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Incubation temperature affects the metabolic cost of thermoregulation in a young precocial bird
Abstract
1. The developmental environment plays a key role in determining offspring phenotype, and the parents' behaviour and physiology often dictates developmental conditions. Despite the plethora of studies documenting the importance of incubation temperature on offspring phenotype in reptiles, very few studies have examined such relationships in birds. 2. Because nearly all birds physically incubate their eggs, altering the nest environment may be an important but previously overlooked way parents can influence their offspring's phenotype. Here, we tested the hypothesis that incubation temperature would affect thermoregulation in wood duck (Aix sponsa) hatchlings. 3. We show that a reduction in < 1 °C in incubation temperature affects the metabolic costs of thermoregulation in offspring of a non-domesticated bird, resulting in 27-40% greater increases in oxygen consumption of ducklings incubated at the lowest temperature relative to ducklings incubated at higher temperatures. 4. Because we demonstrate that incubation temperature affects hatchling phenotypic quality, our findings provide novel support for newly proposed frameworks that highlight the importance of incubation temperature to the evolution of clutch size in birds.
... Even if eggs hatch successfully, variation in incubation temperature may still influence offspring condition. Recent studies show that subtle changes in average incubation temperature can influence avian offspring growth rate, immune function, hormone levels, metabolic rate, thermoregulation, and long-term survival (DuRant et al. 2010;DuRant et al. 2011;Nord and Nilsson 2011;DuRant, Hopkins, Hawley, et al. 2012;DuRant, Hopkins, Wilson, et al. 2012;Hepp and Kennamer 2012;DuRant, Hopkins, Carter, et al. 2013;DuRant et al. 2014;Hepp et al. 2015;Berntsen and Bech 2016;Nord and Nilsson 2016). ...
... Lower performance in low temperature-incubated ducklings is consistent with previous studies that showed that a small decrease in average incubation temperature can produce a diverse array of phenotypic differences in birds. In wood ducks, ducklings incubated at a lower temperature grow slower (DuRant et al. 2010), have reduced locomotor performance , inefficient thermoregulatory abilities (DuRant, Hopkins, Wilson, et al. 2012;DuRant, Hopkins, Carter, et al. 2013), reduced immunocompetence (DuRant, Hopkins, Hawley, et al. 2012), altered glucocorticoid and thyroid hormone levels (DuRant et al. 2010;DuRant et al. 2014), and reduced survival (Hepp and Kennamer 2012), compared with those incubated at a higher temperature. Further, altricial blue tits incubated at lower temperatures have slower growth rates and higher metabolic rates than those incubated at higher temperatures (Nord and Nilsson 2011). ...
... For example, it may be more energetically demanding for a duckling incubated at a lower temperature to jump or climb than it is for a duckling incubated at a higher temperature. DuRant, Hopkins, Wilson, et al. (2012) found that wood ducks incubated at a lower temperature expend more energy during a thermoregulatory challenge than those incubated at higher temperatures, and thus, it is possible that similar inefficiencies exist when jumping and climbing. It is also possible that ducklings incubated at a lower temperature had expended more energy during incubation or depleted more of their yolk reserves before hatching (Olson et al. 2006). ...
The environments that animals experience during development have important fitness consequences. In birds, parents influence the developmental environment of their offspring through incubation. Subtle changes in incubation temperature affect offspring morphology and physiology, such as growth, immune function, and thermoregulation, yet little is known about how it may affect critical early-life behaviors. Because expression of behavior can be influenced by the social environment, the effect of incubation temperature on behavior may be context-dependent. We investigated whether incubation temperature and social context influence a critical early-life task in wood ducks (Aix sponsa). Wood ducks nest in tree cavities and, shortly after hatching, ducklings must jump and climb out of the cavity. Failure to exit the nest is fatal. In 2 experiments, we incubated eggs at different mean temperatures and examined the nest exodus of ducklings individually and in mixed-incubation temperature pairs. When tested individually, ducklings incubated at 35.8 °C and 37.0 °C were ~2.5 times more successful at exiting the nest, and jumped and climbed more often, than those incubated at 35.0 °C. However, in an experiment conducted the following year, we found that social interactions mitigated these effects and there was no difference in nest exodus success when ducklings incubated at 35.0 °C and 36.0 °C were tested together in pairs. This may be because, when in pairs, ducklings incubated at the low-temperature experience social enhancement whereas those incubated at the high temperature maintain similar behaviors. These results advance our understanding of how parental effects influence offspring behaviors and performance within different social contexts.
... In response to a change in ambient temperature, incubation behavior, or clutch size, egg temperature may deviate from what is optimal for embryonic development. This can have short-and long-term consequences on offspring phenotype, survival, and sex ratio in species with genotypic sex determination, such as wood ducks (Aix sponsa; DuRant et al. 2010DuRant et al. , 2012aDuRant et al. , 2012bDuRant et al. , 2016Hopkins et al. 2011), megapodes (Goth and Booth 2005;Eiby et al. 2008;Eiby and Booth 2009), and zebra finches (Wada et al. 2015, forthcoming). In megapodes, which use heat from decomposing plant matter to incubate eggs, higher incubation temperatures cause a female-biased sex ratio because of high male embryonic mortality, while lower incubation temperatures result in a male-biased sex ratio because of high female mortality (Goth and Booth 2005;Eiby et al. 2008 higher adrenocortical responses, slower locomotor performance, and higher metabolic rates during a thermal challenge compared with young hatched from middle or high incubation temperatures (DuRant et al. 2010(DuRant et al. , 2012bHopkins et al. 2011). ...
... This can have short-and long-term consequences on offspring phenotype, survival, and sex ratio in species with genotypic sex determination, such as wood ducks (Aix sponsa; DuRant et al. 2010DuRant et al. , 2012aDuRant et al. , 2012bDuRant et al. , 2016Hopkins et al. 2011), megapodes (Goth and Booth 2005;Eiby et al. 2008;Eiby and Booth 2009), and zebra finches (Wada et al. 2015, forthcoming). In megapodes, which use heat from decomposing plant matter to incubate eggs, higher incubation temperatures cause a female-biased sex ratio because of high male embryonic mortality, while lower incubation temperatures result in a male-biased sex ratio because of high female mortality (Goth and Booth 2005;Eiby et al. 2008 higher adrenocortical responses, slower locomotor performance, and higher metabolic rates during a thermal challenge compared with young hatched from middle or high incubation temperatures (DuRant et al. 2010(DuRant et al. , 2012bHopkins et al. 2011). Similar to precocial birds, suboptimal clutch temperatures have been shown to significantly affect the long-term survival of the altricial zebra finch; eggs incubated at the suboptimal temperature of 39.57C had significantly lower long-term survival compared with eggs incubated at 37.97C (Berntsen and Bech 2016). ...
... Avian embryos are ectothermic, although the pattern of thermoregulatory ability differs between precocial and altricial species (Wada et al. 2018). Numerous studies indicate that embryos incubated at lower temperatures take longer to hatch and expend more energy than those at higher temperatures (Booth 1987;DuRant et al. 2012aDuRant et al. , 2012bWada et al. 2015). DuRant et al. (2011) showed that while energy expenditure before external pipping was similar across all incubation temperature groups, wood duck embryos incubated at low temperature expended the most energy during pipping compared with embryos incubated at middle or high temperatures. ...
In oviparous species, the embryonic environment-particularly temperature-can alter phenotype and survival of an individual by affecting its size as well as its metabolic rate. Previous studies have shown that incubation temperatures can affect sex ratio in birds; specifically, low incubation temperatures were shown to produce a male-biased sex ratio in zebra finches (Taeniopygia guttata) possibly because of a higher pre- or postnatal mortality rate in females. We hypothesized that sexes respond differently to suboptimal incubation temperature, leading to a male-biased sex ratio. To test this hypothesis, zebra finch eggs were incubated at 36.1°, 37.5°, or 38.5°C and hatching success, hatchling mass, residual yolk mass, and pectoralis mass were measured. We found that while hatchling mass was similar between the sexes at 37.5°C, female hatchlings were heavier at 36.1°C, and male hatchlings were heavier at 38.5°C. Pectoralis muscle mass was similar between the sexes at 36.1°C; however, at 37.5°C, female pectoralis mass was heavier at hatching than that of males. Females at 37.5°C also had lower residual yolk at hatching compared with males, reflecting a higher use of energy by female embryos compared with male embryos at this temperature. In contrast, residual yolk was similar between the sexes at 36.1° and 38.5°C. Our results suggest that there are sex differences in how incubation temperature alters organ mass and yolk energy reserve; this can lead to a difference in survival at different incubation temperatures between the sexes. Taken together with previous studies showing that females alter incubation behavior with ambient temperature, rising ambient temperatures could impact phenotype and survival of avian offspring in a sex-specific manner.
... This trade-off can be influenced by variation in environmental conditions, clutch size, and nest insulation (Deeming and Mainwaring, 2015;Mainwaring et al., 2014;Reid, Monaghan, & Ruxton, 2000b), which can lead to variation in incubation temperature among and within nests (Boulton & Cassey, 2012;Coe, Beck, Chin, Jachowski, & Hopkins, 2015;Hepp, Kennamer, & Johnson, 2006;Hope et al., 2018;Reid et al., 2000a). As with non-avian reptiles, small differences in average incubation temperature have major impacts on avian phenotype and fitness (wood ducks: DuRant, Hepp, Moore, Hopkins, & Hopkins, 2010, 2012aDuRant, Hopkins, Wilson, & Hepp, 2012b, 2013aHepp & Kennamer, 2012;Hepp, DuRant, & Hopkins, 2015;blue tits: Nord & Nilsson, 2011;zebra finches: Berntsen & Bech, 2016). Unlike most of their non-avian counterparts, however, parental behavior, including elaborate nest construction and time spent incubating, provides a mechanism for avian parents to buffer their developing embryos from fluctuating environmental conditions, or to actively manipulate offspring phenotype during the course of incubation. ...
