Post-fledging survival of altricial birds: ecological determinants and adaptation

Fledgling developmental stage

We re-analyzed data in Remeš and Martin (2002). These data include estimates of nest survival and relative development of fledglings of 115 species of songbirds. To determine if the developmental stage of fledglings is related to rates of nest predation and to nesting characteristics, we included nest types in our analysis. Our four categories of nest types were ground nests, open exposed nests (close to ground, e.g., in shrubs), open secure nests (e.g., trees, cliffs, and buildings), and cavities. The respective data were collected from www.allaboutbirds.org (Cornell Lab of Ornithology). Analysis of covariance was used to analyze the relationship between relative fledgling mass (fledging mass/adult mass) and adult mass for species in the four nest-type categories. We restricted our analyses to species with body masses below 100 g and excluded two species with extremes in relative fledging mass (Gray-crowned Rosy-Finch, Leucosticte tephrocotis, and Western Meadowlark, Sturnella neglecta).

Post-fledging survival

We searched the large literature databases (JSTOR, Wiley, Wildlife worldwide, Springer Link, Ornithological Worldwide Literature, Searchable Ornithological Research Archive, and Google Scholar) for papers with the relevant keywords (“survival”/“mortality” combined with “fledgling”, “juvenile”, “chick”, “fledging”, “post-fledging”, “first-year”, “age-dependence”, and “independence”). Except for the focus on altricial species, no restriction to taxa was made, i.e., data from studies of small passerines to large birds of prey were included as long as either at least one estimate of survival for the first 2 weeks post-fledging or a series of repeat estimates at weekly or shorter intervals were reported. Reference lists in publications were also checked for additional resources. As a result, we detected some unpublished theses and several papers that were not captured by the key-word search, but that contained post-fledging survival estimates as supplementary information.

We included all quantitative evidence on post-fledging survival, ranging from Cormack-Jolly-Seber estimates for local survival rates to raw proportions of surviving birds calculated from life tables. Similarly, we included data obtained using several observation techniques such as radio-tracking or visual re-observation of marked individuals. We included estimates given relative to time after fledging, but excluded survival rates estimated for seasonal periods because these cannot be accurately related to age post-fledging. We also ignored information given at an ordinal or nominal scale. To extract numerical values from graphically represented data, we used enlarged photographs of published figures and the software package DigitizeIt (Bormann, Braunschweig, Germany).

Raw data were entered in an Excel database and, if necessary, interpolated from the originally used time intervals to the closest weekly interval (e.g., a survival estimate of 0.87 to day 10 post-fledging was calculated as 0.87^(7/10) to day 7). These secondary estimates were used as statistical units and analyzed using general linear models in Statistica Ver.12 (StatSoft Inc., Tulsa, OK).

The primary database included 974 papers matching one or more of the keywords. Of these, we collected 77 references providing point estimates of post-fledging survival for 65 species. In total, we obtained 478 point estimates of weekly survival rates originating from 123 observation series. Depending on species, these estimates covered a period of up to 13 weeks post-fledging (references in Appendix 1).

Statistical analysis

Despite the fair number of observation series from a considerable sample of species, the data set was highly inhomogeneous (descriptive results provided). Therefore, finding an appropriate design for statistical analyses was difficult, and including all potential variables and factors was impossible. We based the analysis on the general hypothesis that the major proximate determinants of post-fledging survival are in the range of individual characteristics and environmental factors. Consequently, the analysis reveals relationships with proximate determinants of post-fledging survival without fully disentangling potential influential factors.

We used General Linear Mixed Models (GLMM) fit by the Laplace approximation to examine factors associated with post-fledging survival. Weekly post-fledging survival estimates were entered as arcsin square root transformed response variables. Time interval, adult body mass, trophic level (predatory or non-predatory), and nest site (ground, open exposed, open secure, or cavity) and the two-way interactions of species characteristics with time interval were included in the model as focus fixed effects. Control variables integrated as fixed effects were the field observation method (visual or telemetry) and the method of analysis (with or without estimation of observation probability). To account for the dependency of survival estimates of different age classes from the same cohort and of different cohorts from the same species, we added the identity of cohort and species as additive random factors. Models were fitted in the program R (R Development Core Team 2013) using the functions glmer from the library lme4 (Bates 2005, 2014). We calculated 95% credible intervals (CrI) for the model parameter estimates as the 2.5% and 97.5% quantiles of 5000 random values sampled from the joint posterior distribution of the model parameters using the function sim() from library arm (Gelman and Hill 2007). Model results are given in back-transformed survival rates.

