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Variation in incubation length and hatching asynchrony in Eastern Kingbirds: Weather eclipses female effects

Variation in incubation length and hatching asynchrony in Eastern Kingbirds: Weather eclipses... Abstract Incubation length and hatching asynchrony are integral elements of the evolved reproductive strategies of birds. We examined intra- and interpopulation variation in both traits for Eastern Kingbird (Tyrannus tyrannus) populations from New York (NY), Kansas (KS), and Oregon (OR) and found that both incubation length and hatching asynchrony were not repeatable among females, after controlling for a repeatable trait, clutch size. Instead, incubation length and clutch size were influenced by ambient temperature and precipitation. Incubation length exhibited the same median (15 days) and range (13–17 days) at all sites. Model selection results indicated that incubation periods for the smallest and largest clutches were longer in NY than KS when rain was frequent throughout incubation, in replacement nests, and likely when ambient temperatures were low during egg-laying. Full hatching usually required 2 days (but up to 3), with synchronous hatching associated with small clutch sizes, short incubation periods, frequent rain during the egg-laying period, and low ambient temperatures during the first half of incubation. Nestling starvation was uncommon (5–9% of nestlings monitored) and not associated with greater hatching asynchrony. These results indicate that while clutch size, a repeatable female trait, contributed to variation in incubation length and hatching asynchrony in Eastern Kingbirds, weather was a greater source of variation, especially for incubation length. RESUMEN La duración de la incubación y la asincronía de la eclosión son elementos integrales de las estrategias reproductivas evolucionadas de las aves. Examinamos la variación intra- e inter-poblacional en ambos rasgos para las poblaciones de Tyrannus tyrannus de Nueva York (NY), Kansas (KS) y Oregón (OR) y encontramos que tanto la duración de la incubación como la asincronía de la eclosión no fueron repetibles entre las hembras, luego de controlar un rasgo repetible como el tamaño de la nidada. En cambio, la duración de la incubación y el tamaño de la nidada fueron influenciados por la temperatura ambiente y la precipitación. La duración de la incubación mostró la misma mediana (15 días) y el mismo rango (13–17 días) en todos los sitios. Los resultados de los modelos de selección indicaron que los períodos de incubación para las nidadas más pequeñas y más grandes fueron más largos en NY que en KS cuando la lluvia fue frecuente a lo largo de la incubación, en los nidos de reemplazo y probablemente cuando las temperaturas ambiente fueron bajas durante la puesta de los huevos. La eclosión completa usualmente requirió 2 días (pero hasta 3), estando la eclosión asociada a pequeños tamaños de nidada, períodos cortos de incubación, lluvia frecuente durante el período de puesta de los huevos y bajas temperaturas ambiente durante la primera mitad de la incubación. La hambruna de los polluelos fue poco común (5–9% de los polluelos monitoreados) y no estuvo asociada con una mayor asincronía de la eclosión. Estos resultados indican que mientras el tamaño de la nidada, un rasgo repetible de las hembras, contribuyó a la variación en la duración de la incubación y en la asincronía de la eclosión en T. tyrannus, el clima fue una fuente mayor de variación, especialmente para la duración de la incubación. Lay Summary • The length of time that eggs remain in a nest exposed to causes of mortality has important influences on the reproductive success of birds. • We collected data on incubation length, the length of time elapsed between the hatching of the first and last egg (called hatching asynchrony), and probability of nestling starvation in Eastern Kingbirds breeding at 3 locations (Kansas, New York, and Oregon). • Incubation length and hatching asynchrony varied considerably within, but also among sites. Incubation length and hatching asynchrony were both greater in nests with more eggs. However, most other variation was likely due to environmental effects. Cool and wet conditions were associated with long incubation periods while greater hatching asynchrony was found during periods when it was warm and dry. • Starvation of nestlings was infrequent, and nests with a greater range of nestling ages (caused by high hatching asynchrony) did not experience greater starvation of young. Nestling starvation was thus not a cost of high-hatching asynchrony. • Our research demonstrates that environmental temperature and frequency of precipitation have greater effects on incubation period compared to clutch size. INTRODUCTION Incubation is a critical period during avian reproduction and the strong allometric relationship between incubation length and egg mass in altricial birds (Birchard and Deeming 2015) suggests selection has shortened incubation length to near its physiological limit. However, the existence of geographic and interspecific differences in incubation length, independent of egg or body size, suggest that other factors are at play (Ricklefs et al. 2017, Martin et al. 2018). Within north temperate regions, variation in incubation length also results from physical influences of the environment (Ardia et al. 2006, MacDonald et al. 2013, Griffith et al. 2016). Embryonic development in birds begins when egg temperature exceeds presumed physiological zero (~26°C; Webb 1987). Higher ambient temperatures can raise egg temperatures (e.g., Wang and Weathers 2009, Nord et al. 2010), but frequent rainfall and wetting of nests, which increases nest thermal conductance (Reid et al. 2002a, Hilton et al. 2004), may cause rapid declines in egg temperature (Hilton et al. 2004). Once embryogenesis begins, embryos of most avian species appear detrimentally affected by time spent below optimal incubation temperatures (36–40°C; Cooper et al. 2005) because it may extend incubation (Ardia et al. 2006, Hepp et al. 2006, Griffith et al. 2016, Martin et al. 2018, de Zwann et al. 2019), reduce hatchling yolk reserves or protein content (Vleck and Hoyt 1980, Hepp et al. 2006, Eiby and Booth 2009), yield smaller and/or lower quality hatchlings (Kim and Monaghan 2006, Olson et al. 2006, Ardia et al. 2010, DuRant et al. 2012), reduce hatching success (Hepp et al. 2006, MacDonald et al. 2013), or yield offspring with weak immune responses (Ardia et al. 2010, DuRant et al. 2012). Higher ambient temperatures and sparse precipitation may thus benefit embryos and adults because of the reduced gradient in temperature between eggs and environment that drive embryo temperatures down when parents leave the nest to feed (Zerba and Morton 1983, Morton and Pereyra 1985, Reid et al. 2002b). However, because all birds lay maximally 1 egg per day and most do not begin incubation with the first egg, ambient conditions that allow eggs to remain above physiological zero for extended periods prior to the start of full incubation may result in a loss of egg viability (Arnold 1993, Stoleson and Beissinger 1999) or initiate embryonic development before termination of egg-laying (Cooper et al. 2005). The latter may result in hatching asynchrony (e.g., Ardia et al. 2006). Hatching asynchrony is often associated with increased nestling starvation (Bancroft 1985, Stouffer and Powers 1991, Murphy 1994, Stoleson and Beissinger 1997) or reduced nestling quality (Clotfelter and Yasukawa 1999) due to asymmetric competition among asynchronously hatched young. Despite apparent negative consequences, hatching asynchrony is generally perceived as an evolved strategy under female control that allows parents to either reduce brood size to a number commensurate with food supplies (Lack 1968, Magrath 1989), or to shorten the time eggs and young spend in the nest exposed to nest predators (Clark and Wilson 1981, Hussell 1985). In both cases, but for different reasons, loss of some young to starvation is seen as the lesser of 2 evils, the greater being the loss of an entire brood. Regardless, environmentally driven hatching asynchrony that causes the loss of young can only be seen as a cost. A growing body of evidence indicates that incubation length and hatching asynchrony vary considerably both among and within populations of the same species, and that they are important for avian reproductive success (e.g., Briskie and Sealy 1989, Magrath 1989). Intrapopulation variation in incubation length among small birds with altricial young ranges from 3 to 4 days, but up to 5 to 6 (e.g., Martin et al. 2018, Sofaer et al. 2020) or more days (Higgott et al. 2020). Clutches of most altricial temperate-zone breeding species hatch within 1 (22.2%) or 2 days (51.8%) days, but 3 days is not uncommon (25.9%; data from Clark and Wilson 1981, plus Bancroft 1985, Smith 1988, Briskie and Sealy 1989, Ardia et al. 2006; n = 27 species), and is occasionally even longer (Lessells and Avery 1989, Beissinger and Waltman 1991). In addition to the potential influence of ambient temperature and precipitation on intraspecific variation in incubation length (Beissinger et al. 2005, Ardia et al. 2006, Nord et al. 2010, MacDonald et al. 2013, Higgott et al. 2020), longer incubation periods have been associated with both smaller (Feldheim 1997, Ardia et al. 2006, Higgott et al. 2020) and larger clutch size (Moreno and Carlson 1989, Magrath 1992, Engstrand and Bryant 2002, Arnold 2011), later seasonal breeding (Moreno and Carlson 1989, Magrath 1992, Veiga 1992, Feldheim 1997, Arnold 2011), and in some cases, larger egg size (Parsons 1972, Arnold 1993; but see Magrath 1992). Hatching asynchrony has been reported to increase with clutch size (Smith 1988, Briskie and Sealy 1989, Magrath 1992, Hébert and Sealy 1993) and late-season breeding (Bancroft 1985, Murphy and Fleischer 1986, Moreno and Carlson 1989, Murphy 1994), but the extent to which daily variation in weather is associated with hatching asynchrony is largely unknown (but see Ardia et al. 2006). Here, we describe intra- and interpopulation variation in incubation length and hatching asynchrony of Eastern Kingbirds (Tyrannus tyrannus; hereafter kingbirds). Kingbird incubation is potentially sensitive to ambient conditions because they are single-sex (female only) intermittent incubators without incubation feeding by males. Moreover, their open-cup nests are built on the edge of tree canopies (Murphy et al. 1997) where they are exposed to the elements when females leave the nest to forage. Our sites in Kansas (KS), New York (NY), and Oregon (OR), combined with extensive annual sampling in NY (13 years) and OR (10 years), allowed us to describe natural variation in incubation length and hatching asynchrony by birds exposed to a wide range of thermal conditions, and which we attempt to use to establish the extent to which female or environmentally based factors influence both traits. Our expectation, if inherent differences among females drive variation in incubation length and hatching asynchrony, is that both should be repeatable. We tested this possibility using a subset of banded females. We also tested for whether timing of breeding (i.e., date of first egg), clutch size, egg mass, or nest status (i.e., initial nests of the season or replacement nests produced after a failure) were sources of variation. Given that kingbird breeding date advances with age (Murphy 2004) and that early breeders have the highest seasonal reproductive success (Cooper et al. 2009), we assumed that the earliest breeders are the highest quality individuals and should have short incubation periods and low hatching asynchrony. Small clutches may be susceptible to more rapid cooling than nests with more eggs when females leave the nest to forage (Reid et al. 2000, 2002b), but large clutches may require more energy to reheat and/or be less efficiently incubated than smaller clutches that females can more effectively cover during incubation (Engstrand and Bryant 2002). Hence, we tested for a quadratic relationship between incubation length and clutch size to account for the possibility that incubation period of both small and large clutches may be prolonged, but anticipated greater hatching asynchrony among larger clutches based on previously reported results (see above). Large eggs lose heat less rapidly than small eggs (Hilton et al. 2004) and thus we also predicted clutches of small eggs would exhibit long incubation. Assuming again that female quality/condition influences incubation efficiency, we predicted that incubation length and hatching asynchrony would be greater in replacement nests because investment in building 2 nests and the production and care of an initial clutch could compromise a female’s capacity to incubate a later clutch or feed a second brood as effectively as her first. Separating intrinsic (i.e., female-based) and extrinsic (i.e., environmental) factors can be difficult, and laying date has an extrinsic component as well because of the steady seasonal increase in ambient temperature (see below) and insect food supplies (Murphy 1986). Hence, the hypothesis that extrinsic factors are primarily responsible for variation in incubation length and hatching asynchrony predicts a seasonal decline in incubation length, but an increase in hatching asynchrony to hasten hatching so that parents can fledge young in time to prepare for migration. If extrinsic factors underlie variation in incubation length and hatching asynchrony then conditions conducive to “ambient incubation” and embryonic development will yield shorter incubation periods and greater hatching asynchrony when ambient temperatures are high and precipitation low. Last, if hatching asynchrony is a “costly outcome” of environmental conditions that promote ambient incubation that enhances hatching asynchrony, we anticipated an increased frequency of starvation among clutches with high levels of hatching asynchrony, especially late in the season. METHODS Study Areas Research in NY included 1 year (1979) in western NY near Eden (Erie County) located southwest of Buffalo, NY (42.65°N, –78.90°W; 234 m.a.s.l. [meters above sea level) followed 10 years later with 12 years of research (1989–2000) in central NY near Oneonta (42.45°N, –75.06°W; 339 m.a.s.l.; Otsego County) and West Davenport (42.47°N, –74.84°W; 354 m.a.s.l.; Delaware County). The Oneonta and West Davenport study sites were separated by only ~10 km, birds dispersed between them, and thus we treated them as a single site. In addition, because the climates of the western and central NY study sites are so similar when compared to the other 2 sites, we combined the single year from western NY with the 12 years from central NY. The eastern KS study site (1980–1983) was located ~6.5 km west of Lawrence (Douglas County), north of Clinton Lake (38.94°N, –95.34°W; 264 m.a.s.l.). Ten years (2002–2011) of research were conducted in southeastern OR at Malheur National Wildlife Refuge (MNWR) in Harney County (42.97°N, –118.87°W; 1,279 m.a.s.l.). At all sites, habitats were primarily open grasslands/wetlands with scattered trees and either lacustrine or riparian zones. Climate is highly seasonal at all 3 sites (National Oceanic and Atmospheric Administration; http://www.yourweatherservice.com/) with annual low and high temperatures occurring in either December or January and July, respectively. Precipitation varies dramatically among sites. Although annual totals are very similar in NY (1,014 mm) and KS (1,028 mm), monthly totals are roughly equal in NY whereas precipitation in KS is highly seasonal with a strong peak in the first 2 months of the breeding season (May and June). MNWR, which is located in the Great Basin Desert, receives much less annual precipitation (277 mm), and excluding the month of May (during which few clutches are produced), the breeding season is the driest season of the year. Field Methods With the exception of the capture and banding of adults, the same methods were used in all years and locations and are detailed elsewhere (Murphy 2000, Redmond and Murphy 2012). Briefly, daily surveys for nests began by May as kingbirds return from migration beginning in early to middle May (Cooper et al. 2009). Once found, nest checks occurred at 1- to 3-day intervals, but more frequently during laying, hatching, and as fledging neared, which allowed documentation of the beginning and ending of egg-laying, clutch size, egg size, hatching dates, number of eggs to hatch, nest fate, and if successful, number of young to fledge. Adults and nestlings were banded (12–14 days of age) in NY and OR using 1 aluminum federal band and 3 colored plastic leg bands. Adults were captured using mist nets at either nests while feeding young, or in the case of males in OR, using song playback during the early morning dawn song period. In all years, except 2009, we measured maximum egg length (L) and width (W; to nearest 0.05 mm with dial calipers) at accessible nests, and for some eggs, mass (M) on the day of laying (to nearest 0.1 g; Pesola scale). Mass was estimated for eggs not weighed on the day of laying using the equation M = C × (L × W2), where C (0.545) was determined from eggs measured on the day of laying after rearrangement of the above equation (Murphy 1983). Kingbirds raise only a single brood per year, but ≥50% of nests fail annually due mainly to nest predation (~90% of nest failures; Murphy 1986, 2000, Murphy et al. 2020). Losses of young to starvation were indicated by poor nestling growth and/or the presence of dead nestlings in the nest. Most pairs that failed in their first attempt produced replacement clutches and we collected identical data for all replacement nests. Freshly hatched young have pink skin and wet and matted down (Murphy 1981); hatch date of nestlings in this condition was known with certainty. Nests were visited only once per day, and thus if on the day after the first hatchling appeared all eggs hatched and none appeared as fresh hatchlings we classified the nest as a synchronous hatch (i.e., all hatched in ≤24 hr). By contrast, if on the day after the hatching of the first egg a hatchling appeared as freshly hatched the nest was classified as asynchronous (≥2 days to hatch all young). If all eggs had not hatched by the second day, a visit was made on the third day to determine if the egg hatched. If it had, but the nestling