... Second, incubation temperature is known to influence boldness and fear-related behaviors in nonavian reptiles (Siviter et al., 2017;Trnik, Albrechtová, & Kratochvíl, 2011), and we suspect a similar effect exists for birds. Third, incubation temperature influences avian corticosterone levels (DuRant et al., 2010;Wada et al., 2015), growth rates (DuRant et al., 2010), and metabolic rates (DuRant et al., 2012b;Nord & Nilsson, 2011), all of which are related to proactive/reactive behavioral traits in other species (Biro & Stamps, 2010;Careau et al., 2008;Carere, Groothuis, Möstl, Daan, & Koolhaas, 2003;Cockrem, 2007;Stamps, 2007;Stöwe, Rosivall, Drent, & Möstl, 2010). ...
... ; Sala-Roca,Martí-Carbonell, Garau, Darbra, & Balada, 2002), or other components of the neuroendocrine system (e.g., hormone receptors, size of brain regions, Duckworth, 2015; number and density of neurons,Amiel et al., 2017) underlie differences in behavioral traits.The observed differences in behavior may be associated with other known effects of incubation temperature on physiology and performance. For example, ducklings incubated at a low temperature (35 • C) have greater energy expenditure while in the egg (DuRant,, lower immune function(DuRant, Hopkins, Hawley, & Hepp, 2012a), higher metabolic rates when faced with a thermoregulatory challenge(DuRant et al., 2012b), decreased locomotor performance, reduced thermoregulatory ability(DuRant et al., 2013a), and altered thyroid hormone levels (DuRant, Carter, Denver, ...
The environment in which animals develop can have important consequences for their phenotype. In reptiles, incubation temperature is a critical aspect of the early developmental environment. Incubation temperature influences morphology, physiology, and behavior of non‐avian reptiles, however, little is known about how incubation temperature influences offspring phenotype and behaviors important to avian survival. To investigate whether incubation temperature influences avian behaviors, we collected wood duck (Aix sponsa) eggs from the field and incubated them at three naturally occurring incubation temperatures (35.0, 35.8, and 37.0°C). We conducted multiple repeated behavioral trials on individual ducklings between 5 and 15 days post‐hatch to assess activity, exploratory, and boldness behaviors, classified along a proactive‐reactive continuum. We measured growth rates and circulating levels of baseline and stress‐induced corticosterone levels to investigate possible physiological correlates of behavior. Ducklings incubated at the lowest temperature displayed more proactive behaviors than those incubated at the two higher temperatures. We also found that younger ducklings exhibited more proactive behavior than older ducklings and males exhibited more proactive behavior than females. Further, duckling behaviors were repeatable across time and contexts, indicative of a proactive–reactive continuum of behavioral tendencies. However, neither corticosterone levels nor growth rates were related to behavior. This provides some of the first evidence that incubation temperature, a critical parental effect, influences avian offspring behaviors that may be important for survival. Our results identify incubation temperature as a mechanism that contributes to the development of behavioral traits and, in part, explains how multiple behavioral types may be maintained within populations.
... Ducklings incubated at the lowest temperature develop more slowly and expend more energy than ducklings incubated at higher temperatures [15]. After hatching, these ducklings also have reduced growth and acquired immune responses [16], higher baseline and stress-induced corticosterone levels [17], reduced locomotor performance [18], and expend more energy to thermoregulate [19] than ducklings incubated at higher temperatures ($35.9uC). It is clear that the incubation environment of wood ducks and other birds can influence phenotypic quality in a number of important ways. ...
... Whether this phenotypic variation influences fitness of neonates currently is not known, but will have important implications for investment decisions made by incubating parents and the evolution of life histories (e.g., egg size and clutch size) [20]. In this study, we manipulated incubation period and neonate phenotype of wood ducks by artificially incubating eggs at temperatures similar to those used by Hepp et al. [3], DuRant et al. [16,17,18,19], and Hopkins et al. [18]. Newly-hatched ducklings were individually marked, and broods containing ducklings from each of the incubation temperatures were placed in nests with foster mothers. ...
... wood ducks incubated at higher temperatures grew faster and were in better condition 9 days after hatching than ducklings incubated at low temperatures (35uC) [17]. Further, even though wood duck ducklings incubated at low temperatures have less residual energy, DuRant et al. [19] found they need to expend more energy to maintain their body temperature during thermal challenges than individuals incubated at higher temperatures. The ability to thermoregulate is especially important for young birds, and hypothermia is often an important source of mortality for young ducklings [39]. ...
Avian parents that physically incubate their eggs must balance demands of self-maintenance with providing the proper thermal environment for egg development. Low incubation temperatures can lengthen the incubation period and produce changes in neonate phenotype that may influence subsequent survival and reproduction. We artificially incubated wood duck (Aix sponsa) eggs at three temperature regimes (low, 35.0; mid, 35.9; and high, 37.3°C) that are within the range of temperatures of naturally-incubated nests. We tested the effect of incubation temperature on duckling body composition, fledging success, the probability that females were recruited to the breeding population, and their subsequent reproductive success. Incubation period was inversely related to incubation temperature, and body mass and lipid mass for newly-hatched ducklings incubated at the lowest temperature were lower than for ducklings produced at higher temperatures. In 2008, ducklings (n = 412) were individually marked and broods (n = 38) containing ducklings from each temperature treatment were placed with wild foster mothers within 24 hrs of hatching. Ducklings incubated at the lowest temperature were less likely to fledge from nest sites than ducklings incubated at the higher temperatures. We recaptured female ducklings as adults when they were either prospecting for nest sites (n = 171; 2009-2011) or nesting (n = 527; 2009-2012). Female ducklings incubated at the lowest temperature were less likely to survive and be recruited to the breeding population than females incubated at higher temperatures. Reproductive success of surviving females also was greater for females that had been incubated at warmer temperatures. To our knowledge, this is the first avian study to link developmental conditions experienced by neonates during incubation with their survival and recruitment to the breeding population, and subsequent reproductive success. These results advance our understanding of incubation as an important reproductive cost in birds and support the potential significance of incubation in influencing the evolution of avian life histories.
... In moderate temperatures (19 to 28°C) gull chicks' T b s remain similar to adult T b s, however in colder temperatures their regulative capacities diminish . Indeed, reducing incubation temperatures by as little as 1°C can influence chick phenotype and translate into a 27 to 40% increased metabolic cost in hatchlings (DuRant et al., 2012). Brooding is often initiated by precocial chicks, as they are capable of behavioural thermoregulation (Sherry, 1981). ...
... Understanding, and representing variations in thermoregulatory behaviour and ability are becoming increasingly important in the inclusion of climate change models, particularly for endotherms which have received less attention when compared with ectotherms (Boyles et al., 2011). Metabolic demands fluctuate in response to environmental temperature changes (Lowell and Spiegelman, 2000) and understanding how these may influence the early life stages of endotherms and the resulting phenotypes of offspring (DuRant et al., 2012) has implication for the survival and genetic structure of future populations. Our results highlight the importance that nest microhabitat, life history strategies, and variations within a species can have in the development of an individual's ability to thermoregulate. ...
... FromFig. 1 it is nonetheless apparent that the majority of the post-fledging mortality in all three experimental groups occurred during early life, before 200 d of age, and was highest in birds incubated under the lowest temperature. If the reported physiological effects of sub-optimal incubation temperature, such as reduced immunocompetence (DuRant et al. 2012 ), increased intensity of energy expenditure (Nord and Nilsson 2011), reduced thermoregulatory ability (DuRant et al. 2011) or higher vulnerability to early stress (DuRant et al. 2010 ), would persist beyond the nestling stage such effects could potentially negatively influence individual survival also during the first 200 d of life. However whether such effects are indeed longterm is currently not known and hence we can only speculate as to what the underlying cause of death in our birds is. ...
... We could not detect any difference in embryonic survival between the three treatment groups (Table 2). This result is in line with what has been found in other studies in which eggs have been artificially incubated (DuRant et al. 2011, 2012, but see Hepp et al. 2006, Nord and Nilsson 2011 there seems to be no available information on zebra finches). The overall embryonic survival was only ∼50% (Table 2), however hatching success in unmanipulated nests in the same population of birds is on average 56% (n 17, ...
In birds parental incubation behaviour is an important factor shaping the environmental conditions under which the embryos develop, and sub-optimal incubation temperatures are known to negatively affect early growth and development. It is less well known if variation in incubation temperature can impose life-long differences in individual performance and survival. In the present study we investigated the effects of incubation temperature on long-term survival in a small passerine bird. Using our captive population of the zebra finch Taeniopygia guttata we artificially incubated eggs at three biologically relevant temperatures (35.9, 37.0 and 37.9 oC) for two-thirds of the incubation period and then monitored individual lifespan of the hatched chicks for two and a half years. We found that individuals from eggs incubated under the lowest temperature exhibited significantly lower long-term survival compared to those which had been incubated at the highest temperature. Our results show that incubation temperature in birds, and thus parental incubation behaviour, play an important role in shaping the life-history trajectories of offspring.This article is protected by copyright. All rights reserved.
