Behavioral Ecology Advance Access published online on February 29, 2008
Behavioral Ecology, doi:10.1093/beheco/arm161
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Does ambient noise affect growth and begging call structure in nestling birds?
Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4J1
Address correspondence to M.L. Leonard. E-mail: mleonard{at}dal.ca.
Received 31 July 2007; revised 3 December 2007; accepted 16 December 2007.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Much of the research examining the effects of ambient noise on communication has focused on adult birds using acoustic signals in mate attraction and territory defense. Here, we examine the effects of noise exposure on young birds, which use acoustic signals to solicit food from parents. We found that nestling tree swallows (Tachycineta bicolor) exposed to playbacks of white noise, within natural amplitude levels, from days 3 to 15 posthatch had begging calls with higher minimum frequencies and narrower frequency ranges than control nestlings raised in nests without added noise. Differences in begging call structure also persisted in the absence of noise. Two days after the noise was removed, experimental nestlings produced calls that were narrower in frequency range and less complex than control nestlings. We found no difference in growth between experimental and control nestlings. Our results suggest that long-term noise exposure affects the structure of nestling begging calls. These effects persist in the absence of noise, suggesting that noise may affect how calls develop.
Key words: ambient noise, begging calls, call structure, nestling birds, parent–offspring communication.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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One of the main ways that environmental noise affects animals is to alter the structure and delivery of their vocal signals (Rabin and Greene 2002
; Brumm and Slabbekoorn 2005; Warren et al. 2006). Indeed, a wide range of animals respond to noise by altering their signals in ways that should reduce its masking effects. For example, many species increase the amplitude of their signals in response to increased noise levels (Brumm and Slabbekoorn 2005; Warren et al. 2006), whereas others shift the frequency of their calls away from the frequencies that predominate in the noise (Slabbekoorn and Peet 2003; Wood and Yezerinac 2006) or increase call rate and, therefore, call redundancy (Lengagne et al. 1999; Penna et al. 2005).
Research examining the effects of noise on signalers has focused almost exclusively on adult animals using acoustic signals in mate attraction and territory defense (Brumm and Slabbekoorn 2005; Patricelli and Blickley 2006). Noise may also affect young animals that use acoustic signals to solicit food from parents. Nestling tree swallows (Tachycineta bicolor), for instance, increase the amplitude of their begging calls in response to short-term (i.e., 1 h) noise exposure in the laboratory, and this adjustment appears to enhance parental discrimination of begging calls in noise (Leonard and Horn 2005). These results suggest that signaling by young animals, like their adult counterparts, may be affected by noise.
Although nestlings appear to respond adaptively to short-term noise exposure, it is not clear how they might be affected by ambient noise that persists over long periods of time. Understanding how acoustic signalers are affected by persistent noise is important because many animals, especially those in or near urban areas, are increasingly exposed to chronic noise (Rabin and Greene 2002; Slabbekoorn and Peet 2003; Warren et al. 2006; Wood and Yezerinac 2006).
Long-term noise exposure could affect nestling birds in several ways. First, like short-term exposure, noise might affect the structure of nestling begging calls. Changes in call structure may be the result of adaptive adjustments by the nestlings to reduce the masking effects of noise, or they may be the result of disruptions to normal call production stemming from interference from the noise. In any case, the changes may be temporary, occurring only in the presence of noise or they may persist in the absence of noise, if noise interferes with call development (Heaton and Brauth 1999; Patricelli and Blickley 2006; Watanabe et al. 2007).
Long-term noise exposure might also affect nestling growth. If call adjustments increase energy expenditure, as has been suggested (Cynx et al. 1998; Brumm 2004; Warren et al. 2006; Wood and Yezerinac 2006), then the response of nestlings to noise could affect growth (but see Chappell and Bachman 2002). Alternatively, in the absence of such call adjustments, noise might interfere with the ability of parents to hear nestling begging calls (Leonard and Horn 2005), which could affect feeding rates to the nest and ultimately growth.
The purpose of our study, therefore, was to determine how prolonged exposure to ambient noise affects nestling birds. Specifically, we exposed nestling tree swallows to noise over the nestling period and compared the growth patterns and begging calls of these birds with a control group reared without added noise.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Study site
This study was conducted in the Gaspereau Valley of Nova Scotia, Canada, between May and July 2005 (study sites described in Leonard and Horn 1996
) using a population of box-nesting tree swallows. Hatching dates were determined by checking nest-boxes daily around the anticipated hatching date.