Supplementary data

To compare post-fledging survival with the survival of juveniles during the nestling stage, we collected information from the Handbook of Central European breeding birds (Glutz von Blotzheim and Bauer 1985, volumes 10-1 to 14-1). We searched the electronic version of the handbook for the terms “Brutdauer” and “Nestlingsdauer” to find information on the duration of the incubation and nestling period and checked the subsequent paragraphs for estimates of total laying-to-fledging survival rates (information about nest survival was not included). From these values, we calculated the average weekly survival rate for the incubation and nestling stages. If available, we also included data provided in the papers on post-fledging survival. In total, 120 estimates of weekly nestling survival for 60 species were collected. Although the species lists for egg-to-fledging survival and for post-fledging survival were not identical, we considered this unproblematic for the inference at the general level given herein.

Developmental stage at fledging

The age and developmental stage at which young birds leave nests are important components of the altricial breeding strategy. For most species of birds, young fledge before they have reached full physical and movement abilities, and are often flightless. Young passerines fledge at ~82% of adult body mass (Remeš and Martin 2002). Young in species under strong predation pressure leave nests at earlier developmental stages and have higher specific growth rates. Our reanalysis of data from Remeš and Martin (2002) revealed additional variation among species with different nest types. For ground-nesting species and species with open exposed nests, slopes were ~0.6 (i.e., nestlings leave nests at 60% of adult mass), whereas the slopes for species that breed in open secure nests and cavities were 0.74 and 0.93, respectively (Table 1, Box 1). These results suggest that the developmental stage at which young birds fledge is adjusted based on environmental factors. Predation is considered the major factor (Box 1). However, questions remain concerning the survival of fledglings to independence. The apparent benefit of leaving nests at an early developmental stage may actually be a disadvantage in terms of survival for the dependent juveniles. Therefore, additional studies are needed to clarify time-survival functions for both the nestling and fledgling life history stages (Roff et al. 2005), and relative to rates of development and allocation of energy to various physical traits.

Table 1. Results of analysis (ANCOVA) accounting for covariate slopes differing between categories of nest types (Overall  = 0.90, F_7,98 = 141.9, P < 0.0001). Dependent variable = fledgling body mass (g), continuous predictor = adult body mass (g), and categorical predictor = nest type (four categories). For ground-nesting species and species with open exposed nests, slopes were ~0.6 (i.e., nestlings leave nests at 60% of adult mass); slopes for species that breed in open secure nests and cavities were 0.74 and 0.93, respectively. Species with an adult body mass below 100 g were included. Data from Remeš and Martin (2002)

Parameter		Coefficient	SE	t	P
	Intercept	0.15	2.035	0.1	0.94
Ground	Slope	0.60	0.074	8.1	<0.0001
Open exposed	Slope	0.59	0.029	20.3	<0.0001
Open secure	Slope	0.74	0.042	17.6	<0.0001
Cavity	Slope	0.93	0.079	11.7	<0.0001
Ground	Intercept	3.21	2.761	1.2	0.25
Open exposed	Intercept	3.85	2.285	1.7	0.095
Open secure	Intercept	3.27	2.504	1.3	0.20
Cavity	Zeroed	0.00

• Statistically significant coefficients are indicated in bold font.

Weekly survival rates

Data extracted from the literature are not homogeneous in terms of time post-fledging, trophic levels, and nest types. Small species are over-represented, and estimates of survival are concentrated on the first 3 weeks post-fledging (Fig. 1A). For week 4 post-fledging and later, few data are available and primarily from larger species.

