 6 0.6 (3) 0.23 6 0.02(3) 0.39 6 0.04 (3) 0.60 6 0.04 (3) 0.62 6 0.11 (3)

11.9 6 04 (5)

13.0 6 0.6 (9)

13.0 6 0.1 (7)

Bird 2 Not moving Moving Bird 35 Not moving Moving Bird 899 Not moving Moving Mean

Data are presented as mean 6 SD with the sample size in brackets. The metabolic rate during singing is shown as multiples of basal metabolic rate (sing 3 BMR) and as multiples of metabolism during sitting (sing 3 sit). Mean values across singing or standing birds were calculated from the average values from individual birds during bouts in which the birds moved. Bouts of sitting, standing and singing lasted 13.4 6 1.9 min, 12.3 6 4.4 min, and 11.0 6 1.9 min, respectively (means of mean values for each of the three birds). The data on individual bird mass show the mean values across the days upon which we collected respirometry data. We calculated the minimum detectable factorial increase in metabolism between standing and singing from the upper boundary of the 95% confidence interval of the difference in metabolism between these activities.

— — 2.6 1.4 2.7 6 0.5 (3) 1.6 6 0.2 (3)

— 1.7 — 2.3 — 0.75 — 0.58 6 0.05 (8) 0.35 6 0.04 (8) — — 0.59 6 0.05 (3) 0.25 —

— 1.6 6 1.0 (8)

0.64 6 0.10 (22) 0.74 6 0.08 (15) 0.43 6 0.03 (3) 0.64 6 0.05 (3) — 0.64 6 0.04 (2) 0.23 —

Mass Bird

Stand

Sing Sit BMR

Song rate (songs/min)

3.4 6 1.6 (22) 3.8 6 2.0 (15)

p

0.83 0.07

— 1.17

1.19 1.15

— 0.25

2.8 3.3 0.13 1.52

1.5 1.7

Sing 3 BMR Z Minimum detectable factorial increase Metabolic rate (W)

Mann-Whitney U test, stand vs. sing

metabolic rate of this bird did not differ between singing without moving and standing without moving (Table 1). All three birds performed bouts of both singing and standing during which they moved. The rate of movement did not differ between singing and standing (4.4 6 4.0 moves/min during singing, 4.9 6 1.4 moves/min during standing; Mann-Whitney U tests, p . .08 in all cases for individual birds, sample sizes in Table 1; Z test, overall Z ¼ 1.02, p ¼ .15, N ¼ 3 birds). Metabolic rate did not differ between the bouts of singing and standing during which the birds moved (Mann-Whitney U tests, p . .07 in all cases for individual birds, sample sizes in Table 1; Z test, overall Z ¼ 0.29, p ¼ .29, N ¼ 3 birds) (Table 1). The upper limit to the 95% confidence interval of the difference between the metabolism of singing and standing birds was equivalent to a 1.12 6 0.04-fold increase in metabolism during bouts of singing over that during standing (Table 1). Because metabolic rate during singing was not significantly greater than that during standing, song production caused a factorial increase in pied flycatcher metabolism of less than 1.12 6 0.04. The mean metabolic rate during singing when the birds also moved was 0.62 6 0.11 W (N ¼ 3 birds), which was equivalent to 2.7 6 0.5 3 BMR (Table 1). The mean metabolic rate during sitting was 0.40 6 0.04 W (N ¼ 3 birds) (Table 1). Thus, metabolic rate during bouts of singing when the birds also moved was 1.6 6 0.2 (N ¼ 3 birds) times greater that of sitting birds (Mann-Whitney U tests, p , .01 in all cases, sample sizes in Table 1). The metabolic rate of the bird that sang without moving (bird 2) was 1.5 times greater than during sitting (Mann-Whitney U test, W ¼ 317, p ¼ .009, sample sizes in Table 1). Metabolic rate did not increase with song rate either for the bird that did not move during song bouts (regression, r2 ¼ .04, p ¼ .3, N ¼ 25) or during bouts of singing during which birds moved (regression: bird 2, song rate, p ¼ .9, movement rate, p ¼ .4, r2 ¼ .07, N ¼ 19; bird 35, song rate, p ¼ .7, movement rate, p ¼ .9, r2 ¼ .02, N ¼ 18; bird 899, metabolic rate decreased with increasing song rate, p ¼ .02, and increased with movement rate, p , .001, r2 ¼ .43, N ¼ 27) (Figure 1). We collected data from one bird (bird 899) that sang inside the respirometry chamber during and after a visual contact with a female, and from the other two birds when they could hear other pied flycatchers singing in the same room. We do not have sufficient data to test whether metabolic rate during singing inside the respirometry chamber varies with the stimulus used to encourage singing, but this seems unlikely because the metabolism of bird 899 (the bird that sang after seeing a female, metabolic rate during singing, 2.6 3 BMR) was intermediate between that of birds 2 and 35 (the birds that sang when they could hear conspecifics singing, 3.3 and 2.3 3 BMR, respectively). The length of time between when birds last ate a mealworm and the midpoint of bouts of singing and standing did not differ significantly between activities (t tests, p . .3 in all cases; Z test, overall Z ¼ 0.46, p ¼ .3, N ¼ 3 birds, mean duration 856 6 110 s for singing and 937 6 115 s for standing). Song amplitude The reduction in amplitude of recordings of the song of bird 2 made when the bird was inside the respirometry chamber compared with those made when the bird was in the holding cage did not differ from the reduction in amplitude of playback of song from inside the respirometry chamber rather than in the holding cage (Mann-Whitney U test, W ¼ 48.5, p ¼ .15, N ¼ 6, median reduction in amplitude of recordings of the bird: 13.1 dB, interquartile range ¼ 12.6–15.4 dB, median reduction in amplitude of recordings of the playback: 11.9 dB, interquartile range ¼ 11.2–13.4 dB). The reduction in the


