Post‐fledging survival of altricial birds: ecological determinants and adaptation
2016; Association of Field Ornithologists; Volume: 87; Issue: 3 Linguagem: Inglês
10.1111/jofo.12157
ISSN1557-9263
AutoresBeat Naef‐Daenzer, Martin U. Grüebler,
Tópico(s)Ecology and Vegetation Dynamics Studies
ResumoFor altricial young, fledging is an abrupt step into an unknown environment. Despite increasing numbers of studies addressing the post-fledging period, our current knowledge of the causes and consequences of post-fledging survival remains fragmentary. Here, we review the literature on post-fledging survival of juvenile altricial birds, addressing the following main questions: Is low post-fledging survival a bottleneck in the altricial reproductive cycle? What is known of proximate and ultimate causal factors such as trophic relations (food and predation), habitat conditions, or abiotic factors acting in the post-fledging period? We analyzed weekly survival estimates from 123 data series based on studies of 65 species, covering weeks 1–13 post-fledging. As a general pattern, survival of fledglings was low during the first week post-fledging (median rate = 0.83), and improved rapidly with time post-fledging (week 4 median rate = 0.96). For ground-nesting species, survival immediately after leaving nests was similar to egg-to-fledging survival. For species breeding above-ground, survival during the first week post-fledging was substantially lower than during both the nestling period and later post-fledging stages. Thus, the early post-fledging period is a bottleneck of markedly elevated mortality for most altricial species. Predation was the main proximate cause of mortality. Various factors such as habitat, annual and seasonal variation in the environment, and the physical condition of fledglings have been found to affect post-fledging survival. Individual survival depended strongly on physical traits such as mass and wing length, which likely influence the ability of fledglings to escape predation. Trophic relationships at various levels are the main ultimate driver of adaptation of traits relevant to survival during the pre- and post-fledging periods. Spatiotemporal dynamics of food resources determine the physical development of juveniles and, in turn, their performance after fledging. However, predators can cause quick and efficient selection for fledgling traits and adult breeding decisions. Parental strategies related to clutch size and timing of breeding, and the age and developmental stage at which young fledge have substantial effects on post-fledging survival. The intensity and duration of post-fledging parental investment also influences fledgling survival. Post-fledging mortality is therefore not a random and inevitable loss. Traits and strategies related to fledging and the post-fledging stage create large fitness differentials and, therefore, are integral, yet poorly understood, parts of the altricial reproductive strategy. Para juveniles altriciales, salir del nido es un paso abrupto hacia un ambiente desconocido. A pesar del incremento en los estudios investigando el periodo posterior a la salida, nuestro conocimiento actual de las causas y consecuencias de la supervivencia luego de salir del nido es fragmentada. Aquí, revisamos la literatura sobre la supervivencia de aves juveniles altriciales posterior a su salida del nido, con el fin de responder las siguientes preguntas principales: es la baja supervivencia luego de salir del nido un cuello de botella en el ciclo reproductivo altricial? Que sabemos sobre los factores causales últimos y proximales, como las relaciones tróficas (comida y depredación), condiciones del hábitat o factores abióticos que influencian el periodo posterior a la salida del nido? Analizamos estimados semanales de supervivencia de 123 series de datos basados en estudios de 65 especies, cubriendo 1–13 semanas posteriores a la salida del nido. Como patrón general, la supervivencia de los volantones fue baja durante la primera semana posterior a la salida (mediana de la tasa = 0.83) y mejoro rápidamente con el tiempo luego de la salida (semana 4 mediana mediana de la tasa = 0.96). Para especies que anidan en el suelo, la supervivencia inmediatamente después de salir del nido fue similar a la supervivencia de huevo a volantón. Para especies que anidan por encima del suelo, supervivencia durante la primera semana posterior a la salida fue substancialmente menor que durante los periodos de anidación y periodos tardíos posteriores a la salida. Consecuentemente, el periodo temprano posterior a la salida del nido es un cuello de botella con una marcada mortalidad elevada para la mayoría de especies altriciales. Depredación fue la principal causa proximal de mortalidad. El hábitat, variación anual y estacional del ambiente y la condición de los volantones han sido reportados como factores que afectan la supervivencia posterior a la salida del nido. La supervivencia individual dependió fuertemente de caracteres físicos como masa, longitud del ala, los cuales probablemente influencian la habilidad de los volantones de escapar a los depredadores. Relaciones tróficas en varios niveles son el factor ultimo de adaptación de caracteres relevantes para la supervivencia durante los periodos previos y posteriores a la salida del nido. La dinámica espacio-temporal de los recursos alimenticios determinan el desarrollo físico de los juveniles y por lo tanto su rendimiento después de salir del nido. Sin embargo, los depredadores pueden causar selección rápida y eficiente para los caracteres de los volantones y de las decisiones de reproducción en los adultos. La intensidad y la duración de la inversión parental posterior a la salida del nido también influencia la supervivencia de los volantones. La mortalidad posterior a la salida del nido es por lo tanto no aleatoria y una perdida inevitable. Los caracteres y las estrategias relacionadas con la salida del nido y la etapa posterior a esta salida, crean diferencias grandes en la aptitud y por lo tanto son una parte integral pero poco comprendida de la estrategia de reproducción altricial. Many physiological and behavioral adaptations within the gradient from precocial to altricial avian reproduction have been described (Ricklefs 1968, Ricklefs and Bloom 1977). Precocial species produce well-developed hatchlings able to move and forage on their own. Parents provide limited post-hatching care, e.g., guiding young to food resources and protecting them from predators (e.g., Dreitz 2009, Rickenbach et al. 2011). The period of chick growth and coherence of families may nevertheless be remarkably long and the precocial reproductive strategy is generally described as "slow", with relatively slow chick growth rates and low parental investment per chick. Among altricial species, reproductive investment appears to be more equally balanced between the sexes. Mates can cooperate in provisioning broods and, as a result of intensive parental care, nestlings grow at rapid rates (Starck and Ricklefs 1998). One potential fitness advantage of the "fast" altricial breeding strategy is that more than one brood can be raised per season. A large range of morphological, physiological, and behavioral species-specific traits is related to the altricial reproductive