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Dawn song of the eastern kingbird: an honest signal of male quality?
ANIMAL BEHAVIOUR, 2008, 75, 1075e1084 doi:10.1016/j.anbehav.2007.08.020
Available online at www.sciencedirect.com
Dawn song of the eastern kingbird: an honest signal of male quality? M ICH A EL T. MURPH Y , KA REN S EXTON , AM Y C . DOLAN & LUK E J. REDMO ND
Department of Biology, Portland State University (Received 9 March 2007; initial acceptance 16 May 2007; final acceptance 7 August 2007; published online 16 January 2008; MS. number: A10714R)
To be used as honest signals of quality, phenotypic traits must vary markedly within populations and show repeatable differences between individuals. Eastern kingbirds, Tyrannus tyrannus, sing a distinctive dawn song in the predawn darkness, and one hypothesis for its function is that it serves as an honest signal of male quality that females use during choice of within-pair or extrapair mates. Over a 2-year period, we quantified dawn songs of males to measure between- and within-season repeatability of the timing (start and end time) and length of song bouts, and song rate. We also measured morphological characters to measure repeatability and describe individual differences in body size and plumage quality. All song traits varied considerably among males, start time and song rates were repeatable between years, and all song rates were repeatable within both years. All morphological characters were significantly repeatable between years. Moreover, early singing males were larger and had relatively long flight feathers, and males that sang at high rates had relatively long flight feathers. Early singing males were also paired to the earliest breeding females, and in one year, male song rate was positively correlated with their social mate’s clutch size. Relatively long flight feathers in other species are typical of older males and individuals of higher body condition, suggesting that, despite being suboscine passerines with relatively simple and innate songs, eastern kingbirds use song performance as an honest signal of male quality that females may use during mate choice. Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Keywords: body size; dawn song; eastern kingbird; honest signalling; mate choice; plumage quality; repeatability; song rate; timing of song; Tyrannus tyrannus
A basic tenet of sexual selection theory is that body size and secondary sexual traits such as plumage, song and other displays are indicators of quality that are used during mate choice (Darwin 1871; Andersson 1994). Such signals serve as measures of quality because their production is costly and only high-quality individuals can presumably afford their expense (Zahavi & Zahavi 1997; Jennions et al. 2001). The ability to support costly signals may come as a product of good genes or body condition, and high-quality females (early breeding and fecund; Hipfner et al. 1999; Wolfenbarger 1999) are presumably attracted to either the high-quality males themselves, or the habitats that they acquire.
Correspondence: M. T. Murphy, Department of Biology, P.O. Box 751, Portland State University, Portland, OR 97207, U.S.A. (email: [email protected]). 0003e 3472/08/$32.00/0
Body size is a ‘static’ trait that is often viewed as an honest signal of quality because it integrates an individual’s ontogenetic history (Thessing & Ekman 1994; Ryan 2001; Searcy et al. 2004). Final size is attained within weeks to months of hatching in small birds (<100 g), and conditions during early development can have lifelong effects on size and morphology (e.g. Garnett 1981; Ryan 2001), but also on other phenotypic traits (Lind¨ m 1999; Nowicki et al. 2002). Plumage and behaviour stro generally represent ‘dynamic’ traits that may be more valuable than body size in providing information on individual quality during mate choice because their expression is likely to be dependent on recent history (plumage) or current conditions (behaviour). Displays are especially useful signals of quality because their expression is likely to be a product of the male’s immediate condition (e.g. Halupka & Borowiec 2006). Song production is energetically costly in some species of
1075 Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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ANIMAL BEHAVIOUR, 75, 3
birds (Eberhardt 1994; Thomas 2002; but see Oberweger & Goller 2001; Ward et al. 2004), especially if performed in place of resting activities (Ward et al. 2003), and is generally regarded as an important cue used by female birds to select mates (e.g. Hofstad et al. 2002; Nolan & Hill 2004; Poesel et al. 2006). Most efforts to relate song to mating success have focused on daytime singing, but song performance in the early dawn chorus may be of particular importance (Poesel et al. 2006), and measures of performance such as the timing of the start of dawn song, song rate, song bout length, or temporal variability of song output may be particularly informative signals that females use to assess male quality (e.g. Marchetti 1998; Christie et al. 2004; Nolan & Hill 2004). If song is an honest measure of male quality, we should find repeatable differences between males in song performance and positive associations between song output, body size and condition, and/or territory quality. Evidence for the latter associations exist (e.g. Enstrom et al. 1997; Møller et al. 1998; Balsby 2000; Poesel et al. 2001; Kipper et al. 2006), but very little information is available to evaluate whether song traits are repeatable (but see Lambrechts & Dhondt 1987; Poesel et al. 2001; Rios Chelen et al. 2005). Suboscines represent roughly 20% of species within the order Passeriformes (1151 species). Unlike oscine passerines, suboscines sing stereotypical songs for which no evidence of song learning exists (Kroodsma 1984; Kroodsma & Konishi 1991), and as a consequence, suboscine song has been relatively neglected compared to the song of oscines. However, recent work has shown that suboscine song structure may vary over large geographical scales (Sedgwick 2001), and that sufficient variability in song structure exists within populations to permit individual recognition of neighbours (Westcott 1997; Lovell & Lein 2004). Some suboscines have diverse and complex vocalizations (e.g. Smith & Smith 1996), and some show a capacity for combinatorial syntax (Leger 2005). Nevertheless, except for its use in species recognition (e.g. Johnson 1980), the role of song in mate choice in suboscines is essentially unexplored. Eastern kingbirds are suboscine, Neotropical migrants that defend territories and form socially monogamous pair bonds. They have a moderate diversity of vocalizations (Smith 1966; Smith & Smith 1992), including a distinctive dawn song produced nearly exclusively in the predawn darkness (Smith 1966; Sexton et al. 2007). As in several other temperate-zone breeding tyrannids (Conrad et al. 1998; Tarof et al. 2004; Woolfenden et al. 2005), extrapair paternity is common in kingbirds (60% of nests; Rowe et al. 2001; Dolan et al. 2007), and we found that the timing of the start of dawn song was the best predictor of male extrapair mating success (Dolan et al. 2007). Females presumably gain indirect genetic benefits for young through extrapair mating because they receive no direct benefits (e.g. male assistance). We therefore hypothesized that male kingbird song performance may serve as an indicator of male quality, one measure of which may be body size. Our goals in this study were therefore to (1) determine the repeatability of morphology and song performance of male eastern kingbirds and (2) measure the degree to which song performance and male body
size and plumage quality covary to test the hypothesis that song conveys honest information about male quality. Finally, we also tested the prediction that song influences within-pair mate choice such that high-quality females pair with males that show high song performance.
METHODS
Study Site and Population Our study was conducted during June and July of 2003 and 2004 at Malheur National Wildlife Refuge (MNWR), OR, U.S.A. (42.84 N, 118.95 W). MNWR is located at the northern end of the Great Basin Desert, and the permanent flow of the Donner und Blitzen River through the high desert habitat (1400 m above sea level) supports the refuge’s marshes and riparian habitats. Kingbirds build open-cup nests in trees, and the MNWR kingbird population nests nearly exclusively in the willow trees (Salix spp.) that line the river’s banks. Our study began in 2002, and the number of breeding pairs was 52 in 2003 and 59 in 2004.
Field Methods Surveys of the study site began by mid-May in all years, and regular nest checks (every 2e3 days) allowed us to closely track pairs to establish breeding date (day first egg was laid), clutch size and hatching and fledging success (Redmond et al. 2007). Adults were captured with mist nets (beginning in 2002) during the nestling period and individuals were fitted with a unique combination of three coloured rings and one aluminium U.S. Fish and Wildlife Service ring. Sex was determined by the presence of a brood patch (females) or cloacal protuberance (males), and by differences in the lengths of the 9th and 10th primary feathers (Pyle 1997). Morphological measurements taken at the time of capture included body mass (nearest 0.1 g; Pesola scale), unflattened wing chord (nearest 0.5 mm; stopped wing ruler) and tarsometatarsus (¼tarsus), bill (nearest 0.1 mm; dial callipers) and tail length (nearest 0.5 mm from uropygial gland to tip of longest rectrix; stopped wing ruler). Because adult return rate is relatively high (w65%), many individuals were already marked at the start of the 2003 (w50%) and 2004 (w60%) seasons. Most nests (107 of 135) were located before or during egg laying, and therefore, the exact stage of the nest cycle was known for 79% of pairs. Nest stage for other nests was determined by backdating from known events (e.g. hatching date). Failed nests are usually replaced with new nests built within 100 m of the failed attempt (M. T. Murphy, personal observation), and we located replacement nests and collected identical data. We have observed only one within-season divorce and change of territory following a nest failure among marked birds in 4 years at MNWR (1 of w90 pairs; M. T. Murphy, personal observation), and therefore, we assumed unmarked birds at replacement nests to be the original resident pair. Kingbirds are aerial-hawking insectivores that capture single prey in primarily horizontal flights from a perch
MURPHY ET AL.: KINGBIRD SONG
(Murphy 1987). As part of a separate but concurrent study, we recorded insect abundance in 2003 and 2004 (Redmond 2005). Abundance was based on 3-min counts of insects that flew between an observer (L.J.R.) and a 1-m2 white sheet placed 5 m from the observer and at the height of herbaceous vegetation (w1 m). Counts were taken at midday (between 1000 and 1400 hours) and weekly from early June to late July in both years (except on days of high winds or rain), and in both years, five replicate counts were made from five habitat types used by kingbirds at MNWR on each sampling date. Weather (air temperature, relative humidity and wind speed) were collected at the end of each 3-min count using a Kestrel 3500 hand-held weather meter.