Table 1 The metabolic rate of 3 male pied flycatchers at night in the thermoneutral zone (BMR) and while sitting, standing and singing during the day

Sing 3 sit

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amplitude of recordings of the song of bird 2 from inside the chamber was therefore owing to sound attenuation by the chamber walls rather than because the bird sang significantly more quietly when inside the chamber. The amplitude of recordings of song from inside the respirometry chamber varied between the three birds (ANOVA F74,2 ¼ 58.7, p , .001). Tukey post-hoc tests showed that bird 899 sang more loudly than did the other two birds (differences between bird 899 and the other two birds, p , .001; no difference between bird 2 and bird 35, p ¼ .13). All the birds from which we report data therefore sang at least as loudly inside the respirometry chamber as bird 2 sang in the holding cage. DISCUSSION

Figure 1 The metabolic rate of three male pied flycatchers in relation to song rate. The different symbols show data from different birds (triangles indicate bird 2; circles, bird 35; and crosses, bird 899). Sample sizes are given in Table 1.

singing inside the respirometry chamber, their behavior differed from that of the birds that did not sing inside the chamber mainly in that birds that sang behaved more normally than those that did not. The stimuli used to encourage the birds to sing inside the respirometry chamber (hearing consecific song or seeing a female bird) are the same as those to which free-living birds would be exposed. The level of arousal of the birds that sang inside the respirometry chamber may therefore have been similar to that of free-living singing birds. Free-living pied flycatchers eat at frequent intervals (H.M. Lampe, personal observations), as did the birds that sang inside the chamber. Thus, the increase in metabolic rate associated with digestion of food is likely to make a similar contribution to the metabolism of free-living birds that sing during the day and as to those inside the respirometry chamber. Song amplitude did not differ between the respirometry chamber and a holding cage. Peak song rates were the same as those typical of free-living birds singing under favorable conditions (seven songs per minute; Gottlander, 1987; Lundberg and Alatalo, 1992), although average song rates were lower inside the respirometry chamber (Figure 1). The metabolic cost of song production increased with song duration in the Carolina wren (Eberhardt, 1994), zebra finch (Franz and Goller, 2003; Oberweger and Goller, 2002), and fife fancy canary (Ward et al., 2003), so the energetic cost of singing may be somewhat greater in free living pied flycatchers than for those that sang inside the respirometry chamber. However, lack of a relationship between metabolic rate and song rate, despite a seven-fold to 14-fold variation in song rate (Figure 1), suggests that metabolic rate does not increase steeply with song rate in pied flycatchers. To assess how much singing might contribute to the daily energy budget of a free-living pied flycatcher, we compared the energetic cost of singing inside the respirometry chamber with the DEE of free-living birds measured with doubly labeled water. We are not aware of any data on the DEE of free-living pied flycatchers during the period that the males sing to attract mates. However, Sætre et al. (1997) have measured the DEE of male pied flycatchers during the nestling rearing period in the study area from which we captured our birds. The DEE of male