... It has been suggested that the earlier in an organism's life history environmental stressors are experienced, the more severe the lasting consequences will be [4][5][6], and there is strong empirical evidence across animal taxa for this assertion (Table S1). This forms the basis of our developmental history hypothesis. ...
... In humans, for example, the environment of the womb can significantly affect an individual's chances of cardiac and other diseases later in life [5,7,8]. In birds, the temperature at which eggs are incubated can affect hatchling body composition, growth, immunocompetence and thermoregulatory ability [4,9]. Developmental temperature also affects survival, growth and behavior of juvenile reptiles (e.g., [10]) (Table S1). ...
The world is increasingly impacted by a variety of stressors that have the potential to differentially influence life history stages of organisms. Organisms have evolved to cope with some stressors, while with others they have little capacity. It is thus important to understand the effects of both developmental and evolutionary history on survival in stressful environments. We present evidence of the effects of both developmental and evolutionary history on survival of a freshwater vertebrate, the rough-skinned newt (Taricha granulosa) in an osmotically stressful environment. We compared the survival of larvae in either NaCl or MgCl2 that were exposed to salinity either as larvae only or as embryos as well. Embryonic exposure to salinity led to greater mortality of newt larvae than larval exposure alone, and this reduced survival probability was strongly linked to the carry-over effect of stunted embryonic growth in salts. Larval survival was also dependent on the type of salt (NaCl or MgCl2) the larvae were exposed to, and was lowest in MgCl2, a widely-used chemical deicer that, unlike NaCl, amphibian larvae do not have an evolutionary history of regulating at high levels. Both developmental and evolutionary history are critical factors in determining survival in this stressful environment, a pattern that may have widespread implications for the survival of animals increasingly impacted by substances with which they have little evolutionary history.
... The decreased activity in females is probably caused by females incubating almost exclusively [57]. This does not necessarily mean that females had a lower energy expenditure during the incubation phase, since maintaining the eggs at temperatures suitable for embryonic development is energetically costly [21]. ...
Background
Long-distance migratory birds undergo complex annual cycles during which they must adjust their behaviour according to the needs and conditions encountered throughout the year. Yet, variation in activity throughout the entire annual cycle has rarely been studied in wild migratory birds.
Methods
We used multisensor data loggers to evaluate the patterns of activity throughout the complete annual cycle of a long-distance migratory bird, the red-backed shrike Lanius collurio . Accelerometer data was used to identify life-history stages and to estimate levels of activity during various phases of the annual cycle. In this study, we analysed the variation in daytime activity along the annual cycle and between migratory and non-migratory days.
Results
The birds’ daytime activity varied throughout the annual cycle while night-time activity was almost exclusively restricted to migratory flights. The highest daytime activity levels were observed during the breeding season, while it remained low during autumn migration and the winter period. Daytime activity differed between sexes during the breeding period, when the males showed the highest level in activity. During migratory periods, both sexes exhibited a higher daytime activity in spring compared to autumn migration, being particularly high in the final migratory leg towards the breeding ground. The birds showed a lower daytime activity on migratory days (days when a migratory flight took place during the succeeding night) than on non-migratory days during both migratory seasons.
Conclusions
Activity measured during daytime results from a combination of several behaviours, and a high daytime activity during spring migration and the breeding period is possibly reflecting particularly energy-demanding periods in the annual cycle of migratory birds. The use of multisensor data loggers to track annual activity provides us with a full annual perspective on variation in activity in long-distance migratory species, an essential approach for understanding possible critical life-history stages and migration ecology.
... In cold conditions, reduction in egg temperature results in longer incubation periods (Järvinen 1990;Martin et al. 2018), even under increased incubation effort (Nord et al. 2010). Furthermore, suboptimal egg temperatures during incubation are known to impinge on nestling phenotype, with short-term effects on the thermogenic costs of thermoregulation (DuRant et al. 2012) and BMR (Nord and Nilsson 2011;Wada et al. 2015) as well as on survival in captivity (Berntsen and Bech 2016). We found evidence for long-term effects of varying temperatures during development in the egg on adult metabolic phenotype that seem to be non-reversible judging from the significant repeatability between winters. ...
Basal metabolic rate (BMR) constitutes the lowest metabolic rate in a resting animal and is, therefore, considered to reflect the energetic cost of maintenance in endotherms. BMR is a reversible plastic trait that changes with environmental and ecological circumstances, albeit being heritable and susceptible to selection. Inter-individual variation within populations of small birds is substantial, and while many of the drivers of such variation have been identified, many remain unexplained. We studied winter BMR variation of juveniles over a 15-year period in a wild population of great tits Parus major at the northern border of their distribution. BMR during winter consistently changed between years, even after controlling for environmental factors, suggestive of a non-reversible developmental plasticity shaping the adult metabolic phenotype. BMR in cohorts of wintering great tits varied among winters as a response to minimum ambient temperatures experienced early in life, during the prehatching period. This developmental plasticity might be adaptive if temperatures experienced by growing embryos would metabolically prime them to an environment that they will likely encounter in future life. However, in line with a more unpredictable future climate, the risk of phenotype-environment mismatch is likely to lead to certain cohorts being poorly adapted to prevailing winter conditions, resulting in wider annual fluctuations in population size.
... In cold conditions, reduction in egg temperature results in longer incubation periods (Järvinen 1990;Martin et al. 2018), even under increased incubation effort (Nord et al. 2010). Furthermore, suboptimal egg temperatures during incubation are known to impinge on nestling phenotype, with short-term effects on the thermogenic costs of thermoregulation (DuRant et al. 2012) and BMR (Nord and Nilsson 2011;Wada et al. 2015) as well as on survival in captivity (Berntsen and Bech 2016). We found evidence for long-term effects of varying temperatures during development in the egg on adult metabolic phenotype that seem to be non-reversible judging from the signi cant repeatability between winters. ...
Basal metabolic rate (BMR) constitutes the lowest metabolic rate in a resting animal and is therefore considered to reflect the energetic cost of maintenance in endotherms. BMR is a reversible plastic trait that changes with environmental and ecological circumstances, albeit being heritable and susceptible to selection. Inter-individual variation within populations of small birds is substantial, and while many of the drivers of such variation have been identified, many remain unexplained. Some of the variation can be ascribed to cohort effects, indicating non-reversible developmental plasticity that will shape the adult metabolic phenotype. We studied winter BMR variation of juveniles over a fifteen-year period in a wild population of great tits Parus major at the northern border of their distribution.
Here we show for the first time that winter BMR in cohorts of great tits changes among winters as a response to minimum ambient temperatures experienced early in life, during the prehatching period. This developmental plasticity might be adaptive if temperatures experienced by growing embryos would metabolically prime them to an environment that they will likely encounter in future life. However, in line with a more unpredictable future climate, the risk of phenotype-environment mismatch is likely to lead to certain cohorts being poorly adapted to prevailing winter conditions, resulting in wider annual fluctuations in population size.
... We should note that our model only looked at acute effects, not cumulative effects of the environmental parameters on survival. Extreme temperatures during avian incubation can reduce hatching success (Hepp et al. 2006;DuRant et al. 2010;Nord and Nilsson 2011;Carroll et al. 2018) thermoregulation (DuRant et al. 2012a), metabolic rate (Nord and Nilsson 2011), locomotor performance , growth (Nord and Nilsson 2011), early life behaviour (Hope et al. 2019), reproduction (Hepp and Kennamer 2012) and survival (Hepp and Kennamer 2012;Berntsen and Bech 2016;Nord and Nilsson 2016) in young birds. This highlights the importance of investigating optimal incubation parameters with technology such as data-loggers and with the continued improvement of this technology, application in captive breeding programmes for other avian species will be possible and valuable. ...
Captive breeding is an increasingly used conservation strategy for species with a high risk of extinction in the wild, but managing a captive breeding programme can be challenging if there is a deficiency in knowledge about the species’ breeding biology. A knowledge gap can make it difficult to evaluate different management options. For avian species, egg hatching success is a key demographic parameter, and data‐logging egg technology can provide important information on optimal species‐specific incubation conditions, which can help inform captive breeding practises and identify efficient captive management options. In the context of a captive breeding programme for endangered Whooping Cranes Grus americana, we investigated associations between hatching success and incubation conditions, including environmental parameters (temperature, relative humidity and egg turning rate), and incubation type (artificial incubation; foster incubation by Sandhill Cranes, Grus canadensis; and Whooping Crane incubation). Finally, we considered both cost and breeding output in an analysis of incubation practises. We found that daily mean temperatures were negatively associated with hatching success, and that hatching success was highest with incubation under Sandhill Cranes. However, incubation by artificial incubators, rather than Sandhill Cranes, provided a trade‐off between cost and breeding output that is likely to be acceptable to many captive programme managers. We encourage other captive breeding programmes to use innovations that help to increase potential release numbers for conservation translocations by considering biological and financial constraints. Captive breeding is an increasingly used conservation strategy for species with a high risk of extinction in the wild, but managing a captive breeding programme can be challenging if there is a deficiency in knowledge about the species’ breeding biology. We used data‐logging technology to help inform the captive breeding practises of Whooping Crane and then used a cost‐benefit analysis to identify efficient management options. We found that daily mean temperatures were negatively associated with hatching success, and that hatching success was highest with incubation under Sandhill Cranes. However, incubation by artificial incubators, rather than Sandhill Cranes, provided a trade‐off between cost and breeding output that is likely to be acceptable to many captive programme managers.