Box 1. Controversial Evidence – A Life-History Paradox

Theories of life history evolution predict selection favoring characteristics of fledglings that minimize mortality during the “post-fledging bottleneck.” In reality, however, fledglings appear poorly equipped to face the many challenges of the habitats they enter. Why is this? Remeš and Martin (2002) analyzed 115 species of songbirds and found that “under-developed” fledging is a common pattern. Interestingly, the relationship between predation pressure and fledgling developmental stage is negative. Thus, young of species with high rates of nest predation leave nests at earlier developmental stages and are often flightless when they “fledge,” although their growth rates are faster than those of species with lower rates of nest predation. Remeš and Martin (2002) and Martin (2015a,b) hypothesized an adaptive trade-off between the benefits of extending the nestling period until physical development is completed and the cost of longer exposure of nests to predators. Growth characteristics and relative fledging mass differ among nesting strategies. Species breeding on the ground or in exposed nests fledge at an earlier developmental stage (~60% of adult mass) than species breeding in either secure nests or cavities (74% and 93% of adult mass, respectively). Ground-nesting species have significantly higher rates of nest predation than either open nesters or cavity-nesting species.

In contrast to these between-species analyses, single-species studies show that advanced developmental condition of fledglings is of prime importance for post-fledging survival. Young approaching adult body mass and wing length are better at avoiding predation. These effects are so substantial that an extension of the nestling period by only 1–2 days would result in markedly improved post-fledging survival and reproductive success. Thus, for an individual fledgling, an advanced developmental stage improves its prospects for survival. However, what are the potential costs of extending the nestling period for a few days?

Available evidence, therefore, suggests that predation pressure during the nestling period favors a short nestling stage. However, predation appears to select strongly for high fledgling mass and advanced physical development (see Box 2). Within this trade-off, altricial birds may have evolved their very high nestling growth rates. Additional studies are needed to clarify the details and trade-offs in this adaptive feedback cycle.

A fledgling Song Thrush (Turdus philomelos) has left its nest even though its wings are so incompletely developed that they hardly would help in escaping from a predator. Why do fledglings leave nests at such early developmental stages? (Photo: A. Saunier).

Developmental stage of fledglings relative to nest predation rates. (A) Box plot for median relative fledging mass (fledging mass/adult mass) for four types of nests. (B) Box plot for median rates of nest predation for different types of nests (percent of nests lost before fledging). Ground-nesting species have the highest rates of nest predation and fledge at earlier developmental stages than young of other species (Data from Remeš and Martin 2002).

Similarly, with respect to nest types (Fig. 1B), ground-nesting species are underrepresented compared to species with other nest types, and non-predators are better represented than predatory species (Fig. 1C). As mentioned previously, this inhomogeneity results in restricted potential for statistical analyses. For example, no ground-breeding predators are represented (we considered Burrowing Owls, Athene cunicularia, to be cavity-breeders), and all species with body masses below 100 g were non-predators.

For all species, post-fledging survival was low immediately after leaving nests, then steadily increased (Fig. 2) up to the age of 5 weeks post-fledging. The median survival rate for the first week post-fledging was 0.83. For week four, median weekly survival was above 0.95. Thus, across species, about a quarter of fledglings died within 1 month after fledging. However, the variance in survival rates varied strongly among species and within species among different data series. During the first week post-fledging, variation in observed survival rates was particularly large (range = 0.37–1.0). In the low quartile of the data series, weekly survival rates were between 0.37 and 0.68, indicating that, for some species and under certain circumstances, survival rates can be very low (Fig. 2).

The most important main effect in the GLM model is the strong time trend in survival rates (Table 2, Fig. 3). Rates for the first week post-fledging were significantly lower than for subsequent weeks (main effect; Figs. 3A and B). We found a substantial additional effect of the trophic state of species. Non-predatory species had lower first-week survival than predatory species (Fig. 3A). This interaction effect approached significance (P = 0.07). The temporal development of weekly survival rates also differed among species with different nest types (interaction week*nest site; Fig. 2B). Ground-nesting species and species with open, exposed nests had lower first-week survival than species with open, secure nests and cavity-nesting species. The model results suggest that these differences were not due to the larger average body mass of predatory birds because adult mass had no significant additive effect on survival rates.

Inference from single-species studies

In studies where survival was estimated for shorter re-encounter intervals, several investigators reported >10% daily mortality during the first 2 d after leaving nests (Naef-Daenzer et al. 2001, Low and Pärt 2009, Balogh et al. 2011, Sim et al. 2013). This suggests that a marked decline in survival can occur as a direct consequence of fledging. Various potential covariates that modify the general pattern have been tested, most frequently the effects of age, habitat, and body condition. An overview is provided by Cox et al. (2014). Here, we discuss examples of potential extrinsic and species-specific causes of variation in post-fledging survival.