strategy (Dial 2003). In the altricial ontogeny, fledging is a unique step. Across species, the timing of fledging varies with the age and the physical development of fledglings. Within-species variation in these traits is small (Roff et al. 2005, Martin 2015a,b), suggesting that the stage at which juveniles leave nests is fitness-relevant and has evolved in response to specific factors. The duration and extent of parental care after young fledge also varies considerably among species. In the context of the ecology and evolution of reproductive systems, altricial birds have been studied extensively, but with a greater focus on the pre-fledging period. Three main points have been the focus. First, studies within and across species show that energetic limitations may drive selection on life-history functions ranging from nest characteristics, number of clutches, and clutch size, to the timing of breeding and food provisioning (e.g., Martin 1987, Newton 1998, Charnov 2000, Verhulst and Nilsson 2008). Second, predation on parents and offspring has been found to exert selection pressure on reproductive traits, e.g., growth rates and timing of fledging (Martin 2009). Third, avian evolutionary ecology is adjusted based on habitat and the availability of resources (Verhulst and Tinbergen 1991, Svensson and Nilsson 1995, Naef-Daenzer et al. 2004, Clutton-Brock and Sheldon 2010, Fuller 2012). In this context, the study of the plasticity, heritability, and adaptation of nestling traits in relation to nesting characteristics and habitat conditions has been prominent (Ricklefs 1977, van Noordwijk et al. 1980, 1995, Roff et al. 2005). In the stages of the altricial ontogeny (nestling, post-fledging, independent juvenile, and recruit), the moment of fledging represents an abrupt transition and fledglings suddenly face new challenges. Obviously, juveniles enter unknown habitats and must cope with the resources and risks in those habitats. Also, the abiotic environment, such as thermal conditions and exposure to precipitation, may change abruptly. These changes may result in increased mortality during the transition between life-history stages (Low and Pärt 2009). Lack (1948) was among the first to recognize the post-fledging period of altricial birds as a life-history stage with importance for reproductive output and thus highly relevant in population dynamics and life history evolution. Studies by Drent (1984) and Nilsson and Smith (1985) provided empirical evidence confirming the importance of the early post-fledging stage in the survival of young. Although altricial species are known to provide parental care after fledging, little quantitative evidence concerning juvenile survival, parental strategies, and causal mechanisms is available. Most studies have either concentrated on the period from laying to fledging or the entire period from fledging to first breeding. As one implication, the demographic consequences and evolutionary significance of post-fledging survival are unknown for most species. Studies that specifically address the period of post-fledging dependence have been impeded by the difficulty of following juvenile birds and their parents after fledging. Hence, a crucial component of the altricial life history has been insufficiently detailed. Over the past few decades, new techniques have increasingly provided new opportunities for investigating the fate of young birds after leaving nests, even to track individuals over entire reproductive cycles (Kenward 2001). Tracking large numbers of individuals allows investigators to estimate survival rates accurately and with high temporal resolution (e.g., Cohen and Lindell 2004, Grüebler and Naef-Daenzer 2010a). Accordingly, we now know more about the fate of juvenile altricial birds after fledging, the duration of the post-fledging period (i.e., time between fledging and family break-up; Russell 2000), survival patterns during this period, and the amount of parental care provided to fledglings. Two recent reviews have addressed selected aspects of juvenile survival during the post-fledging period. These were either concentrated on passerines (Cox et al. 2014) or were based primarily on estimates of first-year survival (Maness and Anderson 2013). These overviews confirmed that post-fledging mortality is high during the first 2 weeks after leaving nests. Accordingly, first-year survival is low compared to that of adults in many species (Maness and Anderson 2013). Thus, mortality during the post-fledging period likely affects key demographic parameters such as population growth rates and age structures. Here, we review the recent literature reporting post-fledging survival of the young of altricial species of birds to address survival and the causes of mortality after leaving nests. Are the general patterns related to age and the characteristics of taxa? What is known about influential factors such as habitat conditions, trophic relations, or abiotic factors acting in the early post-fledging period? Under the general hypothesis that life-history traits are subject to evolutionary adaptation (Stearns 1992, Roff et al. 2005), we discuss whether juvenile and parental strategies may maximize post-fledging survival as an integral component of reproductive output and thus fitness. We evaluate the importance of the post-fledging phase with respect to the cascade of life-history stages in the ontogeny of young and the reproductive cycle of parents. Specifically, our objective was to provide a comprehensive synthesis of the importance of the post-fledging period as a life-history stage in the context of the altricial reproductive strategy. We thus focus our review on studies reporting juvenile survival rates with high temporal resolution allowing inference on short-term variation in survival relative to time post-fledging. We characterize patterns and processes that are directly related to the life-history step of fledging. We address the following specific questions: (1) Because fledging is the (irreversible) start of life outside the nest, what determines the timing of this step in relation to the ontogeny of young? (2) What are the general temporal patterns in survival rates in relation to juvenile ontogeny, to season, or to environmental factors? (3) What are the major ecological determinants of survival during the post-fledging period? (4) Which individual qualities affect post-fledging survival? (5) Does post-fledging survival vary in relation to the individual traits of parents and chicks such as the timing of breeding and the physical condition of fledglings? In this context, post-fledging survival is regarded as a potential determinant of parental fitness. 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). 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). 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. 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. 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. 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. 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. 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). 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. 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
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