... For non-domesticated species, Nord andNilsson (2011) andDuRant et al. (2011), found that blue tits and wood ducks (Aix sponsa) that were incubated in cold temperature throughout the incubation period had higher metabolic rate close to independence, which was interpreted in the same wayi.e. a response that might improve thermogenic capacity. However, wood ducks incubated in this manner were worse, not better, at dealing with a cold challenge shortly after hatching (DuRant et al., 2012(DuRant et al., , 2013. Similar results have been obtained for chickens when incubated in chronically hypothermic conditions (Black and Burggren, 2004), which suggests that there are switch points where a thermal dose during embryogenesis transitions from being ameliorating to being constraining. ...
The ability to maintain a (relatively) stable body temperature in a wide range of thermal environments by use of endogenous heat production is a unique feature of endotherms such as birds. Endothermy is acquired and regulated via various endocrine and molecular pathways, and ultimately allows wide aerial, aquatic, and terrestrial distribution in variable environments. However, due to our changing climate, birds are faced with potential new challenges for thermoregulation, such as more frequent extreme weather events, lower predictability of climate, and increasing mean temperature. We provide an overview on thermoregulation in birds and its endocrine and molecular mechanisms, pinpointing gaps in current knowledge and recent developments, focusing especially on non-model species to understand the generality of, and variation in, mechanisms. We highlight plasticity of thermoregulation and underlying endocrine regulation, because thorough understanding of plasticity is key to predicting responses to changing environmental conditions. To this end, we discuss how changing climate is likely to affect avian thermoregulation and associated endocrine traits, and how the interplay between these physiological processes may play a role in facilitating or constraining adaptation to a changing climate. We conclude that while the general patterns of endocrine regulation of thermogenesis are quite well understood, at least in poultry, the molecular and endocrine mechanisms that regulate, e.g. mitochondrial function and plasticity of thermoregulation over different time scales (from transgenerational to daily variation), need to be unveiled. Plasticity may ameliorate climate change effects on thermoregulation to some extent, but the increased frequency of extreme weather events, and associated changes in resource availability, may be beyond the scope and/or speed for plastic responses. This could lead to selection for more tolerant phenotypes, if the underlying physiological traits harbour genetic and individual variation for selection to act on – a key question for future research.
... Research over the past decade in non-agricultural species representing both ends of the precocial-altricial spectrum demonstrates that temperatures experienced during incubation have dramatic effects on avian offspring phenotypes. These include effects on physiology (e.g., concentrations of developmentallyimportant hormones, thermoregulation, and immune responses; DuRant et al. 2010DuRant et al. , 2012aDuRant et al. , 2012bNord and Nilsson 2011;Wada et al. 2015), morphology (Hepp et al. 2006;DuRant et al. 2012a), behavior and performance (Hopkins et al. 2011;Bertin et al. 2018;Hope et al. 2018a), growth (Ospina et al. 2018a), and even first-year survival and adult body size (Hepp and Kennamer 2012;Nord and Nilsson 2016;Berntsen and Bech 2016). Interestingly, there is some evidence in poultry that brief exposure to heat stress as embryos can improve heat tolerance of chicks (Piestun et al. 2008;Willemsen et al. 2010Willemsen et al. , 2011Nassar et al. 2015), and exposure to heat stress as a juvenile can increase reproductive output as an adult (Hoffman et al. 2018). ...
A major driver of wildlife responses to climate change will include non-genomic effects, like those mediated through parental behavior and physiology (i.e., parental effects). Parental effects can influence lifetime reproductive success and survival, and thus population-level processes. However, the extent to which parental effects will contribute to population persistence or declines in response to climate change is not well understood. These effects may be substantial for species that exhibit extensive parental care behaviors like birds. Environmental temperature is important in shaping avian incubation behavior, both of which interact to determine the thermal conditions embryos are exposed to during development, and subsequently avian phenotypes and secondary sex ratios. In this paper, we argue that incubation behavior may be an important mediator of avian responses to climate change, we compare incubation strategies of two species adapted to different thermal environments nesting in extreme heat, and we present a simple model that estimates changes in egg temperature based on these incubation patterns and predicted increases in maximum daily air temperature. We demonstrate that the predicted increase in air temperature by 2100 in the central United States will increase temperatures eggs experience during afternoon off-bouts, and the proportion of nests exposed to lethal temperatures. To better understand how species and local adaptations and behavioral-plasticity of incubation behavior will contribute to population responses to climate change, comparisons are needed across more avian populations, species, and thermal landscapes.
... While heat stress during organogenesis may be teratogenic also to poikilothermic embryos, they show phenotypic plasticity to moderate changes in incubation temperature that strongly affect embryonic development and may have persistent effects on various phenotypic traits. Ducklings reared at relative low temperature showed slow growth and reduced thermoregulatory capacity after hatching [1], while embryonic temperature influenced growth rate and temperature choice in juvenile snapping turtles (Chelydra serpentine) [2] and swimming performance in wood frog tadpoles (Rana sylvatica) [3]. In zebrafish (Danio rerio), early temperature strongly affected metabolic enzymes in the skeletal muscle, swimming performance and thermal acclimation capacity of the adult fish [4,5]. ...
The development of ectothermic embryos is strongly affected by incubation temperature, and thermal imprinting of body growth and muscle phenotype has been reported in various teleost fishes. The complex epigenetic regulation of muscle development in vertebrates involves DNA methylation of the myogenin promoter. Body growth is a heritable and highly variable trait among fish populations that allows for local adaptations, but also for selective breeding. Here we studied the epigenetic effects of embryonic temperature and genetic background on body growth, muscle cellularity and myogenin expression in farmed Atlantic salmon (Salmo salar). Eggs from salmon families with either high or low estimated breeding values for body growth, referred to as Fast and Slow genotypes, were incubated at 8°C or 4°C until the embryonic ‘eyed-stage’ followed by rearing at the production temperature of 8°C. Rearing temperature strongly affected the growth rates, and the 8°C fish were about twice as heavy as the 4°C fish in the order Fast8>Slow8>Fast4>Slow4 prior to seawater transfer. Fast8 was the largest fish also at harvest despite strong growth compensation in the low temperature groups. Larval myogenin expression was approximately 4–6 fold higher in the Fast8 group than in the other groups and was associated with relative low DNA methylation levels, but was positively correlated with the expression levels of the DNA methyltransferase genes dnmt1, dnmt3a and dnmt3b. Juvenile Fast8 fish displayed thicker white muscle fibres than Fast4 fish, while Slow 8 and Slow 4 showed no difference in muscle cellularity. The impact of genetic background on the thermal imprinting of body growth and muscle development in Atlantic salmon suggests that epigenetic variation might play a significant role in the local adaptation to fluctuating temperatures over short evolutionary time.
... Mothers have a variety of ways to manipulate the composition and/or environment of their eggs, including, but not limited to: hatching asynchrony (Clark and Wilson 1981;Magrath 1990), yolk hormones (Groothuis et al. 2005), sex allocation (Pike and Petrie 2003), egg size (Krist 2011), incubation temperature (DuRant et al. 2009(DuRant et al. , 2011, and carotenoids (Royle et al. 2001;Blount et al. 2002). Assessing how these factors influence the growth and survival of their offspring, however, first requires being able to accurately match hatchlings to their respective eggs. ...
Accurately assigning hatchlings to the eggs from which they hatched is a prerequisite to understanding how the composition and environment of eggs affect the growth and survival of nestlings. Correctly assigning hatchlings to their eggs can be a challenging endeavor, however, because multiple eggs within the same clutch can hatch at essentially the same time. Egg and hatchling mass are highly correlated in most bird species, and thus assigning eggs to hatchlings using their relative mass (e.g., matching the heaviest hatchling to the heaviest candidate egg) could prove extremely useful. To assess its potential utility, I applied relative mass assignment (RMA) retrospectively to a dataset of 133 Common Grackle (Quiscalus quiscula) nests in which all egg-hatchling dyads were determined unequivocally. I found that RMA correctly assigned approximately 90% of hatchlings to their eggs when 2‒4 hatchlings were present between checks. The number of nests in which hatchlings could not be assigned to their egg, however, increased monotonically from 13 to 46 to 78% for nests containing 2, 3, and 4 hatchlings, respectively, due to the greater likelihood that the mass of hatchlings or their candidate eggs was identical. Although RMA correctly identified the vast majority of egg-hatchling dyads, researchers should use this method with caution, because it will always inflate positive egg-size effects and thus could potentially result in erroneously reporting significant effects.
... Though turning rate and angle changes did not vary by incubation period alone, when separated by diurnal cycle, egg-turning behaviors emerged that were not obvious in Shaffer et al. (2014). Differences between early, middle, and late incubation may be more obvious in species that exhibit uniparental incubation or egg neglect, like many passerines, shorebirds, waterbirds, and some burrowing seabirds (Reneerkens et al. 2011, DuRant et al. 2012, Cooper and Voss 2013. Examining incubation behaviors on multiple time scales (diurnal and across incubation phase) may be necessary to capture the subtle but dynamic features of avian incubation behaviors. ...