Experimental design
At hatch, pairs of broods matched for study site, age, and brood size were randomly assigned to an experimental (i.e., noise) or a control (i.e., no added noise) treatment. When broods in each treatment were 3 days old (hatch day = day 1), we placed a pair of Sony 8n8 series earbud speakers in the nest material oriented upward on each side of the nest about midway between the back and front of each nest-box. In the experimental treatment, we attached the speakers to a Sony D-E351 compact disk (CD) player that was placed inside 2 plastic bags at the base of the pole holding the nest-box. In the control treatment, we placed 2 empty plastic bags at the base of the pole. We changed the CD batteries daily in the experimental treatment, and we mimicked these battery changes in the control treatment to control for disturbance. When the broods were 15 days old, the speakers and CD player were removed from the nests.
In the experimental treatment, we played white noise that was computer synthesized at a resolution of 16 bits and a sampling rate of 44 kHz using Audacity version 2.1 (Free Software Corporation, Boston, MA, 1991). The noise ranged from 0 to 22 kHz, which includes the frequency range of nestling calls (2–10 kHz) and was played at 65 dB SPL (reference level 20 µPa here and throughout), which is near the upper end of the amplitude range (41–67 dB SPL) of ambient noise measured in nest-boxes in the field (Leonard and Horn 2005). The white noise, in combination with natural background noise, produced a relatively constant in situ noise level, with spectrum levels varying within ±6 dB over the frequency range of nestling calls (Figure 1).
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Growth
To measure the effect of the noise on nestling growth, we weighed and measured nestlings every 2 days beginning on day 2 (n = 7 broods) or 3 (n = 31 broods) and continuing until day 14 or 15. We weighed nestlings to the nearest 0.1 g using an Ohaus compact electronic scale and measured the length of the flattened right wing chord to the nearest 0.01 mm using Sylvac Euro-cal Mark III electronic calipers. We took 3 measurements for each growth feature and used the average in the analyses.
We also determined overall feeding rates to experimental and control nests by videotaping inside nests (see below for methods) and counting the number of feeding trips during a 1-h filming period (for details, see Leonard and Horn 1996) when nestlings were 5, 10, and 15 days old. We did not distinguish between male and female adults, so feeding rates are for the 2 parents combined.
Begging calls
When experimental and control broods were 5 days old, we opened the hinged side of the nest-box and put a Plexiglas plate in the opening. We then suspended a Genexxa 33-3003 microphone 10 cm over the nest cup and attached the microphone to an Optura 300 digital video camera that was placed on a tripod facing the open side of the box. We covered the camera with a plastic bag and video and audio recorded visits by parents and begging by the brood for 1 h. The video camera digitally recorded sound at a sample rate of 44 kHz and sample size of 16 bits. Recording levels were set manually and kept equal across nests and calibrated by simultaneously recording and measuring the sound pressure level of a standard tone using a Radio Shack 33-2005 sound level meter (C-level weighting) before each recording. We repeated this procedure when broods were 10 and 15 days old (input levels on day 15 were reduced by 20 dB to avoid overloading, and then 20 dB was added to amplitude measurements for analysis).
To determine if differences in call structure between experimental and control broods persisted in the absence of noise and after long-term noise exposure, we recorded nestling begging calls 2 days after the noise had been removed, on day 17. To avoid premature fledging, we blocked the opening to the nest-box and quickly opened the hinged door and taped a Genexxa 33-3003 microphone to the inside of the nest-box. We attached the microphone to a Sony DM-100 digital audio tape recorder. We then removed the block from the opening and recorded the begging calls given during feeding visits by parents for 1 h. After the recording session, we removed the equipment from the nest-box. Recording levels were kept constant between recordings.
Call measurements
We analyzed call features from audio files of the first 5 parental feeding visits in each trial at each age. For days 5, 10, and 15, the audio files were first extracted from video clips using iMovie version 2.1.2 (Apple Computer Inc., Cupertino, CA, 1999–2002) on a Macintosh G4 computer. This step was not needed for day 17 nestlings because calls were recorded on digital audiotape. For all ages, we analyzed the audio files using Canary 1.2 software (Charif et al. 1995). We created a spectrogram (analysis bandwidth 699 Hz, display resolution 22 Hz x 3 ms) of the first 10 calls in each feeding visit that did not overlap in time with other calls. For each call, we measured 4 call features that have been shown to change with noise in various species (Brumm and Slabbekoorn 2005), including tree swallows (Leonard and Horn 2005). Specifically, we measured call length (milliseconds), call amplitude (decibels SPL, minus background amplitude), minimum frequency (kilohertz), maximum frequency (kilohertz, analyzed post hoc), and frequency range (maximum frequency minus minimum frequency, kilohertz). For all measurements, clipping level (the minimum sound level represented on the spectrograph) and input level were held constant, so that differences in call measurements would not be attributable to how calls were displayed.