Comparatively low post-fledging survival rates (weeks 1–2) have, for example, been reported for Florida Scrub-Jays (Aphelocoma coerulsecens, Woolfenden 1978), Whinchats (Saxicola rubetra, Tome and Denac 2012), and Ring Ouzels (Turdus torquata, Sim et al. 2013), and particularly high post-fledging survival has been reported for Burrowing Owls (Davies and Restani 2006), Red-bellied Woodpeckers (Melanerpes carolinus, Cox and Kesler 2012), and Dusky Flycatchers (Empidonax oberholseri, Vormwald et al. 2011). Four species in South Africa had first-week survival rates close to 1.0, including Bar-throated Apalises (Apalis thoracica), Cape Robin-Chats (Cossypha caffra), Cape Penduline Tits (Anthoscopus minutus), and Karoo Prinias (Prinia maculosa) (Lloyd and Martin 2016).

Effects of nest type

Comparison of post-fledging survival with egg-to-fledging survival rates reveals that survival after leaving nests is similar to that during the nestling period for ground-nesting species. In contrast, survival during the first days after fledging for open-nesting species and cavity-nesting birds is markedly lower than during the nestling period (Fig. 4), but fledgling survival after 2 weeks post-fledging is high. The pattern for species with exposed open nests is intermediate, with slightly higher egg-to-fledging survival than for ground-nesting species.

Methodological aspects

With respect to methods used, our data set was also very diverse. Radio-telemetry was frequently used in studies of larger species, whereas studies of smaller species included survival estimates based on detection of re-observation probability. In the current data set, we found no significant difference between studies using telemetry or visual detection or studies with or without detection of re-observation probability (Table 2).

Causes of post-fledging mortality

Almost all authors who referred to causes of mortality after fledging note that predation was the major cause, even for “apex-predators” such as Northern Goshawks (Accipiter gentilis, Wiens et al. 2006) and Great Eagle Owls (Bubo lacteus, Rohner 1996). Thus, predation of fledglings appears to be an important determinant, at least as the proximate mechanism (Fig. 5). Relatively few authors discuss potential intermediate causes that influence post-fledging survival rates. Among the factors modulating post-fledging predation rates, fledgling mass (20% of stated effects), fledging date and annual variation (16% combined), and habitat structure (14%) were the most-frequently mentioned factors. Effects of brood size, parent condition, and weather (7%) on post-fledging survival have rarely been addressed. Authors of four papers reported effects of post-fledging parental care on juvenile survival (3%; Styrsky et al. 2005, Grüebler and Naef-Daenzer 2010a,b, Tarwater and Brawn 2010).

Individual characteristics

As summarized above, altricial fledglings are normally not fully developed when they fledge. The analyses of Remeš and Martin (2002) suggest that the age at which young fledge is a specific trait with limited variation compared to, for example, clutch size or the timing of reproduction (see also Woolfenden 1978, Nur 1984, Naef-Daenzer et al. 2001, Deguchi et al. 2002, Dunn et al. 2010). Strikingly, fledglings leave nests at earlier developmental stages when (nest) predation rates are high.

For some species, developmental traits (mass and wing length) were found to be major determinants of post-fledging survival. Naef-Daenzer et al. (2001) showed that fledging mass and seasonal timing of fledging contributed to large variation in early post-fledging survival of Great (Parus major) and Coal (Periparus ater) tits, with no individual in the category of <80% relative fledging mass surviving to independence. For Barn Swallows (Hirundo rustica), wing length was a strong predictor of post-fledging survival (Grüebler and Naef-Daenzer 2010a,b). Several experimental tests have provided evidence that energy flow to the nestlings is a main determinant of fledgling condition and, thus, survival prospects (e.g., Nager 1993, Naef-Daenzer and Keller 1999, Perrig 2015). Therefore, environmental conditions during reproduction and the provisioning performance of parents are crucial predictors of post-fledging survival rates that act via the developmental stage of fledglings.

