1 INTRODUCTION

Environmental conditions during development are critical for survival and can affect the expression of behavioral and life-history traits (Lindström, 1999; Metcalfe & Monaghan, 2001). Changes in external conditions are particularly relevant for oviparous species (e.g., reptiles and birds). In these species, embryos develop inside an egg and are potentially exposed to environmental shifts that can involve suboptimal conditions for development (Ackerman & Lott, 2004; Ar & Sidis, 2002). In order to reduce such environmental variation, egg-laying species, and birds in particular, have evolved a suite of incubation strategies and behavioral adaptations (Deeming, 2002a; Deeming & Ferguson, 1991).

In birds, eggs are often incubated by breeding individuals in nests (Deeming, 2002a, 2016). The incubating bird forms a functional unit with its nest, providing appropriate conditions for the development of embryos (Deeming, 2016). The functional properties of the bird-nest unit can be shaped by the behavior of the incubating individual (Cooper & Voss, 2013; Deeming, 2002b) and also by the structure and composition of the nest (Hansell, 2000; Hilton et al., 2004). Avian nests vary in composition both among species (Collias, 1997; Hansell, 2000) and within species (e.g., due to adaptive plasticity; Deeming et al., 2012; Mainwaring & Hartley, 2008; Mainwaring et al., 2012; McGowan et al., 2004). Such variation is thought to have an adaptive role in buffering the impact of adverse environmental conditions on the development of embryos and nestlings (Deeming et al., 2012; Mainwaring & Hartley, 2008; Mainwaring et al., 2012). In general, nests built in cold conditions have better thermal insulation (Deeming et al., 2012), for example, at the beginning of the breeding season in temperate habitats (Mainwaring & Hartley, 2008), at high latitudes (Mainwaring et al., 2012, 2014), or at high altitudes (Heenan et al., 2015; but also see Schöll & Hille, 2014). There is, indeed, experimental evidence showing that birds can plastically adjust nest composition in response to shifting environmental conditions (Campbell et al., 2018), which is also supported by correlative studies (Deeming et al., 2012; McGowan et al., 2004).

Materials used by birds to build their nests differ in the thermal properties that they confer (Hilton et al., 2004). In particular, feathers provide high insulation (Hilton et al., 2004; Pinowski et al., 2006; Windsor et al., 2013), which is presumably one reason why feathers are often found at the top layer of nests (i.e., nest cup) in close contact with eggs (Hansell, 2000). Accordingly, nests of several passerine birds contain more feathers when temperatures are colder (e.g., within species, throughout their breeding season; Liljesthröm et al., 2009; Mainwaring & Hartley, 2008; Mainwaring et al., 2012; McGowan et al., 2004). For example, blue tits (Cyanistes caeruleus) and long-tailed tits (Aegithalos caudatus) include more feathers in their nests at the beginning of the breeding season, when temperatures are low, than later in the season when temperatures are higher (Mainwaring & Hartley, 2008; McGowan et al., 2004). The benefits for offspring of adding feathers to the nest are thus predicted to be influenced by variation in environmental conditions. As such, the amount of feathers in nests may have strong positive effects on offspring survival under harsh environmental conditions (e.g., in particularly cold conditions), but weak or no effects in milder environmental conditions. Experimental studies in which the amount of feathers in nests was reduced or increased suggest that feathers have positive effects on the development and survival of nestlings (Dawson et al., 2011; Lombardo et al., 1995; Stephenson et al., 2009; Winkler, 1993). However, there is limited knowledge of the effects of nesting feathers on offspring survival under different environmental conditions (e.g., harsh and mild conditions).

Here, we use detailed data on nest composition, weather conditions, and breeding success to investigate whether the amount of feathers in nests improves the reproductive success of the Eurasian tree sparrow (Passer montanus; Figure 1) and whether detrimental weather effects on breeding success are mitigated by amount of feathers in nests. Tree sparrows show high variation in nest composition, with nests varying in the amount of grasses, human-made materials, and feathers that they contain (Figure 1c; Barlow et al., 2020). In our study population (in a Mediterranean area), tree sparrows have a long breeding season, from April to August. Thus, weather conditions during incubation and nestling growth markedly vary within breeding seasons (i.e., between subsequent breeding attempts of a breeding pair within the same breeding season; see Figure S1) as well as across different breeding seasons. We first evaluate whether environmental conditions have a negative effect on reproductive output in this population of tree sparrows. Then, we investigate whether variation in the amount of feathers in nests is associated with breeding success through the mitigation of negative weather effects on egg and nestling survival. Specifically, if feathers improve nest microclimate, we predict a positive effect of the amount of nesting feathers on egg and nestling survival under harsh weather conditions. We also predict a weak positive effect of feathers, or even no effect, under benign weather conditions. Finally, we investigate temporal variation in the amount of feathers in nests and whether their quantity correlates with environmental conditions. If the use of feathers in nests represents a strategy to cope with adverse environmental conditions in our study population, we predict a negative association between the amount of feathers in nests and air temperature, and a positive association between the amount of feathers in nests and rainfall during reproduction.