Song Data Fertile females are present at MNWR from late May until mid-July because replacement of failed nests is common (Sexton et al. 2007). Presumably in response, males sing dawn songs throughout their social mate’s nest cycle (Sexton et al. 2007), and observations of dawn song were made almost daily from mid-June through the third week of July in both years. Forty individuals from 49 nests were observed in 2003 (88 observations), and 47 individuals were observed from 67 nests in 2004 (107 observations). The number of nests exceeded the number of pairs in 2004 because of high nest loss and replacement, and as a result, some males were observed at multiple nests and up to five times per season. The mean SD time between successive observations of the same male was 11 7.8 days (N ¼ 83, range 1e35), but was more often 5 (24.1%) or 6 (18.0%) days. Males failed to sing during 22 observation periods and these were omitted from analyses. This left 173 song bouts during which males were observed once (N ¼ 22), twice (N ¼ 22), three times (N ¼ 10), four times (N ¼ 10), or five or more times (N ¼ 6) over the 2-year period. Rings could not be used to identify males during observations because dawn song generally began an hour or more before sunrise (see below). However, preliminary work showed that males usually sang from perches located no more than 100 m from the nest (see also Mayer 1952; Smith 1966), and given that distances between nearest nests averaged 250 m (Redmond 2005), we assumed that a male singing within 100 m of the nest was the resident. Our assumption was confirmed in every case either when rings could be seen as light improved, or as we tracked the flight path of the bird to the nest at the end of dawn song. Depending on the number of observers, three to five birds were observed daily (one bird per observer). We arrived at the nest site before singing began (between 0315 and 0415 hours Pacific Standard Time, PST) and remained until the end of the bout. A song was defined as the ‘regular repeated vocalization’ (RRV) described by Smith (1966). Each song lasts 2e8 s depending on the number of repeated notes, but is separated from the next by a distinct final note and pause. Once begun, singing continued until the end of the song bout unless the male was
interrupted by another bird. The end was usually marked by a chatter-zeer vocalization (Smith & Smith 1992) and a flight over the territory. The start and end of the song bout were calculated to the nearest minute relative to sunrise (time for sunrise was obtained from official records for the weather station at Burns Airport located 40e60 km north of our site, depending on the nest): large negative values indicate an early start or end. Song bout length was the absolute difference between start and end time. We recorded the number of RRVs per min for the first 30 min of song to define song output in three ways. Thirty-minute song rate (30MSR) was calculated as the average number of RRVs per minute for the first 30 min, regardless of whether the bird sang for the entire time. Actual song rate (ASR) was the average number of RRVs per minute during the time the bird actually sang within the first 30 min, and peak song rate (PSR) was the average number of RRVs per minute for the 5-min period during which song rate was highest.
Statistical Analyses Comparisons of insect counts between years were made after first using multiple regression to control for seasonal growth of insect populations and variation in flight activity associated with weather (Redmond 2005). We calculated between-year repeatability (Lessels & Boag 1987) of morphology for males captured in multiple years, and to maximize sample size, we expanded our analyses to include individuals remeasured through 2007. We also calculated repeatability of song traits both between and within years for individual males with multiple observations of song bouts. Song repeatabilities were calculated after we first tested for and removed possible effects of calendar date, nest stage of the male’s social mate, fertility status of social mate and sociobiological factors that might affect song behaviour (e.g. density of pairs, number of fertile females within 600 m, and within the total population). We used best subsets regression analyses to identify the combination of variables (all P 0.05 based on type III sums of squares) that accounted for the maximum variation in each song variable. The analyses are described elsewhere (Sexton et al. 2007), but here we use the residuals from the latter regressions. Repeatabilities were also calculated for the raw data, and the results were qualitatively identical with only two exceptions that we describe below. We assumed that an early start to dawn song, high song rates and long song bouts were costly and characteristic of only high-quality males. We also assumed that highquality males were larger and had longer flight feathers, and thus tested for positive relationships between song performance and overall size and flight feather length. Of the 87 males for whom multiple observations of song behaviour existed, 40 were not used in these analyses either because morphological data were missing or a 2-year gap existed between measurement of morphology and song. Of the remainder, 15 were captured and measured in the year before their song was documented (either in 2002 or in 2003), while 32 were captured and measured in the same year that their song behaviour was quantified. Each male
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ANIMAL BEHAVIOUR, 75, 3
was used once and song behaviour was averaged over multiple song recording bouts to obtain a single measure of behaviour. In the interest of uniformity, songs from the first year were used for males recorded in both years. We used principal component analysis (PCA) of linear measures of size to describe variability in body size and shape. Stepwise regression analysis (type III sums of squares) was then used to test for associations between all six song traits and individual male morphological traits, PC1 and PC2 (see below), and year (2003 ¼ 1, 2004 ¼ 2). We separately analysed the 32 individuals for whom morphology and song behaviour were recorded in the same year, and included body mass as an additional predictor variable of song behaviour. Mass never entered the models as a significant predictor of song behaviour, and the results were qualitatively unchanged from the analyses of 47 birds. We therefore report only the latter results. Laying dates and clutch sizes of first nests of the season were compared to all six song characters using stepwise regression (as above) for males with at least two observations of song in the same year. Except for five cases where data for the first nest in the first year were incomplete, we used only the first year that a male was observed to avoid pseudoreplication. Laying date was significantly later in 2004 than in 2003 (M. T. Murphy, unpublished data) and therefore date was standardized to a mean of zero by subtracting the true mean from all dates for each year. Clutch size declines seasonally in kingbirds (Murphy 1996), and therefore, we compared residual clutch size (date effects removed using regression) to male traits. All analyses were performed using STATISTIX8 (Analytical Software, Tallahassee, FL, U.S.A.) or SPSS, version 10 (SPSS Inc., Chicago, IL, U.S.A.). We report standardized regression coefficients (b), means SDs and sample size (N ), and significance was accepted at P 0.05 unless otherwise stated. All reported correlation coefficients are Pearson’s r, and all t tests were two-sample t tests.
30 May Mean air temperature (C)
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June
July
25 20 15 10 5 0 10
20
30
40
50
60
70
80
90
Date (1 = 1 May) Figure 1. Seasonal variation in temperature at MNWR in 2003 (C) and 2004 (B) between mid-May and the end of July.
the first 30 min. Song rate during the actual song bout (ASR) was 15% higher, but PSR was nearly 50% higher than 30MSR (Table 1). Most males stopped singing about 30 min before dawn, and thus, song bout length averaged just over 30 min (Table 1). Start time was the least variable song trait (coefficients of variation, CV, in Table 1), but even start time was three to five times more variable than morphology (Table 1). Start time was significantly repeatable between years (Fig. 2a), but not when each year was examined separately (Table 2). On the other hand, repeatability for end time was not significant in between-year comparisons, but was significant in 2003 (Table 2), and ultimately, song bout length gave no indication of being repeatable. Seven of the nine possible repeatabilities of song rates (30MSR, ASR, PSR) were significant (at P 0.051), and of the two that were not (30MSR and ASR in 2003), both approached significance (P 0.10; Table 2). Moreover, both of the latter rates yielded significant repeatabilities (P 0.043)
RESULTS
Environmental Conditions: Annual Comparisons Kingbirds first arrive at MNWR between 10 and 15 May. Air temperatures between mid-May and the end of July were on average higher in 2003 (Fig. 1), and, after controlling for date of observation and meteorological conditions, flying insects were also more abundant in 2003 (8.4 4.82 insects/3 min, N ¼ 179) than in 2004 (5.9 4.17 insects/ 5 min, N ¼ 179; t356 ¼ 5.23, P < 0.001). Breeding began significantly earlier in 2003 (11 June 6.6 days, N ¼ 51) than in 2004 (19 June 6.2 days, N ¼ 43; t92 ¼ 5.85, P < 0.001), and females also produced larger initial clutches in 2003 (2003: 3.8 0.47 eggs, N ¼ 54; 2004: 3.4 0.85 eggs, N ¼ 42; t94 ¼ 3.09, P ¼ 0.003).
Repeatability of Song Traits Dawn song began roughly 1-h before sunrise, and males averaged roughly nine songs/min (30MSR; Table 1) during
Table 1. Summary statistics (CV ¼ coefficient of variation) describing morphological and song traits recorded from male eastern kingbirds in 2003 and 2004 at Malheur National Wildlife Refuge, OR, U.S.A. (N ¼ 87 and N ¼ 47 for song and morphological variables, respectively) Trait
MeanSD
Start time 63.89.2 (min before dawn) 30-min song rate 9.33.5 (30MSR; songs/min) Actual song rate 10.73.0 (ASR; songs/min) Peak song rate 13.63.5 (PSR; songs/min) End time 29.97.5 (min before dawn) Song bout length 33.810.6 (min) Bill length (mm) 14.740.74 Tail length (mm) 88.523.09 Tarsus length (mm) 20.230.98 Wing chord (mm) 121.72.8
Range
CV
84 to 37
14.46
1.2 to 16.1
37.72
3.2 to 17.9
28.06
5.6 to 20.8
26.13
52 to 11
25.13
7.0 to 55.7
31.23
13.20 to 16.70 82.0 to 97.0 17.60 to 23.30 115.0 to 128.0
5.04 3.49 4.86 2.29
MURPHY ET AL.: KINGBIRD SONG
−45
Start time 2004
−50
Morphological Analysis (a)
−55 −60 −65 −70 −75 −80 −85
−80
−75
−70 −65 −60 Start time 2003
−55
−50
−45
2 (b) Peak song rate 2004
1.5 1 0.5 0 −0.5 −1 −1.5 −1.5
−1
0 0.5 1 −0.5 Peak song rate 2003
1.5
2
Figure 2. A comparison of (a) unadjusted start time and (b) adjusted peak song rate (PSR) for 16 male kingbirds whose songs were documented in both 2003 and 2004.
when the analyses were based on uncorrected values. PSR was the most repeatable (0.376e0.460) of the three song rates (Fig. 2b), followed by ASR (0.194e0.374) and then 30MSR (0.179e0.226). The mean SD repeatability of start time and song rates based on between- and withinseason measures was 0.251 0.116 (N ¼ 12, 95% confidence interval ¼ 0.178e0.326).