We found one example for a deviating life history (Tarof et al. 2011). Purple Martins (Progne subis) have an extraordinarily long nestling period of ~4 weeks and, in contrast to most species, fledglings fly instantly over remarkable distances. The authors report a first-week survival rate of 1.0 and a rate of 0.73 to the onset of migration at an age of ~3 weeks, which is markedly higher than reported for other species of swallows (Tarof et al. 2011). For Barn Swallows, by comparison, the rates were 0.81 and 0.40, respectively (Grüebler and Naef-Daenzer 2010a,b).

Parental breeding traits

As introduced in Box 2, parental breeding decisions have been the focus of studies of the evolutionary ecology and reproductive performance of several species (e.g., van Noordwijk et al. 1995, Verboven and Visser 1998, Dawson 2008, Dixon and Haffield 2013). Although investigators have reported differential survival relative to fledgling condition/quality (mainly estimated as fledging mass; e.g., Krementz et al. 1989, Yackel Adams et al. 2001, 2006, Perrig et al. 2014), few have analyzed the potential mechanisms involved (e.g., timing of breeding or post-fledging parental care). Therefore, except for a few species, the impact of variation in parental reproductive traits, their interaction with environmental factors, and the final reproductive output is unclear.

In the first experimental investigation of the effect of parental breeding decisions, the impact of the duration of parental care during the post-fledging period of Barn Swallows was examined. Using a cross-fostering experiment, Grüebler and Naef-Daenzer (2010a) showed that the duration of post-fledging parental care varied markedly among pairs and was the major determinant of post-fledging survival and thus the number of independent offspring produced. Parents caring for their fledglings for 14 d produced 2.5 times more independent offspring than pairs providing 6 d of post-fledging care. With a longer period of parental care, the peak in chick mortality was lower and occurred later. Analyzing timing effects on second broods, Grüebler and Naef-Daenzer (2008, 2010b) found a strong decline in survival of second-brood juveniles with date, particularly during the post-fledging period. Thus, parents have to trade off the benefits of caring longer for first broods against the costs of delaying the start of second broods.

Box 2. Controversial Evidence – The Case of Great Tits

The famous long-term investigations of Great Tits (Parus major) in the Wytham Woods (UK), the Hoghe Veluwe (NL), and on Vlieland (NL) were among the first to reveal evidence concerning the ecological determinants of juvenile survival. Later empirical and experimental studies of the adaptation of clutch size, nestling growth, and timing of breeding have accumulated exemplary insight into the reproductive ecology of the species.

Intriguingly, the early evidence was controversial with respect of the causal mechanisms involved. At the population level, band recoveries suggested that the earliest breeders produced the most recruits (Kluyver 1970, Verboven and Visser 1998, Verhulst and Nilsson 2008). In contrast, studies of individual growth performance showed that it was not the earliest, but those that benefited most from the seasonal development of resources (the “caterpillar peak”) that appeared to have the greatest fitness (Perrins 1991, van Noordwijk et al. 1995, Perrins and McCleery 2001). Studies of the breeding ecology and nestling diet of a major predator, the Eurasian Sparrowhawk (Accipiter nisus), revealed the key role of predation. More than half the diet of nestling Eurasian Sparrowhawks may consist of juvenile birds, creating a marked “tit fledgling peak” in their diet (Geer 1982, Newton and Marquiss 1982, Götmark 2002). However, the interacting effects of food availability and predation remained unclear.

In a pioneering study, Drent (1984) tracked families of Great Tits during the first weeks after fledging by relocating families acoustically and by visual observation of color-banded birds. He found that the first days after leaving nests were a critical bottleneck in the life history of Great Tits. This was later confirmed by radio-tracking fledglings, with particularly high mortality rates during the first 2 days after leaving nests (Naef-Daenzer et al. 2001). Predation is the major determinant of fledgling survival, resulting in immediate selection for high fledging mass and early breeding. Selection differentials for fledging mass are particularly high later in the season, when predation rates are maximal (Naef-Daenzer et al. 2001). The condition of fledglings is also a predictor of their mobility and of the size of family home ranges (Naef-Daenzer and Grüebler 2008). Recent research identified Eurasian Sparrowhawks as the agent of selection for fledging mass (Vedder et al. 2014) and breeding phenology (Götmark 2002).