was not “fresh” we assumed it hatched the previous day after our visit and that the entire clutch hatched within 2 days. However, if the new hatchling was fresh we recorded the nest as requiring 3 days to hatch. Incubation length was the number of days elapsed between the laying of the last egg and the appearance of the last hatchling (Nice 1954). Data Analysis Daily low and high temperature and daily precipitation for the breeding season at all sites were obtained from either NOAA’s National Centers for Environmental Information for permanent weather stations located near the NY and KS study sites, or from data provided by the Eastern Oregon Agricultural Research Center. We used the Buffalo Niagara International Airport (42.93°N, –78.73°W; 34 km from the center of study site) for the western NY site, and Cooperstown, NY (42.68°N, –74.92°W) for the central NY sites; both Oneonta and West Davenport were ~25 km from the weather station. In KS, data were obtained from the Topeka Regional Airport (38.95°N, –95.65°W; 28 km), while data for OR came from the P-Hill weather station located near Frenchglen, OR (42.83°N, –118.93°W; 1.5 km from the SW corner of our study site). To characterize the typical ambient temperatures faced by incubating females at all sites, we compared (analysis of variance) daily low, high, and mean ([low + high]/2) temperature for all days falling within the middle 90% of days during which eggs were in nests for all years of study at each site (KS: 1980–1983, 204 days; NY: 1989–2000, 648 days; OR: 2002–2011, 490 days). We then tallied the number of days when daily maximum temperature (A) exceeded presumptive physiological zero of embryos (26°C), (B) was at or above temperatures that could likely support embryo development due to “ambient incubation” (≥30°C), (C) fell within the optimal range for embryo development (36–40°C), or (D) reached temperatures that may detrimentally affect embryo development (>40°C). To allow direct visual comparisons (Figure 1), the midpoint of dates at sites was set to a value of zero by subtracting the absolute value of the midpoint (all dates counted continuously from May 1 = 1) from all other dates. Similarly, at each site, we subtracted the mean breeding date from the breeding date of individual clutches so that the mean breeding date was zero at all sites. Figure 1. Open in new tabDownload slide Variation in maximum daily temperature over the period of time eggs of Eastern Kingbirds were being incubated in Kansas (A), New York (B), and Oregon (C). Data are restricted to the middle 90% of the latter period at each site from 1980 to 1982 (Kansas), 1989 to 2000 (New York), and 2002 to 2011 (Oregon). Dates are standardized to a mean of zero at all sites to account for differences in breeding schedules. Horizontal lines represent presumed physiological zero for embryo development (26°C), moderate ambient temperatures above which cooling of unattended eggs would be slow (30°C), and optimal temperature for incubation (36–40°C). Figure 1. Open in new tabDownload slide Variation in maximum daily temperature over the period of time eggs of Eastern Kingbirds were being incubated in Kansas (A), New York (B), and Oregon (C). Data are restricted to the middle 90% of the latter period at each site from 1980 to 1982 (Kansas), 1989 to 2000 (New York), and 2002 to 2011 (Oregon). Dates are standardized to a mean of zero at all sites to account for differences in breeding schedules. Horizontal lines represent presumed physiological zero for embryo development (26°C), moderate ambient temperatures above which cooling of unattended eggs would be slow (30°C), and optimal temperature for incubation (36–40°C). Total number of nests found over the period of study was 2,237, but because nest failure was common and missing data existed for some variables, we conducted our analysis on nests that had little to no hatching failure and with complete information on laying dates, clutch size, hatching dates, number of eggs to hatch, and number of young to fledge (n = 342). One egg did not hatch in 40 of the 342 nests (11.7%), but for various reasons (e.g., egg had been marked by us or was distinctively colored) we were certain the unhatched egg was not the last egg laid. If it had been the last laid egg, and assuming hatching asynchrony was common, our expectation was that both incubation length and the time to hatch all eggs would be less in nests with unhatched eggs. Incubation length did not differ between nests that did or did not have hatching failure (t340 = 0.60, P = 0.552). After accounting for effects of clutch size on hatching duration (see below), there was no difference in time to hatch all eggs for nests in which eggs did (1.87 ± 0.029 days [SE], n = 302) or did not (1.99 ± 0.075 days, n = 40) all hatch (F1,339 = 2.35, P = 0.126). The 4 dependent variables in our analysis were (1) incubation length, (2) number of days to completely hatch the clutch (1, 2, or 3 days, with hatching asynchrony ≥2 days), (3) whether a brood experienced starvation, and (4) number of fledged young. Analysis of incubation length and hatching asynchrony included all nests that survived to hatching, while the occurrence of starvation and number of fledged young included all nests that survived to fledging. An expectation of the hypothesis that variation in incubation length and hatching asynchrony derive from intrinsic differences among females is that both are statistically repeatable. We therefore calculated repeatability (Lessells and Boag 1987) of both traits, along with breeding date (corrected for site differences in date), clutch size, and egg mass, for the 34 individually banded females with multiple nest records. The 34 females contributed 26% of the observations in our sample, but we chose to treat all cases of incubation length and the other response variables as independent observations because (A) no female contributed more than 1.4% to the data (and most with multiple years of data individually contributed only 0.6%), and (B) restricting the analyses to individually identifiable females would have eliminated the 253 nests produced by an unknown number of different females. Moreover, as shown below, incubation length and hatching asynchrony were not repeatable, indicating that each reproductive attempt by a female yielded unique information. We examined variation in incubation length in relation to date of laying, clutch size (as a quadratic function), nest status (i.e., first or replacement nest), and for the subset of nests with available data, egg mass. However, because phenological changes continue throughout the breeding season (e.g., vegetation changes and invertebrate prey populations grow), we acknowledge that date also has potential effects extrinsic to the female, which sets it apart from the potential influence that extrinsic factors such as ambient temperature and precipitation may have on reproduction. To quantify weather, daily low and high temperatures were averaged to yield the daily mean, while precipitation was treated as a binary variable based on whether measurable precipitation fell (“no” [0], or “yes” [1]; Higgott et al. 2020). To assess the importance of weather, we quantified temperature and precipitation during the egg-laying period (TempEgg-laying, RainEgg-laying), the first (Temp1stHalf, Rain2ndHalf) and second halves (Temp2ndHalf, Rain2ndHalf) of incubation, and for precipitation, the total period that eggs were in the nest (RainTotal). Precipitation was represented as the percentage of days during each period when rainfall was recorded (Higgott et al. 2020). As a priori observations indicated that kingbirds often begin incubation with the penultimate egg, we included the last day of egg-laying with Temp1stHalf and Rain1stHalf. We divided incubation into halves because it is common for birds to gradually increase incubation intensity over the first few days of incubation but then maintain high incubation intensity over the second half (Zerba and Morton 1983, Morton and Pereyra 1985, Wiebe et al. 1998, Wang and Beissinger 2009). If incubation length was an odd number of days the first half of incubation was the longer period. Hatching asynchrony was examined in relation to the same set of intrinsic (now also including incubation length) and extrinsic variables. Because of the potential importance of egg mass for incubation and hatching success (Kirst 2011), we omitted all nests lacking data on egg mass and reanalyzed the reduced data set (n = 281 nests) using identical procedures but with egg mass as an additional predictor variable for both incubation length and hatching asynchrony. To test the possibility that nestling starvation was associated with hatching asynchrony, we examined the probability of nestling starvation in relation to hatching asynchrony while accounting for possible effects of brood size, incubation length, laying date, and nest status. We conducted our analysis of incubation length using generalized linear models (GLMs). In all models, we treated site as a categorical factor, and as per our hypotheses, we included as additional predictors clutch size (as a quadratic), date, and to avoid overfitting models, each temperature variable paired to each of the 4 measures of precipitation (e.g., TempEgg-laying with RainEgg-laying, TempEgg-laying with Rain1stHalf, etc.). We did not enter date and nest status together because replacement nests were invariably produced later in the season than initial nests (t = 12.32, P < 0.001) and instead replaced date with nest status before rerunning all 12 models. All models within 2 AICc units (Akaike’s information criterion corrected for small sample size) of the top model were considered competitive. Hatching asynchrony was analyzed identically except that clutch size was entered as a linear term, and incubation length was included as an additional predictor. We then restricted our analyses to nests with data on egg mass, and reran our analyses of incubation length and hatching asynchrony with the same set of predictors. GLMs were run with distribution set as normal, and with an identity link function. Probability of nestling starvation was analyzed using GLMs but with distribution set as binomial (“no” [0], no nestling starved, or “yes” [1], ≥ 1 nestling starved). Brood size was included as a predictor variable, along with hatching asynchrony, because our expectation was that starvation was more likely to occur in nests with large broods and when hatching was highly asynchronous. Additional predictors included site and incubation length. Date and nest status were also included, but because of the strong covariation between them (see above), they were used in separate models. Number of young to starve was likewise examined using GLMs with the same set of variables as for probability that a nest experienced starvation, but with distribution set as normal. All statistical analyses were conducted using STATSTIX (analytical software v. 9) except for the GLMs which were run using JMP12. Statistics are reported as mean ± SE and n. RESULTS Site Differences in Climate and Reproduction Low, high, and mean ambient temperatures during the period when eggs were in the nest were greater in KS than at other sites (Table 1). Mean low temperature was lower in OR than NY, but mean maximum temperature was also greater in OR (Table 1, Figure 1). Consequently, mean daily temperature during the period when eggs were in the nest did not differ between NY and OR (Table 1) because of greater diel temperature variation in OR (20.6 ± 0.21°C) compared to NY (13.3 ± 0.18°C) and KS (11.9 ± 0.25°C; F2, 1,338 = 469.20, P < 0.001). Table 1. Comparison of average minimum, maximum, and mean ambient temperature (SE) among study sites during the middle 90% of the period during which eggs were being incubated. Averages sharing superscripted letters do not differ significantly (Tukey’s test). Also reported are the percentage of days during the same period during which ambient maximum temperature exceeded 26°C, 30°C, and 40°C, along with the percentage of days during which maximum ambient temperature fell within the optimal temperature range for incubation (36–40°C). Site . Ambient temperature (°C) . Percentage of days maximum temperature . . Minimum . Maximum . Mean . >26°C . >30°C . 36–40°C . >40°C . NY (648) 11.3 (0.18)b 24.6 (0.17)c 18.0 (0.15)b 41.7 8.0 0.0 0.0 KS (204) 18.5 (0.30)a 30.4 (0.36)a 24.4 (0.31)a 86.8 73.5 7.8 5.4 OR (490) 7.3 (0.18)c 27.9 (0.27)b 17.6 (0.20)b 64.1 39.8 4.3 0.6 Site . Ambient temperature (°C) . Percentage of days maximum temperature . . Minimum . Maximum . Mean . >26°C . >30°C . 36–40°C . >40°C . NY (648) 11.3 (0.18)b 24.6 (0.17)c 18.0 (0.15)b 41.7 8.0 0.0 0.0 KS (204) 18.5 (0.30)a 30.4 (0.36)a 24.4 (0.31)a 86.8 73.5 7.8 5.4 OR (490) 7.3 (0.18)c 27.9 (0.27)b 17.6 (0.20)b 64.1 39.8 4.3 0.6 Minimum: F = 478.47; Maximum: F = 124.34; Mean: F = 220.16, P < 0.001 for all. Open in new tab Table 1. Comparison of average minimum, maximum, and mean ambient temperature (SE) among study sites during the middle 90% of the period during which eggs were being incubated. Averages sharing superscripted letters do not differ significantly (Tukey’s test). Also reported are the percentage of days during the same period during which ambient maximum temperature exceeded 26°C, 30°C, and 40°C, along with the percentage of days during which maximum ambient temperature fell within the optimal temperature range for incubation (36–40°C). Site . Ambient temperature (°C) . Percentage of days maximum temperature . . Minimum . Maximum . Mean . >26°C . >30°C . 36–40°C . >40°C . NY (648) 11.3 (0.18)b 24.6 (0.17)c 18.0 (0.15)b 41.7 8.0 0.0 0.0 KS (204) 18.5 (0.30)a 30.4 (0.36)a 24.4 (0.31)a 86.8 73.5 7.8 5.4 OR (490) 7.3 (0.18)c 27.9 (0.27)b 17.6 (0.20)b 64.1 39.8 4.3 0.6 Site . Ambient temperature (°C) . Percentage of days maximum temperature . . Minimum . Maximum . Mean . >26°C . >30°C . 36–40°C . >40°C . NY (648) 11.3 (0.18)b 24.6 (0.17)c 18.0 (0.15)b 41.7 8.0 0.0 0.0 KS (204) 18.5 (0.30)a 30.4 (0.36)a 24.4 (0.31)a 86.8 73.5 7.8 5.4 OR (490) 7.3 (0.18)c 27.9 (0.27)b 17.6 (0.20)b 64.1 39.8 4.3 0.6 Minimum: F = 478.47; Maximum: F = 124.34; Mean: F = 220.16, P < 0.001 for all. Open in new tab Daily maximum temperature differed dramatically among sites (Table 1, Figure 1). Daily highs exceeded presumed physiological zero of embryos on 42% of days in NY, but roughly 1.5 and 2 times more often in OR and KS, respectively (Table 1, Figure 1). Likewise, temperatures conducive to “ambient incubation” (>30°C) occurred commonly in OR and especially KS, but infrequently in NY (Table 1, Figure 1). In NY, daily high temperature never fell within the optimal range (36–40°C) for avian incubation, but did so in OR and KS on 4.3% and 7.8% of days, respectively. Daily high temperature also exceeded that which is assumed to represent a potential threat to embryos (>40°C) on 5% of days in KS, but almost never elsewhere. Except for measures of nesting outcome, all reproductive variables differed among sites (Table 2). Breeding occurred later in OR compared to NY and KS (which did not differ), but clutch size was smaller in NY than at both other sites (which did not differ). Egg mass was smallest in KS and largest in OR (Table 2). Median incubation length was 15 days at all locations, and with the exception of one 18-day incubation period in OR, ranged everywhere from 13 to 17 days (Figure 2). Omitting the single 18-day incubation period, incubation length differed significantly among all sites, being shorter by half a day in KS compared to NY, with OR being intermediate (Table 2). Although modest, hatching asynchrony also differed among sites. Ignoring one nest in OR with a 5-day hatching spread, all sites exhibited the same median (2 days) and range (1–3 days; Figure 2), but the average number of days to fully hatch a clutch was 10.5% greater in OR compared to NY (KS intermediate; Table 2). By contrast, of nests that survived to fledge young, there were no site differences in number of young to fledge or starve, or either the percentage of young to starve or the percentage of nests to lose one or more nestlings to starvation (Table 2). Table 2. Comparisons of Eastern Kingbird reproduction from New York (1979, 1989–2000), Kansas (1980–1982), and Oregon (2002–2011). Comparisons of the number of young to fledge and the 3 measures of the intensity of nestling starvation were restricted to nests that survived to fledge young. Values are means ± SE with sample size of nests in parentheses. Breeding statistics that share uppercase superscripted letters did not differ significantly. Variable . Site . . . NY . KS . OR . F (P) . Breeding date June 9 ± 0.5 days (181)A June 6 ± 1.5 days (34)A June 21 ± 0.8 days (127)B 109.77 (<0.001) Clutch size 3.30 ± 0.04 eggs (181)B 3.62 ± 0.10 eggs (34)A 3.60 ± 0.05 eggs (127)A 12.11 (<0.001) Egg mass 4.06 ± 0.03 g (170)B 3.81 ± 0.05 g (32)C 4.29 ± 0.04 g (79)A 27.36 (<0.001) Incubation length 15.1 ± 0.05 days (181)A 14.6 ± 0.13 days (34)C 14.9 ± 0.06 days (127)B 9.82 (<0.001) Days to hatch 1.8 ± 0.04 days (181)B 1.9 ± 0.09 days (34)AB 2.0 ± 0.04 days (127)A 4.49 (0.012) Number fledged 2.8 ± 0.08 young (130) 2.9 ± 0.30 young (16) 3.0 ± 0.10 young (86) 0.84 (0.433) Number starved 0.2 ± 0.06 young (130) 0.3 ± 0.22 young (16) 0.2 ± 0.05 young (86) 0.00 (0.999)a Young starved (%) 6.7 ± 1.78 (130) 9.4 ± 6.80 (16) 5.0 ± 1.48 (86) 0.00 (0.999)a Nests with starvation (%) 13.6 ± 3.0 (130) 12.5 ± 8.54 (16) 13.8 ± 3.72 (86) 0.01 (0.990)a Variable . Site . . . NY . KS . OR . F (P) . Breeding date June 9 ± 0.5 days (181)A June 6 ± 1.5 days (34)A June 21 ± 0.8 days (127)B 109.77 (<0.001) Clutch size 3.30 ± 0.04 eggs (181)B 3.62 ± 0.10 eggs (34)A 3.60 ± 0.05 eggs (127)A 12.11 (<0.001) Egg mass 4.06 ± 0.03 g (170)B 3.81 ± 0.05 g (32)C 4.29 ± 0.04 g (79)A 27.36 (<0.001) Incubation length 15.1 ± 0.05 days (181)A 14.6 ± 0.13 days (34)C 14.9 ± 0.06 days (127)B 9.82 (<0.001) Days to hatch 1.8 ± 0.04 days (181)B 1.9 ± 0.09 days (34)AB 2.0 ± 0.04 days (127)A 4.49 (0.012) Number fledged 2.8 ± 0.08 young (130) 2.9 ± 0.30 young (16) 3.0 ± 0.10 young (86) 0.84 (0.433) Number starved 0.2 ± 0.06 young (130) 0.3 ± 0.22 young (16) 0.2 ± 0.05 young (86) 0.00 (0.999)a Young starved (%) 6.7 ± 1.78 (130) 9.4 ± 6.80 (16) 5.0 ± 1.48 (86) 0.00 (0.999)a Nests with starvation (%) 13.6 ± 3.0 (130) 12.5 ± 8.54 (16) 13.8 ± 3.72 (86) 0.01 (0.990)a aKruskal–Wallis test. Open in new tab Table 