Our analyses suggested that differences in call structure persisted after the noise was removed from the experimental nests (see below). We therefore conducted post hoc tests to determine if vocal complexity, which can be reduced when hearing is compromised (e.g., Dooling et al. 1987; Eda-Fujiwara et al. 1995; Zevin et al. 2004; Watanabe et al. 2007), differed between the experimental and the control nestlings at day 17. We measured call complexity as the number of elements (i.e., the number of down swept whistles; see examples in Figure 3 of the results) per call and the average number of frequency changes and breaks per element in each call (see Figure 3). We selected the last call from the fifth feeding visit that was at least 70 dB SPL for analyses. We selected the fifth visit because it was the latest feeding in each trial that could be measured for all trials (i.e., some trials had only 5 feeding visits), and we chose the last call to reduce the chance of overlap with other nestling calls. We used a criterion amplitude (i.e., 70 dB) because at this age, calls of reduced amplitude are often atypical in structure. These measurements were taken using Raven 1.2.1 software (Cornell Laboratory of Ornithology Bioacoustics Research Program 2003–2004), using a Hann 5-ms x 287-Hz analysis window and 21-Hz grid with 98% overlap.
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Statistical analyses
At every age, we averaged each growth measurement (mass and wing length) across nestlings in a brood, so that each nest contributed only 1 data point per variable per age to the analyses. We tested for treatment effects using a mixed model analysis of variance (ANOVA) on each measure, with treatment (noise or control) as a fixed effect, age as a continuous effect, the treatment by age interaction, and nest (nested within treatment) as a random variable. For mass, which increases curvilinearly with age (McCarty 2001
), we included a quadratic component, together with its interaction with treatment.
We also averaged call variables across nestlings in each brood, so that each nest contributed 1 data point per variable at each of the 3 ages. We tested for treatment effects using a mixed model ANOVA on each measure, with treatment (noise or control) as a fixed effect, age as a continuous effect, the treatment by age interaction, and nest (nested within treatment) as a random variable. Age has a strong effect on call structure (Leonard and Horn 2007). Here, we were interested in the effect of age on treatment, so we report only the results for its interaction with treatment (for information on the effects of age on call structure, see Leonard and Horn 2007). To test for treatment effects on call variables at day 17, we used 1-way ANOVAs.
Analyses were performed using JMP 6 (SAS Institute Inc. 2005). Data were normally distributed (Shapiro–Wilk tests, P > 0.10) except for call length, which was log transformed, to produce a normal distribution before analysis. Where 0.05 < P < 0.10, we report the minimum effect size the analysis could detect with a power of 0.80. All means are reported ± standard error. P values less than 0.05 are considered significant.
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RESULTS |
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Growth
Neither mass gain nor wing length differed significantly between experimental and control nests (mass: treatment effect F1,27 = 0.01, P = 0.93; mean mass over measurement period—experimental: 15.6 ± 0.23 g, control: 15.6 ± 0.20 g; wing length: treatment effect F1,29 = 1.62, P = 0.21; mean wing length over measurement period—experimental: 31.5 ± 0.78 mm, control: 32.8 ± 0.69 mm). This result was consistent across age for both variables (mass: treatment x age interaction, linear component F1,194 = 0.00, P = 0.99; quadratic component F1,194 = 0.11, P = 0.74; wing length: treatment x age interaction F1,27 = 0.27, P = 0.60).
Feeding rates did not differ significantly between experimental and control nests (treatment effect F1,32 = 1.74, P = 0.20; experimental: 7.0 ± 0.79 feeds per h, control: 8.5 ± 0.82 feeds per h), an effect that was consistent across age (treatment x age interaction F1,30 = 0.42, P = 0.52).