New insights into the post-fledging period suggest that counteracting evolutionary responses to two seasonal trends in the environment shape reproductive traits. The “caterpillar peak” favors breeders with nestling periods that coincide with the maximum availability of food. However, predation rates of fledglings increase later in the breeding season (the “predation peak”) which results in strong selection pressure for breeding early. Thus, studies conducted during the post-fledging period provided explanations for apparently controversial findings. Optimal laying relative to the availability of resources maximizes the number and quality of chicks before fledging, but optimal laying relative to seasonal variation in predation pressure maximizes the number of fledglings surviving to independence. The resulting trade-off results in a narrow optimal time window for breeding by Great Tits.

The timing of fledging of Great Tits in relation to the peak in food availability (“caterpillar peak”) and the later peak in predation pressure. Top panel: Declining food availability and increasing predation pressure create a narrow time window for optimal fledging dates. Bottom panel: The frequency distributions of fledging dates of all fledglings (black bars) and of those surviving to independence (grey bars) indicates that the overwhelming proportion of birds fledging outside the optimal time window were eliminated during the post-fledging dependence period (Data from Naef-Daenzer et al. 2001).

Habitat

Several investigators have addressed the question of whether post-fledging survival rates are affected by habitat conditions. For example, Cohen and Lindell (2004) found that survival of young White-throated Robins (Irania gutturalis) was best in forest habitat, moderate in pastures, and poor in coffee plantations. Furthermore, nestlings in pasture nests fledged at an earlier age than those in nests in coffee plantations. Slagsvold et al. (2013) reported altitudinal moves by families of Great Tits, apparently following the phenology of food resources. Rohner (1996) found that survival rates of young Great Horned Owls (Bubo virginianus) varied relative to the abundance of their main prey. Balogh et al. (2011) found a marked correlation between spatial variation in post-fledging survival of Gray Catbirds (Dumetella carolinensis) and predator abundance. Haché et al. (2014) found that survival of young Ovenbirds (Seiurus aurocapilla) depended on spatio-temporal variation in predator abundance. Other investigators have reported no relationship between post-fledging survival and habitat characteristics (Robles et al. 2007), forest management (Moore et al. 2010), or a gradient in urbanization (Ausprey and Rodewald 2011, 2013). However, this may be due to the fact that complex patterns in range use may develop soon after fledging (e.g., Ciudad et al. 2009, Maness and Anderson 2013, Cox et al. 2014).

Evolutionary significance

Several investigators have reported that strong selection for certain reproductive traits may occur (Lindén et al. 1992, Perrins and McCleery 2001, Monrós et al. 2002). van Noordwijk et al. (1995) demonstrated marked selection for timing of breeding and fledging mass. Naef-Daenzer et al. (2001) suggested that this selective pressure likely operates during the early post-fledging period for Great Tits (Box 2). The selection differential for fledging mass in Great Tits was up to 1.5 g (adult body mass = ~18 g) and increased with season, suggesting that being heavier is particularly important later in the breeding season when predation pressure is higher. For Great Tits, predation by Eurasian Sparrowhawks (Accipiter nisus) was identified as the major selecting force (Götmark 2002, Vedder et al. 2014).

Remeš and Martin (2002) made clear that nestling growth rates and, in turn, the developmental stages of fledglings vary broadly among species. They suggested that predation pressure is a major driver of this variation, with higher predation rates favoring faster-growing nestlings and shorter nestling periods. Adaptation within the multiple trade-offs in clutch size, chick growth trajectories, and allocation of energy to various physical traits (e.g., mass vs. wing length) may explain general—even global—patterns in the reproductive strategies of altricial species of birds (Martin 2015b). Because physical traits at fledging have frequently been detected as proximate determinants of juvenile survival, potential causal mechanisms for adaptation may operate during the post-fledging period (Magrath 1991, Wiens et al. 2006, Lloyd et al. 2009, Vitz and Rodewald 2011). Even among cavity-nesting species in primeval habitats, the impact of predation on nest and nestling survival is high (Wesolowski 2002, Wesolowski and Tomialojć 2005), suggesting that the mechanism operates similarly (but with varying intensity) over the entire range of nesting strategies.