2. Comparisons of Eastern Kingbird reproduction from New York (1979, 1989–2000), Kansas (1980–1982), and Oregon (2002–2011). Comparisons of the number of young to fledge and the 3 measures of the intensity of nestling starvation were restricted to nests that survived to fledge young. Values are means ± SE with sample size of nests in parentheses. Breeding statistics that share uppercase superscripted letters did not differ significantly. Variable . Site . . . NY . KS . OR . F (P) . Breeding date June 9 ± 0.5 days (181)A June 6 ± 1.5 days (34)A June 21 ± 0.8 days (127)B 109.77 (<0.001) Clutch size 3.30 ± 0.04 eggs (181)B 3.62 ± 0.10 eggs (34)A 3.60 ± 0.05 eggs (127)A 12.11 (<0.001) Egg mass 4.06 ± 0.03 g (170)B 3.81 ± 0.05 g (32)C 4.29 ± 0.04 g (79)A 27.36 (<0.001) Incubation length 15.1 ± 0.05 days (181)A 14.6 ± 0.13 days (34)C 14.9 ± 0.06 days (127)B 9.82 (<0.001) Days to hatch 1.8 ± 0.04 days (181)B 1.9 ± 0.09 days (34)AB 2.0 ± 0.04 days (127)A 4.49 (0.012) Number fledged 2.8 ± 0.08 young (130) 2.9 ± 0.30 young (16) 3.0 ± 0.10 young (86) 0.84 (0.433) Number starved 0.2 ± 0.06 young (130) 0.3 ± 0.22 young (16) 0.2 ± 0.05 young (86) 0.00 (0.999)a Young starved (%) 6.7 ± 1.78 (130) 9.4 ± 6.80 (16) 5.0 ± 1.48 (86) 0.00 (0.999)a Nests with starvation (%) 13.6 ± 3.0 (130) 12.5 ± 8.54 (16) 13.8 ± 3.72 (86) 0.01 (0.990)a Variable . Site . . . NY . KS . OR . F (P) . Breeding date June 9 ± 0.5 days (181)A June 6 ± 1.5 days (34)A June 21 ± 0.8 days (127)B 109.77 (<0.001) Clutch size 3.30 ± 0.04 eggs (181)B 3.62 ± 0.10 eggs (34)A 3.60 ± 0.05 eggs (127)A 12.11 (<0.001) Egg mass 4.06 ± 0.03 g (170)B 3.81 ± 0.05 g (32)C 4.29 ± 0.04 g (79)A 27.36 (<0.001) Incubation length 15.1 ± 0.05 days (181)A 14.6 ± 0.13 days (34)C 14.9 ± 0.06 days (127)B 9.82 (<0.001) Days to hatch 1.8 ± 0.04 days (181)B 1.9 ± 0.09 days (34)AB 2.0 ± 0.04 days (127)A 4.49 (0.012) Number fledged 2.8 ± 0.08 young (130) 2.9 ± 0.30 young (16) 3.0 ± 0.10 young (86) 0.84 (0.433) Number starved 0.2 ± 0.06 young (130) 0.3 ± 0.22 young (16) 0.2 ± 0.05 young (86) 0.00 (0.999)a Young starved (%) 6.7 ± 1.78 (130) 9.4 ± 6.80 (16) 5.0 ± 1.48 (86) 0.00 (0.999)a Nests with starvation (%) 13.6 ± 3.0 (130) 12.5 ± 8.54 (16) 13.8 ± 3.72 (86) 0.01 (0.990)a aKruskal–Wallis test. Open in new tab Figure 2. Open in new tabDownload slide Variation in incubation length (above) and hatching asynchrony (below) for Eastern Kingbirds breeding in New York (n = 181 nests), Kansas (n = 34 nests), and Oregon (n = 127 nests). Figure 2. Open in new tabDownload slide Variation in incubation length (above) and hatching asynchrony (below) for Eastern Kingbirds breeding in New York (n = 181 nests), Kansas (n = 34 nests), and Oregon (n = 127 nests). Repeatability of Reproductive Traits Two to 5 years of data (mean = 2.6 ± 0.15 years) were available for banded females from NY (n = 13) and OR (n = 21). Breeding date was not repeatable (first nests of season only; r = 0.013, F27,70 = 1.03, P = 0.453), but clutch size (r = 0.348, F33,88 = 2.39, P = 0.002), egg mass (r = 0.699, F25,39 = 6.80, P < 0.001), and incubation length (r = 0.239, F33,88 = 1.82, P = 0.024) were. By contrast, hatching asynchrony (r = 0.040, F33,55 = 1.11, P = 0.360), number of young to fledge (r = 0.028, F33,85 = 1.07, P = 0.404), and number of young to starve (nests that did not fail due to predation or weather; r = 0.076, F21,30 = 0.82, P = 0.681) were not repeatable. Incubation length varied with clutch size (see below), and given the moderately high repeatability of clutch size, it seemed possible that repeatability of incubation length arose from its relationship with clutch size. After statistically accounting for effects of clutch size, incubation length no longer varied repeatably among females (F33,88 = 1.36, P = 0.157). Variation in Incubation Length The top model of the analysis of incubation length for all nests and only those nests with data on egg mass were qualitatively identical (Table 3). In both, incubation length was shorter in KS than NY, was shortest in intermediate-sized clutches of 3 and 4 eggs (Figure 3), but long in nests that experienced frequent rain while eggs were in the nest (RainTotal; Figure 4) and when temperatures during egg-laying (TempEgg-laying) were low (Figure 4). Incubation also tended to be longer in replacement nests. Egg mass was an uninformative variable as ∆AIC of the model with the above variables and egg mass was 1.782; thus, there was no association between incubation length and egg mass. The 3 other competitive models of incubation length for the full sample of nests were subsets of the top model that eliminated first TempEgg-laying, then nest status, and finally, both variables. The association of incubation length with site, the quadratic of clutch size, and RainTotal were unaffected by the progressive elimination of TempEgg-laying and nest status from the top model (Table 3). Table 3. Results of the generalized linear model analysis of variation in incubation length of Eastern Kingbirds breeding in Kansas (1980–1983), New York (1979, 1989–2000), and Oregon (2002–2011). Predictor variables included site, the quadratic of clutch size, either breeding date or nest status (first nest of the season or replacement nest), and each of 3 measures of ambient temperature (TempEgg-laying, Temp1stHalf, and Temp2ndHalf) combined in pairwise fashion with all 4 measures of precipitation (RainEgg-laying, Rain1stHalf, Rain2ndHalf, and RainTotal). The reported results are limited to models that were within 2 AICc units of the top model. Separate analyses were conducted for the full sample of nests (egg mass not included) and the subset of nests with information on egg mass. Egg mass was included in all of the latter analyses. Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests) Site – 2 14.139 <0.001 0.000  Clutch size –0.964 ± 0.366 1 6.865 0.009  Clutch size2 0.121 ± 0.054 1 5.032 0.025  RainTotal 0.866 ± 0.249 1 11.857 <0.001  Nest status 0.205 ± 0.111 1 3.387 0.066  TempEgg-laying –0.019 ± 0.010 1 3.161 0.075 Site – 2 18.957 <0.001 1.052  Clutch size –0.993 ± 0.367 1 7.226 0.007  Clutch size2 0.126 ± 0.054 1 5.418 0.020  RainTotal 0.927 ± 0.248 1 13.700 <0.001  Nest status 0.168 ± 0.109 1 2.337 0.126 Site – 2 13.012 0.002 1.277  Clutch size –0.954 ± 0.368 1 6.669 0.010  Clutch size2 0.116 ± 0.054 1 4.589 0.032  RainTotal 0.835 ± 0.250 1 10.983 <0.001  TempEgg-laying –0.015 ± 0.010 1 2.111 0.146 Site – 2 13.012 0.002 1.292  Clutch size –0.980 ± 0.368 1 7.000 0.008  Clutch size2 0.121 ± 0.054 1 4.975 0.026  RainTotal 0.891 ± 0.250 1 12.697 <0.001 Egg mass included (n = 281 nests) Site – 2 13.032 <0.001 0.000  Clutch size –1.036 ± 0.429 1 5.779 0.016  Clutch size2 0.139 ± 0.063 1 4.828 0.028  RainTotal 0.668 ± 0.254 1 6.849 0.009  Nest status 0.334 ± 0.123 1 7.315 0.007  TempEgg-laying –0.022 ± 0.011 1 4.208 0.040 Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests) Site – 2 14.139 <0.001 0.000  Clutch size –0.964 ± 0.366 1 6.865 0.009  Clutch size2 0.121 ± 0.054 1 5.032 0.025  RainTotal 0.866 ± 0.249 1 11.857 <0.001  Nest status 0.205 ± 0.111 1 3.387 0.066  TempEgg-laying –0.019 ± 0.010 1 3.161 0.075 Site – 2 18.957 <0.001 1.052  Clutch size –0.993 ± 0.367 1 7.226 0.007  Clutch size2 0.126 ± 0.054 1 5.418 0.020  RainTotal 0.927 ± 0.248 1 13.700 <0.001  Nest status 0.168 ± 0.109 1 2.337 0.126 Site – 2 13.012 0.002 1.277  Clutch size –0.954 ± 0.368 1 6.669 0.010  Clutch size2 0.116 ± 0.054 1 4.589 0.032  RainTotal 0.835 ± 0.250 1 10.983 <0.001  TempEgg-laying –0.015 ± 0.010 1 2.111 0.146 Site – 2 13.012 0.002 1.292  Clutch size –0.980 ± 0.368 1 7.000 0.008  Clutch size2 0.121 ± 0.054 1 4.975 0.026  RainTotal 0.891 ± 0.250 1 12.697 <0.001 Egg mass included (n = 281 nests) Site – 2 13.032 <0.001 0.000  Clutch size –1.036 ± 0.429 1 5.779 0.016  Clutch size2 0.139 ± 0.063 1 4.828 0.028  RainTotal 0.668 ± 0.254 1 6.849 0.009  Nest status 0.334 ± 0.123 1 7.315 0.007  TempEgg-laying –0.022 ± 0.011 1 4.208 0.040 Open in new tab Table 3. Results of the generalized linear model analysis of variation in incubation length of Eastern Kingbirds breeding in Kansas (1980–1983), New York (1979, 1989–2000), and Oregon (2002–2011). Predictor variables included site, the quadratic of clutch size, either breeding date or nest status (first nest of the season or replacement nest), and each of 3 measures of ambient temperature (TempEgg-laying, Temp1stHalf, and Temp2ndHalf) combined in pairwise fashion with all 4 measures of precipitation (RainEgg-laying, Rain1stHalf, Rain2ndHalf, and RainTotal). The reported results are limited to models that were within 2 AICc units of the top model. Separate analyses were conducted for the full sample of nests (egg mass not included) and the subset of nests with information on egg mass. Egg mass was included in all of the latter analyses. Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests) Site – 2 14.139 <0.001 0.000  Clutch size –0.964 ± 0.366 1 6.865 0.009  Clutch size2 0.121 ± 0.054 1 5.032 0.025  RainTotal 0.866 ± 0.249 1 11.857 <0.001  Nest status 0.205 ± 0.111 1 3.387 0.066  TempEgg-laying –0.019 ± 0.010 1 3.161 0.075 Site – 2 18.957 <0.001 1.052  Clutch size –0.993 ± 0.367 1 7.226 0.007  Clutch size2 0.126 ± 0.054 1 5.418 0.020  RainTotal 0.927 ± 0.248 1 13.700 <0.001  Nest status 0.168 ± 0.109 1 2.337 0.126 Site – 2 13.012 0.002 1.277  Clutch size –0.954 ± 0.368 1 6.669 0.010  Clutch size2 0.116 ± 0.054 1 4.589 0.032  RainTotal 0.835 ± 0.250 1 10.983 <0.001  TempEgg-laying –0.015 ± 0.010 1 2.111 0.146 Site – 2 13.012 0.002 1.292  Clutch size –0.980 ± 0.368 1 7.000 0.008  Clutch size2 0.121 ± 0.054 1 4.975 0.026  RainTotal 0.891 ± 0.250 1 12.697 <0.001 Egg mass included (n = 281 nests) Site – 2 13.032 <0.001 0.000  Clutch size –1.036 ± 0.429 1 5.779 0.016  Clutch size2 0.139 ± 0.063 1 4.828 0.028  RainTotal 0.668 ± 0.254 1 6.849 0.009  Nest status 0.334 ± 0.123 1 7.315 0.007  TempEgg-laying –0.022 ± 0.011 1 4.208 0.040 Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests) Site – 2 14.139 <0.001 0.000  Clutch size –0.964 ± 0.366 1 6.865 0.009  Clutch size2 0.121 ± 0.054 1 5.032 0.025  RainTotal 0.866 ± 0.249 1 11.857 <0.001  Nest status 0.205 ± 0.111 1 3.387 0.066  TempEgg-laying –0.019 ± 0.010 1 3.161 0.075 Site – 2 18.957 <0.001 1.052  Clutch size –0.993 ± 0.367 1 7.226 0.007  Clutch size2 0.126 ± 0.054 1 5.418 0.020  RainTotal 0.927 ± 0.248 1 13.700 <0.001  Nest status 0.168 ± 0.109 1 2.337 0.126 Site – 2 13.012 0.002 1.277  Clutch size –0.954 ± 0.368 1 6.669 0.010  Clutch size2 0.116 ± 0.054 1 4.589 0.032  RainTotal 0.835 ± 0.250 1 10.983 <0.001  TempEgg-laying –0.015 ± 0.010 1 2.111 0.146 Site – 2 13.012 0.002 1.292  Clutch size –0.980 ± 0.368 1 7.000 0.008  Clutch size2 0.121 ± 0.054 1 4.975 0.026  RainTotal 0.891 ± 0.250 1 12.697 <0.001 Egg mass included (n = 281 nests) Site – 2 13.032 <0.001 0.000  Clutch size –1.036 ± 0.429 1 5.779 0.016  Clutch size2 0.139 ± 0.063 1 4.828 0.028  RainTotal 0.668 ± 0.254 1 6.849 0.009  Nest status 0.334 ± 0.123 1 7.315 0.007  TempEgg-laying –0.022 ± 0.011 1 4.208 0.040 Open in new tab Figure 3. Open in new tabDownload slide Mean incubation length (±SE) vs. clutch size of Eastern Kingbirds for birds breeding in New York, Kansas, and Oregon. Clutch sizes sharing letters (above SE) did not differ significantly. Sample sizes are 13, 169, 156, and 4 for clutches of 2, 3, 4, and 5, respectively. Figure 3. Open in new tabDownload slide Mean incubation length (±SE) vs. clutch size of Eastern Kingbirds for birds breeding in New York, Kansas, and Oregon. Clutch sizes sharing letters (above SE) did not differ significantly. Sample sizes are 13, 169, 156, and 4 for clutches of 2, 3, 4, and 5, respectively. Figure 4. Open in new tabDownload slide Incubation length of Eastern Kingbirds breeding in New York, Kansas, and Oregon in relation to variation in ambient temperature during the egg-laying period (top frame: r = –0.153, P = 0.004) and the percentage of days on which measurable rain fell during the entire period eggs were in the nest (bottom frame: r = 0.192, P < 0.001). Figure 4. Open in new tabDownload slide Incubation length of Eastern Kingbirds breeding in New York, Kansas, and Oregon in relation to variation in ambient temperature during the egg-laying period (top frame: r = –0.153, P = 0.004) and the percentage of days on which measurable rain fell during the entire period eggs were in the nest (bottom frame: r = 0.192, P < 0.001). Hatching Asynchrony Our analyses of variation in hatching asynchrony for the full sample of nests and the subset with egg data both yielded 2 competitive models. In all 4, hatching asynchrony was greater in nests with large clutches and when clutches experienced low RainEgg-laying and high Temp1stHalf (Table 4). Within the full sample of nests, asynchrony was also greater when incubation was long, and as suggested by the top model, in replacement nests (Table 4). Greater hatching asynchrony in the subset of nests with egg mass was associated with larger average egg mass in both competitive models, and in the top model, hatching asynchrony tended to be shorter in NY than the other sites (Table 4). Table 4. Results of the generalized linear model analysis of variation in hatching asynchrony of Eastern Kingbirds breeding in Kansas (1980–1983), New York (1979, 1989–2000), and Oregon (2002–2011). Predictor variables included site, clutch size, incubation length, either breeding date or nest status (first nest of the season or replacement nest), and each of 3 measures of ambient temperature (TempEgg-laying, Temp1stHalf, and Temp2ndHalf) combined in pairwise fashion with all 4 measures of precipitation (RainEgg-laying, Rain1stHalf, Rain2ndHalf, and RainTotal). The reported results are limited to models that were within 2 AICc units of the top model. Separate analyses were conducted for the full sample of nests (egg mass not included) and the subset of nests with information on egg mass. Egg mass was included in all of the latter analyses. Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests)  Clutch size 0.312 ± 0.043 1 48.319 <0.001 0.000  RainEgg-laying –0.279 ± 0.074 1 13.754 <0.001  Temp1stHalf 0.020 ± 0.009 1 4.533 0.033  Incubation length 0.081 ± 0.036 1 4.958 0.026  Nest status 0.117 ± 0.076 1 2.365 0.124  Clutch size 0.303 ± 0.043 1 46.204 <0.001 0.280  RainEgg-laying –0.289 ± 0.074 1 14.801 <0.001  Temp1stHalf 0.024 ± 0.009 1 7.155 0.008  Incubation length 0.085 ± 0.036 1 5.512 0.019 Egg mass included (n = 281 nests) Site – 2 4.983 0.083 0.000  Clutch size 0.380 ± 0.049 1 54.190 <0.001  RainEgg-laying –0.276 ± 0.084 1 10.563 0.001  Temp1stHalf 0.044 ± 0.012 1 12.418 <0.001  Egg mass 0.179 ± 0.084 1 4.516 0.034  Clutch size 0.342 ± 0.046 1 49.431 <0.001 0.761  RainEgg-laying –0.255 ± 0.082 1 9.472 0.002  Temp1stHalf 0.0294 ± 0.010 1 8.342 0.004  Egg mass 0.164 ± 0.079 1 4.306 0.038 Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests)  Clutch size 0.312 ± 0.043 1 48.319 <0.001 0.000  RainEgg-laying –0.279 ± 0.074 1 13.754 <0.001  Temp1stHalf 0.020 ± 0.009 1 4.533 0.033  Incubation length 0.081 ± 0.036 1 4.958 0.026  Nest status 0.117 ± 0.076 1 2.365 0.124  Clutch size 0.303 ± 0.043 1 46.204 <0.001 0.280  RainEgg-laying –0.289 ± 0.074 1 14.801 <0.001  Temp1stHalf 0.024 ± 0.009 1 7.155 0.008  Incubation length 0.085 ± 0.036 1 5.512 0.019 Egg mass included (n = 281 nests) Site – 2 4.983 0.083 0.000  Clutch size 0.380 ± 0.049 1 54.190 <0.001  RainEgg-laying –0.276 ± 0.084 1 10.563 0.001  Temp1stHalf 0.044 ± 0.012 1 12.418 <0.001  Egg mass 0.179 ± 0.084 1 4.516 0.034  Clutch size 0.342 ± 0.046 1 49.431 <0.001 0.761  RainEgg-laying –0.255 ± 0.082 1 9.472 0.002  Temp1stHalf 0.0294 ± 0.010 1 8.342 0.004  Egg mass 0.164 ± 0.079 1 4.306 0.038 Open in new tab Table 4. Results of the generalized linear model analysis of variation in hatching asynchrony of Eastern Kingbirds breeding in Kansas (1980–1983), New York (1979, 1989–2000), and Oregon (2002–2011). Predictor variables included site, clutch size, incubation length, either breeding date or nest status (first nest of the season or replacement nest), and each of 3 measures of ambient temperature (TempEgg-laying, Temp1stHalf, and Temp2ndHalf) combined in pairwise fashion with all 4 measures of precipitation (RainEgg-laying, Rain1stHalf, Rain2ndHalf, and RainTotal). The reported results are limited to models that were within 2 AICc units of the top model. Separate analyses were conducted for the full sample of nests (egg mass not included) and the subset of nests with information on egg mass. Egg mass was included in all of the latter analyses. Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests)  Clutch size 0.312 ± 0.043 1 48.319 <0.001 0.000  RainEgg-laying –0.279 ± 0.074 1 13.754 <0.001  Temp1stHalf 0.020 ± 0.009 1 4.533 0.033  Incubation length 0.081 ± 0.036 1 4.958 0.026  Nest status 0.117 ± 0.076 1 2.365 0.124  Clutch size 0.303 ± 0.043 1 46.204 <0.001 0.280  RainEgg-laying –0.289 ± 0.074 1 14.801 <0.001  Temp1stHalf 0.024 ± 0.009 1 7.155 0.008  Incubation length 0.085 ± 0.036 1 5.512 0.019 Egg mass included (n = 281 nests) Site – 2 4.983 0.083 0.000  Clutch size 0.380 ± 0.049 1 54.190 <0.001  RainEgg-laying –0.276 ± 0.084 1 10.563 0.001  Temp1stHalf 0.044 ± 0.012 1 12.418 <0.001  Egg mass 0.179 ± 0.084 1 4.516 0.034  Clutch size 0.342 ± 0.046 1 49.431 <0.001 0.761  RainEgg-laying –0.255 ± 0.082 1 9.472 0.002  Temp1stHalf 0.0294 ± 0.010 1 8.342 0.004  Egg mass 0.164 ± 0.079 1 4.306 0.038 Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests)  Clutch size 0.312 ± 0.043 1 48.319 <0.001 0.000  RainEgg-laying –0.279 ± 0.074 1 13.754 <0.001  Temp1stHalf 0.020 ± 0.009 1 4.533 0.033  Incubation length 0.081 ± 0.036 1 4.958 0.026  Nest status 0.117 ± 0.076 1 2.365 0.124  Clutch size 0.303 ± 0.043 1 46.204 <0.001 0.280  RainEgg-laying –0.289 ± 0.074 1 14.801 <0.001  Temp1stHalf 0.024 ± 0.009 1 7.155 0.008  Incubation length 0.085 ± 0.036 1 5.512 0.019 Egg mass included (n = 281 nests) Site – 2 4.983 0.083 0.000  Clutch size 0.380 ± 0.049 1 54.190 <0.001  RainEgg-laying –0.276 ± 0.084 1 10.563 0.001  Temp1stHalf 0.044 ± 0.012 1 12.418 <0.001  Egg mass 0.179 ± 0.084 1 4.516 0.034  Clutch size 0.342 ± 0.046 1 49.431 <0.001 0.761  RainEgg-laying –0.255 ± 0.082 1 9.472 0.002  Temp1stHalf 0.0294 ± 0.010 1 8.342 0.004  Egg mass 0.164 ± 0.079 1 4.306 0.038 Open in new tab Nestling Starvation The probability that a nest experienced starvation was greatest in nests in which incubation was long and brood size large (Table 5). And although trending in the predicted direction of increasing likelihood of starvation with greater hatching asynchrony (Figure 5), hatching asynchrony was an uninformative variable (sensuArnold 2010) and the combination of incubation length, brood size, and hatching asynchrony was therefore not a competitive model (Table 5). All other combination of variables with incubation length and brood size produced models with ΔAICc ≥ 3.714. Predictably, the number of young fledged increased with brood size, and the only apparent competitive models included either incubation length or hatching asynchrony (Table 5). However, both variables were also uninformative (sensuArnold 2010). Moreover, neither hatching asynchrony (Figure 5) nor incubation length contributed significantly to variation in number of young fledged. Hence, hatching asynchrony did not influence the likelihood that a nest would experience starvation or affect the number of young fledged. Table 5. Results of the generalized linear model analysis of variation in the probability that a nest experienced starvation and number of young fledged/successful nest by Eastern Kingbirds breeding in Kansas (1980–1983), New York (1979, 1989–2000), and Oregon (2002–2011). Predictor variables included site, hatching asynchrony, brood size, incubation length, and either breeding date or nest status (first nest of the season or replacement nest. Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Probability that a nest experienced starvation  Incubation length 0.810 ± 0.290 1 8.777 0.003 0.000  Brood size 0.756 ± 0.322 1 6.107 0.014  Incubation length 0.785 ± 0.284 1 7.974 0.005 1.831  Brood size 0.756 ± 0.322 1 6.107 0.014  Hatching asynchrony 0.192 ± 0.392 1 0.240 0.624 Number of young to fledge  Brood size 0.784 ± 0.076 1 87.955 <0.001 0.000  Brood size 0.773 ± 0.076 1 85.293 <0.001 0.485  Incubation length –0.087 ± 0.069 1 1.587 0.208  Brood size 0.797 ± 0.079 1 84.970 <0.001 1.710  Hatching asynchrony –0.062 ± 0.103 1 0.361 0.548 Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Probability that a nest experienced starvation  Incubation length 0.810 ± 0.290 1 8.777 0.003 0.000  Brood size 0.756 ± 0.322 1 6.107 0.014  Incubation length 0.785 ± 0.284 1 7.974 0.005 1.831  Brood size 0.756 ± 0.322 1 6.107 0.014  Hatching asynchrony 0.192 ± 0.392 1 0.240 0.624 Number of young to fledge  Brood size 0.784 ± 0.076 1 87.955 <0.001 0.000  Brood size 0.773 ± 0.076 1 85.293 <0.001 0.485  Incubation length –0.087 ± 0.069 1 1.587 0.208  Brood size 0.797 ± 0.079 1 84.970 <0.001 1.710  Hatching asynchrony –0.062 ± 0.103 1 0.361 0.548 Open in new tab Table 5. Results of the generalized linear model analysis of variation in the probability that a nest experienced starvation and number of young fledged/successful nest by Eastern Kingbirds breeding in Kansas (1980–1983), New York (1979, 1989–2000), and Oregon (2002–2011). Predictor variables included site, hatching asynchrony, brood size, incubation length, and either breeding date or nest status (first nest of the season or replacement nest. Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Probability that a nest experienced starvation  Incubation length 0.810 ± 0.290 1 8.777 0.003 0.000  Brood size 0.756 ± 0.322 1 6.107 0.014  Incubation length 0.785 ± 0.284 1 7.974 0.005 1.831  Brood size 0.756 ± 0.322 1 6.107 0.014  Hatching asynchrony 0.192 ± 0.392 1 0.240 0.624 Number of young to fledge  Brood size 0.784 ± 0.076 1 87.955 <0.001 0.000  Brood size 0.773 ± 0.076 1 85.293 <0.001 0.485  Incubation length –0.087 ± 0.069 1 1.587 0.208  Brood size 0.797 ± 0.079 1 84.970 <0.001 1.710  Hatching asynchrony –0.062 ± 0.103 1 0.361 0.548 Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Probability that a nest experienced starvation  Incubation length 0.810 ± 0.290 1 8.777 0.003 0.000  Brood size 0.756 ± 0.322 1 6.107 0.014  Incubation length 0.785 ± 0.284 1 7.974 0.005 1.831  Brood size 0.756 ± 0.322 1 6.107 0.014  Hatching asynchrony 0.192 ± 0.392 1 0.240 0.624 Number of young to fledge  Brood size 0.784 ± 0.076 1 87.955 <0.001 0.000  Brood size 0.773 ± 0.076 1 85.293 <0.001 0.485  Incubation length –0.087 ± 0.069 1 1.587 0.208  Brood size 0.797 ± 0.079 1 84.970 <0.001 1.710  Hatching asynchrony –0.062 ± 0.103 1 0.361 0.548 Open in new tab Figure 5. Open in new tabDownload slide Variation (mean ± SE) in the percentage of nests to experience starvation (white bars) and number of young to fledge (gray bar) in relation to degree of hatching asynchrony for nests of Eastern Kingbirds from New York, Kansas, and Oregon that survived to fledge young. Figure 5. Open in new tabDownload slide Variation (mean ± SE) in the percentage of nests to experience starvation (white bars) and number of young to fledge (gray bar) in relation to degree of hatching asynchrony for nests of Eastern Kingbirds from New York, Kansas, and Oregon that survived to fledge young. DISCUSSION We found that both incubation length and hatching asynchrony of Eastern Kingbirds varied geographically, that neither trait was individually repeatable, and that both varied with ambient temperature and precipitation. Indeed, although geographic differences in incubation length (NY > KS) might be related to unmeasured variables such as food supply (which might affect female incubation behavior), we suspect that site differences were almost certainly driven by climatic differences among sites (Figure 1). We also found that intermediate-size clutches appeared to require the fewest days to complete incubation, and as predicted, hatching asynchrony increased with clutch size. However, our data did not support the hypothesis that increased nestling starvation was a cost of hatching asynchrony. While repeatability of egg size, clutch size, and laying date among birds is well documented (Christians 2002), to our knowledge, we are only the second (see Higgott et al. 2020) to test for the repeatability of incubation length, and the first to test for the repeatability of hatching asynchrony. Neither was repeatable, but for incubation length, this was dependent on establishing that clutch size was highly repeatable and that an apparent association of variation of incubation length with different females arose from the dependence of incubation length on clutch size. Higgott et al. (2020) likewise showed that incubation length was not repeatable in Long-tailed Tits (Aegithalos caduatus). Repeatability represents a potential upper limit to the heritability of a trait (Falconer and Mackay 1996), and given probable strong selection to minimize length of exposure to nest predators (Remeš 2007), which is the main source of nest loss in both kingbirds and Long-tailed Tits (Higgott et al. 2020), minimal heritable variation in either trait is expected (Falconer and Mackay 1996). Incubation length for most female kingbirds was 15 days, and the allometrically predicted (Birchard and Deeming 2015) length, based on mean egg mass for these populations (Table 2), was longer (15.5–16.0 days) than the observed mean (≤15.1 days). Thus, the absence of repeatable variation in incubation length and shorter than predicted incubation periods suggest past strong selection to reduce time in incubation. Nonetheless, incubation length ranged from 13 to 17 days. Clutch size was the only female trait that contributed consistently to variation in incubation length, except possibly for nest status; incubation length was longer in replacement nests in the subset of nests with egg mass, suggesting a possible negative carryover effect from the first attempt. Much if not most of the existing variation in incubation length seems more likely driven by environmental factors, namely daily variation in ambient temperature and precipitation. Admittedly, our analyses did not account for most of the variation in either trait, but we strongly suspect this was a consequence of, given the distances between nests and weather stations, the coarseness of our metrics of daily weather. Negative effects of low ambient temperature on incubation length are known (e.g., Ardia et al. 2006, Vincze et al. 2016), but much less studied is the potential impact of precipitation (but see Higgott et al. 2020). The frequent wetting of nests from rainfall, and consequent increase in nest thermal conductance (Reid et al. 2002a, Hilton et al. 2004), likely causes rapid heat loss from eggs. We thus predicted longer incubation periods during periods of frequent rain, and indeed, longer incubation periods were associated with both low temperatures and frequent rain. However, an equally likely alternative explanation, given that male kingbirds neither share in incubation duties nor feed incubating females, and that low temperatures and precipitation reduce the availability of flying insects for aerial foraging birds such as kingbirds (Bryant 1975, Davies 1977, Järvinen and Väisänen 1984, Nooker et al. 2005), is that the extended incubation associated with low temperature and frequent precipitation arose from the need for females to remain off the nest longer to meet energy requirements. Indeed, it seems likely that the 2 effects may act additively. Predicted incubation length, based on results of our regression analyses, for 2 and 5 egg clutches at the lowest TempEgg-laying and highest RainTotal were 16.0 and 15.5 days, respectively. Comparable figures under the best of conditions for those same periods predicted incubation periods of 14.6 and 14.4 days, respectively, for clutches of 3 and 4 eggs. Thus, the combination of clutch size and daily weather appears to account for nearly a third of the range of variation in incubation length (1.6 days/5 days = 0.32). Given that nest construction, including materials of variable insulative value (Hilton et al. 2004), is likely to affect heat loss (Windsor et al. 2013, Rohwer et al. 2015), we suggest it likely that a significant portion of the remaining variation is attributable to microclimatic differences among nests and differences in nest quality. Although our limited sample of 5-egg clutches urges caution in concluding that the largest clutches are inherently disadvantaged by a long incubation, such results are not unprecedented (Moreno and Carlson 1989, Magrath 1992, Engstrand and Bryant 2002, Arnold 2011). Why incubation length was shortest for intermediate-sized clutches is potentially explained by several hypotheses, none of which can be eliminated with our data. For 2-egg clutches, incubation may have been long because of the low thermal inertia and greater rate of heat loss from eggs in small clutches when females were off the nest feeding (e.g., Reid et al. 2000, 2002b). Extrinsic to the clutch itself, and assuming that small clutches are typical of either low-quality females or occupation of a low-quality habitat, such females may have had lower average egg temperatures because of their need to spend more time off the nest feeding. The long incubation length of large clutches was potentially a consequence of greater energy demand of keeping more eggs warm (Ardia et al. 2006), and consequent lower average egg temperature (Nord et al. 2010). Equally likely, larger clutches may have taken longer to incubate because of low efficiency of incubation (e.g., Engstrand and Bryant 2002). Clutches of 5 eggs are uncommon to rare in all kingbird populations (M. T. Murphy, personal communication), and brood patches may have evolved for optimal incubation of the intermediate-sized clutches that comprise >90% of all kingbird reproductive attempts. A third possibility, given that hatching asynchrony increased with clutch size, is the need to provide food for hatchlings may have caused female “neglect” of last laid eggs, leading to delayed hatching. Hatching asynchrony is widespread and the proposed explanations for why incubation is usually initiated with the penultimate egg in north temperate breeding birds (Clark and Wilson 1981) are numerous (Stoleson and Beissinger 1995). Our intent was not to test alternative hypotheses, but instead, we sought to describe potential geographic differences in hatching patterns, identify sources of variation, and assess whether hatching asynchrony was costly (i.e., greater nestling starvation). The 2 days required to hatch most kingbird clutches at all sites is common among north temperate breeding passerines, but the 3 days required for some broods (7.6% of total) is less common. Hatching asynchrony increased with clutch size, as found in other species (Smith 1988, Briskie and Sealy 1989, Magrath 1992, Hébert and Sealy 1993), and the significant site differences in kingbird hatching asynchrony (NY < OR) that emerged from the univariate analyses were likely attributable to geographic differences in clutch size (OR > NY) and weather (Table 4). Contrary to some (Bancroft 1985, Murphy and Fleischer 1986, Moreno and Carlson 1989, Magrath 1992, Murphy 1994) we did not find that hatching asynchrony was more common later in the breeding season. Nor did there appear to be a carryover effect from first to replacement nest as hatching asynchrony did not differ between them. On the other hand, we found, as have a few others (Veiga 1992, Ardia et al. 2006, Griffith et al. 2016), a greater degree of hatching asynchrony when clutches experienced higher ambient temperatures early in incubation. Revealingly, hatching asynchrony was also greater in nests that experienced dry conditions during egg-laying, the exact period when staggered development is likely established. The higher thermal conductivity of wet nests would compromise a female’s ability to maintain the higher egg temperatures needed to induce developmental differences among embryos (Hilton et al. 2004). However, an alternative explanation again exists because we cannot rule out the possibility that, regardless of the nest’s thermal environment, drier and warmer conditions during these periods allowed females to begin and maintain incubation in earnest earlier in the egg-laying and incubation periods, respectively (see Ardia et al. 2006). Regardless, the degree of hatching asynchrony, while possibly being a female strategy to maximize offspring production (Lack 1968, Clark and Wilson 1981), was in part a product of the ambient thermal conditions. Why large eggs would be associated with greater hatching asynchrony is unclear. Repeatability of egg size of kingbirds is particularly high (see above and Murphy 2004), and one possible explanation for the positive association of egg size and hatching asynchrony is that higher quality females may produce large eggs, and these same high-quality females may be able to also initiate incubation earlier than other females (e.g., Grimaudo et al. 2020). Importantly, although a tendency existed for an increased likelihood of starvation as hatching asynchrony increased (Figure 5), it was not significant and the number of young fledged was independent of hatching asynchrony (Figure 5). Hence, regardless of the age disparities of young, above-average hatching asynchrony did not appear to be costly to parental fitness. The question of why broods are usually hatched asynchronously (81% of broods) remains, but the facts that most nests fail because of nest predators (Murphy 1986, 2000, Murphy et al. 2020), and nestling starvation was uncommon (only 6.2% of young in nests that survived to fledging), casts doubt on the hypothesis that hatching asynchrony evolved as a strategy to bring brood size in line with current food supplies (Lack 1968). SUMMARY Our attempts to determine whether variation in incubation length and hatching asynchrony derive mainly from properties intrinsic to females or the extrinsic environment suggest that the latter is likely the dominant influence for incubation length. Hatching asynchrony, as in other species (e.g., Gilby et al. 2013), is probably primarily under female control but ambient temperature and precipitation may dampen or heighten its expression. Given the dramatic differences in ambient temperature (Figure 1) and precipitation among sites, it seems surprising that even larger differences in incubation length and possibly hatching asynchrony were not recorded, especially since our analyses ignored all aspects of nest exposure to solar radiation and wind, the former of which is likely to exacerbate high-temperature effects for kingbird nests that are frequently placed on the canopy edge of trees and fully exposed to the sun (Murphy et al. 1997). This attests to the importance of female behavior and possibly also to selection of nest microhabitats and insulative properties of nests (e.g., Crossman et al. 2011, Windsor et al. 2013, Rohwer et al. 2015). Much additional work is needed to reveal the proximate mechanisms, including potentially female incubation rhythms (Rohwer and Purcell 2019), but also nest site choice, nest properties, clutch size, and egg size and composition, used by females to successfully bring eggs through incubation to hatch in the face of often extreme physical challenges. ACKNOWLEDGMENTS We would like to thank the numerous private landowners in Kansas and New York who granted permission to work on their land, and the staff of Malheur National Wildlife Refuge and the Malheur Field Station for their support. David Bohnert of Oregon State University and the Eastern Oregon Agricultural Research Center provided access to weather data. Helpful comments on an earlier version were provided by Nathan W. Cooper, Daniel R. Ardia, and 2 anonymous reviewers. Funding statement: Research was supported by grants from the U.S. National Science Foundation to MTM (BSR-9106854 and IOB-0539370), an NSERC grant from the Canadian Government, and additional student grants provided by the Forbes-Lea Fund of Portland State University, the E. Alexander Bergstrom Memorial Research Award of the Association of Field Ornithologists, the Frank M. Chapman Fund from the American Museum of Natural History, the American Ornithologists’ Union Student Research Fund, and the Association for the Study of Animal Behaviour. Ethics statement: All capture, handling, and banding of birds were conducted under USGS permit number 22230 of MTM, while permission to conduct research in Oregon at Malheur National Wildlife Refuge was through permits to MTM (13570-030117, 13570-060205, 13570-06008). Research at other locations was conducted with the permission of private landowners. 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Variation in incubation length and hatching asynchrony in Eastern Kingbirds: Weather eclipses female effects