The metabolic rate of singing pied flycatchers did not differ significantly from that during standing. Statistical tests on our data had sufficient power to detect a factorial increase of 1.12 6 0.04 between the metabolic rate of standing and singing birds, so we concluded that song production increased the metabolism of pied flycatchers by less than a factor of 1.12. The lack of variation found in the metabolic rate of pied flycatchers across a sevenfold to14-fold variation in song rate (Figure 1) also supports our conclusion that song production is not energetically costly in this species in relation to other sources of variation in metabolism. Metabolism during singing was 1.6 6 0.2 times greater than that during sitting and 2.7 6 0.5 3 BMR. These differences were mainly for reasons other than song production. Measurements of BMR were made in the thermoneutral zone (30 C) when digestion of food would have made a minimal contribution to metabolism, whereas the metabolic rate of singing birds was measured at lower temperatures (20 C–22 C) when the birds would have been digesting food. We also measured BMR at night while the pied flycatchers sang during the day. Increased thermoregulatory costs, the contribution of digestion to metabolism, the higher level of basal metabolism, and greater alertness during the day (Calder and King, 1974; Ricklefs, 1974) account for most of the difference between BMR and the metabolic rate of singing birds. Free-living birds would not be able to reduce their metabolic rate to BMR instead of singing during the day, but they could potentially reduce their metabolism to the level during sitting by altering their posture and reducing their level of alertness. The metabolic rates of singing and sitting birds were both measured at the same range in air temperature and similar stage in the daily cycle of metabolism. Sitting birds often closed their eyes, fluffed out their contour feathers, and covered their legs with their breast feathers, which would have decreased their thermoregulatory costs (Hill et al., 1980; Ward et al., 1999) and hence their metabolic rate, compared with levels for standing or singing birds. However, reduced alertness during sitting would be a disadvantage to free-living birds because it would lead to lower ability to detect food, predators, females, or rival males. Free-living pied flycatchers do not normally use this behavior during the day (H.M. Lampe, personal observations). Singing by pied flycatchers is thus energetically cheap if the alternative activity is standing but substantially more costly if singing were to replace sitting. This result confirms the data of Thomas (2002), which show that the rate of overnight mass loss increases with the duration of nocturnal song by nightingales when singing presumably replaces sleeping. Singing during the dawn chorus could also increase metabolism more than does song during the day if singing replaced sitting. The energetic cost of pied flycatcher song inside the respirometry chamber during our experiments was likely to be representative of song under more normal circumstances. Although we were only able to collect data from three birds


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Table 2 Metabolic rate during singing by passerine birds Day Species

3BMR Night

Carolina wren European starling Zebra finch Wasserslager canary Fife fancy canary Roller canary Pied flycatcher Mean Mean

3.9 2.1 2.0 2.6 2.5 2.1 2.7 2.6 2.3

6 6 6 6 6 6 6 6 6

1.4 0.2 0.4 1.0 0.7 0.1 0.3 0.8 (5) 0.3 (4)

3 Sit

3Stand

— — — — 1.4 1.4 1.6 1.5 1.5

3.6 1.1 1.3 1.0 1.07 1.05 ,1.12 1.6 1.1

6 6 6 6 6

0.2 0.1 0.2 0.1 (2) 0.1 (2)

6 6 6 6 6 6 6 6 6

1.1 0.04 0.2 0.02 0.10 0.07 0.04 1.1 (5) 0.1 (4)

n

Study

4 3 4 4 8 6 3 — —

Eberhardt, 1994 Oberweger and Goller, 2001 Oberweger and Goller, 2001 Oberweger and Goller, 2001 Ward et al., 2003 Ward et al., 2003 this study all species excluding Carolina wren

Metabolic rate during singing is shown as a multiples of basal metabolic rate (3 BMR), metabolic rate during sitting (3 sit), and metabolic rate during standing (3 stand). Metabolic rate is dimensionless when presented in this way. The data are presented as mean 6 SD. Mean values across species are calculated by using average data across the three studies of canaries. The maximum factorial increase in pied flycatcher metabolism over that of standing birds was included in the calculation of the mean value across species.