As presented in Box 1, Remes and Martin (2002) and Martin (2005a,b) built models for the adaptation of fledging age relative to stage-specific mortality rates based on the hypothesis that nestlings are expected to fledge when time-dependent mortality inside the nest exceeds the rate outside. A critical issue in such models is to know the time-dependent survival functions (Roff et al. 2005). These appear not to be uniformly continuous. In contrast, an abrupt change of survival rates linked with fledging is frequent (saw-tooth function, Low and Pärt 2009, Fig. 5). Actually, broader insight into the form of the survival function from egg to independence is lacking.

Differential individual post-fledging survival

First, and possibly most importantly, fledglings face poor survival prospects during the first few days after leaving nests. However, the general pattern varies with species characteristics. For predators, the decline in survival rates after fledging is less pronounced than for non-predators (irrespective of adult body mass). Compared to survival during the nestling period, post-fledging survival of ground-nesting species of birds does not appear to change substantially. In contrast, for species that nest above ground or in cavities, survival during the first week post-fledging has been found to be markedly lower than during the nestling period or the later post-fledging period, creating a marked “bottleneck.” However, post-fledging survival is strongly influenced by environmental factors, individual traits, and condition, and by the breeding decisions of parents. Studies of Great Tits (Box 2) have revealed that the reproductive cycles and phenology of food resources as well as of predators can create quick and strong selection pressures (Naef-Daenzer et al. 2001, Götmark 2002). Therefore, parental breeding decisions and individual characteristics result directly in fitness differentials. In combination with the considerable heritability of reproductive traits (Gebhardt-Henrich and van Noordwijk 1991, Freeman-Gallant and Rothstein 1999, MacColl and Hatchwell 2003), this strongly supports a rapid evolutionary feed-back cycle. Data provided in our review and by Maness and Anderson (2013) support the hypothesis that advanced developmental stages of nestlings (mass and wing length) result in higher post-fledging survival. Further analyses, particularly comparisons between and among species with different nesting characteristics, will be needed to reveal the detailed mechanisms.

Individual traits and behavior

Much evidence for the importance of the development of important physical traits is available in the literature, but few data are available concerning post-fledging behavior and range use. Why, for example, are juvenile birds so noisy? Begging for parental care involves considerable costs in terms of increased risk of predation (Redondo and Castro 1992, Haskell 1994). During the post-fledging period, both the need to beg for parental attention and the probability of attracting predators may be accentuated because young birds are no longer bound to a fixed site.

There are important gaps in our knowledge of the behavior and range use of families of birds during the post-fledging period. In seasonal environments, having young fledge at a relatively early stage may be advantageous because family groups can move to areas with rich resources (e.g., Drent 1984). Similarly, frequent and fast movements may reduce the conspicuousness of young to predators (Naef-Daenzer and Grüebler 2008).

Methodological considerations

Studies of the post-fledging period are still limited by technical and methodological difficulties. Although innovative tracking techniques allow following juvenile birds for increasing periods, other fundamental problems associated with large tracking projects persist.

To estimate survival rates with good precision over short intervals requires large sample sizes. An evident issue is that a sample of birds surviving from one re-encounter interval to the next steadily decreases with the duration of the study. If initial sample sizes are small, the increasing uncertainty of estimates for later stages restrains time-dependent modeling. Therefore, testing mechanistic models that improve survival estimates by including large samples and accounting for re-observation probabilities is important (Naef-Daenzer and Grüebler 2014). However, difficulties at the logistic, personnel, and financial levels rapidly increase with the number of birds to be tracked.

Most studies to date have been correlative, revealing general patterns as a basis to build testable hypotheses about ecological mechanisms and evolutionary consequences. We suggest that studies that include cohorts differing in target variables (e.g., habitat) or that use experimental approaches to manipulate target variables (e.g., age of fledging) would greatly advance our knowledge of the pre- and post-fledging life-history stages. Comparison of post-fledging survival in differing habitats has revealed a strong environmental component (e.g., Cohen and Lindell 2004, Balogh et al. 2011). Experimental approaches such as food supplementation (Thorup et al. 2010, Perrig et al. 2014, Perrig 2015) have tested variation in the energy flow to the brood and its consequences for post-fledging survival. A cross-fostering experiment by Grüebler and Naef-Daenzer (2010a) created variation in the experienced duration of post-fledging parental care and gave insight into the immediate effect of post-fledging parental care.