Ornithology , Volume Advance Article – May 18, 2021

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10.1093/ornithology/ukab031
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Abstract

Abstract Incubation length and hatching asynchrony are integral elements of the evolved reproductive strategies of birds. We examined intra- and interpopulation variation in both traits for Eastern Kingbird (Tyrannus tyrannus) populations from New York (NY), Kansas (KS), and Oregon (OR) and found that both incubation length and hatching asynchrony were not repeatable among females, after controlling for a repeatable trait, clutch size. Instead, incubation length and clutch size were influenced by ambient temperature and precipitation. Incubation length exhibited the same median (15 days) and range (13–17 days) at all sites. Model selection results indicated that incubation periods for the smallest and largest clutches were longer in NY than KS when rain was frequent throughout incubation, in replacement nests, and likely when ambient temperatures were low during egg-laying. Full hatching usually required 2 days (but up to 3), with synchronous hatching associated with small clutch sizes, short incubation periods, frequent rain during the egg-laying period, and low ambient temperatures during the first half of incubation. Nestling starvation was uncommon (5–9% of nestlings monitored) and not associated with greater hatching asynchrony. These results indicate that while clutch size, a repeatable female trait, contributed to variation in incubation length and hatching asynchrony in Eastern Kingbirds, weather was a greater source of variation, especially for incubation length. RESUMEN La duración de la incubación y la asincronía de la eclosión son elementos integrales de las estrategias reproductivas evolucionadas de las aves. Examinamos la variación intra- e inter-poblacional en ambos rasgos para las poblaciones de Tyrannus tyrannus de Nueva York (NY), Kansas (KS) y Oregón (OR) y encontramos que tanto la duración de la incubación como la asincronía de la eclosión no fueron repetibles entre las hembras, luego de controlar un rasgo repetible como el tamaño de la nidada. En cambio, la duración de la incubación y el tamaño de la nidada fueron influenciados por la temperatura ambiente y la precipitación. La duración de la incubación mostró la misma mediana (15 días) y el mismo rango (13–17 días) en todos los sitios. Los resultados de los modelos de selección indicaron que los períodos de incubación para las nidadas más pequeñas y más grandes fueron más largos en NY que en KS cuando la lluvia fue frecuente a lo largo de la incubación, en los nidos de reemplazo y probablemente cuando las temperaturas ambiente fueron bajas durante la puesta de los huevos. La eclosión completa usualmente requirió 2 días (pero hasta 3), estando la eclosión asociada a pequeños tamaños de nidada, períodos cortos de incubación, lluvia frecuente durante el período de puesta de los huevos y bajas temperaturas ambiente durante la primera mitad de la incubación. La hambruna de los polluelos fue poco común (5–9% de los polluelos monitoreados) y no estuvo asociada con una mayor asincronía de la eclosión. Estos resultados indican que mientras el tamaño de la nidada, un rasgo repetible de las hembras, contribuyó a la variación en la duración de la incubación y en la asincronía de la eclosión en T. tyrannus, el clima fue una fuente mayor de variación, especialmente para la duración de la incubación. Lay Summary • The length of time that eggs remain in a nest exposed to causes of mortality has important influences on the reproductive success of birds. • We collected data on incubation length, the length of time elapsed between the hatching of the first and last egg (called hatching asynchrony), and probability of nestling starvation in Eastern Kingbirds breeding at 3 locations (Kansas, New York, and Oregon). • Incubation length and hatching asynchrony varied considerably within, but also among sites. Incubation length and hatching asynchrony were both greater in nests with more eggs. However, most other variation was likely due to environmental effects. Cool and wet conditions were associated with long incubation periods while greater hatching asynchrony was found during periods when it was warm and dry. • Starvation of nestlings was infrequent, and nests with a greater range of nestling ages (caused by high hatching asynchrony) did not experience greater starvation of young. Nestling starvation was thus not a cost of high-hatching asynchrony. • Our research demonstrates that environmental temperature and frequency of precipitation have greater effects on incubation period compared to clutch size. INTRODUCTION Incubation is a critical period during avian reproduction and the strong allometric relationship between incubation length and egg mass in altricial birds (Birchard and Deeming 2015) suggests selection has shortened incubation length to near its physiological limit. However, the existence of geographic and interspecific differences in incubation length, independent of egg or body size, suggest that other factors are at play (Ricklefs et al. 2017, Martin et al. 2018). Within north temperate regions, variation in incubation length also results from physical influences of the environment (Ardia et al. 2006, MacDonald et al. 2013, Griffith et al. 2016). Embryonic development in birds begins when egg temperature exceeds presumed physiological zero (~26°C; Webb 1987). Higher ambient temperatures can raise egg temperatures (e.g., Wang and Weathers 2009, Nord et al. 2010), but frequent rainfall and wetting of nests, which increases nest thermal conductance (Reid et al. 2002a, Hilton et al. 2004), may cause rapid declines in egg temperature (Hilton et al. 2004). Once embryogenesis begins, embryos of most avian species appear detrimentally affected by time spent below optimal incubation temperatures (36–40°C; Cooper et al. 2005) because it may extend incubation (Ardia et al. 2006, Hepp et al. 2006, Griffith et al. 2016, Martin et al. 2018, de Zwann et al. 2019), reduce hatchling yolk reserves or protein content (Vleck and Hoyt 1980, Hepp et al. 2006, Eiby and Booth 2009), yield smaller and/or lower quality hatchlings (Kim and Monaghan 2006, Olson et al. 2006, Ardia et al. 2010, DuRant et al. 2012), reduce hatching success (Hepp et al. 2006, MacDonald et al. 2013), or yield offspring with weak immune responses (Ardia et al. 2010, DuRant et al. 2012). Higher ambient temperatures and sparse precipitation may thus benefit embryos and adults because of the reduced gradient in temperature between eggs and environment that drive embryo temperatures down when parents leave the nest to feed (Zerba and Morton 1983, Morton and Pereyra 1985, Reid et al. 2002b). However, because all birds lay maximally 1 egg per day and most do not begin incubation with the first egg, ambient conditions that allow eggs to remain above physiological zero for extended periods prior to the start of full incubation may result in a loss of egg viability (Arnold 1993, Stoleson and Beissinger 1999) or initiate embryonic development before termination of egg-laying (Cooper et al. 2005). The latter may result in hatching asynchrony (e.g., Ardia et al. 2006). Hatching asynchrony is often associated with increased nestling starvation (Bancroft 1985, Stouffer and Powers 1991, Murphy 1994, Stoleson and Beissinger 1997) or reduced nestling quality (Clotfelter and Yasukawa 1999) due to asymmetric competition among asynchronously hatched young. Despite apparent negative consequences, hatching asynchrony is generally perceived as an evolved strategy under female control that allows parents to either reduce brood size to a number commensurate with food supplies (Lack 1968, Magrath 1989), or to shorten the time eggs and young spend in the nest exposed to nest predators (Clark and Wilson 1981, Hussell 1985). In both cases, but for different reasons, loss of some young to starvation is seen as the lesser of 2 evils, the greater being the loss of an entire brood. Regardless, environmentally driven hatching asynchrony that causes the loss of young can only be seen as a cost. A growing body of evidence indicates that incubation length and hatching asynchrony vary considerably both among and within populations of the same species, and that they are important for avian reproductive success (e.g., Briskie and Sealy 1989, Magrath 1989). Intrapopulation variation in incubation length among small birds with altricial young ranges from 3 to 4 days, but up to 5 to 6 (e.g., Martin et al. 2018, Sofaer et al. 2020) or more days (Higgott et al. 2020). Clutches of most altricial temperate-zone breeding species hatch within 1 (22.2%) or 2 days (51.8%) days, but 3 days is not uncommon (25.9%; data from Clark and Wilson 1981, plus Bancroft 1985, Smith 1988, Briskie and Sealy 1989, Ardia et al. 2006; n = 27 species), and is occasionally even longer (Lessells and Avery 1989, Beissinger and Waltman 1991). In addition to the potential influence of ambient temperature and precipitation on intraspecific variation in incubation length (Beissinger et al. 2005, Ardia et al. 2006, Nord et al. 2010, MacDonald et al. 2013, Higgott et al. 2020), longer incubation periods have been associated with both smaller (Feldheim 1997, Ardia et al. 2006, Higgott et al. 2020) and larger clutch size (Moreno and Carlson 1989, Magrath 1992, Engstrand and Bryant 2002, Arnold 2011), later seasonal breeding (Moreno and Carlson 1989, Magrath 1992, Veiga 1992, Feldheim 1997, Arnold 2011), and in some cases, larger egg size (Parsons 1972, Arnold 1993; but see Magrath 1992). Hatching asynchrony has been reported to increase with clutch size (Smith 1988, Briskie and Sealy 1989, Magrath 1992, Hébert and Sealy 1993) and late-season breeding (Bancroft 1985, Murphy and Fleischer 1986, Moreno and Carlson 1989, Murphy 1994), but the extent to which daily variation in weather is associated with hatching asynchrony is largely unknown (but see Ardia et al. 2006). Here, we describe intra- and interpopulation variation in incubation length and hatching asynchrony of Eastern Kingbirds (Tyrannus tyrannus; hereafter kingbirds). Kingbird incubation is potentially sensitive to ambient conditions because they are single-sex (female only) intermittent incubators without incubation feeding by males. Moreover, their open-cup nests are built on the edge of tree canopies (Murphy et al. 1997) where they are exposed to the elements when females leave the nest to forage. Our sites in Kansas (KS), New York (NY), and Oregon (OR), combined with extensive annual sampling in NY (13 years) and OR (10 years), allowed us to describe natural variation in incubation length and hatching asynchrony by birds exposed to a wide range of thermal conditions, and which we attempt to use to establish the extent to which female or environmentally based factors influence both traits. Our expectation, if inherent differences among females drive variation in incubation length and hatching asynchrony, is that both should be repeatable. We tested this possibility using a subset of banded females. We also tested for whether timing of breeding (i.e., date of first egg), clutch size, egg mass, or nest status (i.e., initial nests of the season or replacement nests produced after a failure) were sources of variation. Given that kingbird breeding date advances with age (Murphy 2004) and that early breeders have the highest seasonal reproductive success (Cooper et al. 2009), we assumed that the earliest breeders are the highest quality individuals and should have short incubation periods and low hatching asynchrony. Small clutches may be susceptible to more rapid cooling than nests with more eggs when females leave the nest to forage (Reid et al. 2000, 2002b), but large clutches may require more energy to reheat and/or be less efficiently incubated than smaller clutches that females can more effectively cover during incubation (Engstrand and Bryant 2002). Hence, we tested for a quadratic relationship between incubation length and clutch size to account for the possibility that incubation period of both small and large clutches may be prolonged, but anticipated greater hatching asynchrony among larger clutches based on previously reported results (see above). Large eggs lose heat less rapidly than small eggs (Hilton et al. 2004) and thus we also predicted clutches of small eggs would exhibit long incubation. Assuming again that female quality/condition influences incubation efficiency, we predicted that incubation length and hatching asynchrony would be greater in replacement nests because investment in building 2 nests and the production and care of an initial clutch could compromise a female’s capacity to incubate a later clutch or feed a second brood as effectively as her first. Separating intrinsic (i.e., female-based) and extrinsic (i.e., environmental) factors can be difficult, and laying date has an extrinsic component as well because of the steady seasonal increase in ambient temperature (see below) and insect food supplies (Murphy 1986). Hence, the hypothesis that extrinsic factors are primarily responsible for variation in incubation length and hatching asynchrony predicts a seasonal decline in incubation length, but an increase in hatching asynchrony to hasten hatching so that parents can fledge young in time to prepare for migration. If extrinsic factors underlie variation in incubation length and hatching asynchrony then conditions conducive to “ambient incubation” and embryonic development will yield shorter incubation periods and greater hatching asynchrony when ambient temperatures are high and precipitation low. Last, if hatching asynchrony is a “costly outcome” of environmental conditions that promote ambient incubation that enhances hatching asynchrony, we anticipated an increased frequency of starvation among clutches with high levels of hatching asynchrony, especially late in the season. METHODS Study Areas Research in NY included 1 year (1979) in western NY near Eden (Erie County) located southwest of Buffalo, NY (42.65°N, –78.90°W; 234 m.a.s.l. [meters above sea level) followed 10 years later with 12 years of research (1989–2000) in central NY near Oneonta (42.45°N, –75.06°W; 339 m.a.s.l.; Otsego County) and West Davenport (42.47°N, –74.84°W; 354 m.a.s.l.; Delaware County). The Oneonta and West Davenport study sites were separated by only ~10 km, birds dispersed between them, and thus we treated them as a single site. In addition, because the climates of the western and central NY study sites are so similar when compared to the other 2 sites, we combined the single year from western NY with the 12 years from central NY. The eastern KS study site (1980–1983) was located ~6.5 km west of Lawrence (Douglas County), north of Clinton Lake (38.94°N, –95.34°W; 264 m.a.s.l.). Ten years (2002–2011) of research were conducted in southeastern OR at Malheur National Wildlife Refuge (MNWR) in Harney County (42.97°N, –118.87°W; 1,279 m.a.s.l.). At all sites, habitats were primarily open grasslands/wetlands with scattered trees and either lacustrine or riparian zones. Climate is highly seasonal at all 3 sites (National Oceanic and Atmospheric Administration; http://www.yourweatherservice.com/) with annual low and high temperatures occurring in either December or January and July, respectively. Precipitation varies dramatically among sites. Although annual totals are very similar in NY (1,014 mm) and KS (1,028 mm), monthly totals are roughly equal in NY whereas precipitation in KS is highly seasonal with a strong peak in the first 2 months of the breeding season (May and June). MNWR, which is located in the Great Basin Desert, receives much less annual precipitation (277 mm), and excluding the month of May (during which few clutches are produced), the breeding season is the driest season of the year. Field Methods With the exception of the capture and banding of adults, the same methods were used in all years and locations and are detailed elsewhere (Murphy 2000, Redmond and Murphy 2012). Briefly, daily surveys for nests began by May as kingbirds return from migration beginning in early to middle May (Cooper et al. 2009). Once found, nest checks occurred at 1- to 3-day intervals, but more frequently during laying, hatching, and as fledging neared, which allowed documentation of the beginning and ending of egg-laying, clutch size, egg size, hatching dates, number of eggs to hatch, nest fate, and if successful, number of young to fledge. Adults and nestlings were banded (12–14 days of age) in NY and OR using 1 aluminum federal band and 3 colored plastic leg bands. Adults were captured using mist nets at either nests while feeding young, or in the case of males in OR, using song playback during the early morning dawn song period. In all years, except 2009, we measured maximum egg length (L) and width (W; to nearest 0.05 mm with dial calipers) at accessible nests, and for some eggs, mass (M) on the day of laying (to nearest 0.1 g; Pesola scale). Mass was estimated for eggs not weighed on the day of laying using the equation M = C × (L × W2), where C (0.545) was determined from eggs measured on the day of laying after rearrangement of the above equation (Murphy 1983). Kingbirds raise only a single brood per year, but ≥50% of nests fail annually due mainly to nest predation (~90% of nest failures; Murphy 1986, 2000, Murphy et al. 2020). Losses of young to starvation were indicated by poor nestling growth and/or the presence of dead nestlings in the nest. Most pairs that failed in their first attempt produced replacement clutches and we collected identical data for all replacement nests. Freshly hatched young have pink skin and wet and matted down (Murphy 1981); hatch date of nestlings in this condition was known with certainty. Nests were visited only once per day, and thus if on the day after the first hatchling appeared all eggs hatched and none appeared as fresh hatchlings we classified the nest as a synchronous hatch (i.e., all hatched in ≤24 hr). By contrast, if on the day after the hatching of the first egg a hatchling appeared as freshly hatched the nest was classified as asynchronous (≥2 days to hatch all young). If all eggs had not hatched by the second day, a visit was made on the third day to determine if the egg hatched. If it had, but the nestling was not “fresh” we assumed it hatched the previous