In most avian species, egg-turning behavior during incubation is vital for proper embryonic development and hatching success. However, changes in turning behaviors are rarely studied across different temporal scales (e.g., day–night or across incubation phases), though the timing of incubation behaviors affects reproductive success. We used data loggers encapsulated in artificial eggs to measure turning rates and angle changes of eggs in Western Gull (Larus occidentalis) and Laysan Albatross (Phoebastria immutabilis) nests. We examined diurnal and daily cycles in egg-turning behaviors across early, middle, and late incubation phases. Our results indicate that (1) egg-turning behaviors remain similar throughout incubation, resulting in a consistent environment for developing chicks; (2) egg-turning rates and angle changes vary according to diurnal cycles and day length in each species; and (3) egg-turning rates, but not angle changes, were similar between species. Egg-turning behaviors may vary am...
... More recently variation in incubation temperatures has been shown to influence phenotypic expression in chicks, which has implications for species fitness (DuRant et al., 2013b; Coe et al., 2015; Nord and Nilsson, 2016). In wild birds, hatchling body size and composition (Hepp et al., 2006), sex ratios (Goth and Booth, 2005), immune responses (Ardia et al., 2010; DuRant et al., 2012a), growth and stress physiology (DuRant et al., 2010), locomotor performance (DuRant et al., 2013b), metabolism, and thermoregulation (DuRant et al., 2012b) are influenced by incubation temperatures. Olsen and Baker (2001) suggest that incubation costs for kestrels (Falco cenchroides) in warmer climates may be less than those that breed in colder climates. ...
... Even small reductions in incubating temperature can have large impacts on hatching success. Low incubating temperatures slow down development, reduces the 'quality' of the hatchlings, and increases the chances of predation (Tombre & Erikstad 1996;Hepp et al. 2006;Martin et al. 2007;DuRant et al. 2012;Hepp et al. 2015). ...
Arctic terrestrial ecosystems are ideal systems to study host-parasite interactions because they
are sensitive and have fewer confounding interactions than lower latitudes. Since the Arctic is
experiencing rapid climate change, research there can provide models to better understand
and predict future changes in other systems. The Barnacle goose (Branta leucopsis) and its
ectoparasite the flea (Ceratophyllus vagabundus vagabundus) is an ideal Arctic host-parasite
system to study because Barnacle geese have important roles in Arctic ecosystems as
selective grazers and prey items and have been intensively studied for decades. Also, recent
studies suggest that Arctic avian flea infestations may be increasing, possibly due to climate
change. However, few studies have considered the effect of fleas on Arctic nesting birds and
little is known of Arctic avian flea ecology, most importantly whether they overwinter in the
High Arctic or are reintroduced each summer by migrating birds. Furthermore, sampling
methods for avian fleas are time-consuming and semi-invasive to their hosts. Therefore, the
project had four aims: (i) contribute to the knowledge of Arctic flea ecology by looking for
evidence of overwintering, (ii) use an experimental study to assess the impact of flea
infestations on the hatching success of Barnacle goose eggs, (iii) assess the simple and
disturbance-free method of estimating fleas with photographs of blood spots on goose eggs,
(iv) and test the results of both the experimental study as well as the application of blood
spots as a proxy measure for flea infestations through a larger observational study. It was
found that fleas were likely overwintering in empty nest bowls and some evidence indicated
that they might be capable of a two-year life cycle in the High Arctic. The findings from the
experimental study indicated that heavy flea infestations had a negative impact on the
hatching success of Barnacle goose eggs. It was also determined that blood spots were a good
proxy measure of flea infestations, but become less accurate through incubation due to wear
from incubating birds. Finally, the observational study supported the findings of the
experimental study and demonstrated the power and simplicity of using blood spots as a
proxy measure for flea infestations. Based on these findings, it is suggested that researchers
interested in either reproductive success or incubation behavior of Barnacle geese should
include a measure of flea infestations in their studies and using blood spots as a proxy
measure is a simple and disturbance-free method of doing this.
... Regular egg turning behavior can also lead to increased hatching success, chick health, and overall reproductive success (Deeming 2002a, Tona et al. 2005, Elibol and Brake 2006. Maintaining egg temperatures is also important for proper embryonic development (Turner 2002, DuRant et al. 2012. Incubation temperatures and egg turning rates have been studied extensively in the poultry industry to maximize the hatchability of domestic fowl (Deeming 2002a). ...
... There may have been an effect on the offspring phenotype that was not evaluated, because most adults maintained nest temperatures within a high, narrow range, despite the cost of incubation. Many studies show that embryos incubated at low temperatures have slower growth and lower body condi-tion, as well as reduced immune responses (DuRant et al. 2010), thermoregulatory performance (DuRant et al. 2012), and locomotory performance (Hopkins et al. 2011). ...
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... While egg turning behavior has not been studied as extensively as parental attendance patterns, egg physiology, or hatching success, a number of studies have revealed that a lack of egg turning can retard the utilization of albumen by the embryo, resulting in abnormal chick development and reduced hatching success [5,6]. Incubation temperatures are also critical for embryonic development, hatching success, and sometimes offspring phenotype [1,[7][8][9]. The poultry industry uses knowledge of optimal egg turning rates, magnitude of angle changes, humidity, and temperatures to maximize hatchability of domestic fowl [6,[10][11][12][13]. ...
Egg turning is unique to birds and critical for embryonic development in most avian species. Technology that can measure changes in egg orientation and temperature at fine temporal scales (1 Hz) was neither readily available nor small enough to fit into artificial eggs until recently. Here we show the utility of novel miniature data loggers equipped with 3-axis (i.e., triaxial) accelerometers, magnetometers, and a temperature thermistor to study egg turning behavior in free-ranging birds. Artificial eggs containing egg loggers were deployed in the nests of three seabird species for 1-7 days of continuous monitoring. These species (1) turned their eggs more frequently (up to 6.5 turns h-1) than previously reported for other species, but angular changes were often small (1-10° most common), (2) displayed similar mean turning rates (ca. 2 turns h-1) despite major differences in reproductive ecology, and (3) demonstrated distinct diurnal cycling in egg temperatures that varied between 1.4 and 2.4°C. These novel egg loggers revealed high-resolution, three-dimensional egg turning behavior heretofore never measured in wild birds. This new form of biotechnology has broad applicability for addressing fundamental questions in avian breeding ecology, life history, and development, and can be used as a tool to monitor birds that are sensitive to disturbance while breeding.
... On the contrary, studies in Hungary (Lovaszi et al. 2000) and Poland have found a negative correlation between the temperature and the presence of L. collurio. According to Roos (2004) and DuRant et al. (2012) air temperature is an important factor affecting egg brooding behavior in birds. Hence, hatching success may be influenced by egg size, which depends on the weather conditions at the time of laying (Londono et al. 2008, Aslan andYavuz 2010). ...
This study was conducted in two different Mediterranean areas of central Greece and aimed at (i) comparing the breeding density and frequency of occurrence of shrike species between these two areas, (ii) identifying the key characteristics of habitats for each species, and (iii) evaluating possible underlying environmental factors determining the shrike’s presence. To assess which factors mostly affect density, estimated with the point count method, we used the non-parametric test Kruskal - Wallis, Spearman's
correlation coefficient, Canonical Analysis and Canonical Correspondence Analysis (CCA). Environmental variables tested were microclimate (air temperature and humidity), vegetation (herbaceous cover, shrub cover and shrub height), topography (altitude, slope, road presence, distance from nearest road, settlement and river) and habitat type (broad leaf forest, agricultural land, rangeland and abandoned olive groves). Between the two areas types, only Lanius senator mean breeding density was significantly different. The CCA model was significant (p < 0.05). Our results highlighted that L. minor did not occupy plots of agricultural land (cereals) and was negatively related to the distance of the nearest road. L. senator did not occupy plots of broad leaf forest and was positively related to the existence of the nearest road. Furthermore, the species exhibited the habit of perching along roadsides. On the contrary, L. collurio was characterized as habitat
generalist in landscapes of central Greece.
Birds use contact incubation to warm their eggs above ambient temperature required for embryonic development. In contrast, birds in the industry as well as many birds in breeding programs and scientific studies are incubated in conventional incubators that warm eggs via circulating warm air. This means that contact incubated eggs have different thermal properties than eggs incubated in a conventional incubator. In light of previous studies showing that small differences in incubation temperature can affect chicks post-hatching phenotype, we investigated the consequences of incubating Red jungle fowl eggs at the same temperature (37 °C) either via contact incubation or warm air incubation. We found that contact incubated chicks had a more robust body composition, were more explorative and had a higher temperature preference early in life, as well as a sex dependent difference in plasma Corticosterone levels pre-hatch (measured in down-feathers) and post-hatch (measured in plasma) compared to chicks incubated in a conventional warm air incubator. While previous studies have demonstrated that embryonic development and post-hatch phenotype is sensitive to small variations in temperature, our study demonstrates for the first time that the way heat is distributed to the egg has a similar magnitude of effect on post-hatch phenotype and highlights the sensitivity of the incubation period in shaping birds post-hatch phenotype.