Bill (r ¼ 0.751, F17,25 ¼ 8.23, P < 0.001) and tarsus (r ¼ 0.636, F17,25 ¼ 5.02, P ¼ 0.001) lengths both exhibited high individual repeatability. Repeatability of wing chord (r ¼ 0.482, F17,25 ¼ 3.23, P ¼ 0.004) and tail length (r ¼ 0.372, F17,25 ¼ 2.85, P ¼ 0.009) were not as high, but both were also significant (effective cell size ¼ 2.4 for all). Neither the nonplumage characters nor wing chord changed as the bird aged (bill length: F2,40 ¼ 1.40, P ¼ 0.258; tarsus length: F2,40 ¼ 0.01, P ¼ 0.996; wing chord: F2,40 ¼ 0.39, P ¼ 0.679), but tail length increased between the first (88.2 1.66 mm, N ¼ 18), second (90.0 1.47 mm, N ¼ 13), and later years of capture (91.9 1.85 mm, N ¼ 12; F2,40 ¼ 17.90, P < 0.001). Low repeatability for tail length thus appeared to be associated with change in size with approximate age (i.e. year of capture). The first two principal components accounted for 67.7% of individual variation in morphology for birds with song data. Factor loadings for tail length (0.579), wing chord (0.524), bill length (0.522) and tarsus length (0.343) were all positive on factor 1 (eigenvalue ¼ 1.456, 36.4% of variability), indicating that PC1 could be interpreted as a measure of general size. Tarsus (0.652) and bill lengths (0.459) loaded negatively on factor 2, while wing chord (0.478) and tail length (0.368) loaded positively (eigenvalue ¼ 1.250, 31.3% of variability). PC2 thus described a contrast of flight feather length (wing chord and tail length) with structural size (bill and tarsus lengths). The strength of the relationship between PC2 and the quotient obtained by dividing the sum of wing chord and tail length by the sum of tarsus and bill lengths approached 1.00 (r45 ¼ 0.984, P < 0.0001), and indicated clearly that males with high scores on PC2 had long flight feathers relative to the lengths of their tarsi and bills. Hence, we refer to PC1 as ‘body size’ and PC2 as ‘relative flight feather length’.
Relationships between Morphology and Song Our multiple regression analyses detected statistically significant relationships between male morphology and
Table 2. Repeatabilities of dawn song behaviours of eastern kingbirds from Malheur National Wildlife Refuge, OR, U.S.A., based on betweenyear and within-year comparisons Between years F15,56 (P) Start time 30MSR ASR PSR End time Song bout length Sample size Cell size
2003 r
2.16 (0.019) 0.205 2.09 (0.024) 0.195 2.08 (0.025) 0.194 3.71 (0.000) 0.376 1.19 (0.306) 0.040 1.13 (0.354) 0.028 16 males; 72 bouts 4.5
F22,39 (P) 1.42 1.59 1.69 3.30 2.98 0.84 2.7
2004 r
(0.167) 0.134 (0.102) 0.179 (0.076) 0.203 (0.001) 0.460 (0.001) 0.423 (0.660) 0.062 23 males; 62 bouts
F34,47 (P)
r
1.23 (0.251) 0.092 1.67 (0.051) 0.226 2.37 (0.003) 0.374 2.44 (0.002) 0.385 1.05 (0.428) 0.023 1.02 (0.470) 0.008 35 males; 82 bouts 2.3
Results of analyses of variance (F, P) and repeatability (r) were calculated as per Lessels & Boag (1987). Significant results (P 0.05) are given in bold. 30MSR ¼ 30-min song rate (songs/min); ASR ¼ actual song rate (songs/min); PSR ¼ peak song rate (songs/min).
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ANIMAL BEHAVIOUR, 75, 3
Table 3. Results of the stepwise regression analyses relating variation in song traits to morphological traits of male eastern kingbirds
Start time
Predictor variables
b (P)
(a) 1
2
R
Tarsus length 0.842 (0.000) Flight feather length 0.743 (0.000) 0.319
0.521 (0.001) 30-min song Flight feather length rate Year 0.035 (0.026) 0.202 Actual song rate
Flight feather length 0.537 (0.001) Year 0.290 (0.051) 0.207
Peak song rate
Flight feather length 0.550 (0.000) Year 0.415 (0.005) 0.249
Bout length
Wing chord
Residual start time
Song trait
1.5
0.5 0 −0.5 −1 −1.5
Column entries are standardized regression coefficients (b; P in parentheses) and coefficients of determination (R2) for the final model (N ¼ 47 for all analyses).
−1
0 0.5 −0.5 Relative flight feather length
1
1.5
2
Residual start time
1.5
five of six song behaviours (Table 3), the exception being end time. Nearly one-third of the variability in start time was associated with relative flight feather length and tarsus length: the earliest singers had relatively long flight feathers (Fig. 3a) and long tarsi (Fig. 3b). Year and relative flight feather length accounted for between 20% and 25% of the variability of the three song rates (Table 3). Song rates tended to be higher in 2003 (e.g. peak rate was 14.4 0.72 songs/min, N ¼ 29, in 2003 versus 13.7 1.01 songs/min, N ¼ 19, in 2004; t46 ¼ 2.49, P ¼ 0.019), and males with relatively long flight feathers sang at the highest rates (e.g. Fig. 4). Song bout length was also positively correlated with wing chord (Table 3). Assuming that females use song to identify quality males, we performed simple correlation analyses between song variables and both body size and relative flight feather length to identify the best predictor of each. Start time was the best predictor of body size (PC1): early singing males tended to be large (r45 ¼ 0.365, P < 0.012). And after accounting for a year effect, the best predictor of relative flight feather length (PC2) was PSR (r45 ¼ 0.507, P < 0.001).
r = -0.533, P < 0.001
−2 −1.5
0.373 (0.010) 0.139
(b)
1 0.5 0 −0.5 −1 −1.5
r = -0.581, P < 0.001
−2 −1.5
−1
−0.5
0 0.5 Tarsus (mm)
1
1.5
Figure 3. Partial plots of start time against (a) relative flight feather length, with effects of tarsus length removed and (b) tarsus length, with effects of relative flight feather length removed. Data are presented as standardized scores.
DISCUSSION We found that male morphology was highly repeatable between years, and that most song behaviours were also repeatable. In addition, both static (structural size) and dynamic characters (plumage) correlated with song
Reproductive Correlates of Song Performance Laying date and start time showed a positive and statistically significant relationship that indicated that the earliest singing males were paired to the earliest breeding females (r37 ¼ 0.368, P ¼ 0.021; Fig. 5). All other correlations of laying date with song traits were not significant (Table 4). Within years, we found the same relationship between breeding date and start time in 2004 (r19 ¼ 0.453, P ¼ 0.039), but in 2003, although the relationship was similar, it was not significant (r16 ¼ 0.224, P ¼ 0.370). Clutch size was independent of all song traits in the composite sample of both years (Table 4). There was also no evidence of a relationship between clutch size and song traits in 2004 (Table 4). However, song rate during the period that the male actually sang and peak song rate both showed positive but marginally nonsignificant relationships with clutch size in 2003 (Table 4).
Actual song rate (songs/min)
1080
2.5
r = 0.488, P < 0.001
1.5 0.5 −0.5 −1.5 −2.5 −2
−1.5
−1
−0.5
0
0.5
1
1.5
2
2.5
Relative flight feather length Figure 4. Partial plot of adjusted actual song rate against relative flight feather length after controlling for the effects of year (2003 > 2004). Data are presented as standardized scores.
MURPHY ET AL.: KINGBIRD SONG
Few estimates of the repeatability of song exist for birds, but Lambrechts & Dhondt (1987) and Poesel et al. (2001) found significant repeatability of song strophe length (r ¼ 0.23) and percentage performance time (r ¼ 0.74) in great tits, Parus major, and blue tits, Cyanistes caeruleus, respectively, while Rios Chelen et al. (2005) showed significant repeatability for seven aspects of song structure (ranging in value from 0.24 to 0.68) in vermillion flycatchers, Pyrocephalus rubinus. The two former studies compared song traits within the same bout, whereas Rios Chelen et al. (2005) and we compared bouts separated by a number of days, or in our case, a year. Despite the difference in time between measurements, the repeatabilities in all four studies are similar, and compare favourably with repeatabilities for reproductive traits such as laying date (mean ¼ 0.35, range 0.00e0.73) and clutch size (mean ¼ 0.39, range 0.08e0.86) of birds (see Christians 2002).
25 r = 0.368, P = 0.021 20
Breeding date
15 10 5 0 −5 −10 −1.5
−1
−0.5
0
0.5 1 Start time
1.5
2
2.5
Figure 5. Laying date of kingbirds at Malheur National Wildlife Refuge in 2003 and 2004 (mean standardized to zero) versus start time (standardized scores).
Associations between Song and Morphology Song is thought to communicate information to enable females to assess male quality (see Introduction), but little is known about the degree to which song varies with static traits such as body size or more dynamic properties such as plumage. Colour is an important signal of quality (Wolfenbarger 1999; Blount et al. 2003; Hill & McGraw 2006), but lengths of the flight surfaces (wings and tail) are also likely to be important correlates (Møller et al. 1998; Balsby 2000), especially in monochromatic species like kingbirds in which males perform flight displays (Smith 1966). Territory quality and flight feather length (i.e. male quality) might be confounded if males with long wings are the first to arrive from migration and acquire the highest-quality territories, but return date and wing chord are not correlated in kingbirds (N. W. Cooper & M. T. Murphy, unpublished data). Gil & Gahr (2002) argued that timing of song might be affected mainly by environmental conditions such as weather, whereas song rate was likely to depend more on body size. We found, however, that morphology accounted for nearly one-third of the variability in start time in kingbirds. Tarsus length is considered to be the single best measure of structural size in birds (Rising & Somers 1989; Senar & Pascual 1997), and given that tarsus
behaviour, and vigorous singers (i.e. those with early start times and high song rates) were paired to females that expressed traits indicative of high female quality.