day after our visit and that the entire clutch hatched within 2 days. However, if the new hatchling was fresh we recorded the nest as requiring 3 days to hatch. Incubation length was the number of days elapsed between the laying of the last egg and the appearance of the last hatchling (Nice 1954). Data Analysis Daily low and high temperature and daily precipitation for the breeding season at all sites were obtained from either NOAA’s National Centers for Environmental Information for permanent weather stations located near the NY and KS study sites, or from data provided by the Eastern Oregon Agricultural Research Center. We used the Buffalo Niagara International Airport (42.93°N, –78.73°W; 34 km from the center of study site) for the western NY site, and Cooperstown, NY (42.68°N, –74.92°W) for the central NY sites; both Oneonta and West Davenport were ~25 km from the weather station. In KS, data were obtained from the Topeka Regional Airport (38.95°N, –95.65°W; 28 km), while data for OR came from the P-Hill weather station located near Frenchglen, OR (42.83°N, –118.93°W; 1.5 km from the SW corner of our study site). To characterize the typical ambient temperatures faced by incubating females at all sites, we compared (analysis of variance) daily low, high, and mean ([low + high]/2) temperature for all days falling within the middle 90% of days during which eggs were in nests for all years of study at each site (KS: 1980–1983, 204 days; NY: 1989–2000, 648 days; OR: 2002–2011, 490 days). We then tallied the number of days when daily maximum temperature (A) exceeded presumptive physiological zero of embryos (26°C), (B) was at or above temperatures that could likely support embryo development due to “ambient incubation” (≥30°C), (C) fell within the optimal range for embryo development (36–40°C), or (D) reached temperatures that may detrimentally affect embryo development (>40°C). To allow direct visual comparisons (Figure 1), the midpoint of dates at sites was set to a value of zero by subtracting the absolute value of the midpoint (all dates counted continuously from May 1 = 1) from all other dates. Similarly, at each site, we subtracted the mean breeding date from the breeding date of individual clutches so that the mean breeding date was zero at all sites. Figure 1. Open in new tabDownload slide Variation in maximum daily temperature over the period of time eggs of Eastern Kingbirds were being incubated in Kansas (A), New York (B), and Oregon (C). Data are restricted to the middle 90% of the latter period at each site from 1980 to 1982 (Kansas), 1989 to 2000 (New York), and 2002 to 2011 (Oregon). Dates are standardized to a mean of zero at all sites to account for differences in breeding schedules. Horizontal lines represent presumed physiological zero for embryo development (26°C), moderate ambient temperatures above which cooling of unattended eggs would be slow (30°C), and optimal temperature for incubation (36–40°C). Figure 1. Open in new tabDownload slide Variation in maximum daily temperature over the period of time eggs of Eastern Kingbirds were being incubated in Kansas (A), New York (B), and Oregon (C). Data are restricted to the middle 90% of the latter period at each site from 1980 to 1982 (Kansas), 1989 to 2000 (New York), and 2002 to 2011 (Oregon). Dates are standardized to a mean of zero at all sites to account for differences in breeding schedules. Horizontal lines represent presumed physiological zero for embryo development (26°C), moderate ambient temperatures above which cooling of unattended eggs would be slow (30°C), and optimal temperature for incubation (36–40°C). Total number of nests found over the period of study was 2,237, but because nest failure was common and missing data existed for some variables, we conducted our analysis on nests that had little to no hatching failure and with complete information on laying dates, clutch size, hatching dates, number of eggs to hatch, and number of young to fledge (n = 342). One egg did not hatch in 40 of the 342 nests (11.7%), but for various reasons (e.g., egg had been marked by us or was distinctively colored) we were certain the unhatched egg was not the last egg laid. If it had been the last laid egg, and assuming hatching asynchrony was common, our expectation was that both incubation length and the time to hatch all eggs would be less in nests with unhatched eggs. Incubation length did not differ between nests that did or did not have hatching failure (t340 = 0.60, P = 0.552). After accounting for effects of clutch size on hatching duration (see below), there was no difference in time to hatch all eggs for nests in which eggs did (1.87 ± 0.029 days [SE], n = 302) or did not (1.99 ± 0.075 days, n = 40) all hatch (F1,339 = 2.35, P = 0.126). The 4 dependent variables in our analysis were (1) incubation length, (2) number of days to completely hatch the clutch (1, 2, or 3 days, with hatching asynchrony ≥2 days), (3) whether a brood experienced starvation, and (4) number of fledged young. Analysis of incubation length and hatching asynchrony included all nests that survived to hatching, while the occurrence of starvation and number of fledged young included all nests that survived to fledging. An expectation of the hypothesis that variation in incubation length and hatching asynchrony derive from intrinsic differences among females is that both are statistically repeatable. We therefore calculated repeatability (Lessells and Boag 1987) of both traits, along with breeding date (corrected for site differences in date), clutch size, and egg mass, for the 34 individually banded females with multiple nest records. The 34 females contributed 26% of the observations in our sample, but we chose to treat all cases of incubation length and the other response variables as independent observations because (A) no female contributed more than 1.4% to the data (and most with multiple years of data individually contributed only 0.6%), and (B) restricting the analyses to individually identifiable females would have eliminated the 253 nests produced by an unknown number of different females. Moreover, as shown below, incubation length and hatching asynchrony were not repeatable, indicating that each reproductive attempt by a female yielded unique information. We examined variation in incubation length in relation to date of laying, clutch size (as a quadratic function), nest status (i.e., first or replacement nest), and for the subset of nests with available data, egg mass. However, because phenological changes continue throughout the breeding season (e.g., vegetation changes and invertebrate prey populations grow), we acknowledge that date also has potential effects extrinsic to the female, which sets it apart from the potential influence that extrinsic factors such as ambient temperature and precipitation may have on reproduction. To quantify weather, daily low and high temperatures were averaged to yield the daily mean, while precipitation was treated as a binary variable based on whether measurable precipitation fell (“no” [0], or “yes” [1]; Higgott et al. 2020). To assess the importance of weather, we quantified temperature and precipitation during the egg-laying period (TempEgg-laying, RainEgg-laying), the first (Temp1stHalf, Rain2ndHalf) and second halves (Temp2ndHalf, Rain2ndHalf) of incubation, and for precipitation, the total period that eggs were in the nest (RainTotal). Precipitation was represented as the percentage of days during each period when rainfall was recorded (Higgott et al. 2020). As a priori observations indicated that kingbirds often begin incubation with the penultimate egg, we included the last day of egg-laying with Temp1stHalf and Rain1stHalf. We divided incubation into halves because it is common for birds to gradually increase incubation intensity over the first few days of incubation but then maintain high incubation intensity over the second half (Zerba and Morton 1983, Morton and Pereyra 1985, Wiebe et al. 1998, Wang and Beissinger 2009). If incubation length was an odd number of days the first half of incubation was the longer period. Hatching asynchrony was examined in relation to the same set of intrinsic (now also including incubation length) and extrinsic variables. Because of the potential importance of egg mass for incubation and hatching success (Kirst 2011), we omitted all nests lacking data on egg mass and reanalyzed the reduced data set (n = 281 nests) using identical procedures but with egg mass as an additional predictor variable for both incubation length and hatching asynchrony. To test the possibility that nestling starvation was associated with hatching asynchrony, we examined the probability of nestling starvation in relation to hatching asynchrony while accounting for possible effects of brood size, incubation length, laying date, and nest status. We conducted our analysis of incubation length using generalized linear models (GLMs). In all models, we treated site as a categorical factor, and as per our hypotheses, we included as additional predictors clutch size (as a quadratic), date, and to avoid overfitting models, each temperature variable paired to each of the 4 measures of precipitation (e.g., TempEgg-laying with RainEgg-laying, TempEgg-laying with Rain1stHalf, etc.). We did not enter date and nest status together because replacement nests were invariably produced later in the season than initial nests (t = 12.32, P < 0.001) and instead replaced date with nest status before rerunning all 12 models. All models within 2 AICc units (Akaike’s information criterion corrected for small sample size) of the top model were considered competitive. Hatching asynchrony was analyzed identically except that clutch size was entered as a linear term, and incubation length was included as an additional predictor. We then restricted our analyses to nests with data on egg mass, and reran our analyses of incubation length and hatching asynchrony with the same set of predictors. GLMs were run with distribution set as normal, and with an identity link function. Probability of nestling starvation was analyzed using GLMs but with distribution set as binomial (“no” [0], no nestling starved, or “yes” [1], ≥ 1 nestling starved). Brood size was included as a predictor variable, along with hatching asynchrony, because our expectation was that starvation was more likely to occur in nests with large broods and when hatching was highly asynchronous. Additional predictors included site and incubation length. Date and nest status were also included, but because of the strong covariation between them (see above), they were used in separate models. Number of young to starve was likewise examined using GLMs with the same set of variables as for probability that a nest experienced starvation, but with distribution set as normal. All statistical analyses were conducted using STATSTIX (analytical software v. 9) except for the GLMs which were run using JMP12. Statistics are reported as mean ± SE and n. RESULTS Site Differences in Climate and Reproduction Low, high, and mean ambient temperatures during the period when eggs were in the nest were greater in KS than at other sites (Table 1). Mean low temperature was lower in OR than NY, but mean maximum temperature was also greater in OR (Table 1, Figure 1). Consequently, mean daily temperature during the period when eggs were in the nest did not differ between NY and OR (Table 1) because of greater diel temperature variation in OR (20.6 ± 0.21°C) compared to NY (13.3 ± 0.18°C) and KS (11.9 ± 0.25°C; F2, 1,338 = 469.20, P < 0.001). Table 1. Comparison of average minimum, maximum, and mean ambient temperature (SE) among study sites during the middle 90% of the period during which eggs were being incubated. Averages sharing superscripted letters do not differ significantly (Tukey’s test). Also reported are the percentage of days during the same period during which ambient maximum temperature exceeded 26°C, 30°C, and 40°C, along with the percentage of days during which maximum ambient temperature fell within the optimal temperature range for incubation (36–40°C). Site . Ambient temperature (°C) . Percentage of days maximum temperature . . Minimum . Maximum . Mean . >26°C . >30°C . 36–40°C . >40°C . NY (648) 11.3 (0.18)b 24.6 (0.17)c 18.0 (0.15)b 41.7 8.0 0.0 0.0 KS (204) 18.5 (0.30)a 30.4 (0.36)a 24.4 (0.31)a 86.8 73.5 7.8 5.4 OR (490) 7.3 (0.18)c 27.9 (0.27)b 17.6 (0.20)b 64.1 39.8 4.3 0.6 Site . Ambient temperature (°C) . Percentage of days maximum temperature . . Minimum . Maximum . Mean . >26°C . >30°C . 36–40°C . >40°C . NY (648) 11.3 (0.18)b 24.6 (0.17)c 18.0 (0.15)b 41.7 8.0 0.0 0.0 KS (204) 18.5 (0.30)a 30.4 (0.36)a 24.4 (0.31)a 86.8 73.5 7.8 5.4 OR (490) 7.3 (0.18)c 27.9 (0.27)b 17.6 (0.20)b 64.1 39.8 4.3 0.6 Minimum: F = 478.47; Maximum: F = 124.34; Mean: F = 220.16, P < 0.001 for all. Open in new tab Table 1. Comparison of average minimum, maximum, and mean ambient temperature (SE) among study sites during the middle 90% of the period during which eggs were being incubated. Averages sharing superscripted letters do not differ significantly (Tukey’s test). Also reported are the percentage of days during the same period during which ambient maximum temperature exceeded 26°C, 30°C, and 40°C, along with the percentage of days during which maximum ambient temperature fell within the optimal temperature range for incubation (36–40°C). Site . Ambient temperature (°C) . Percentage of days maximum temperature . . Minimum . Maximum . Mean . >26°C . >30°C . 36–40°C . >40°C . NY (648) 11.3 (0.18)b 24.6 (0.17)c 18.0 (0.15)b 41.7 8.0 0.0 0.0 KS (204) 18.5 (0.30)a 30.4 (0.36)a 24.4 (0.31)a 86.8 73.5 7.8 5.4 OR (490) 7.3 (0.18)c 27.9 (0.27)b 17.6 (0.20)b 64.1 39.8 4.3 0.6 Site . Ambient temperature (°C) . Percentage of days maximum temperature . . Minimum . Maximum . Mean . >26°C . >30°C . 36–40°C . >40°C . NY (648) 11.3 (0.18)b 24.6 (0.17)c 18.0 (0.15)b 41.7 8.0 0.0 0.0 KS (204) 18.5 (0.30)a 30.4 (0.36)a 24.4 (0.31)a 86.8 73.5 7.8 5.4 OR (490) 7.3 (0.18)c 27.9 (0.27)b 17.6 (0.20)b 64.1 39.8 4.3 0.6 Minimum: F = 478.47; Maximum: F = 124.34; Mean: F = 220.16, P < 0.001 for all. Open in new tab Daily maximum temperature differed dramatically among sites (Table 1, Figure 1). Daily highs exceeded presumed physiological zero of embryos on 42% of days in NY, but roughly 1.5 and 2 times more often in OR and KS, respectively (Table 1, Figure 1). Likewise, temperatures conducive to “ambient incubation” (>30°C) occurred commonly in OR and especially KS, but infrequently in NY (Table 1, Figure 1). In NY, daily high temperature never fell within the optimal range (36–40°C) for avian incubation, but did so in OR and KS on 4.3% and 7.8% of days, respectively. Daily high temperature also exceeded that which is assumed to represent a potential threat to embryos (>40°C) on 5% of days in KS, but almost never elsewhere. Except for measures of nesting outcome, all reproductive variables differed among sites (Table 2). Breeding occurred later in OR compared to NY and KS (which did not differ), but clutch size was smaller in NY than at both other sites (which did not differ). Egg mass was smallest in KS and largest in OR (Table 2). Median incubation length was 15 days at all locations, and with the exception of one 18-day incubation period in OR, ranged everywhere from 13 to 17 days (Figure 2). Omitting the single 18-day incubation period, incubation length differed significantly among all sites, being shorter by half a day in KS compared to NY, with OR being intermediate (Table 2). Although modest, hatching asynchrony also differed among sites. Ignoring one nest in OR with a 5-day hatching spread, all sites exhibited the same median (2 days) and range (1–3 days; Figure 2), but the average number of days to fully hatch a clutch was 10.5% greater in OR compared to NY (KS intermediate; Table 2). By contrast, of nests that survived to fledge young, there were no site differences in number of young to fledge or starve, or either the percentage of young to starve or the percentage of nests to lose one or more nestlings to starvation (Table 2). Table 2. Comparisons of Eastern Kingbird reproduction from New York (1979, 1989–2000), Kansas (1980–1982), and Oregon (2002–2011). Comparisons of the number of young to fledge and the 3 measures of the intensity of nestling starvation were restricted to nests that survived to fledge young. Values are means ± SE with sample size of nests in parentheses. Breeding statistics that share uppercase superscripted letters did not differ significantly. Variable . Site . . . NY . KS . OR . F (P) . Breeding date June 9 ± 0.5 days (181)A June 6 ± 1.5 days (34)A June 21 ± 0.8 days (127)B 109.77 (<0.001) Clutch size 3.30 ± 0.04 eggs (181)B 3.62 ± 0.10 eggs (34)A 3.60 ± 0.05 eggs (127)A 12.11 (<0.001) Egg mass 4.06 ± 0.03 g (170)B 3.81 ± 0.05 g (32)C 4.29 ± 0.04 g (79)A 27.36 (<0.001) Incubation length 15.1 ± 0.05 days (181)A 14.6 ± 0.13 days (34)C 14.9 ± 0.06 days (127)B 9.82 (<0.001) Days to hatch 1.8 ± 0.04 days (181)B 1.9 ± 0.09 days (34)AB 2.0 ± 0.04 days (127)A 4.49 (0.012) Number fledged 2.8 ± 0.08 young (130) 2.9 ± 0.30 young (16) 3.0 ± 0.10 young (86) 0.84 (0.433) Number starved 0.2 ± 0.06 young (130) 0.3 ± 0.22 young (16) 0.2 ± 0.05 young (86) 0.00 (0.999)a Young starved (%) 6.7 ± 1.78 (130) 9.4 ± 6.80 (16) 5.0 ± 1.48 (86) 0.00 (0.999)a Nests with starvation (%) 13.6 ± 3.0 (130) 12.5 ± 8.54 (16) 13.8 ± 3.72 (86) 0.01 (0.990)a Variable . Site . . . NY . KS . OR . F (P) . Breeding date June 9 ± 0.5 days (181)A June 6 ± 1.5 days (34)A June 21 ± 0.8 days (127)B 109.77 (<0.001) Clutch size 3.30 ± 0.04 eggs (181)B 3.62 ± 0.10 eggs (34)A 3.60 ± 0.05 eggs (127)A 12.11 (<0.001) Egg mass 4.06 ± 0.03 g (170)B 3.81 ± 0.05 g (32)C 4.29 ± 0.04 g (79)A 27.36 (<0.001) Incubation length 15.1 ± 0.05 days (181)A 14.6 ± 0.13 days (34)C 14.9 ± 0.06 days (127)B 9.82 (<0.001) Days to hatch 1.8 ± 0.04 days (181)B 1.9 ± 0.09 days (34)AB 2.0 ± 0.04 days (127)A 4.49 (0.012) Number fledged 2.8 ± 0.08 young (130) 2.9 ± 0.30 young (16) 3.0 ± 0.10 young (86) 0.84 (0.433) Number starved 0.2 ± 0.06 young (130) 0.3 ± 0.22 young (16) 0.2 ± 0.05 young (86) 0.00 (0.999)a Young starved (%) 6.7 ± 1.78 (130) 9.4 ± 6.80 (16) 5.0 ± 1.48 (86) 0.00 (0.999)a Nests with starvation (%) 13.6 ± 3.0 (130) 12.5 ± 8.54 (16) 13.8 ± 3.72 (86) 0.01 (0.990)a aKruskal–Wallis test. Open in new tab Table 2. Comparisons of Eastern Kingbird reproduction