The thermal environment experienced by birds during early postembryonic development may be an important factor shaping growth and survival. However, few studies have directly manipulated nest temperature (T n) during the nestling phase, and none have measured the consequences of experimental heat stress on nestlings’ body temperature (T b). It is therefore not known to what extent any fitness consequences of development in a thermally challenging environment arise as a direct, or indirect, effect of heat stress. We, therefore, studied how experimentally increased T n affected T b in 8–12 d old blue tit Cyanistes caeruleus nestlings, to investigate if increased thermoregulatory demands to maintain normothermic T b influenced nestling growth and apparent long-term survival. Nestlings in heated nest-boxes had significantly higher T b compared to unheated nestlings during most of the experimental period. Yet, despite facing T n 50°C (as measured in the bottom of the nest cup below the nestlings), the highest nestling T b recorded was 43.8°C with nestlings showing evidence of controlled facultative hyperthermia without any increased nestling mortality in heated nests. However, body mass gain was lower in these nestlings compared to nestlings from control nest-boxes. Contrary to our prediction, a larger proportion of nestlings from heated nest-boxes were recaptured during their first winter, or subsequently recruited into the breeding population as first- or second-year breeders. This result should, however, be treated with caution because of low recapture rates. This study highlights the importance of the thermal environment during nestling development, and its role in shaping both growth patterns and possibly also apparent survival.
En aves el cuidado parental durante la anidación involucra una gran inversión de energía para mantener la estabilidad térmica (homeotermia) de la progenie. Conservar la homotermia y mantener alta la temperatura en el nido se favorece por selección, al estar relacionado positivamente con el éxito de eclosión de los huevos, la sobrevivencia de los polluelos y con ello en el éxito reproductivo de los padres. En los colibríes, caracterizados por sus altos requerimientos metabólicos y un cuidado exclusivamente materno de la progenie, es factible pensar que las hembras optimizan el tiempo y energía dedicados a diferentes conductas relacionadas con el cuidado parental durante la anidación, y en particular aquellos que mantienen la homotermia del nido. En este estudio evaluamos el efecto de algunas conductas de cuidado materno en el ambiente térmico de la progenie de un nido del colibrí ermitaño cola larga (Phaethornis longirostris). Para ello utilizamos un termopar ultradelgado conectado a un termómetro electrónico con el que registramos la temperatura dentro de un nido de esta especie. Observamos que la hembra realiza salidas de forrajeo muy prolongadas, pero esto no modificó la estabilidad térmica dentro del nido, el cual mantuvo su variación en menos de 1ºC. Esto nos permite sugerir que la hembra que atendía el nido efectivamente optimizó sus conductas de cuidado parental (i.e. incubación y forrajeo), a fin de minimizar la oscilación térmica de la progenie. Sin embargo, aún es necesario evaluar la contribución de otras decisiones de la hembra relacionadas con la conducta de anidación: la forma, materiales de construcción y elección del sitio de anidación, en la homeotermia del nido.
In birds, as in other endothermic vertebrates with parental care, during nesting, parents must invest large amounts of time and energy to maintain thermal stability of eggs and chicks. Nest homeothermy is selectively advantageous for parents as it increase hatching success, offspring survival, and offspring development rate. Hummingbirds, characterized by their high metabolic rates and exclusively maternal care, the females must optimize time and energy devoted to different behaviors related to parental care during nesting and in particular to maintain nest homeothermy. In this study we evaluated in a nest of a Long-tailed Hermit hummingbird (Phaethornis longirostris), the effect of maternal care on quality and stability of the thermal environment of its progeny. We used an ultra thin thermocouple connected to an electronic thermometer to record thermal variation ambient inside the nest. Our results showed that although the female leaves the nest for long periods to feed, their nest and progeny maintains a great thermal stability (variation less than 1ºC). This suggests that the female attending her nest optimized its maternal care patterns (i.e. incubation and foraging), in order to minimize thermal oscillation experienced by its progeny. Although we still need to assess the contribution of other maternal care decision such as building materials and nest shape as well as the election of nesting site in thermal stability of the nest.
High levels of anthropogenic noise produced in urban areas are known to negatively affect wildlife. Although most research has been focused on the disturbances of communication systems, chronic noise exposure can also lead to physiological and behavioural changes that have strong consequences for fitness. For instance, behavioural changes mediated by anthropogenic noise (e.g. quality of parental care) may alter development and could influence nestling phenotype. We tested if nestling metabolism was influence by traffic noise in an urban exploiter, the house sparrow Passer domesticus. We experimentally exposed breeding house sparrows from a rural area to a playback of traffic noise and we examined the impacts of this experimental procedure on metabolic rates and morphology of nestlings. We did not find an effect of traffic noise on the morphology of nestlings. Surprisingly, we found that disturbed nestlings had overall lower metabolic rates and mass-adjusted metabolic rates than undisturbed birds. Our results suggest a specific effect of noise exposure per se, rather than an indirect effect of anthropogenic noise through the quality of parental care. Both the proximate mechanisms and the ultimate consequences of such metabolic changes on nestlings remain unknown and deserve future experimental studies.
Short and medium-distance migrant birds that return to the breeding grounds early can usually take better-quality territory leading to higher breeding success than of congeners arriving later. On the other hand, early breeders usually have to face severe weather conditions. 109 Black-headed Gulls which had begun laying in a breeding colony (N-Poland) earlier than the remaining 960 females lost 66.2% of eggs because of severely adverse weather. On 9 April 2012 ambient temperature fell to -4.6°C during the first two hours after sunrise (06:00-07:59) resulting in eggs cracking during the adults’ first feeding bout after the night. Up to 1 mm wide cracks in eggshells were from 3 mm to 24 mm long; in some eggs the external shell membrane also broke. Pairs that lost eggs did not repeat broods. In this way in 2012 this colony suffered the greatest loss of eggs during its 15-years history. This event showed that even in the temperate climate, adverse weather, a consequence of the global climate change, does have negative impact on life history traits of birds.
Incubation is an important component of avian parental care and slight changes in incubation temperature can affect offspring phenotype. Although many extrinsic and intrinsic factors may generate variation in incubation temperature, they remain underexplored under natural conditions. Using a robust data set encompassing 55 nests, 22 816 behavioral observations, and > 1 million paired ambient and egg temperatures, we describe the relationships among abiotic factors, female incubation behavior, incubation temperature, and incubation period for tree swallows Tachycineta bicolor. We report a large amount of individual variation in incubation behaviors and average incubation temperatures for our study population. The average on-bout incubation temperature was 34.1°C, with daily egg temperatures ranging from 18.0–39.2°C. Females modulated the number of times they left the nest and the amount of time they stayed off the nest according to interactions between precipitation and temperature patterns. Models generated from our observations predicted that the number of female off-bouts was the lowest under warm and dry conditions while more off-bouts were taken under cold and dry or warm and wet conditions. During cold and dry conditions, females stayed off their nest ∼4 times longer than under warm and dry conditions. However, this pattern was reversed under periods of rainfall; females tended to take shorter off-bouts when it was rainy and cold compared to longer off-bouts during warmer rain events. Furthermore, variation in female behavior was associated with differences in overall incubation temperature such that females that maintained greater incubation constancy produced higher incubation temperatures at a given ambient temperature than those that displayed lower incubation constancy. Our results provide perspective on the timing of breeding, as some of the advantages of breeding early may be countered by cooler, early season temperatures and precipitation that cause reproducing females to favor self-maintenance at a potential cost to optimal incubation temperatures for offspring development.
Optimal development of avian embryos occurs within a narrow range of incubation temperatures. Most parents that physically incubate their eggs through direct contact are challenged to balance their time on the nest with taking foraging recesses to satisfy their energetic requirements. To explore the costs and investment strategies of incubating female Wood Ducks (Aix sponsa), we manipulated the nnicroclimate of nests by reducing down insulation from the typical 4.0 g to 0.5 g. Cooling rates of clutches during morning recesses increased when down insulation was reduced, especially at low ambient temperatures. Females with reduced down responded to increased cooling rates by shortening morning recesses and increasing daily incubation constancy, and these behavioral changes were independent of their body mass at the start of incubation. Females in both treatment groups responded similarly to changes in ambient temperature and spent less time incubating as ambient temperatures increased. Clutch temperatures at the end of morning recesses were similar for females with reduced and normal insulation. Average clutch temperatures for the full incubation period did not differ between treatments, and, correspondingly, there were no differences in length of the incubation period, hatching success, or duckling phenotype. Our results show that female Wood Ducks were sensitive to changes in both clutch temperature and ambient temperature and that they modified their time on the nest to provide developing eggs with an optimal thermal environment without negatively affecting their body mass at the end of incubation. Further examination of the limits of behavioral plasticity in incubating birds will be essential, particularly in light of future challenges presented by climate change.
Conspecific brood parasitism (CBP) occurs in various insects, fishes and birds, but it is disproportionately common in waterfowl (Anatidae). Studies of CBP in Anatids therefore have helped to develop a fundamental conceptual framework with which to explain this intriguing behaviour. Yom-Tov (1980) first drew attention to CBP, and Andersson and Eriksson (1982) also hinted at the fascinating behavioural, ecological and evolutionary aspects of CBP in waterfowl. Several reviews followed these early papers, but much has been learned more recently about CBP in waterfowl. Here we aim to review the traditional conceptual framework of CBP in waterfowl and to consider empirical studies that have attempted to test related hypotheses. The survey provided support for the hypotheses that CBP allows some females to reproduce when not otherwise possible, whereas other females use parasitic egg-laying as a way to enhance their fecundity. A recently developed framework that considers CBP as part of a flexible life-history strategy could provide a useful direction for future studies of CBP. A second aim of this review is to consider the use of cues by conspecific brood parasites seeking suitable places to lay eggs parasitically. Recent studies have revealed remarkable cognitive abilities in parasitic females, but the actual mechanisms remain unknown. Clearly, breeding females are sensitive to cues such as nest site security, patterns of previous nest use or success, clutch size, and perhaps even the degree of kinship between hosts and other parasites. Indeed, additional investigations of CBP are needed to provide a better understanding of the processes and patterns of this avian reproductive strategy.