Repeatability of Song Traits Repeatability reflects the combined influence of inheritance and environment on phenotypic expression. Factors such as early nutrition often have permanent effects on phenotypes (Lindstro¨m 1999; Nowicki et al. 2002; Searcy et al. 2004) and, therefore, only in the absence of environmental influences will heritability approach repeatability (Falconer 1981). In any case, honest signals of quality are expected to be both costly (to avoid cheating by low-quality individuals; Zahavi & Zahavi 1997) and repeatable. We found statistically significant repeatabilities for most song traits, and they tended to be stronger for between- than for within-year comparisons. Overall, the mean repeatability of song rates and start time suggested that about one-fourth of the differences between males was repeatable variation, but some variables (peak song rate) showed repeatabilities in the range of 0.40.
Table 4. Results of Pearson correlations describing associations between relative breeding date and song traits, and between relative clutch size and song traits for 39 male kingbirds with at least two samples of song behaviour Clutch size
Song behaviour Start time 30-min song rate Actual song rate Peak song rate End time Song bout length
Breeding date
2003 and 2004
2003
2004
r (P)
r (P)
r (P)
r (P)
0.369 0.154 0.086 0.093 0.186 0.164
(0.021) (0.351) (0.603) (0.574) (0.264) (0.318)
0.176 0.038 0.026 0.006 0.097 0.082
(0.284) (0.820) (0.876) (0.972) (0.555) (0.622)
0.120 0.344 0.465 0.462 0.279 0.013
(0.635) (0.162) (0.052) (0.053) (0.262) (0.958)
0.357 0.250 0.291 0.198 0.046 0.125
(0.113) (0.275) (0.201) (0.389) (0.842) (0.588)
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ANIMAL BEHAVIOUR, 75, 3
length is the best predictor of body mass for kingbirds (r119 ¼ 0.324, P < 0.001 for birds measured between 2002 and 2007), the negative association of start time with tarsus length suggests that the earliest singers were heavy birds. The inverse relationship of start time with relative flight feather length indicates that early singers also had relatively long wings and tails. The dawn song period is likely to be one of the most energetically stressful periods of the day for kingbirds because they have fasted for 6e 7 h, and at least at our study site, experienced thermally stressful conditions. Mean SD air temperature in the predawn period of June and July at MNWR in 2003 and 2004 was 7.6 4.05 C (N ¼ 122), and on 17% of days was below 4 C, temperatures well below the thermoneutral zone of kingbirds (Yarbrough 1971). Laboratory measurements of the energetic cost of song under thermoneutral conditions suggest that singing may not be costly (Oberweger & Goller 2001; Ward et al. 2004). However, food supplementation of free-living birds indicates that extra food enhances song production (Gottlander 1987; Cuthill & Macdonald 1990; Thomas 2002; Berg et al. 2005), suggesting that singing is energetically costly in the wild. Although we cannot eliminate the hypothesis that large males dominated smaller individuals and suppressed song production, our finding that the earliest singers tended to be large and have high-quality plumage is consistent with the hypothesis that conditions during the predawn period forced small and/or low-quality males to delay dawn song. Song rate in kingbirds also failed to conform to Gil & Gahr’s (2002) prediction that song rates are likely to be dependent on body size. Instead, song rates were higher in males with relatively long flight feathers and in 2003 when warmer conditions prevailed and insects were more abundant. The later breeding dates and smaller clutch sizes of 2004 are consistent with the conclusion that 2004 was a poorer year. Singing appears to be energetically costly for free-living birds (see above), and we suggest that the lower song rates in 2004 are attributable to poorer environmental conditions. High song rates among males with long flight feathers, and long song bouts by males with long wing chords, are consistent with the assumption that song is costly and able to be maintained only by high-quality males. Flight surfaces of passerines often increase in length between at least during the first and second breeding seasons (Fugle & Rothstein 1985; Stutchbury & Robertson 1987; Regosin & Pruett-Jones 2001). In our limited sample (18 males), wing chord did not increase over years but tail length did. Higher song performance of males with relatively long flight feathers was thus probably due to higher output by intrinsically higher-quality males, but possibly also to improvement with age.
Reproductive Correlates of Song Behaviour Among species with pronounced dawn songs, males that begin to sing earliest (Cuthill & Macdonald 1990; Otter et al. 1997; Christie et al. 2004; Poesel et al. 2006) and at high rates (Arvidsson & Neergaard 1991; Marchetti
1998; Poesel et al. 2001; Hofstad et al. 2002; Christie et al. 2004) are generally viewed as high-quality individuals. Early singing and high song output were associated with relatively long flight feathers in kingbirds, and early singers were also large males. Song thus appeared to provide honest information regarding male quality. We have shown that early singing males acquire the most extrapair fertilizations (Dolan et al. 2007). Extrapair mating success is not confounded by territory quality because extrapair females gain no direct benefits from extrapair mates, which suggests that females have a preference for early singing males, or a correlate such as body size. Given this, our finding that the timing of the start of dawn song was the best predictor of the date on which a male’s partner laid her first egg, and that clutch size (in 2003) varied positively with song rate suggests also that high-quality females may have preferred vigorously singing males as social mates. Nevertheless, alternative interpretations exist, and it remains to be determined whether females actively seek to pair with such males, or whether the pairing of high-quality males and females is a consequence of mutual attraction to high-quality territories. Kingbirds sing relatively simple songs, yet differences in song performance emerged as strong correlates of male quality, the quality of within-pair mates, and as we have shown elsewhere (Dolan et al. 2007), extrapair mating success. Suboscine song has been vastly understudied relative to the songs of oscines, and our results perhaps serve to place suboscine song in a new light. We suggest that greater effort be expended in describing the diversity of their songs and their relationships to mating and social systems. Acknowledgments We are most grateful to Cal and Alice Eltshoff and Malheur Wildlife Associates for giving us access to the ‘bunkhouse’ and for the kindness and friendship that they showed over the course of our study. We are also indebted to Rick Roy and the staff at Malheur National Wildlife Refuge for their invaluable help and continuing support, and thank Kelly Hoffman and Rick Ernst for their assistance in collecting the song data. Portions of this research were supported by funds provided to A.C.D. from the American Ornithologists’ Union Student Research Award and The American Museum of Natural History’s Frank M. Chapman Research Fund. Last, we are very grateful to the insights that Drs W. John Smith, Elena Berg and two anonymous referees provided on earlier drafts of the manuscript. References Andersson, M. 1994. Sexual Selection. Princeton, New Jersey: Princeton University Press. Arvidsson, B. L. & Neergaard, R. 1991. Mate choice in the willow warbler: a field experiment. Behavioral Ecology and Sociobiology, 29, 225e229. Balsby, T. J. S. 2000. Song activity and variability in relation to male quality and female choice in whitethroats Sylvia communis. Journal of Avian Biology, 31, 56e62.