2 METHODS

3 RESULTS

3.1 Weather effects on reproductive success

Broods experienced, on average, 19.99 mm of rainfall during the incubation period (standard deviation = 18.92; range = 0–64.3 mm) and 10.24 mm of rainfall during nestling development (SD = 12.51; range = 0–54.3). In these two reproductive stages, mean daily minimum temperatures were similar: 12.60°C (SD = 4.01°C) during incubation and 14.17°C (SD = 4.06°C) during nestling development (see Figure S1 for an illustration of weather conditions throughout the breeding season). First broods were laid between 15 April and 6 June (mean ± SD = 6 May ± 13.18 days) in 2012 and between 10 April and 10 July (mean ± SD = 7 May ± 18.37 days) in 2013. Second broods were laid, on average, 30 days later than first broods in 2012 (mean ± SD = 6 June ± 12.96 days) and 40 days later than first broods in 2013 (mean ± SD = 17 June ± 17.18 days).

The number of nestlings that survived to fledging was strongly and negatively affected by the amount of rainfall fallen during nestling development (i.e., first ten days after hatching; Table 1a; Figure 2). Our analyses indicated a 24% reduction in the number of nestlings that survived to fledgling per 10 mm of rainfall fallen during nestling development. As expected, clutch size had a positive effect on the number of fledged nestlings (ΔAIC = 7.8; Table 1a). The top-model set explaining variation in the number of nestlings that fledged also included effects of clutch completion date, temperature, rainfall during incubation, and breeding year, but models containing these predictors received weak statistical support (Table 1a). Environmental conditions during incubation did not predict the number of nestlings that fledged (Table 1a). We did not find important environmental effects on the number of eggs that hatched (Table 1b). Minimum temperatures and total rainfall during incubation, and clutch completion date, appeared in the top-model set but models without these predictors received very similar statistical support (Table 1b). The number of eggs that hatched was only positively predicted by clutch size (ΔAIC = 16.4; Table 1b). Top models explaining variation in the number of nestlings that fledged and the number of eggs that hatched explained 24.57% and 15.08% of the total variation in each trait (i.e., R² – Nakagawa & Schielzeth, 2013).

TABLE 1. Environmental effects on (a) number of tree sparrow nestlings that successfully fledged and (b) on number of hatched eggs per brood

a) Number of nestlings that fledged (N = 157 broods)
Intercept	Rainfall (incubation)	Rainfall (nestling phase)	Minimum temperature (nestling phase)	Minimum temperature (nestling phase)2	Clutch size	Clutch completion date	Breeding yeara	k	AIC	ΔAIC
0.982		−0.366			0.162	−0.102		6	591.7	0.0
0.980		−0.206	0.067	−0.139	0.149			7	592.1	0.4
0.995	0.071	−0.302			0.158		0.081	7	592.3	0.6
0.997		−0.277			0.148		0.080	6	592.3	0.6
0.982	0.071	−0.321			0.170			6	592.8	1.1
0.984		−0.303			0.161			5	592.8	1.1
0.985			0.217	−0.220	0.146			6	594.2	2.5

b) Number of eggs that hatched (N = 157 clutches)
Intercept	Rainfall (incubation)	Minimum temperature (incubation)	Clutch size	Brood orderb	Clutch completion date	Clutch completion date2	K	AIC	ΔAIC
1.243	0.270	0.230	0.190		0.016	−0.111	8	590.6	0.0
1.248	0.165	0.163	0.199				6	590.9	0.3
1.290	0.091		0.200	−0.112			6	591.0	0.4
1.249			0.190				4	591.3	0.7

Note

• Models within a ΔAIC value of six retained after applying the nesting rule (Richards, 2008) are shown. Model coefficients are mean-centered and scaled by one standard deviation. N = sample size; k = number of model parameters. “Site” and “nest-box ID” were included as random intercepts. Predictors that did not appear in any model within a ΔAIC value of six after applying the nesting rule are not presented in this table (see methods for a full list of predictors included in these models). Top models in a and b explained 24.57% and 15.08% of the total variation in the number of nestlings that fledged and the number of eggs that hatched.
• ^a Estimate for the 2012 breeding year
• ^b Estimate for 1st clutches