from New York (1979, 1989–2000), Kansas (1980–1982), and Oregon (2002–2011). Comparisons of the number of young to fledge and the 3 measures of the intensity of nestling starvation were restricted to nests that survived to fledge young. Values are means ± SE with sample size of nests in parentheses. Breeding statistics that share uppercase superscripted letters did not differ significantly. Variable . Site . . . NY . KS . OR . F (P) . Breeding date June 9 ± 0.5 days (181)A June 6 ± 1.5 days (34)A June 21 ± 0.8 days (127)B 109.77 (<0.001) Clutch size 3.30 ± 0.04 eggs (181)B 3.62 ± 0.10 eggs (34)A 3.60 ± 0.05 eggs (127)A 12.11 (<0.001) Egg mass 4.06 ± 0.03 g (170)B 3.81 ± 0.05 g (32)C 4.29 ± 0.04 g (79)A 27.36 (<0.001) Incubation length 15.1 ± 0.05 days (181)A 14.6 ± 0.13 days (34)C 14.9 ± 0.06 days (127)B 9.82 (<0.001) Days to hatch 1.8 ± 0.04 days (181)B 1.9 ± 0.09 days (34)AB 2.0 ± 0.04 days (127)A 4.49 (0.012) Number fledged 2.8 ± 0.08 young (130) 2.9 ± 0.30 young (16) 3.0 ± 0.10 young (86) 0.84 (0.433) Number starved 0.2 ± 0.06 young (130) 0.3 ± 0.22 young (16) 0.2 ± 0.05 young (86) 0.00 (0.999)a Young starved (%) 6.7 ± 1.78 (130) 9.4 ± 6.80 (16) 5.0 ± 1.48 (86) 0.00 (0.999)a Nests with starvation (%) 13.6 ± 3.0 (130) 12.5 ± 8.54 (16) 13.8 ± 3.72 (86) 0.01 (0.990)a Variable . Site . . . NY . KS . OR . F (P) . Breeding date June 9 ± 0.5 days (181)A June 6 ± 1.5 days (34)A June 21 ± 0.8 days (127)B 109.77 (<0.001) Clutch size 3.30 ± 0.04 eggs (181)B 3.62 ± 0.10 eggs (34)A 3.60 ± 0.05 eggs (127)A 12.11 (<0.001) Egg mass 4.06 ± 0.03 g (170)B 3.81 ± 0.05 g (32)C 4.29 ± 0.04 g (79)A 27.36 (<0.001) Incubation length 15.1 ± 0.05 days (181)A 14.6 ± 0.13 days (34)C 14.9 ± 0.06 days (127)B 9.82 (<0.001) Days to hatch 1.8 ± 0.04 days (181)B 1.9 ± 0.09 days (34)AB 2.0 ± 0.04 days (127)A 4.49 (0.012) Number fledged 2.8 ± 0.08 young (130) 2.9 ± 0.30 young (16) 3.0 ± 0.10 young (86) 0.84 (0.433) Number starved 0.2 ± 0.06 young (130) 0.3 ± 0.22 young (16) 0.2 ± 0.05 young (86) 0.00 (0.999)a Young starved (%) 6.7 ± 1.78 (130) 9.4 ± 6.80 (16) 5.0 ± 1.48 (86) 0.00 (0.999)a Nests with starvation (%) 13.6 ± 3.0 (130) 12.5 ± 8.54 (16) 13.8 ± 3.72 (86) 0.01 (0.990)a aKruskal–Wallis test. Open in new tab Figure 2. Open in new tabDownload slide Variation in incubation length (above) and hatching asynchrony (below) for Eastern Kingbirds breeding in New York (n = 181 nests), Kansas (n = 34 nests), and Oregon (n = 127 nests). Figure 2. Open in new tabDownload slide Variation in incubation length (above) and hatching asynchrony (below) for Eastern Kingbirds breeding in New York (n = 181 nests), Kansas (n = 34 nests), and Oregon (n = 127 nests). Repeatability of Reproductive Traits Two to 5 years of data (mean = 2.6 ± 0.15 years) were available for banded females from NY (n = 13) and OR (n = 21). Breeding date was not repeatable (first nests of season only; r = 0.013, F27,70 = 1.03, P = 0.453), but clutch size (r = 0.348, F33,88 = 2.39, P = 0.002), egg mass (r = 0.699, F25,39 = 6.80, P < 0.001), and incubation length (r = 0.239, F33,88 = 1.82, P = 0.024) were. By contrast, hatching asynchrony (r = 0.040, F33,55 = 1.11, P = 0.360), number of young to fledge (r = 0.028, F33,85 = 1.07, P = 0.404), and number of young to starve (nests that did not fail due to predation or weather; r = 0.076, F21,30 = 0.82, P = 0.681) were not repeatable. Incubation length varied with clutch size (see below), and given the moderately high repeatability of clutch size, it seemed possible that repeatability of incubation length arose from its relationship with clutch size. After statistically accounting for effects of clutch size, incubation length no longer varied repeatably among females (F33,88 = 1.36, P = 0.157). Variation in Incubation Length The top model of the analysis of incubation length for all nests and only those nests with data on egg mass were qualitatively identical (Table 3). In both, incubation length was shorter in KS than NY, was shortest in intermediate-sized clutches of 3 and 4 eggs (Figure 3), but long in nests that experienced frequent rain while eggs were in the nest (RainTotal; Figure 4) and when temperatures during egg-laying (TempEgg-laying) were low (Figure 4). Incubation also tended to be longer in replacement nests. Egg mass was an uninformative variable as ∆AIC of the model with the above variables and egg mass was 1.782; thus, there was no association between incubation length and egg mass. The 3 other competitive models of incubation length for the full sample of nests were subsets of the top model that eliminated first TempEgg-laying, then nest status, and finally, both variables. The association of incubation length with site, the quadratic of clutch size, and RainTotal were unaffected by the progressive elimination of TempEgg-laying and nest status from the top model (Table 3). Table 3. Results of the generalized linear model analysis of variation in incubation length of Eastern Kingbirds breeding in Kansas (1980–1983), New York (1979, 1989–2000), and Oregon (2002–2011). Predictor variables included site, the quadratic of clutch size, either breeding date or nest status (first nest of the season or replacement nest), and each of 3 measures of ambient temperature (TempEgg-laying, Temp1stHalf, and Temp2ndHalf) combined in pairwise fashion with all 4 measures of precipitation (RainEgg-laying, Rain1stHalf, Rain2ndHalf, and RainTotal). The reported results are limited to models that were within 2 AICc units of the top model. Separate analyses were conducted for the full sample of nests (egg mass not included) and the subset of nests with information on egg mass. Egg mass was included in all of the latter analyses. Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests) Site – 2 14.139 <0.001 0.000  Clutch size –0.964 ± 0.366 1 6.865 0.009  Clutch size2 0.121 ± 0.054 1 5.032 0.025  RainTotal 0.866 ± 0.249 1 11.857 <0.001  Nest status 0.205 ± 0.111 1 3.387 0.066  TempEgg-laying –0.019 ± 0.010 1 3.161 0.075 Site – 2 18.957 <0.001 1.052  Clutch size –0.993 ± 0.367 1 7.226 0.007  Clutch size2 0.126 ± 0.054 1 5.418 0.020  RainTotal 0.927 ± 0.248 1 13.700 <0.001  Nest status 0.168 ± 0.109 1 2.337 0.126 Site – 2 13.012 0.002 1.277  Clutch size –0.954 ± 0.368 1 6.669 0.010  Clutch size2 0.116 ± 0.054 1 4.589 0.032  RainTotal 0.835 ± 0.250 1 10.983 <0.001  TempEgg-laying –0.015 ± 0.010 1 2.111 0.146 Site – 2 13.012 0.002 1.292  Clutch size –0.980 ± 0.368 1 7.000 0.008  Clutch size2 0.121 ± 0.054 1 4.975 0.026  RainTotal 0.891 ± 0.250 1 12.697 <0.001 Egg mass included (n = 281 nests) Site – 2 13.032 <0.001 0.000  Clutch size –1.036 ± 0.429 1 5.779 0.016  Clutch size2 0.139 ± 0.063 1 4.828 0.028  RainTotal 0.668 ± 0.254 1 6.849 0.009  Nest status 0.334 ± 0.123 1 7.315 0.007  TempEgg-laying –0.022 ± 0.011 1 4.208 0.040 Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests) Site – 2 14.139 <0.001 0.000  Clutch size –0.964 ± 0.366 1 6.865 0.009  Clutch size2 0.121 ± 0.054 1 5.032 0.025  RainTotal 0.866 ± 0.249 1 11.857 <0.001  Nest status 0.205 ± 0.111 1 3.387 0.066  TempEgg-laying –0.019 ± 0.010 1 3.161 0.075 Site – 2 18.957 <0.001 1.052  Clutch size –0.993 ± 0.367 1 7.226 0.007  Clutch size2 0.126 ± 0.054 1 5.418 0.020  RainTotal 0.927 ± 0.248 1 13.700 <0.001  Nest status 0.168 ± 0.109 1 2.337 0.126 Site – 2 13.012 0.002 1.277  Clutch size –0.954 ± 0.368 1 6.669 0.010  Clutch size2 0.116 ± 0.054 1 4.589 0.032  RainTotal 0.835 ± 0.250 1 10.983 <0.001  TempEgg-laying –0.015 ± 0.010 1 2.111 0.146 Site – 2 13.012 0.002 1.292  Clutch size –0.980 ± 0.368 1 7.000 0.008  Clutch size2 0.121 ± 0.054 1 4.975 0.026  RainTotal 0.891 ± 0.250 1 12.697 <0.001 Egg mass included (n = 281 nests) Site – 2 13.032 <0.001 0.000  Clutch size –1.036 ± 0.429 1 5.779 0.016  Clutch size2 0.139 ± 0.063 1 4.828 0.028  RainTotal 0.668 ± 0.254 1 6.849 0.009  Nest status 0.334 ± 0.123 1 7.315 0.007  TempEgg-laying –0.022 ± 0.011 1 4.208 0.040 Open in new tab Table 3. Results of the generalized linear model analysis of variation in incubation length of Eastern Kingbirds breeding in Kansas (1980–1983), New York (1979, 1989–2000), and Oregon (2002–2011). Predictor variables included site, the quadratic of clutch size, either breeding date or nest status (first nest of the season or replacement nest), and each of 3 measures of ambient temperature (TempEgg-laying, Temp1stHalf, and Temp2ndHalf) combined in pairwise fashion with all 4 measures of precipitation (RainEgg-laying, Rain1stHalf, Rain2ndHalf, and RainTotal). The reported results are limited to models that were within 2 AICc units of the top model. Separate analyses were conducted for the full sample of nests (egg mass not included) and the subset of nests with information on egg mass. Egg mass was included in all of the latter analyses. Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests) Site – 2 14.139 <0.001 0.000  Clutch size –0.964 ± 0.366 1 6.865 0.009  Clutch size2 0.121 ± 0.054 1 5.032 0.025  RainTotal 0.866 ± 0.249 1 11.857 <0.001  Nest status 0.205 ± 0.111 1 3.387 0.066  TempEgg-laying –0.019 ± 0.010 1 3.161 0.075 Site – 2 18.957 <0.001 1.052  Clutch size –0.993 ± 0.367 1 7.226 0.007  Clutch size2 0.126 ± 0.054 1 5.418 0.020  RainTotal 0.927 ± 0.248 1 13.700 <0.001  Nest status 0.168 ± 0.109 1 2.337 0.126 Site – 2 13.012 0.002 1.277  Clutch size –0.954 ± 0.368 1 6.669 0.010  Clutch size2 0.116 ± 0.054 1 4.589 0.032  RainTotal 0.835 ± 0.250 1 10.983 <0.001  TempEgg-laying –0.015 ± 0.010 1 2.111 0.146 Site – 2 13.012 0.002 1.292  Clutch size –0.980 ± 0.368 1 7.000 0.008  Clutch size2 0.121 ± 0.054 1 4.975 0.026  RainTotal 0.891 ± 0.250 1 12.697 <0.001 Egg mass included (n = 281 nests) Site – 2 13.032 <0.001 0.000  Clutch size –1.036 ± 0.429 1 5.779 0.016  Clutch size2 0.139 ± 0.063 1 4.828 0.028  RainTotal 0.668 ± 0.254 1 6.849 0.009  Nest status 0.334 ± 0.123 1 7.315 0.007  TempEgg-laying –0.022 ± 0.011 1 4.208 0.040 Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests) Site – 2 14.139 <0.001 0.000  Clutch size –0.964 ± 0.366 1 6.865 0.009  Clutch size2 0.121 ± 0.054 1 5.032 0.025  RainTotal 0.866 ± 0.249 1 11.857 <0.001  Nest status 0.205 ± 0.111 1 3.387 0.066  TempEgg-laying –0.019 ± 0.010 1 3.161 0.075 Site – 2 18.957 <0.001 1.052  Clutch size –0.993 ± 0.367 1 7.226 0.007  Clutch size2 0.126 ± 0.054 1 5.418 0.020  RainTotal 0.927 ± 0.248 1 13.700 <0.001  Nest status 0.168 ± 0.109 1 2.337 0.126 Site – 2 13.012 0.002 1.277  Clutch size –0.954 ± 0.368 1 6.669 0.010  Clutch size2 0.116 ± 0.054 1 4.589 0.032  RainTotal 0.835 ± 0.250 1 10.983 <0.001  TempEgg-laying –0.015 ± 0.010 1 2.111 0.146 Site – 2 13.012 0.002 1.292  Clutch size –0.980 ± 0.368 1 7.000 0.008  Clutch size2 0.121 ± 0.054 1 4.975 0.026  RainTotal 0.891 ± 0.250 1 12.697 <0.001 Egg mass included (n = 281 nests) Site – 2 13.032 <0.001 0.000  Clutch size –1.036 ± 0.429 1 5.779 0.016  Clutch size2 0.139 ± 0.063 1 4.828 0.028  RainTotal 0.668 ± 0.254 1 6.849 0.009  Nest status 0.334 ± 0.123 1 7.315 0.007  TempEgg-laying –0.022 ± 0.011 1 4.208 0.040 Open in new tab Figure 3. Open in new tabDownload slide Mean incubation length (±SE) vs. clutch size of Eastern Kingbirds for birds breeding in New York, Kansas, and Oregon. Clutch sizes sharing letters (above SE) did not differ significantly. Sample sizes are 13, 169, 156, and 4 for clutches of 2, 3, 4, and 5, respectively. Figure 3. Open in new tabDownload slide Mean incubation length (±SE) vs. clutch size of Eastern Kingbirds for birds breeding in New York, Kansas, and Oregon. Clutch sizes sharing letters (above SE) did not differ significantly. Sample sizes are 13, 169, 156, and 4 for clutches of 2, 3, 4, and 5, respectively. Figure 4. Open in new tabDownload slide Incubation length of Eastern Kingbirds breeding in New York, Kansas, and Oregon in relation to variation in ambient temperature during the egg-laying period (top frame: r = –0.153, P = 0.004) and the percentage of days on which measurable rain fell during the entire period eggs were in the nest (bottom frame: r = 0.192, P < 0.001). Figure 4. Open in new tabDownload slide Incubation length of Eastern Kingbirds breeding in New York, Kansas, and Oregon in relation to variation in ambient temperature during the egg-laying period (top frame: r = –0.153, P = 0.004) and the percentage of days on which measurable rain fell during the entire period eggs were in the nest (bottom frame: r = 0.192, P < 0.001). Hatching Asynchrony Our analyses of variation in hatching asynchrony for the full sample of nests and the subset with egg data both yielded 2 competitive models. In all 4, hatching asynchrony was greater in nests with large clutches and when clutches experienced low RainEgg-laying and high Temp1stHalf (Table 4). Within the full sample of nests, asynchrony was also greater when incubation was long, and as suggested by the top model, in replacement nests (Table 4). Greater hatching asynchrony in the subset of nests with egg mass was associated with larger average egg mass in both competitive models, and in the top model, hatching asynchrony tended to be shorter in NY than the other sites (Table 4). Table 4. Results of the generalized linear model analysis of variation in hatching asynchrony of Eastern Kingbirds breeding in Kansas (1980–1983), New York (1979, 1989–2000), and Oregon (2002–2011). Predictor variables included site, clutch size, incubation length, either breeding date or nest status (first nest of the season or replacement nest), and each of 3 measures of ambient temperature (TempEgg-laying, Temp1stHalf, and Temp2ndHalf) combined in pairwise fashion with all 4 measures of precipitation (RainEgg-laying, Rain1stHalf, Rain2ndHalf, and RainTotal). The reported results are limited to models that were within 2 AICc units of the top model. Separate analyses were conducted for the full sample of nests (egg mass not included) and the subset of nests with information on egg mass. Egg mass was included in all of the latter analyses. Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests)  Clutch size 0.312 ± 0.043 1 48.319 <0.001 0.000  RainEgg-laying –0.279 ± 0.074 1 13.754 <0.001  Temp1stHalf 0.020 ± 0.009 1 4.533 0.033  Incubation length 0.081 ± 0.036 1 4.958 0.026  Nest status 0.117 ± 0.076 1 2.365 0.124  Clutch size 0.303 ± 0.043 1 46.204 <0.001 0.280  RainEgg-laying –0.289 ± 0.074 1 14.801 <0.001  Temp1stHalf 0.024 ± 0.009 1 7.155 0.008  Incubation length 0.085 ± 0.036 1 5.512 0.019 Egg mass included (n = 281 nests) Site – 2 4.983 0.083 0.000  Clutch size 0.380 ± 0.049 1 54.190 <0.001  RainEgg-laying –0.276 ± 0.084 1 10.563 0.001  Temp1stHalf 0.044 ± 0.012 1 12.418 <0.001  Egg mass 0.179 ± 0.084 1 4.516 0.034  Clutch size 0.342 ± 0.046 1 49.431 <0.001 0.761  RainEgg-laying –0.255 ± 0.082 1 9.472 0.002  Temp1stHalf 0.0294 ± 0.010 1 8.342 0.004  Egg mass 0.164 ± 0.079 1 4.306 0.038 Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests)  Clutch size 0.312 ± 0.043 1 48.319 <0.001 0.000  RainEgg-laying –0.279 ± 0.074 1 13.754 <0.001  Temp1stHalf 0.020 ± 0.009 1 4.533 0.033  Incubation length 0.081 ± 0.036 1 4.958 0.026  Nest status 0.117 ± 0.076 1 2.365 0.124  Clutch size 0.303 ± 0.043 1 46.204 <0.001 0.280  RainEgg-laying –0.289 ± 0.074 1 14.801 <0.001  Temp1stHalf 0.024 ± 0.009 1 7.155 0.008  Incubation length 0.085 ± 0.036 1 5.512 0.019 Egg mass included (n = 281 nests) Site – 2 4.983 0.083 0.000  Clutch size 0.380 ± 0.049 1 54.190 <0.001  RainEgg-laying –0.276 ± 0.084 1 10.563 0.001  Temp1stHalf 0.044 ± 0.012 1 12.418 <0.001  Egg mass 0.179 ± 0.084 1 4.516 0.034  Clutch size 0.342 ± 0.046 1 49.431 <0.001 0.761  RainEgg-laying –0.255 ± 0.082 1 9.472 0.002  Temp1stHalf 0.0294 ± 0.010 1 8.342 0.004  Egg mass 0.164 ± 0.079 1 4.306 0.038 Open in new tab Table 4. Results of the generalized linear model analysis of variation in hatching asynchrony of Eastern Kingbirds breeding in Kansas (1980–1983), New York (1979, 1989–2000), and Oregon (2002–2011). Predictor variables included site, clutch size, incubation length, either breeding date or nest status (first nest of the season or replacement nest), and each of 3 measures of ambient temperature (TempEgg-laying, Temp1stHalf, and Temp2ndHalf) combined in pairwise fashion with all 4 measures of precipitation (RainEgg-laying, Rain1stHalf, Rain2ndHalf, and RainTotal). The reported results are limited to models that were within 2 AICc units of the top model. Separate analyses were conducted for the full sample of nests (egg mass not included) and the subset of nests with information on egg mass. Egg mass was included in all of the latter analyses. Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests)  Clutch size 0.312 ± 0.043 1 48.319 <0.001 0.000  RainEgg-laying –0.279 ± 0.074 1 13.754 <0.001  Temp1stHalf 0.020 ± 0.009 1 4.533 0.033  Incubation length 0.081 ± 0.036 1 4.958 0.026  Nest status 0.117 ± 0.076 1 2.365 0.124  Clutch size 0.303 ± 0.043 1 46.204 <0.001 0.280  RainEgg-laying –0.289 ± 0.074 1 14.801 <0.001  Temp1stHalf 0.024 ± 0.009 1 7.155 0.008  Incubation length 0.085 ± 0.036 1 5.512 0.019 Egg mass included (n = 281 nests) Site – 2 4.983 0.083 0.000  Clutch size 0.380 ± 0.049 1 54.190 <0.001  RainEgg-laying –0.276 ± 0.084 1 10.563 0.001  Temp1stHalf 0.044 ± 0.012 1 12.418 <0.001  Egg mass 0.179 ± 0.084 1 4.516 0.034  Clutch size 0.342 ± 0.046 1 49.431 <0.001 0.761  RainEgg-laying –0.255 ± 0.082 1 9.472 0.002  Temp1stHalf 0.0294 ± 0.010 1 8.342 0.004  Egg mass 0.164 ± 0.079 1 4.306 0.038 Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Egg mass excluded (n = 342 nests)  Clutch size 0.312 ± 0.043 1 48.319 <0.001 0.000  RainEgg-laying –0.279 ± 0.074 1 13.754 <0.001  Temp1stHalf 0.020 ± 0.009 1 4.533 0.033  Incubation length 0.081 ± 0.036 1 4.958 0.026  Nest status 0.117 ± 0.076 1 2.365 0.124  Clutch size 0.303 ± 0.043 1 46.204 <0.001 0.280  RainEgg-laying –0.289 ± 0.074 1 14.801 <0.001  Temp1stHalf 0.024 ± 0.009 1 7.155 0.008  Incubation length 0.085 ± 0.036 1 5.512 0.019 Egg mass included (n = 281 nests) Site – 2 4.983 0.083 0.000  Clutch size 0.380 ± 0.049 1 54.190 <0.001  RainEgg-laying –0.276 ± 0.084 1 10.563 0.001  Temp1stHalf 0.044 ± 0.012 1 12.418 <0.001  Egg mass 0.179 ± 0.084 1 4.516 0.034  Clutch size 0.342 ± 0.046 1 49.431 <0.001 0.761  RainEgg-laying –0.255 ± 0.082 1 9.472 0.002  Temp1stHalf 0.0294 ± 0.010 1 8.342 0.004  Egg mass 0.164 ± 0.079 1 4.306 0.038 Open in new tab Nestling Starvation The probability that a nest experienced starvation was greatest in nests in which incubation was long and brood size large (Table 5). And although trending in the predicted direction of increasing likelihood of starvation with greater hatching asynchrony (Figure 5), hatching asynchrony was an uninformative variable (sensuArnold 2010) and the combination of incubation length, brood size, and hatching asynchrony was therefore not a competitive model (Table 5). All other combination of variables with incubation length and brood size produced models with ΔAICc ≥ 3.714. Predictably, the number of young fledged increased with brood size, and the only apparent competitive models included either incubation length or hatching asynchrony (Table 5). However, both variables were also uninformative (sensuArnold 2010). Moreover, neither hatching asynchrony (Figure 5) nor incubation length contributed significantly to variation in number of young fledged. Hence, hatching asynchrony did not influence the likelihood that a nest would experience starvation or affect the number of young fledged. Table 5. Results of the generalized linear model analysis of variation in the probability that a nest experienced starvation and number of young fledged/successful nest by Eastern Kingbirds breeding in Kansas (1980–1983), New York (1979, 1989–2000), and Oregon (2002–2011). Predictor variables included site, hatching asynchrony, brood size, incubation length, and either breeding date or nest status (first nest of the season or replacement nest. Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Probability that a nest experienced starvation  Incubation length 0.810 ± 0.290 1 8.777 0.003 0.000  Brood size 0.756 ± 0.322 1 6.107 0.014  Incubation length 0.785 ± 0.284 1 7.974 0.005 1.831  Brood size 0.756 ± 0.322 1 6.107 0.014  Hatching asynchrony 0.192 ± 0.392 1 0.240 0.624 Number of young to fledge  Brood size 0.784 ± 0.076 1 87.955 <0.001 0.000  Brood size 0.773 ± 0.076 1 85.293 <0.001 0.485  Incubation length –0.087 ± 0.069 1 1.587 0.208  Brood size 0.797 ± 0.079 1 84.970 <0.001 1.710  Hatching asynchrony –0.062 ± 0.103 1 0.361 0.548 Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Probability that a nest experienced starvation  Incubation length 0.810 ± 0.290 1 8.777 0.003 0.000  Brood size 0.756 ± 0.322 1 6.107 0.014  Incubation length 0.785 ± 0.284 1 7.974 0.005 1.831  Brood size 0.756 ± 0.322 1 6.107 0.014  Hatching asynchrony 0.192 ± 0.392 1 0.240 0.624 Number of young to fledge  Brood size 0.784 ± 0.076 1 87.955 <0.001 0.000  Brood size 0.773 ± 0.076 1 85.293 <0.001 0.485  Incubation length –0.087 ± 0.069 1 1.587 0.208  Brood size 0.797 ± 0.079 1 84.970 <0.001 1.710  Hatching asynchrony –0.062 ± 0.103 1 0.361 0.548 Open in new tab Table 5. Results of the generalized linear model analysis of variation in the probability that a nest experienced starvation and number of young fledged/successful nest by Eastern Kingbirds breeding in Kansas (1980–1983), New York (1979, 1989–2000), and Oregon (2002–2011). Predictor variables included site, hatching asynchrony, brood size, incubation length, and either breeding date or nest status (first nest of the season or replacement nest. Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Probability that a nest experienced starvation  Incubation length 0.810 ± 0.290 1 8.777 0.003 0.000  Brood size 0.756 ± 0.322 1 6.107 0.014  Incubation length 0.785 ± 0.284 1 7.974 0.005 1.831  Brood size 0.756 ± 0.322 1 6.107 0.014  Hatching asynchrony 0.192 ± 0.392 1 0.240 0.624 Number of young to fledge  Brood size 0.784 ± 0.076 1 87.955 <0.001 0.000  Brood size 0.773 ± 0.076 1 85.293 <0.001 0.485  Incubation length –0.087 ± 0.069 1 1.587 0.208  Brood size 0.797 ± 0.079 1 84.970 <0.001 1.710  Hatching asynchrony –0.062 ± 0.103 1 0.361 0.548 Variable . Coefficient (±SE) . df . χ 2 . P . ΔAICc . Probability that a nest experienced starvation  Incubation length 0.810 ± 0.290 1 8.777 0.003 0.000  Brood size 0.756 ± 0.322 1 6.107 0.014  Incubation length 0.785 ± 0.284 1 7.974 0.005 1.831  Brood size 0.756 ± 0.322 1 6.107 0.014  Hatching asynchrony 0.192 ± 0.392 1 0.240 0.624 Number of young to fledge  Brood size 0.784 ± 0.076 1 87.955 <0.001 0.000  Brood size 0.773 ± 0.076 1 85.293 <0.001 0.485  Incubation length –0.087 ± 0.069 1 1.587 0.208  Brood size 0.797 ± 0.079 1 84.970 <0.001 1.710  Hatching asynchrony –0.062 ± 0.103 1 0.361 0.548 Open in new tab Figure 5. Open in new tabDownload slide Variation (mean ± SE) in the percentage of nests to experience starvation (white bars) and number of young to fledge (gray bar) in relation to degree of hatching asynchrony for nests of Eastern Kingbirds from New York, Kansas, and Oregon that survived to fledge young. Figure 5. Open in new tabDownload slide Variation (mean ± SE) in the percentage of nests to experience starvation (white bars) and number of young to fledge (gray bar) in relation to degree of hatching asynchrony for nests of Eastern Kingbirds from New York, Kansas, and Oregon that survived to fledge young. DISCUSSION We found that both incubation length and hatching asynchrony of Eastern Kingbirds varied geographically, that neither trait was individually repeatable, and that both varied with ambient temperature and precipitation. Indeed, although geographic differences in incubation length (NY > KS) might be related to unmeasured variables such as food supply (which might affect female incubation behavior), we suspect that site differences were almost certainly driven by climatic differences among sites (Figure 1). We also found that intermediate-size clutches appeared to require the fewest days to complete incubation, and as predicted, hatching asynchrony increased with clutch size. However, our data did not support the hypothesis that increased nestling starvation was a cost of hatching asynchrony. While repeatability of egg size, clutch size, and laying date among birds is well documented (Christians 2002), to our knowledge, we are only the second (see Higgott et al. 2020) to test for the repeatability of incubation length, and the first to test for the repeatability of hatching asynchrony. Neither was repeatable, but for incubation length, this was dependent on establishing that clutch size was highly repeatable and that an apparent association of variation of incubation length with different females arose from the dependence of incubation length on clutch size. Higgott et al. (2020) likewise showed that incubation length was not repeatable in Long-tailed Tits (Aegithalos caduatus). Repeatability represents a potential upper limit to the heritability of a trait (Falconer and Mackay 1996), and given probable strong selection to minimize length of exposure to nest predators (Remeš 2007), which is the main source of nest loss in both kingbirds and Long-tailed Tits (Higgott et al. 2020), minimal heritable variation in either trait is expected (Falconer and Mackay 1996). Incubation length for most female kingbirds was 15 days, and the allometrically predicted (Birchard and Deeming 2015) length, based on mean egg mass for these populations (Table 2), was longer (15.5–16.0 days) than the observed mean (≤15.1 days). Thus, the absence of repeatable variation in incubation length and shorter than predicted incubation periods suggest past strong selection to reduce time in incubation. Nonetheless, incubation length ranged from 13 to 17 days. Clutch size was the only female trait that contributed consistently to variation in incubation length, except possibly for nest status; incubation length was longer in replacement nests in the subset of nests with egg mass, suggesting a possible negative carryover effect from the first attempt. Much if not most of the existing variation in incubation length seems more likely driven by environmental factors, namely daily variation in ambient temperature and precipitation. Admittedly, our analyses did not account for most of the variation in either trait, but we strongly suspect this was a consequence of, given the distances between nests and weather stations, the coarseness of our metrics of daily weather. Negative effects of low ambient temperature on incubation length are known (e.g., Ardia et al. 2006, Vincze et al. 2016), but much less studied is the potential impact of precipitation (but see Higgott et al. 2020). The frequent wetting of nests from rainfall, and consequent increase in nest thermal conductance (Reid et al. 2002a, Hilton et al. 2004), likely causes rapid heat loss from eggs. We thus predicted longer incubation periods during periods of frequent rain, and indeed, longer incubation periods were associated with both low temperatures and frequent rain. However, an equally likely alternative explanation, given that male kingbirds neither share in incubation duties nor feed incubating females, and that low temperatures and precipitation reduce the availability of flying insects for aerial foraging birds such as kingbirds (Bryant 1975, Davies 1977, Järvinen and Väisänen 1984, Nooker et al. 2005), is that the extended incubation associated with low temperature and frequent precipitation arose from the need for females to remain off the nest longer to meet energy requirements. Indeed, it seems likely that the 2 effects may act additively. Predicted incubation length, based on results of our regression analyses, for 2 and 5 egg clutches at the lowest TempEgg-laying and highest RainTotal were 16.0 and 15.5 days, respectively. Comparable figures under the best of conditions for those same periods predicted incubation periods of 14.6 and 14.4 days, respectively, for clutches of 3 and 4 eggs. Thus, the combination of clutch size and daily weather appears to account for nearly a third of the range of variation in incubation length (1.6 days/5 days = 0.32). Given that nest construction, including materials of variable insulative value (Hilton et al. 2004), is likely to affect heat loss (Windsor et al. 2013, Rohwer et al. 2015), we suggest it likely that a significant portion of the remaining variation is attributable to microclimatic differences among nests and differences in nest quality. Although our limited sample of 5-egg clutches urges caution in concluding that the largest clutches are inherently disadvantaged by a long incubation, such results are not unprecedented (Moreno and Carlson 1989, Magrath 1992, Engstrand and Bryant 2002, Arnold 2011). Why incubation length was shortest for intermediate-sized clutches is potentially explained by several hypotheses, none of which can be eliminated with our data. For 2-egg clutches, incubation may have been long because of the low thermal inertia and greater rate of heat loss from eggs in small clutches when females were off the nest feeding (e.g., Reid et al. 2000, 2002b). Extrinsic to the clutch itself, and assuming that small clutches are typical of either low-quality females or occupation of a low-quality habitat, such females may have had lower average egg temperatures because of their need to spend more time off the nest feeding. The long incubation length of large clutches was potentially a consequence of greater energy demand of keeping more eggs warm (Ardia et al. 2006), and consequent lower average egg temperature (Nord et al. 2010). Equally likely, larger clutches may have taken longer to incubate because of low efficiency of incubation (e.g., Engstrand and Bryant 2002). Clutches of 5 eggs are uncommon to rare in all kingbird populations (M. T. Murphy, personal communication), and brood patches may have evolved for optimal incubation of the intermediate-sized clutches that comprise >90% of all kingbird reproductive attempts. A third possibility, given that hatching asynchrony increased with clutch size, is the need to provide food for hatchlings may have caused female “neglect” of last laid eggs, leading to delayed hatching. Hatching asynchrony is widespread and the proposed explanations for why incubation is usually initiated with the penultimate egg in north temperate breeding birds (Clark and Wilson 1981) are numerous (Stoleson and Beissinger 1995). Our intent was not to test alternative hypotheses, but instead, we sought to describe potential geographic differences in hatching patterns, identify sources of variation, and assess whether hatching asynchrony was costly (i.e., greater nestling starvation). The 2 days required to hatch most kingbird clutches at all sites is common among north temperate breeding passerines, but the 3 days required for some broods (7.6% of total) is less common. Hatching asynchrony increased with clutch size, as found in other species (Smith 1988, Briskie and Sealy 1989, Magrath 1992, Hébert and Sealy 1993), and the significant site differences in kingbird hatching asynchrony (NY < OR) that emerged from the univariate analyses were likely attributable to geographic differences in clutch size (OR > NY) and weather (Table 4). Contrary to some (Bancroft 1985, Murphy and Fleischer 1986, Moreno and Carlson 1989, Magrath 1992, Murphy 1994) we did not find that hatching asynchrony was more common later in the breeding season. Nor did there appear to be a carryover effect from first to replacement nest as hatching asynchrony did not differ between them. On the other hand, we found, as have a few others (Veiga 1992, Ardia et al. 2006, Griffith et al. 2016), a greater degree of hatching asynchrony when clutches experienced higher ambient temperatures early in incubation. Revealingly, hatching asynchrony was also greater in nests that experienced dry conditions during egg-laying, the exact period when staggered development is likely established. The higher thermal conductivity of wet nests would compromise a female’s ability to maintain the higher egg temperatures needed to induce developmental differences among embryos (Hilton et al. 2004). However, an alternative explanation again exists because we cannot rule out the possibility that, regardless of the nest’s thermal environment, drier and warmer conditions during these periods allowed females to begin and maintain incubation in earnest earlier in the egg-laying and incubation periods, respectively (see Ardia et al. 2006). Regardless, the degree of hatching asynchrony, while possibly being a female strategy to maximize offspring production (Lack 1968, Clark and Wilson 1981), was in part a product of the ambient thermal conditions. Why large eggs would be associated with greater hatching asynchrony is unclear. Repeatability of egg size of kingbirds is particularly high (see above and Murphy 2004), and one possible explanation for the positive association of egg size and hatching asynchrony is that higher quality females may produce large eggs, and these same high-quality females may be able to also initiate incubation earlier than other females (e.g., Grimaudo et al. 2020). Importantly, although a tendency existed for an increased likelihood of starvation as hatching asynchrony increased (Figure 5), it was not significant and the number of young fledged was independent of hatching asynchrony (Figure 5). Hence, regardless of the age disparities of young, above-average hatching asynchrony did not appear to be costly to parental fitness. The question of why broods are usually hatched asynchronously (81% of broods) remains, but the facts that most nests fail because of nest predators (Murphy 1986, 2000, Murphy et al. 2020), and nestling starvation was uncommon (only 6.2% of young in nests that survived to fledging), casts doubt on the hypothesis that hatching asynchrony evolved as a strategy to bring brood size in line with current food supplies (Lack 1968). SUMMARY Our attempts to determine whether variation in incubation length and hatching asynchrony derive mainly from properties intrinsic to females or the extrinsic environment suggest that the latter is likely the dominant influence for incubation length. Hatching asynchrony, as in other species (e.g., Gilby et al. 2013), is probably primarily under female control but ambient temperature and precipitation may dampen or heighten its expression. Given the dramatic differences in ambient temperature (Figure 1) and precipitation among sites, it seems surprising that even larger differences in incubation length and possibly hatching asynchrony were not recorded, especially since our analyses ignored all aspects of nest exposure to solar radiation and wind, the former of which is likely to exacerbate high-temperature effects for kingbird nests that are frequently placed on the canopy edge of trees and fully exposed to the sun (Murphy et al. 1997). This attests to the importance of female behavior and possibly also to selection of nest microhabitats and insulative properties of nests (e.g., Crossman et al. 2011, Windsor et al. 2013, Rohwer et al. 2015). Much additional work is needed to reveal the proximate mechanisms, including potentially female incubation rhythms (Rohwer and Purcell 2019), but also nest site choice, nest properties, clutch size, and egg size and composition, used by females to successfully bring eggs through incubation to hatch in the face of often extreme physical challenges. ACKNOWLEDGMENTS We would like to thank the numerous private landowners in Kansas and New York who granted permission to work on their land, and the staff of Malheur National Wildlife Refuge and the Malheur Field Station for their support. David Bohnert of Oregon State University and the Eastern Oregon Agricultural Research Center provided access to weather data. Helpful comments on an earlier version were provided by Nathan W. Cooper, Daniel R. Ardia, and 2 anonymous reviewers. Funding statement: Research was supported by grants from the U.S. National Science Foundation to MTM (BSR-9106854 and IOB-0539370), an NSERC grant from the Canadian Government, and additional student grants provided by the Forbes-Lea Fund of Portland State University, the E. Alexander Bergstrom Memorial Research Award of the Association of Field Ornithologists, the Frank M. Chapman Fund from the American Museum of Natural History, the American Ornithologists’ Union Student Research Fund, and the Association for the Study of Animal Behaviour. Ethics statement: All capture, handling, and banding of birds were conducted under USGS permit number 22230 of MTM, while permission to conduct research in Oregon at Malheur National Wildlife Refuge was through permits to MTM (13570-030117, 13570-060205, 13570-06008). Research at other locations was conducted with the permission of private landowners. 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OrnithologyOxford University Press

Published: May 18, 2021

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