Begging calls
Neither call length nor amplitude differed significantly between experimental and control nests over the 3 ages (length: treatment effect F1,22 = 4.10, P = 0.06, detectable difference = 1.5 ms, treatment x age interaction F1,46 = 2.96, P = 0.09, detectable difference = 1.3 ms; amplitude: treatment effect F1,22 = 1.08, P = 0.31, treatment x age interaction F1,46 = 2.86, P = 0.10, detectable difference = 4.6 dB; Figure 2a,b).
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In contrast, minimum call frequency differed significantly between experimental and control nests (treatment effect F1,22 = 11.26, P = 0.0029; Figure 2c), with higher minimum frequencies in experimental than control nests. This difference, however, decreased with age (treatment x age interaction F1,46 = 13.03, P = 0.0008; Figure 2c). Frequency range also differed significantly between experimental and control nests (treatment effect F1,22 = 8.18, P = 0.009), with a narrower frequency range in the experimental treatment across all ages (treatment x age interaction F1,46 = 0.03, P = 0.86; Figure 2d). The persistence of a treatment effect on frequency range across age (Figure 2d) in the face of a declining difference between treatments in minimum frequency (Figure 2c) suggested that maximum frequency might also have differed between treatments. Maximum frequency did not show an overall treatment effect (F1,22 = 0.04, P = 0.84), but it did show a significant treatment x age interaction (F1,46 = 7.24, P = 0.01), with experimental nestlings giving calls with a lower maximum frequency than control nestlings as they aged.
The difference in frequency range between experimental and control nestlings was also evident at day 17 (treatment effect F1,29 = 6.45, P = 0.0167; experimental: 3.30 ± 0.077 kHz, control: 3.58 ± 0.075 kHz), despite the removal of the noise 2 days earlier. Otherwise, the calls of day 17 nestlings did not differ significantly between experimental and control nests (length: F1,29 = 0.10, P = 0.75; amplitude: F1,29 = 3.76, P = 0.06, detectable difference = 2.8 dB; minimum frequency: F1,29 = 0.69, P = 0.41; maximum frequency: F1,29 = 3.26, P = 0.08, detectable difference = 0.2 kHz).
Visual inspection of the spectrograms of the day 17 calls suggested that they were less complex in experimental broods than in control broods (Figure 3). Post hoc analyses showed that the number of elements per call did not differ significantly between treatments (experimental: 3.33 ± 0.17, control: 3.44 ± 0.17, F1,29 = 0.18, P = 0.67), but the total number of frequency changes and breaks per element did differ significantly (F1,29 = 4.58, P = 0.041). Experimental nestlings showed nearly half as many frequency changes and breaks as control nestlings (experimental: 0.24 ± 0.07, control: 0.46 ± 0.07).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Our results showed that playback of noise through the nestling period affected the structure of tree swallow begging calls. Specifically, nestlings in the noise treatment had calls with a higher minimum frequency and a narrower frequency range than control nestlings. Differences in call structure between treatments persisted for at least 2 days after the noise was removed, suggesting that noise might have long-lasting effects on call structure.
Growth
We found no evidence for an impact of noise on nestling growth. Sustained loud calling is expected to be energetically costly (Brumm 2004; Patricelli and Blickley 2006; Warren et al. 2006), so we had hypothesized that if nestlings adjusted their calls in response to noise, particularly by increasing call amplitude, we might see a concomitant decline in growth as energy was diverted to calling. Our results, in fact, showed no significant difference in mass gain or wing growth between the 2 treatments. One possible reason for this result is that the observed adjustments appeared to be mostly in the frequency components of the call, which could require increased energy (Lambrechts 1996), but possibly less than calling at high amplitudes. Alternatively, the energetic cost of begging in general appears to be low for several species, including tree swallows (Chappell and Bachman 2002), so changes to the call, regardless of form, may not affect energy consumption. Whatever the case, it appears that the levels of white noise presented here had little effect on nestling energy budgets.
Begging calls
We found that across the 3 ages, nestlings in the experimental treatment had calls with a narrower frequency range than nestlings in the control treatment. This effect was found initially because experimental nestlings had a higher minimum frequency; however, by the late nestling period, the effect was mostly due to a decrease in maximum frequency in the experimental group.