likely to be representative of most passerine birds because the energetic cost of singing has not been found to vary with song structure or complexity (Oberweger and Goller, 2002; Ward et al., 2003). Whether such an energetic cost represents a fitness cost to a singing bird will depend on the circumstances, because the marginal cost of a given activity depends on how much energy is available to an individual as well as on the energetic cost of the activity (Verhulst and Wiersma, 1997; Ward et al., 2003). Although song production has a modest energetic cost, it could still act as a condition-dependent signal of the quality of the singer because birds cannot sing and eat simultaneously. Poorer-quality birds (or those that possess territories where foraging success is lower) will be closer to energy imbalance and will be able to spend less time singing than will high-quality birds. This is consistent with the observation that male pied flycatchers with brown plumage stop singing during cold weather, whereas those with black plumage do not (Ilyina and Ivankina, 2001) because blacker male pied flycatchers are generally older higher-quality individuals (Dale et al., 2002; Lundberg and Alatalo, 1992). Field observations that song rate decreases during cold weather and increases when the food supply is experimentally increased (Alatalo et al., 1990; Gottlander, 1987; Lambrechts, 1996) are more likely to be the result of time constraint than of energetic cost of singing (Thomas et al., 2003). It is more important for birds that are close to energy imbalance to spend time foraging rather than singing, even if song production has a low energetic cost. Song is important in mate choice by female pied flycatchers. Male pied flycatcher song attracts females (Eriksson and Wallin, 1986). Females prefer males with more complex song (Lampe and Espmark, 2003; Lampe and Sætre, 1995) and higher song rates (Alatalo et al., 1990; Gottlander, 1987). Higher-quality males have larger song repertoires and greater versatility (Lampe and Espmark, 1994). Our data show that female preference for males with higher song rates is not linked directly to production of an honest display through a substantial energetic cost for song production. However, the energy requirement for sound production is not the only cost that might be associated with bird song. Singing could increase predation risk if song attracts predators as well as mates (Andersson, 1994; Go¨tmark, 1997; Slagsvold et al., 1995), although predation risk may be low for singing birds that have a good view of the surroundings and will therefore be able to detect approaching predators (Krams, 2001). Song repertoire size is often also related to the size of specialized areas of the brain (De Voogd et al., 1993) that could be costly to develop or


birds feeding broods of five to six chicks was 66.25 6 6.44 kJ/day (Sætre et al., 1997). If singing increased the metabolic rate of pied flycatchers to 1.12 times that during standing (i.e., 1.12 3 0.60 W, the maximum cost of singing compatible with our data) (Table 1), each hour of singing rather than standing would require an additional 0.26 kJ. If the DEE of male pied flycatchers during the period that they sing to attract mates is similar to that during nestling rearing, each hour of singing rather than standing would increase DEE by 0.4%. Pied flycatchers sing most frequently from 0600–1300 h, although individual birds do not sing for the entire period (H.M. Lampe, personal observations). A bird that sang rather than stood for 7 h would increase DEE by 2.7%. Such a change in metabolism is smaller than the variation in DEE between males during nestling-rearing measured by Sætre et al. (1997) and represents a cost that is unlikely to be important in relation to the daily energy budget under most circumstances. This conclusion is not sensitive to potential errors in estimates of either the cost of song production or the DEE of free-living male birds. If the cost of song production was 10% greater and DEE was 10% lower than the estimates used in the calculation above, each hour spent singing rather than standing would only increase DEE by 0.5%. The factorial increase in metabolism during singing by pied flycatchers was similar to that of zebra finches, European starlings, and canaries (Table 2). These data suggest that singing is not more energetically costly in wild-caught birds than in strains of birds that have been subject to artificial selection during many generations in captivity. The greater factorial increase in metabolism of Carolina wrens than of the other species (Table 2) could be owing to differences in the cost of singing between wrens and other birds or greater accuracy in the experimental methods of subsequent studies (Gaunt et al., 1996; Oberweger and Goller, 2002; Thomas, 2002; Ward et al., 2003). Small movements, such as hopping between the perch and the floor of the respirometry chamber by our pied flycatchers, did not increase metabolic rate during song bouts to the level measured in Carolina wrens. The respirometry chambers in which the Carolina wrens sang were, however, much larger than the ones that we used (Eberhardt, 1994), so more extensive movements by the Carolina wrens might have contributed to their greater metabolic rate. Across the species from which data have been collected, singing inside respirometry chambers caused a modest increase in metabolic rate over that during standing (1.6 6 1.1fold, N ¼ 5 species, or 1.1 6 0.1-fold, N ¼ 4 species if data from the Carolina wren were excluded) (Table 2). This increase is

Ward et al.

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maintain (Gil and Gahr, 2001), although this does not seem to be the case in the pied flycatcher (data not shown). Time spent singing is not available for other activities, such as feeding. Birds that spend more time singing have less time for feeding and must therefore forage at higher rates in order to maintain energy balance. Spending time singing could therefore provide an honest signal of male foraging ability or territory quality, even though song production is not energetically costly. Alternatively, higher song rates may be attractive to female pied flycatchers because singing birds will be detected sooner (Parker, 1983) or because males that are already paired sing less (Stenmark et al., 1988).

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We are grateful to Arnfinn Aulie, Kjell Fugelli, and Øivind Tøien for technical advice and loan of equipment; to Murray Coutts for designing the interface box and writing the LabView program; to Ivar Asbjørn Bredesen for help looking after the birds; to Lucy Gilbert, Vincent Janik, and Nigel Mann for discussion of our work; and to the anonymous reviewers for constructive comments upon an earlier version of the manuscript. Our work was funded by the BBSRC.

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