3.2 Do feathers in nests mitigate the negative effects of weather conditions on reproductive success?

Overall, nests contained 5.71 g (SD = 3.56 g) of feathers (i.e., 8% of dry nest weight), with similar amounts across the two years of study (Table S1). Nests contained more feathers when minimum temperatures during nestling development were low (Table 2; Figure 3). Despite a moderate correlation between minimum temperatures during nestling development and clutch completion dates, the effect of minimum temperature during development received much stronger statistical support than the effect of clutch completion date in predicting the amount of feathers in nests (Table 2).

TABLE 2. Nests contained more feathers when minimum temperatures were low

Intercept	Clutch completion date	Minimum temperature (nestling phase)	Rainfall (nestling phase)	Breeding yeara	k	AIC	ΔAIC
0.011		−0.461			5	91.7	0.0
0.042	−0.325				5	95.4	3.6
0.022			0.309		5	95.6	3.9
−0.009				−0.274	5	95.7	4.0
0.029					4	97.1	5.4

Note

• The amount of feathers in nests was negatively predicted by minimum temperatures during the nestling rearing phase of reproduction. Models within a ΔAIC value of six retained after applying the nesting rule (Richards, 2008) are shown. Model coefficients are mean-centered and scaled by one standard deviation. N = 32 first broods. k = number of model parameters. “Site” and “nest-box ID” were included as random intercepts. Predictors that did not appear in any model within a ΔAIC value of six after applying the nesting rule are not presented in this table (see methods for a full list of predictors included in these models). Top model explained 44.31% of the total variation in the amount of feathers in nests (i.e., conditional R² - (Nakagawa & Schielzeth, 2013).
• ^a Estimate for the 2012 breeding year.

The amount of feathers in nests did not predict the number of nestlings successfully fledged in our population of tree sparrows (Table S2). Our analysis revealed no effects of nesting feathers on nestling survival, either in isolation or in interaction with environmental conditions (Table S2). Similarly, the number of eggs that survived to hatching was not predicted by the amount of feathers in nests. Clutch size again was the only variable found to strongly determine the number of hatchlings per brood. These results did not significantly change when only first broods were considered (N = 32 broods).

4 DISCUSSION

Nests are key structures for avian reproduction in altricial birds. As well as providing a physical support for eggs and their incubation, nests can function as a protection against detrimental fluctuations in environmental conditions for developing individuals (Ar & Sidis, 2002; Deeming, 2016). In our urban population of tree sparrows, we found a strong negative effect of rainfall on the number of nestlings that fledged per brood, but this negative effect was not mitigated by the amount of feathers added by breeding adult birds to their nests. We did not find evidence suggesting that the amount of feathers, a material with insulation properties, was associated with improved egg survival to hatching or nestling survival to fledgling. The amount of feathers in nests was negatively associated with the minimum temperatures experienced by nestlings during development; however, variation in minimum temperatures during incubation or nestling development did not impact reproductive performance.

Persistent rainfall during the development of nestlings could have negative effects on nestling survival through several mechanisms. Rainfall could have a direct negative effect on the survival of nestlings if it soaks them, increasing their thermoregulatory demands (Kennedy, 1970; Lustick & Adams, 1977; Webb & King, 1984; Wilson et al., 2004). Although this direct negative effect of rainfall could have contributed toward decreasing the overall survival of nestlings in our population of tree sparrows, its contribution was likely of minor importance given that the study species nested in artificial nest boxes (e.g., Wesolowski et al., 2002). If rainfall had entered nest boxes and directly affected developing nestlings, we may have expected a similar negative effect on egg survival (which we did not find), possibly via indirect negative effects on the incubating individual (Coe et al., 2015). Rainfall can also have a negative impact on nestling survival via indirect effects on parental foraging behavior. For example, the feeding rate to offspring decreased in rainy days in small tree finches (Camarhynchus parvulus; Heyer et al., 2020) and great tits (Parus major; Radford et al., 2001). A similar pattern was found in northern wheatears (Oenanthe oenanthe; Öberg et al., 2015) and gray catbirds (Dumetella carolinensis; Johnson & Best, 1982), with rainfall decreasing nest visitation rates by adults and, in turn, nestlings survival (Öberg et al., 2015). Feeding rates of adults to offspring were not recorded in our study, but they could well represent the main mechanism through which rainfall negatively impacted nestling survival in our urban population of tree sparrows.