MURPHY ET AL.: KINGBIRD SONG
Berg, M. L., Beintema, N. H., Welbergen, J. A. & Komdeur, J. 2005. Singing as a handicap: the effects of food availability and weather on song output in the Australian reed warbler Acrocephalus australis. Journal of Avian Biology, 36, 102e109. Blount, J. D., Metcalfe, N. B., Birkhead, T. R. & Surai, P. F. 2003. Carotenoid modulation of immune function and sexual advertisement in zebra finches. Science, 300, 125e127. Christians, J. K. 2002. Avian egg size: variation within species and inflexibility within individuals. Biological Review, 77, 1e26. Christie, P. J., Mennill, D. J. & Ratcliffe, L. M. 2004. Pitch shifts and song structure indicate male quality in the dawn chorus of blackcapped chickadees. Behavioral Ecology and Sociobiology, 55, 341e348. Conrad, K. F., Robertson, R. J. & Boag, P. T. 1998. Frequency of extrapair young increases in second broods of eastern phoebes. Auk, 115, 497e502. Cuthill, I. C. & Macdonald, W. A. 1990. Experimental manipulation of the dawn and dusk chorus in the blackbird Turdus merula. Behavioral Ecology and Sociobiology, 26, 209e216. Darwin, C. 1871. The Descent of Man, and Selection in Relation to Sex. London: Murray. Dolan, A. C., Murphy, M. T., Redmond, L. J., Sexton, K. & Duffield, D. 2007. Extra-pair paternity and the opportunity for sexual selection in a socially monogamous passerine. Behavioral Ecology, 18, 985e993. Eberhardt, L. 1994. Oxygen consumption during singing by male Carolina wrens (Thryothorus ludovicianus). Auk, 111, 124e130. Enstrom, D. A., Ketterson, E. D. & Nolan, V., Jr. 1997. Testosterone and mate choice in the dark-eyed junco. Animal Behaviour, 54, 1135e1146. Falconer, D. S. 1981. Introduction to Quantitative Genetics. 2nd edn. London: Longman. Fugle, G. N. & Rothstein, S. I. 1985. Age- and sex-related variation in size and crown plumage brightness in wintering white-crowned sparrows. Journal of Field Ornithology, 56, 356e368. Garnett, M. C. 1981. Body size, its heritability and influence on juvenile survival among great tits, Parus major. Ibis, 123, 31e41. Gil, D. & Gahr, M. 2002. The honesty of bird song: multiple constraints for multiple traits. Trends in Ecology & Evolution, 17, 133e141. Gottlander, K. 1987. Variation in song rate of the male pied flycatcher Ficedula hypoleuca: causes and consequences. Animal Behaviour, 35, 1037e1043. Halupka, K. & Borowiec, M. 2006. Male whitethroats, Sylvia communis, advertise their future contribution to parental care. Behaviour, 143, 1e14. Hill, G. E. & McGraw, K. J. 2006. Bird Coloration. Vol. 2: Function and Evolution. Cambridge, Massachusetts: Harvard University Press. Hipfner, J. M., Gaston, A. J., Martin, D. L. & Jones, I. L. 1999. Seasonal declines in replacement egg-layings in a long-lived Arctic seabird: costs of late breeding or variation in female quality? Journal of Animal Ecology, 68, 988e998. Hofstad, E., Espmark, Y., Moksnes, A., Haugen, T. & Ingebrigtsen, M. 2002. The relationship between song performance and male quality in snow buntings (Plectrophenax nivalis). Canadian Journal of Zoology, 80, 524e531. Jennions, M. D., Møller, A. P. & Petrie, M. 2001. Sexually selected traits and adult survival: a meta-analysis. Quarterly Review of Biology, 76, 3e36. Johnson, N. K. 1980. Character Variation and Evolution of Sibling Species in the Empidonax difficiliseflavescens Complex (Aves: Tyrannidae). Berkeley: University of California Press. Kipper, S., Mundry, R., Sommer, C., Hultsch, H. & Todt, D. 2006. Song repertoire size is correlated with body measures and arrival
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Tarof, S. A., Ratcliffe, L. M., Kasumovic, M. M. & Boag, P. T. 2004. Are least flycatcher (Empidonax minimus) clusters hidden leks? Behavioral Ecology, 16, 207e217. Thessing, A. & Ekman, J. 1994. Selection on the genetical and environmental components of tarsal growth in juvenile willow tits (Parus montanus). Journal of Evolutionary Biology, 7, 713e726. Thomas, R. J. 2002. The costs of singing in nightingales. Animal Behaviour, 63, 959e966. Ward, S., Spearman, J. R. & Slater, P. J. B. 2003. The energy cost of song in the canary, Serinus canaria. Animal Behaviour, 66, 893e902. Ward, S., Lampe, H. M. & Slater, P. J. B. 2004. Singing is not energetically demanding for pied flycatchers, Ficedula hypoleuca. Behavioral Ecology, 15, 477e484. Westcott, D. A. 1997. Neighbours, strangers and male-male aggression as a determinant of lek size. Behavioral Ecology and Sociobiology, 40, 235e242. Wolfenbarger, L. L. 1999. Red coloration of male northern cardinals correlates with male quality and territory quality. Behavioral Ecology, 10, 80e90. Woolfenden, B. E., Stutchbury, B. J. M. & Morton, E. S. 2005. Male Acadian flycatchers, Empidonax virescens, obtain extrapair fertilizations with distant females. Animal Behaviour, 69, 921e 929. Yarbrough, C. G. 1971. The influence of distribution and ecology on the thermoregulation of small birds. Comparative Biochemistry and Physiology, 39A, 235e256. Zahavi, A. & Zahavi, A. 1997. The Handicap Principle. New York: Oxford University Press.
Available online at www.sciencedirect.com
Dawn song of the eastern kingbird: an honest signal of male quality? M ICH A EL T. MURPH Y , KA REN S EXTON , AM Y C . DOLAN & LUK E J. REDMO ND
Department of Biology, Portland State University (Received 9 March 2007; initial acceptance 16 May 2007; final acceptance 7 August 2007; published online 16 January 2008; MS. number: A10714R)
To be used as honest signals of quality, phenotypic traits must vary markedly within populations and show repeatable differences between individuals. Eastern kingbirds, Tyrannus tyrannus, sing a distinctive dawn song in the predawn darkness, and one hypothesis for its function is that it serves as an honest signal of male quality that females use during choice of within-pair or extrapair mates. Over a 2-year period, we quantified dawn songs of males to measure between- and within-season repeatability of the timing (start and end time) and length of song bouts, and song rate. We also measured morphological characters to measure repeatability and describe individual differences in body size and plumage quality. All song traits varied considerably among males, start time and song rates were repeatable between years, and all song rates were repeatable within both years. All morphological characters were significantly repeatable between years. Moreover, early singing males were larger and had relatively long flight feathers, and males that sang at high rates had relatively long flight feathers. Early singing males were also paired to the earliest breeding females, and in one year, male song rate was positively correlated with their social mate’s clutch size. Relatively long flight feathers in other species are typical of older males and individuals of higher body condition, suggesting that, despite being suboscine passerines with relatively simple and innate songs, eastern kingbirds use song performance as an honest signal of male quality that females may use during mate choice. Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Keywords: body size; dawn song; eastern kingbird; honest signalling; mate choice; plumage quality; repeatability; song rate; timing of song; Tyrannus tyrannus
A basic tenet of sexual selection theory is that body size and secondary sexual traits such as plumage, song and other displays are indicators of quality that are used during mate choice (Darwin 1871; Andersson 1994). Such signals serve as measures of quality because their production is costly and only high-quality individuals can presumably afford their expense (Zahavi & Zahavi 1997; Jennions et al. 2001). The ability to support costly signals may come as a product of good genes or body condition, and high-quality females (early breeding and fecund; Hipfner et al. 1999; Wolfenbarger 1999) are presumably attracted to either the high-quality males themselves, or the habitats that they acquire.
Correspondence: M. T. Murphy, Department of Biology, P.O. Box 751, Portland State University, Portland, OR 97207, U.S.A. (email: [email protected]). 0003e 3472/08/$32.00/0
Body size is a ‘static’ trait that is often viewed as an honest signal of quality because it integrates an individual’s ontogenetic history (Thessing & Ekman 1994; Ryan 2001; Searcy et al. 2004). Final size is attained within weeks to months of hatching in small birds (<100 g), and conditions during early development can have lifelong effects on size and morphology (e.g. Garnett 1981; Ryan 2001), but also on other phenotypic traits (Lind¨ m 1999; Nowicki et al. 2002). Plumage and behaviour stro generally represent ‘dynamic’ traits that may be more valuable than body size in providing information on individual quality during mate choice because their expression is likely to be dependent on recent history (plumage) or current conditions (behaviour). Displays are especially useful signals of quality because their expression is likely to be a product of the male’s immediate condition (e.g. Halupka & Borowiec 2006). Song production is energetically costly in some species of
1075 Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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ANIMAL BEHAVIOUR, 75, 3
birds (Eberhardt 1994; Thomas 2002; but see Oberweger & Goller 2001; Ward et al. 2004), especially if performed in place of resting activities (Ward et al. 2003), and is generally regarded as an important cue used by female birds to select mates (e.g. Hofstad et al. 2002; Nolan & Hill 2004; Poesel et al. 2006). Most efforts to relate song to mating success have focused on daytime singing, but song performance in the early dawn chorus may be of particular importance (Poesel et al. 2006), and measures of performance such as the timing of the start of dawn song, song rate, song bout length, or temporal variability of song output may be particularly informative signals that females use to assess male quality (e.g. Marchetti 1998; Christie et al. 2004; Nolan & Hill 2004). If song is an honest measure of male quality, we should find repeatable differences between males in song performance and positive associations between song output, body size and condition, and/or territory quality. Evidence for the latter associations exist (e.g. Enstrom et al. 1997; Møller et al. 1998; Balsby 2000; Poesel et al. 2001; Kipper et al. 2006), but very little information is available to evaluate whether song traits are repeatable (but see Lambrechts & Dhondt 1987; Poesel et al. 2001; Rios Chelen et al. 2005). Suboscines represent roughly 20% of species within the order Passeriformes (1151 species). Unlike oscine passerines, suboscines sing stereotypical songs for which no evidence of song learning exists (Kroodsma 1984; Kroodsma & Konishi 1991), and as a consequence, suboscine song has been relatively neglected compared to the song of oscines. However, recent work has shown that suboscine song structure may vary over large geographical scales (Sedgwick 2001), and that sufficient variability in song structure exists within populations to permit individual recognition of neighbours (Westcott 1997; Lovell & Lein 2004). Some suboscines have diverse and complex vocalizations (e.g. Smith & Smith 1996), and some show a capacity for combinatorial syntax (Leger 2005). Nevertheless, except for its use in species recognition (e.g. Johnson 1980), the role of song in mate choice in suboscines is essentially unexplored. Eastern kingbirds are suboscine, Neotropical migrants that defend territories and form socially monogamous pair bonds. They have a moderate diversity of vocalizations (Smith 1966; Smith & Smith 1992), including a distinctive dawn song produced nearly exclusively in the predawn darkness (Smith 1966; Sexton et al. 2007). As in several other temperate-zone breeding tyrannids (Conrad et al. 1998; Tarof et al. 2004; Woolfenden et al. 2005), extrapair paternity is common in kingbirds (60% of nests; Rowe et al. 2001; Dolan et al. 2007), and we found that the timing of the start of dawn song was the best predictor of male extrapair mating success (Dolan et al. 2007). Females presumably gain indirect genetic benefits for young through extrapair mating because they receive no direct benefits (e.g. male assistance). We therefore hypothesized that male kingbird song performance may serve as an indicator of male quality, one measure of which may be body size. Our goals in this study were therefore to (1) determine the repeatability of morphology and song performance of male eastern kingbirds and (2) measure the degree to which song performance and male body
size and plumage quality covary to test the hypothesis that song conveys honest information about male quality. Finally, we also tested the prediction that song influences within-pair mate choice such that high-quality females pair with males that show high song performance.
METHODS
Study Site and Population Our study was conducted during June and July of 2003 and 2004 at Malheur National Wildlife Refuge (MNWR), OR, U.S.A. (42.84 N, 118.95 W). MNWR is located at the northern end of the Great Basin Desert, and the permanent flow of the Donner und Blitzen River through the high desert habitat (1400 m above sea level) supports the refuge’s marshes and riparian habitats. Kingbirds build open-cup nests in trees, and the MNWR kingbird population nests nearly exclusively in the willow trees (Salix spp.) that line the river’s banks. Our study began in 2002, and the number of breeding pairs was 52 in 2003 and 59 in 2004.