Producing calls with a narrow frequency range should improve signal transmission in noise (Patricelli and Blickley 2006; Warren et al. 2006). A narrow frequency range would concentrate more signal energy in the adjusted frequency band and improve the signal to noise ratio in that band (Lohr et al. 2003). Some frogs and birds living next to running water appear to use this strategy to overcome the noise of the water (Dubois and Martens 1984). Similarly, a number of species show narrower frequency ranges in noise, often because their calls have higher minimum frequencies than calls produced at lower noise levels (Patricelli and Blickley 2006). Maintaining calls at higher frequencies shifts them away from the frequencies predominating in many forms of ambient noise and, thus, reduces masking effects. Whereas the noise we presented to nestlings did not emphasize lower frequencies, much abiotic natural noise such as wind does (Bradbury and Vehrencamp 1998), so producing a higher frequency call might be adaptive under natural conditions. Given this, it is not clear why this effect did not persist over age.
Contrary to our current results, in an earlier correlational study (Leonard and Horn 2005), we found a positive relationship between the frequency range of nestling begging calls and the amplitude of ambient noise around the nest (Leonard and Horn 2005). Given that the present results are experimental while the previous results were correlational, we suspect that the latter results arose because frequency range was correlated to an intervening variable and not ambient noise. A less parsimonious, albeit more interesting, possibility is that the response of the nestlings varies with the quality of ambient noise, which differed between the 2 studies. In the earlier study, noise was generated by wind, traffic, water, and other birds, whereas in the current study, the main source was synthesized white noise.
The results of the current study on prolonged noise exposure differed from those of our previous laboratory study (Leonard and Horn 2005) that showed a strong increase in call amplitude in relation to short-term noise exposure. This difference is probably not due to differences in the experimental protocol between the studies because the amplitude effect appeared to hold under short-term noise exposure in the field (Leonard ML, Horn AG, unpublished data). It does, however, raise the interesting possibility that nestlings may use different strategies for dealing with noise on the long and short term.
Finally, we have assumed to this point that the changes in call structure observed in the noise treatment were adaptive and functioned to improve call transmission in noise. It is possible, however, that increased noise might simply disrupt normal call production, yielding calls with abnormal frequency structures. Although the observed changes are predicted to improve signal transmission in noise (Lohr et al. 2003) and are consistent with responses shown by some acoustic signalers in the presence of noise (Patricelli and Blickley 2006; Warren et al. 2006), we cannot rule out the possibility that the changes are not adaptive.
Noise and call development
Our results also suggest that long-term noise exposure could have lasting effects on call structure that persist in the absence of noise. Two days after the noise had been removed, nestlings raised in noise had calls with narrower frequency ranges and less complexity (i.e., fewer frequency changes and breaks) than control nestlings. Although it is not clear whether these differences would persist over time, the result suggests that noise exposure could permanently affect call structure.
Studies on chickens and rats suggest that moderate levels of noise, like those used here, may delay auditory development, although their effect on vocalizations per se is unknown (Philbin et al. 1993; Chang and Merzenich 2003). Several studies on song development and retention in birds have found that exposure to relatively high noise levels (ca. 100 dB SPL) result in songs with abnormal sequences of syllables and syllables and calls with abnormal structure (Marler and Waser 1977; Woolley and Rubel 2002; Zevin et al. 2004). In these cases, however, the noise deafened birds either by directly damaging auditory receptor cells or by effectively masking sounds, including much of the bird's own acoustic output. The results of our study suggest that noise levels well below those described above and within the range of naturally occurring noise levels may also affect call development.
Changes to begging call structure could have implications for parent–offspring communication beyond the nestling stage. Swallow begging calls eventually develop into calls that are used during the fledgling period to maintain contact among family members (Beecher IM and Beecher MD 1983; Brown CR and Brown MB 1995; Leonard ML, Horn AG, unpublished data). If call stereotypy is set before fledging (Medvin et al. 1993; Leonard et al. 1997), then the effects of noise exposure during the nestling period might well persist into the fledgling period and affect interactions between siblings and parents. Whether these effects would be detrimental is not clear, given that they do not involve wholesale changes in call structure. Similarly, noise-induced changes to begging call structure might also have positive effects on later communication if calls are altered in ways that improve signal transmission in noise (Patricelli and Blickley 2006).
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FUNDING |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Natural Sciences and Engineering Research Council Discovery Grant (RGPIN/227150 to M.L.).
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ACKNOWLEDGEMENTS |
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We are grateful to Sarah Pannozzo and Nicole White for help in the field and the Coldwell, Hynes, and Minor families for allowing us to work on their land. We also thank 2 anonymous reviewers for their helpful comments on the paper.
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