By reducing energy allocation of nestlings to thermoregulation during rainfall periods, the amount of feathers in nests could alleviate the negative consequences of rainfall for nestling survival. However, we found no evidence for that prediction as negative rainfall effects on the number of nestlings that survived to fledging did not depend on the amount of feathers in nests. Thermal insulation offered by feathers decreases when feathers are wet (Hilton et al., 2004) and, therefore, it is likely that the benefits of using feathers as nest materials may disappear or be reduced when rainfall occurs. Finding that the amount of feathers in nests was associated with minimum temperatures during nestling development contrasts with the lack of an effect of this nest material on nestlings and egg survival. Associations between the amount of nest cup lining, of which feathers are an important component, and spring temperatures have been found in blue tits (Cyanistes caeruleus) and great tits (Parus major) (Deeming et al., 2012; Mainwaring et al., 2012). In such observational studies, early breeders, that experienced colder temperatures, built nests with more lining material than late breeders, as observed here for tree sparrows. In an experimental manipulation of long-tailed tit (Aegithalos caudatus) nests, McGowan et al. (2004) showed that the amount of feathers in nests decreased along the breeding season but experimentally adding feathers to nests did not increase the total amount of feathers in nests and, importantly, did not affect the insulation properties of nests (McGowan et al., 2004). That study indicates low natural variation in the insulation properties of nests despite high variation in the amount of feathers present in nests (McGowan et al., 2004). It is possible, then, that by adjusting the amount of feathers in nests according to environmental temperatures, tree sparrows reduced natural variation in the insulation properties of nests (i.e., keeping nest microclimate within a narrow optimal range) and, hence, the lack of a positive effect of feathers in nests on egg and nestling survival reported here (but see Winkler, 1993). An experimental manipulation of the amount of feathers in nests and nest microclimate would help consolidate our findings that nesting feathers do not improve egg or nestling survival in our population of tree sparrows.

The lack of a positive effect of the amount of nesting feathers in the reproductive success of tree sparrows is in line with experimental studies that showed no relationship between the supplementation of feathers to nests and egg or nestling survival (Dawson et al., 2011; Jarvinen et al., 2017; McGowan et al., 2004). However, by creating subtle changes in nest microclimate, feathers in nests could also improve the body condition of nestlings (Dawson et al., 2005; Lombardo et al., 1995). Our data do not allow us to investigate this possibility, but we cannot discard that natural variation in the amount of feathers in tree sparrow nests was associated with morphological or body condition differences among offspring. The absence of an effect of feathers in nests on the reproductive success of tree sparrows in this study could also be explained by at least two other alternative explanations. First, when nest composition is assessed at the end of the breeding season, the signal of an association between nesting feathers and breeding success may have been weakened if adult tree sparrows extract nest materials from preexisting nests of other tree sparrow pairs (as it happens in other species—e.g., Slager et al., 2012). Second, this negative result may be explained by low variation in temperatures due to living in an urban habitat (Arnfield, 2003). In this context, it is conceivable that the potential benefits of bringing feathers to nests are reduced in cities if urban birds are exposed to milder environmental conditions than nonurban bird populations.

In conclusion, this study provides evidence for negative effects of rainfall on reproduction in an urban cavity-nesting bird population, similarly to those detrimental rainfall effects reported for other species (Heyer et al., 2020; Öberg et al., 2015; Radford et al., 2001; Schöll & Hille, 2020). Additionally, we show that nest composition (i.e., the amount of feathers in nests) did not mitigate these strong negative effects of rainfall on nestling survival; nor did it modulate any effect of temperature on egg or nestling survival. These results suggest that the use of feathers as a nest material has limited consequences for how offspring survive inside nests and cope with short-term fluctuations in environmental conditions.

CONFLICT OF INTEREST

The authors declare that there is no conflict of interest.

AUTHOR CONTRIBUTION

Pablo Capilla-Lasheras: Conceptualization (lead); Data curation (lead); Formal analysis (lead); Funding acquisition (equal); Investigation (lead); Methodology (lead); Project administration (supporting); Visualization (lead); Writing-original draft (lead); Writing-review & editing (lead). Blanca Bondía: Conceptualization (supporting); Data curation (supporting); Investigation (supporting); Writing-review & editing (supporting). Jose Ignacio Aguirre: Conceptualization (supporting); Funding acquisition (equal); Project administration (lead); Resources (lead); Supervision (lead); Writing-review & editing (supporting).