Nest microclimate, particularly temperature, can affect energy balance of both parents and offspring. Here I investigate patterns of correlation between internal temperatures of artificial nestboxes and fitness in Tree Swallows (Tachycineta bicolor). Nests with cold overnight temperatures were less likely to fledge offspring. Conversely, nests with high daytime temperatures were also less likely to fledge offspring. In particular, nest success declined when internal nestbox temperatures exceeded 35°C. To investigate a potential physiological cause for reduced fitness, I tested whether haematocrit, a rough indicator of blood volume, was related to warmer nest temperatures. Whilst variable, nests with higher temperatures had higher average haematocrit of nestlings on day 13. This may indicate greater evaporative heat loss reflected in lower plasma volumes. These results as a whole indicate that temperatures outside the thermo-neutral zone may influence energy balance of both parents and offspring and may have an important effect on fitness.
Parental effects are influential sources of phenotypic variation in offspring. Incubation temperature in birds, which is largely driven by parental behavior and physiology, affects a suite of phenotypic traits in offspring including growth, immune function, stress endocrinology, and sex ratios. The importance of average incubation temperature on offspring phenotype has recently been described in birds, but parental incubation behaviors like the duration and frequency of recesses from the nest can be variable. There are few studies describing how or if thermal variation as a result of variable incubation affects offspring phenotype. We incubated wood duck Aix sponsa eggs under three different incubation regimes, based on patterns that occur in nature, which varied in off-bout duration and/or temperature. We measured incubation period, morphometrics at hatching, and monitored growth and body condition for nine days post hatch. When average incubation temperature was allowed to drop from 35.9°C to 35.5°C as a result of doubled off-bout duration, we found a significant 2 d extension in incubation period, but no effects on duckling hatch mass, or growth and body condition up to nine days post hatch. However, when average incubation temperatures were equivalent (35.9°C), doubling the duration of the simulated off-bouts did not influence incubation period or any post hatch parameters. Our results suggest that if incubating parents can maintain favorable thermal environments in the nest via altered behavior (e.g. manipulating nest insulation) and/or physiology (e.g. heat production), parents may be able to avoid the costs of longer incubation periods resulting from increased off-bout duration.
Temperature plays a central role in the life of birds, especially during egg incubation and nestling thermal brooding. I investigated nest temperature variation relative to ambient temperature during incubation in an enclosed nest-builder species (Spanish sparrow Passer hispaniolensis) and an open-cup nest-builder species (Iberian azurewinged magpie yanopica cooki). The data for empty enclosed nests showed that the nest structure acted as a temperature buffer which reduced the impact of night-time temperature variation within the nest. The buffer effect was reduced as ambient temperature increased at dawn. The presence of an adult increased the difference between nest temperature and ambient temperature, and dissociated its variation from the ambient temperature variation. The enclosed nest also retained the body heat released by an adult in the nest. Both effects had a positive effect on the temperature balance in the nest. By contrast, open-cup nest temperature was more affected by the ambient temperature, although it did not affect the egg temperature directly. Thus the absence of an incubating parent would endanger the hatchability in open-cup nests more rapidly than in enclosed nests. The life histories of the investigated species correspond to these findings, i.e. a more pronounced presence of the female in the Iberian azure-winged magpie nests.
Abstract Recent research in birds suggests that investing in incubation is one mechanism by which parents can enhance the phenotype of their offspring. Posthatch environmental conditions can also shape an individual's phenotype, and it is thus possible for pre- and posthatch conditions to have interactive effects on an individual's phenotype. In this study, we examined the individual and interactive effects of prehatch incubation temperature and posthatch food availability on growth, food consumption, and thermoregulatory ability in wood duck (Aix sponsa) ducklings. Eggs were incubated at one of three temperatures (35.0°, 35.9°, or 37.0°C), and then ducklings were reared on an either ad lib. or time-restricted diet for 12 d after hatching. We found that food availability influenced duckling growth, with the slowest growth occurring in ducklings fed the restricted diet. Incubation temperature also interacted with food conditions to influence duckling growth: ducklings fed ad lib. from the lowest incubation temperature grew slower than ducklings fed ad lib. from the higher incubation temperatures. Most importantly, we found that the improvement in a duckling's ability to maintain body temperature in the face of a thermal challenge was influenced by embryonic incubation temperature but not feeding conditions. Ducklings from the highest incubation temperature experienced the greatest improvement in thermoregulatory performance with age. Our findings suggest that the prehatch environment is more important than posthatch resource conditions in determining some physiological functions and underscores the important role that incubation temperature plays in determining offspring phenotype in birds.
Environmental conditions during early development can profoundly influence an individual's phenotype. Development requires simultaneous maturation and orchestration of multiple physiological systems creating the potential for interaction among key systems and requiring substantial resources. We investigated the influence of thermoregulation on immunocompetence in Wood Duck ducklings (Aix sponsa). At both 1 and 2 days post hatch (dph) we evaluated ducklings' abilities to thermoregulate during a thermal challenge at one of four temperatures (36 [thermoneutral controls], 20, 10, or 5°C). At 3 dph, ducklings received a superficial wound, which was monitored until full recovery to quantify wound healing ability, an ecologically relevant, integrative measure of immune function. We demonstrated that duckling body temperature decreased with increasing thermal challenge severity, thermoregulatory ability increased with age, and thermoregulation had temperature-dependent effects on the immune system. Specifically, a more severe thermal challenge (5°C) resulted in decreased immune performance when compared to a mild challenge (20°C). We conclude that early thermoregulatory experiences are influential in shaping immune responses early in development. Furthermore, our results emphasize that future studies of environmental stressors need to consider multiple physiological endpoints since interaction among systems can result in competing physiological demands. J. Exp. Zool. 9999A: 1-8, 2013. © 2013 Wiley Periodicals, Inc.
Incubation is a vital component of reproduction and parental care in birds. Maintaining temperatures within a narrow range is necessary for embryonic development and hatching of young, and exposure to both high and low temperatures can be lethal to embryos. Although it is widely recognized that temperature is important for hatching success, little is known about how variation in incubation temperature influences the post-hatching phenotypes of avian offspring. However, among reptiles it is well known that incubation temperature affects many phenotypic traits of offspring with implications for their future survival and reproduction. Although most birds, unlike reptiles, physically incubate their eggs, and thus behaviourally control nest temperatures, variation in temperature that influences embryonic development still occurs among nests within a population. Recent research in birds has primarily been limited to populations of megapodes and waterfowl; in each group, incubation temperature has substantial effects on hatchling phenotypic traits important for future development, survival, and reproduction. Such observations suggest that incubation temperature (and incubation behaviours of parents) is an important but underappreciated parental effect in birds and may represent a selective force instrumental in shaping avian reproductive ecology and life-history traits. However, much more research is needed to understand how pervasive phenotypic effects of incubation temperature are among birds, the sources of variation in incubation temperature, and how effects on phenotype arise. Such insights will not only provide foundational information regarding avian evolution and ecology, but also contribute to avian conservation.
We examined sources of variation in incubation patterns among female Wood Ducks (Aix sponsa), and investigated the effect of female nest attentiveness on incubation period. Data were collected from 44 females (n = 911 days) using temperature data loggers to monitor nest attendance throughout incubation. Mean (± SE) incubation constancy was 86.9 ± 0.6% and incubation period averaged 30.9 ± 0.2 days. Females took an average of two bimodally-distributed recesses per day. Duration of recesses averaged 98.6 ± 3.4 min, but were shorter in the morning than in mid-day or late afternoon. Body mass of incubating females declined 0.68 ± 0.2 g day-1, but there was no relationship between constancy and early incubation body mass or weight change of females. Incubation constancy was not correlated with length of the incubation period. For most females, incubation constancy and recess frequency did not change as incubation progressed. The fact that incubating females only lost an average of 3% of body mass, and constancy was not related to either body mass or length of the incubation period, suggests that females were not constrained energetically. Finally, we propose that the combination of reduced predation risk and the need of neonates to be more functionally mature at hatching has selected for longer incubation periods in Wood Ducks and other cavity-nesting waterfowl.
Survival characteristics of 25 broods of Mallards (Anas platyrhynchos) were determined on a study area in the Missouri Coteau of south-central North Dakota in 1976-1977. Radio-equipped Mallard hens fledged at least one duckling in 7 of 16 (44%) broods produced in 1976, 5 of 9 (55%) in 1977, and 12 of 25 (48%) for both years combined. Of the 13 broods in which all young were lost, 11 (85%) were lost within the first two weeks after hatching. All losses of entire broods occurred in wetlands; few ducklings and no entire broods were lost during overland travel. Predation by mink (Mustela vison) was apparently the principal cause of duckling mortality.