Field Methods Surveys of the study site began by mid-May in all years, and regular nest checks (every 2e3 days) allowed us to closely track pairs to establish breeding date (day first egg was laid), clutch size and hatching and fledging success (Redmond et al. 2007). Adults were captured with mist nets (beginning in 2002) during the nestling period and individuals were fitted with a unique combination of three coloured rings and one aluminium U.S. Fish and Wildlife Service ring. Sex was determined by the presence of a brood patch (females) or cloacal protuberance (males), and by differences in the lengths of the 9th and 10th primary feathers (Pyle 1997). Morphological measurements taken at the time of capture included body mass (nearest 0.1 g; Pesola scale), unflattened wing chord (nearest 0.5 mm; stopped wing ruler) and tarsometatarsus (¼tarsus), bill (nearest 0.1 mm; dial callipers) and tail length (nearest 0.5 mm from uropygial gland to tip of longest rectrix; stopped wing ruler). Because adult return rate is relatively high (w65%), many individuals were already marked at the start of the 2003 (w50%) and 2004 (w60%) seasons. Most nests (107 of 135) were located before or during egg laying, and therefore, the exact stage of the nest cycle was known for 79% of pairs. Nest stage for other nests was determined by backdating from known events (e.g. hatching date). Failed nests are usually replaced with new nests built within 100 m of the failed attempt (M. T. Murphy, personal observation), and we located replacement nests and collected identical data. We have observed only one within-season divorce and change of territory following a nest failure among marked birds in 4 years at MNWR (1 of w90 pairs; M. T. Murphy, personal observation), and therefore, we assumed unmarked birds at replacement nests to be the original resident pair. Kingbirds are aerial-hawking insectivores that capture single prey in primarily horizontal flights from a perch
MURPHY ET AL.: KINGBIRD SONG
(Murphy 1987). As part of a separate but concurrent study, we recorded insect abundance in 2003 and 2004 (Redmond 2005). Abundance was based on 3-min counts of insects that flew between an observer (L.J.R.) and a 1-m2 white sheet placed 5 m from the observer and at the height of herbaceous vegetation (w1 m). Counts were taken at midday (between 1000 and 1400 hours) and weekly from early June to late July in both years (except on days of high winds or rain), and in both years, five replicate counts were made from five habitat types used by kingbirds at MNWR on each sampling date. Weather (air temperature, relative humidity and wind speed) were collected at the end of each 3-min count using a Kestrel 3500 hand-held weather meter.
Song Data Fertile females are present at MNWR from late May until mid-July because replacement of failed nests is common (Sexton et al. 2007). Presumably in response, males sing dawn songs throughout their social mate’s nest cycle (Sexton et al. 2007), and observations of dawn song were made almost daily from mid-June through the third week of July in both years. Forty individuals from 49 nests were observed in 2003 (88 observations), and 47 individuals were observed from 67 nests in 2004 (107 observations). The number of nests exceeded the number of pairs in 2004 because of high nest loss and replacement, and as a result, some males were observed at multiple nests and up to five times per season. The mean SD time between successive observations of the same male was 11 7.8 days (N ¼ 83, range 1e35), but was more often 5 (24.1%) or 6 (18.0%) days. Males failed to sing during 22 observation periods and these were omitted from analyses. This left 173 song bouts during which males were observed once (N ¼ 22), twice (N ¼ 22), three times (N ¼ 10), four times (N ¼ 10), or five or more times (N ¼ 6) over the 2-year period. Rings could not be used to identify males during observations because dawn song generally began an hour or more before sunrise (see below). However, preliminary work showed that males usually sang from perches located no more than 100 m from the nest (see also Mayer 1952; Smith 1966), and given that distances between nearest nests averaged 250 m (Redmond 2005), we assumed that a male singing within 100 m of the nest was the resident. Our assumption was confirmed in every case either when rings could be seen as light improved, or as we tracked the flight path of the bird to the nest at the end of dawn song. Depending on the number of observers, three to five birds were observed daily (one bird per observer). We arrived at the nest site before singing began (between 0315 and 0415 hours Pacific Standard Time, PST) and remained until the end of the bout. A song was defined as the ‘regular repeated vocalization’ (RRV) described by Smith (1966). Each song lasts 2e8 s depending on the number of repeated notes, but is separated from the next by a distinct final note and pause. Once begun, singing continued until the end of the song bout unless the male was
interrupted by another bird. The end was usually marked by a chatter-zeer vocalization (Smith & Smith 1992) and a flight over the territory. The start and end of the song bout were calculated to the nearest minute relative to sunrise (time for sunrise was obtained from official records for the weather station at Burns Airport located 40e60 km north of our site, depending on the nest): large negative values indicate an early start or end. Song bout length was the absolute difference between start and end time. We recorded the number of RRVs per min for the first 30 min of song to define song output in three ways. Thirty-minute song rate (30MSR) was calculated as the average number of RRVs per minute for the first 30 min, regardless of whether the bird sang for the entire time. Actual song rate (ASR) was the average number of RRVs per minute during the time the bird actually sang within the first 30 min, and peak song rate (PSR) was the average number of RRVs per minute for the 5-min period during which song rate was highest.
Statistical Analyses Comparisons of insect counts between years were made after first using multiple regression to control for seasonal growth of insect populations and variation in flight activity associated with weather (Redmond 2005). We calculated between-year repeatability (Lessels & Boag 1987) of morphology for males captured in multiple years, and to maximize sample size, we expanded our analyses to include individuals remeasured through 2007. We also calculated repeatability of song traits both between and within years for individual males with multiple observations of song bouts. Song repeatabilities were calculated after we first tested for and removed possible effects of calendar date, nest stage of the male’s social mate, fertility status of social mate and sociobiological factors that might affect song behaviour (e.g. density of pairs, number of fertile females within 600 m, and within the total population). We used best subsets regression analyses to identify the combination of variables (all P 0.05 based on type III sums of squares) that accounted for the maximum variation in each song variable. The analyses are described elsewhere (Sexton et al. 2007), but here we use the residuals from the latter regressions. Repeatabilities were also calculated for the raw data, and the results were qualitatively identical with only two exceptions that we describe below. We assumed that an early start to dawn song, high song rates and long song bouts were costly and characteristic of only high-quality males. We also assumed that highquality males were larger and had longer flight feathers, and thus tested for positive relationships between song performance and overall size and flight feather length. Of the 87 males for whom multiple observations of song behaviour existed, 40 were not used in these analyses either because morphological data were missing or a 2-year gap existed between measurement of morphology and song. Of the remainder, 15 were captured and measured in the year before their song was documented (either in 2002 or in 2003), while 32 were captured and measured in the same year that their song behaviour was quantified. Each male
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ANIMAL BEHAVIOUR, 75, 3
was used once and song behaviour was averaged over multiple song recording bouts to obtain a single measure of behaviour. In the interest of uniformity, songs from the first year were used for males recorded in both years. We used principal component analysis (PCA) of linear measures of size to describe variability in body size and shape. Stepwise regression analysis (type III sums of squares) was then used to test for associations between all six song traits and individual male morphological traits, PC1 and PC2 (see below), and year (2003 ¼ 1, 2004 ¼ 2). We separately analysed the 32 individuals for whom morphology and song behaviour were recorded in the same year, and included body mass as an additional predictor variable of song behaviour. Mass never entered the models as a significant predictor of song behaviour, and the results were qualitatively unchanged from the analyses of 47 birds. We therefore report only the latter results. Laying dates and clutch sizes of first nests of the season were compared to all six song characters using stepwise regression (as above) for males with at least two observations of song in the same year. Except for five cases where data for the first nest in the first year were incomplete, we used only the first year that a male was observed to avoid pseudoreplication. Laying date was significantly later in 2004 than in 2003 (M. T. Murphy, unpublished data) and therefore date was standardized to a mean of zero by subtracting the true mean from all dates for each year. Clutch size declines seasonally in kingbirds (Murphy 1996), and therefore, we compared residual clutch size (date effects removed using regression) to male traits. All analyses were performed using STATISTIX8 (Analytical Software, Tallahassee, FL, U.S.A.) or SPSS, version 10 (SPSS Inc., Chicago, IL, U.S.A.). We report standardized regression coefficients (b), means SDs and sample size (N ), and significance was accepted at P 0.05 unless otherwise stated. All reported correlation coefficients are Pearson’s r, and all t tests were two-sample t tests.
30 May Mean air temperature (C)
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June
July
25 20 15 10 5 0 10
20
30
40
50
60
70
80
90
Date (1 = 1 May) Figure 1. Seasonal variation in temperature at MNWR in 2003 (C) and 2004 (B) between mid-May and the end of July.
the first 30 min. Song rate during the actual song bout (ASR) was 15% higher, but PSR was nearly 50% higher than 30MSR (Table 1). Most males stopped singing about 30 min before dawn, and thus, song bout length averaged just over 30 min (Table 1). Start time was the least variable song trait (coefficients of variation, CV, in Table 1), but even start time was three to five times more variable than morphology (Table 1). Start time was significantly repeatable between years (Fig. 2a), but not when each year was examined separately (Table 2). On the other hand, repeatability for end time was not significant in between-year comparisons, but was significant in 2003 (Table 2), and ultimately, song bout length gave no indication of being repeatable. Seven of the nine possible repeatabilities of song rates (30MSR, ASR, PSR) were significant (at P 0.051), and of the two that were not (30MSR and ASR in 2003), both approached significance (P 0.10; Table 2). Moreover, both of the latter rates yielded significant repeatabilities (P 0.043)
RESULTS
Environmental Conditions: Annual Comparisons Kingbirds first arrive at MNWR between 10 and 15 May. Air temperatures between mid-May and the end of July were on average higher in 2003 (Fig. 1), and, after controlling for date of observation and meteorological conditions, flying insects were also more abundant in 2003 (8.4 4.82 insects/3 min, N ¼ 179) than in 2004 (5.9 4.17 insects/ 5 min, N ¼ 179; t356 ¼ 5.23, P < 0.001). Breeding began significantly earlier in 2003 (11 June 6.6 days, N ¼ 51) than in 2004 (19 June 6.2 days, N ¼ 43; t92 ¼ 5.85, P < 0.001), and females also produced larger initial clutches in 2003 (2003: 3.8 0.47 eggs, N ¼ 54; 2004: 3.4 0.85 eggs, N ¼ 42; t94 ¼ 3.09, P ¼ 0.003).
Repeatability of Song Traits Dawn song began roughly 1-h before sunrise, and males averaged roughly nine songs/min (30MSR; Table 1) during
Table 1. Summary statistics (CV ¼ coefficient of variation) describing morphological and song traits recorded from male eastern kingbirds in 2003 and 2004 at Malheur National Wildlife Refuge, OR, U.S.A. (N ¼ 87 and N ¼ 47 for song and morphological variables, respectively) Trait
MeanSD
Start time 63.89.2 (min before dawn) 30-min song rate 9.33.5 (30MSR; songs/min) Actual song rate 10.73.0 (ASR; songs/min) Peak song rate 13.63.5 (PSR; songs/min) End time 29.97.5 (min before dawn) Song bout length 33.810.6 (min) Bill length (mm) 14.740.74 Tail length (mm) 88.523.09 Tarsus length (mm) 20.230.98 Wing chord (mm) 121.72.8
Range
CV
84 to 37
14.46
1.2 to 16.1
37.72
3.2 to 17.9
28.06
5.6 to 20.8
26.13
52 to 11
25.13
7.0 to 55.7
31.23
13.20 to 16.70 82.0 to 97.0 17.60 to 23.30 115.0 to 128.0
5.04 3.49 4.86 2.29
MURPHY ET AL.: KINGBIRD SONG
−45
Start time 2004
−50
Morphological Analysis (a)
−55 −60 −65 −70 −75 −80 −85
−80
−75
−70 −65 −60 Start time 2003
−55
−50
−45
2 (b) Peak song rate 2004
1.5 1 0.5 0 −0.5 −1 −1.5 −1.5
−1
0 0.5 1 −0.5 Peak song rate 2003
1.5
2
Figure 2. A comparison of (a) unadjusted start time and (b) adjusted peak song rate (PSR) for 16 male kingbirds whose songs were documented in both 2003 and 2004.
when the analyses were based on uncorrected values. PSR was the most repeatable (0.376e0.460) of the three song rates (Fig. 2b), followed by ASR (0.194e0.374) and then 30MSR (0.179e0.226). The mean SD repeatability of start time and song rates based on between- and withinseason measures was 0.251 0.116 (N ¼ 12, 95% confidence interval ¼ 0.178e0.326).
Bill (r ¼ 0.751, F17,25 ¼ 8.23, P < 0.001) and tarsus (r ¼ 0.636, F17,25 ¼ 5.02, P ¼ 0.001) lengths both exhibited high individual repeatability. Repeatability of wing chord (r ¼ 0.482, F17,25 ¼ 3.23, P ¼ 0.004) and tail length (r ¼ 0.372, F17,25 ¼ 2.85, P ¼ 0.009) were not as high, but both were also significant (effective cell size ¼ 2.4 for all). Neither the nonplumage characters nor wing chord changed as the bird aged (bill length: F2,40 ¼ 1.40, P ¼ 0.258; tarsus length: F2,40 ¼ 0.01, P ¼ 0.996; wing chord: F2,40 ¼ 0.39, P ¼ 0.679), but tail length increased between the first (88.2 1.66 mm, N ¼ 18), second (90.0 1.47 mm, N ¼ 13), and later years of capture (91.9 1.85 mm, N ¼ 12; F2,40 ¼ 17.90, P < 0.001). Low repeatability for tail length thus appeared to be associated with change in size with approximate age (i.e. year of capture). The first two principal components accounted for 67.7% of individual variation in morphology for birds with song data. Factor loadings for tail length (0.579), wing chord (0.524), bill length (0.522) and tarsus length (0.343) were all positive on factor 1 (eigenvalue ¼ 1.456, 36.4% of variability), indicating that PC1 could be interpreted as a measure of general size. Tarsus (0.652) and bill lengths (0.459) loaded negatively on factor 2, while wing chord (0.478) and tail length (0.368) loaded positively (eigenvalue ¼ 1.250, 31.3% of variability). PC2 thus described a contrast of flight feather length (wing chord and tail length) with structural size (bill and tarsus lengths). The strength of the relationship between PC2 and the quotient obtained by dividing the sum of wing chord and tail length by the sum of tarsus and bill lengths approached 1.00 (r45 ¼ 0.984, P < 0.0001), and indicated clearly that males with high scores on PC2 had long flight feathers relative to the lengths of their tarsi and bills. Hence, we refer to PC1 as ‘body size’ and PC2 as ‘relative flight feather length’.
Relationships between Morphology and Song Our multiple regression analyses detected statistically significant relationships between male morphology and
Table 2. Repeatabilities of dawn song behaviours of eastern kingbirds from Malheur National Wildlife Refuge, OR, U.S.A., based on betweenyear and within-year comparisons Between years F15,56 (P) Start time 30MSR ASR PSR End time Song bout length Sample size Cell size
2003 r
2.16 (0.019) 0.205 2.09 (0.024) 0.195 2.08 (0.025) 0.194 3.71 (0.000) 0.376 1.19 (0.306) 0.040 1.13 (0.354) 0.028 16 males; 72 bouts 4.5
F22,39 (P) 1.42 1.59 1.69 3.30 2.98 0.84 2.7
2004 r
(0.167) 0.134 (0.102) 0.179 (0.076) 0.203 (0.001) 0.460 (0.001) 0.423 (0.660) 0.062 23 males; 62 bouts
F34,47 (P)
r
1.23 (0.251) 0.092 1.67 (0.051) 0.226 2.37 (0.003) 0.374 2.44 (0.002) 0.385 1.05 (0.428) 0.023 1.02 (0.470) 0.008 35 males; 82 bouts 2.3
Results of analyses of variance (F, P) and repeatability (r) were calculated as per Lessels & Boag (1987). Significant results (P 0.05) are given in bold. 30MSR ¼ 30-min song rate (songs/min); ASR ¼ actual song rate (songs/min); PSR ¼ peak song rate (songs/min).
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ANIMAL BEHAVIOUR, 75, 3
Table 3. Results of the stepwise regression analyses relating variation in song traits to morphological traits of male eastern kingbirds
Start time
Predictor variables
b (P)
(a) 1
2
R
Tarsus length 0.842 (0.000) Flight feather length 0.743 (0.000) 0.319
0.521 (0.001) 30-min song Flight feather length rate Year 0.035 (0.026) 0.202 Actual song rate
Flight feather length 0.537 (0.001) Year 0.290 (0.051) 0.207
Peak song rate
Flight feather length 0.550 (0.000) Year 0.415 (0.005) 0.249
Bout length
Wing chord
Residual start time
Song trait
1.5
0.5 0 −0.5 −1 −1.5
Column entries are standardized regression coefficients (b; P in parentheses) and coefficients of determination (R2) for the final model (N ¼ 47 for all analyses).
−1
0 0.5 −0.5 Relative flight feather length
1
1.5
2
Residual start time
1.5
five of six song behaviours (Table 3), the exception being end time. Nearly one-third of the variability in start time was associated with relative flight feather length and tarsus length: the earliest singers had relatively long flight feathers (Fig. 3a) and long tarsi (Fig. 3b). Year and relative flight feather length accounted for between 20% and 25% of the variability of the three song rates (Table 3). Song rates tended to be higher in 2003 (e.g. peak rate was 14.4 0.72 songs/min, N ¼ 29, in 2003 versus 13.7 1.01 songs/min, N ¼ 19, in 2004; t46 ¼ 2.49, P ¼ 0.019), and males with relatively long flight feathers sang at the highest rates (e.g. Fig. 4). Song bout length was also positively correlated with wing chord (Table 3). Assuming that females use song to identify quality males, we performed simple correlation analyses between song variables and both body size and relative flight feather length to identify the best predictor of each. Start time was the best predictor of body size (PC1): early singing males tended to be large (r45 ¼ 0.365, P < 0.012). And after accounting for a year effect, the best predictor of relative flight feather length (PC2) was PSR (r45 ¼ 0.507, P < 0.001).
r = -0.533, P < 0.001
−2 −1.5
0.373 (0.010) 0.139
(b)
1 0.5 0 −0.5 −1 −1.5
r = -0.581, P < 0.001
−2 −1.5
−1
−0.5
0 0.5 Tarsus (mm)
1
1.5
Figure 3. Partial plots of start time against (a) relative flight feather length, with effects of tarsus length removed and (b) tarsus length, with effects of relative flight feather length removed. Data are presented as standardized scores.
DISCUSSION We found that male morphology was highly repeatable between years, and that most song behaviours were also repeatable. In addition, both static (structural size) and dynamic characters (plumage) correlated with song
Reproductive Correlates of Song Performance Laying date and start time showed a positive and statistically significant relationship that indicated that the earliest singing males were paired to the earliest breeding females (r37 ¼ 0.368, P ¼ 0.021; Fig. 5). All other correlations of laying date with song traits were not significant (Table 4). Within years, we found the same relationship between breeding date and start time in 2004 (r19 ¼ 0.453, P ¼ 0.039), but in 2003, although the relationship was similar, it was not significant (r16 ¼ 0.224, P ¼ 0.370). Clutch size was independent of all song traits in the composite sample of both years (Table 4). There was also no evidence of a relationship between clutch size and song traits in 2004 (Table 4). However, song rate during the period that the male actually sang and peak song rate both showed positive but marginally nonsignificant relationships with clutch size in 2003 (Table 4).
Actual song rate (songs/min)
1080
2.5
r = 0.488, P < 0.001
1.5 0.5 −0.5 −1.5 −2.5 −2
−1.5
−1
−0.5
0
0.5
1
1.5
2
2.5
Relative flight feather length Figure 4. Partial plot of adjusted actual song rate against relative flight feather length after controlling for the effects of year (2003 > 2004). Data are presented as standardized scores.
MURPHY ET AL.: KINGBIRD SONG
Few estimates of the repeatability of song exist for birds, but Lambrechts & Dhondt (1987) and Poesel et al. (2001) found significant repeatability of song strophe length (r ¼ 0.23) and percentage performance time (r ¼ 0.74) in great tits, Parus major, and blue tits, Cyanistes caeruleus, respectively, while Rios Chelen et al. (2005) showed significant repeatability for seven aspects of song structure (ranging in value from 0.24 to 0.68) in vermillion flycatchers, Pyrocephalus rubinus. The two former studies compared song traits within the same bout, whereas Rios Chelen et al. (2005) and we compared bouts separated by a number of days, or in our case, a year. Despite the difference in time between measurements, the repeatabilities in all four studies are similar, and compare favourably with repeatabilities for reproductive traits such as laying date (mean ¼ 0.35, range 0.00e0.73) and clutch size (mean ¼ 0.39, range 0.08e0.86) of birds (see Christians 2002).
25 r = 0.368, P = 0.021 20
Breeding date
15 10 5 0 −5 −10 −1.5
−1
−0.5
0
0.5 1 Start time
1.5
2
2.5
Figure 5. Laying date of kingbirds at Malheur National Wildlife Refuge in 2003 and 2004 (mean standardized to zero) versus start time (standardized scores).
Associations between Song and Morphology Song is thought to communicate information to enable females to assess male quality (see Introduction), but little is known about the degree to which song varies with static traits such as body size or more dynamic properties such as plumage. Colour is an important signal of quality (Wolfenbarger 1999; Blount et al. 2003; Hill & McGraw 2006), but lengths of the flight surfaces (wings and tail) are also likely to be important correlates (Møller et al. 1998; Balsby 2000), especially in monochromatic species like kingbirds in which males perform flight displays (Smith 1966). Territory quality and flight feather length (i.e. male quality) might be confounded if males with long wings are the first to arrive from migration and acquire the highest-quality territories, but return date and wing chord are not correlated in kingbirds (N. W. Cooper & M. T. Murphy, unpublished data). Gil & Gahr (2002) argued that timing of song might be affected mainly by environmental conditions such as weather, whereas song rate was likely to depend more on body size. We found, however, that morphology accounted for nearly one-third of the variability in start time in kingbirds. Tarsus length is considered to be the single best measure of structural size in birds (Rising & Somers 1989; Senar & Pascual 1997), and given that tarsus
behaviour, and vigorous singers (i.e. those with early start times and high song rates) were paired to females that expressed traits indicative of high female quality.
Repeatability of Song Traits Repeatability reflects the combined influence of inheritance and environment on phenotypic expression. Factors such as early nutrition often have permanent effects on phenotypes (Lindstro¨m 1999; Nowicki et al. 2002; Searcy et al. 2004) and, therefore, only in the absence of environmental influences will heritability approach repeatability (Falconer 1981). In any case, honest signals of quality are expected to be both costly (to avoid cheating by low-quality individuals; Zahavi & Zahavi 1997) and repeatable. We found statistically significant repeatabilities for most song traits, and they tended to be stronger for between- than for within-year comparisons. Overall, the mean repeatability of song rates and start time suggested that about one-fourth of the differences between males was repeatable variation, but some variables (peak song rate) showed repeatabilities in the range of 0.40.
Table 4. Results of Pearson correlations describing associations between relative breeding date and song traits, and between relative clutch size and song traits for 39 male kingbirds with at least two samples of song behaviour Clutch size
Song behaviour Start time 30-min song rate Actual song rate Peak song rate End time Song bout length
Breeding date
2003 and 2004
2003
2004
r (P)
r (P)
r (P)
r (P)
0.369 0.154 0.086 0.093 0.186 0.164
(0.021) (0.351) (0.603) (0.574) (0.264) (0.318)
0.176 0.038 0.026 0.006 0.097 0.082
(0.284) (0.820) (0.876) (0.972) (0.555) (0.622)
0.120 0.344 0.465 0.462 0.279 0.013
(0.635) (0.162) (0.052) (0.053) (0.262) (0.958)
0.357 0.250 0.291 0.198 0.046 0.125
(0.113) (0.275) (0.201) (0.389) (0.842) (0.588)
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length is the best predictor of body mass for kingbirds (r119 ¼ 0.324, P < 0.001 for birds measured between 2002 and 2007), the negative association of start time with tarsus length suggests that the earliest singers were heavy birds. The inverse relationship of start time with relative flight feather length indicates that early singers also had relatively long wings and tails. The dawn song period is likely to be one of the most energetically stressful periods of the day for kingbirds because they have fasted for 6e 7 h, and at least at our study site, experienced thermally stressful conditions. Mean SD air temperature in the predawn period of June and July at MNWR in 2003 and 2004 was 7.6 4.05 C (N ¼ 122), and on 17% of days was below 4 C, temperatures well below the thermoneutral zone of kingbirds (Yarbrough 1971). Laboratory measurements of the energetic cost of song under thermoneutral conditions suggest that singing may not be costly (Oberweger & Goller 2001; Ward et al. 2004). However, food supplementation of free-living birds indicates that extra food enhances song production (Gottlander 1987; Cuthill & Macdonald 1990; Thomas 2002; Berg et al. 2005), suggesting that singing is energetically costly in the wild. Although we cannot eliminate the hypothesis that large males dominated smaller individuals and suppressed song production, our finding that the earliest singers tended to be large and have high-quality plumage is consistent with the hypothesis that conditions during the predawn period forced small and/or low-quality males to delay dawn song. Song rate in kingbirds also failed to conform to Gil & Gahr’s (2002) prediction that song rates are likely to be dependent on body size. Instead, song rates were higher in males with relatively long flight feathers and in 2003 when warmer conditions prevailed and insects were more abundant. The later breeding dates and smaller clutch sizes of 2004 are consistent with the conclusion that 2004 was a poorer year. Singing appears to be energetically costly for free-living birds (see above), and we suggest that the lower song rates in 2004 are attributable to poorer environmental conditions. High song rates among males with long flight feathers, and long song bouts by males with long wing chords, are consistent with the assumption that song is costly and able to be maintained only by high-quality males. Flight surfaces of passerines often increase in length between at least during the first and second breeding seasons (Fugle & Rothstein 1985; Stutchbury & Robertson 1987; Regosin & Pruett-Jones 2001). In our limited sample (18 males), wing chord did not increase over years but tail length did. Higher song performance of males with relatively long flight feathers was thus probably due to higher output by intrinsically higher-quality males, but possibly also to improvement with age.
Reproductive Correlates of Song Behaviour Among species with pronounced dawn songs, males that begin to sing earliest (Cuthill & Macdonald 1990; Otter et al. 1997; Christie et al. 2004; Poesel et al. 2006) and at high rates (Arvidsson & Neergaard 1991; Marchetti
1998; Poesel et al. 2001; Hofstad et al. 2002; Christie et al. 2004) are generally viewed as high-quality individuals. Early singing and high song output were associated with relatively long flight feathers in kingbirds, and early singers were also large males. Song thus appeared to provide honest information regarding male quality. We have shown that early singing males acquire the most extrapair fertilizations (Dolan et al. 2007). Extrapair mating success is not confounded by territory quality because extrapair females gain no direct benefits from extrapair mates, which suggests that females have a preference for early singing males, or a correlate such as body size. Given this, our finding that the timing of the start of dawn song was the best predictor of the date on which a male’s partner laid her first egg, and that clutch size (in 2003) varied positively with song rate suggests also that high-quality females may have preferred vigorously singing males as social mates. Nevertheless, alternative interpretations exist, and it remains to be determined whether females actively seek to pair with such males, or whether the pairing of high-quality males and females is a consequence of mutual attraction to high-quality territories. Kingbirds sing relatively simple songs, yet differences in song performance emerged as strong correlates of male quality, the quality of within-pair mates, and as we have shown elsewhere (Dolan et al. 2007), extrapair mating success. Suboscine song has been vastly understudied relative to the songs of oscines, and our results perhaps serve to place suboscine song in a new light. We suggest that greater effort be expended in describing the diversity of their songs and their relationships to mating and social systems. Acknowledgments We are most grateful to Cal and Alice Eltshoff and Malheur Wildlife Associates for giving us access to the ‘bunkhouse’ and for the kindness and friendship that they showed over the course of our study. We are also indebted to Rick Roy and the staff at Malheur National Wildlife Refuge for their invaluable help and continuing support, and thank Kelly Hoffman and Rick Ernst for their assistance in collecting the song data. Portions of this research were supported by funds provided to A.C.D. from the American Ornithologists’ Union Student Research Award and The American Museum of Natural History’s Frank M. Chapman Research Fund. Last, we are very grateful to the insights that Drs W. John Smith, Elena Berg and two anonymous referees provided on earlier drafts of the manuscript. References Andersson, M. 1994. Sexual Selection. Princeton, New Jersey: Princeton University Press. Arvidsson, B. L. & Neergaard, R. 1991. Mate choice in the willow warbler: a field experiment. Behavioral Ecology and Sociobiology, 29, 225e229. Balsby, T. J. S. 2000. Song activity and variability in relation to male quality and female choice in whitethroats Sylvia communis. Journal of Avian Biology, 31, 56e62.
MURPHY ET AL.: KINGBIRD SONG
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