Explaining patterns of latitudinal and seasonal trends in clutch size are two of the oldest and most fundamental endeavors in avian life history research. Underlying the majority of studies regarding any type of clutch size variation (i.e., individual, seasonal, latitudinal) of altricial birds is the premise that the primary cost of reproduction stems from feeding offspring. However, both altricial and precocial species of birds display latitudinal and seasonal variation in clutch size. Additionally, individual variation in costs of laying and incubation, recently demonstrated, indicates that understanding latitudinal and seasonal clutch size trends will require increased attention to earlier phases of reproduction. Given the strength and ubiquity of the clutch size patterns, many environmental factors, such as food supply and predation, have been proposed to account for the patterns, but temperature has been largely overlooked. Gradients in many variables may be important because the primacy of selection pressures may also vary in space and time. Furthermore, physiological systems may constrain responses to selection pressures. Thus, it is possible that intraspecific geographic and seasonal patterns in clutch size are at least partially influenced by temperature-dependent physiological processes. Therefore, we suggest that it is important to examine physiological responses of birds (e.g., embryo development, incubation energetics) directly influenced by physical properties of the environment, which exhibit predictable types of spatial and temporal variation (e.g., temperature, humidity, day length). We review two recently proposed, complementary hypotheses that are excellent candidates for this approach. By one mechanism, the thermal inertia of large clutches makes them favorable in cooler weather (the clutch-cooling hypothesis of J. M. Reid et al.). By the other, the reduction in egg viability under warm temperatures favors small clutches (the egg-viability hypothesis of S. H. Stoleson and S. R. Beissinger). Using general linear mixed models, we found that large-scale nesting patterns of Eastern Bluebirds and Red-winged Blackbirds are consistent with the egg-viability hypothesis in that females appear to initiate incubation before clutch completion when they lay large clutches at low latitudes. Although attempts have been made to overcome the logistical obstacles associated with studying large-scale phenomena through meta-analyses and multiple small-scale study sites, we demonstrate the significant potential of new technologies combined with volunteer-based studies to validate these hypotheses as we outline directions for future research.
Determining the consequences of body size and body temperature (Tb) variation is critical to understanding many aspects of snake ecology, because size and temperature play such important roles in the biology of ectotherms. Here, we investigate the effects of body size and temperature variation on the energetics of the largest species of rattlesnake, the Eastern Diamondback Rattlesnake (Crotalus adamanteus). Specifically, we measured oxygen consumption to estimate the standard metabolic rate (SMR) of five C. adamanteus (mass range 800–4980 g) at 5-degree increments from 5–35 C. A multiple regression model indicated that SMR increased with body size and temperature. Q10s were generally high (range 1.82–4.20) compared to other squamates but were similar to the high values calculated for other large rattlesnakes. An energy balance model for C. adamanteus predicted that as Tb increases, so must prey consumption to meet annual SMR energy demands. Thus, Tb variation likely affects patterns of energy acquisition and use and, in turn, influences processes such as growth and reproduction.
Parental effects play a vital role in shaping offspring phenotype. In birds, incubation behaviour is a critical parental effect because it influences the early developmental environment and can therefore have lifelong consequences for offspring phenotype. Recent studies that manipulated incubation temperature found effects on hatchling body composition, condition and growth, suggesting that incubation temperature could also affect energetically costly physiological processes of young birds that are important to survival (e.g. immune responses). We artificially incubated wood duck (Aix sponsa) eggs at three biologically relevant temperatures. Following incubation, we used two immunoassays to measure acquired immune responses of ducklings. Ducklings incubated at the lowest temperature had reduced growth, body condition and responses to both of our immune challenges, compared with those from the higher temperatures. Our results show that incubation temperatures can be an important driver of phenotypic variation in avian populations.
Nest microclimate can have strong effects that can carry over to later life-history stages. We experimentally cooled the nests of tree swallows (Tachycineta bicolor). Females incubating in cooled nests reduced incubation time and allowed egg temperatures to drop, leading to extended incubation periods. We partially cross-fostered nestlings to test carry-over effects of cooling during incubation on nestling innate constitutive immunity, assessed through bacteria killing ability (BKA) of blood. Nestlings that had been cooled as eggs showed a lower ability to kill bacteria than control nestlings, regardless of the treatment of their foster mother. However, there was no effect of treatment of rearing females on nestling BKA in control nestlings, even though cooled females made significantly fewer feeding visits than did control females. This suggests that the effect of cooling occurred during incubation and was not due to carry-over effects on nestling condition. Nestlings that were exposed to experimental cooling as embryos had lower residual body mass and absolute body mass at all four ages measured. Our results indicate that environmental conditions and trade-offs experienced during one stage of development can have important carry-over effects on later life-history stages.
Early developmental experiences, such as incubation conditions, can have important consequences for post-hatching fitness in birds. Although the effects of incubation temperature on phenotype of avian hatchlings are poorly understood, recent research suggests that subtle changes in incubation conditions can influence hatchling characteristics, including body size and condition. We designed an experiment to explore the effects of incubation temperature on hatching success, survival to 9 days post hatch, growth and the hypothalamo-pituitary-adrenal (HPA) axis in wood ducks (Aix sponsa). Wood duck eggs were collected from nest boxes and experimentally incubated at three temperatures (35.0, 35.9 and 37.0 degrees C), each falling within the range of temperatures of naturally incubated wood duck nests. Survival and growth were monitored in ducklings fed ad libitum for 9 days post hatch. In addition, baseline and stress-induced plasma corticosterone concentrations were measured in 2 and 9 day old ducklings. Hatching success and survival to 9 days was greatest in ducks incubated at the intermediate temperature. Ducklings incubated at 35.9 degrees C and 37.0 degrees C had 43% higher growth rates than ducklings incubated at 35.0 degrees C. In addition, ducklings incubated at 35.0 degrees C had higher baseline (17-50%) and stress-induced (32-84%) corticosterone concentrations than ducklings incubated at 35.9 degrees C and 37.0 degrees C at 2 and 9 days post hatch. We also found a significant negative correlation between body size and plasma corticosterone concentrations (baseline and stress-induced) in 9 day old ducklings. To our knowledge, this is the first study to demonstrate that thermal conditions experienced during embryonic development can influence the HPA axis of young birds. Our results illustrate that subtle changes (<1.0 degrees C) in the incubation environment can have important consequences for physiological traits important to fitness.
Life-history theory predicts that increased current reproductive effort should lead to a fitness cost. This cost of reproduction may be observed as reduced survival or future reproduction, and may be caused by temporal suppression of immune function in stressed or hard-working individuals. In birds, consideration of the costs of incubating eggs has largely been neglected in favour of the costs of brood rearing. We manipulated incubation demand in two breeding seasons (2000 and 2001) in female common eiders (Somateria mollissima) by creating clutches of three and six eggs (natural range 3-6 eggs). The common eider is a long-lived sea-duck where females do not eat during the incubation period. Mass loss increased and immune function (lymphocyte levels and specific antibody response to the non-pathogenic antigens diphtheria and tetanus toxoid) was reduced in females incubating large clutches. The increased incubation effort among females assigned to large incubation demand did not lead to adverse effects on current reproduction or return rate in the next breeding season. However, large incubation demand resulted in long-term fitness costs through reduced fecundity the year after manipulation. Our data show that in eiders, a long-lived species, the cost of high incubation demand is paid in the currency of reduced future fecundity, possibly mediated by reduced immune function.
Life-history theory predicts that parents produce the number of offspring that maximizes their fitness. In birds, natural selection on parental decisions regarding clutch size may act during egg laying, incubation or nestling phase. To study the fitness consequences of clutch size during the incubation phase, we manipulated the clutch sizes during this phase only in three breeding seasons and measured the fitness consequences on the short and the long term. Clutch enlargement did not affect the offspring fitness of the manipulated first clutches, but fledging probability of the subsequent clutch in the same season was reduced. Parents incubating enlarged first clutches provided adequate care for the offspring of their first clutches during the nestling phase, but paid the price when caring for the offspring of their second clutch. Parents that incubated enlarged first clutches had lower local survival in the 2 years when the population had a relatively high production of second clutches, but not in the third year when there was a very low production of second clutches. During these 2 years, the costs of incubation were strong enough to change positive selection, as established by brood size manipulations in this study population, into stabilizing selection through the negative effect of incubation on parental fitness.
Oxygen consumption of Rhea (Rhea americana) and Emu (Dromiceius novaehollandiae) eggs increases exponentially during the first 70% of incubation and reaches a maximum about three-quarters of the way through incubation. Rate of O₂ consumption then declines to about 75% of the peak value, increasing again just prior to pipping. We suggest the decline in rate of O₂ consumption is due to a decline in growth rate, and that growth of the embryo of ratites is essentially complete at the time of the peak in O₂ consumption. Completion of growth prior to the normal end of incubation may permit ratite eggs of different ages to synchronize hatching within a clutch. Rates of O₂ consumption just prior to the initiation of pulmonary respiration are 104 ± 7 cm³ h⁻¹ in Rhea eggs and 75 ± 7 cm³ h⁻¹ in Emu eggs. Calculated and measured air-cell gas tensions at this stage of incubation vary systematically with egg size between species of birds. Large eggs have higher air-cell O₂ tensions and lower air-cell CO₂ tensions than do small eggs. Water vapor conductance of Emu eggs is 46.2 ± 9.6 mg· day⁻¹ torr⁻¹, much lower than predicted on the basis of egg size and incubation period.
Duckling survival, an important factor affecting annual recruitment, has not been determined adequately for canvasbacks (Aythya valisineria). We investigated the magnitude, timing, and causes of mortality of canvasback ducklings from hatch to fledging at the Agassiz National Wildlife Refuge (NWR) in northwestern Minnesota during 1987-90. During the 4 years, 217 day-old ducklings were radiomarked and released in 52 broods. Another 141 ducklings were radiomarked at ≥4weeks of age. Survival was estimated with the Kaplan-Meier nonparametric estimator and the Weibull parametric model. Most mortalities occurred within 10 days after hatch. Total brood loss occurred in 18 (35%) of 52 broods released. The primary sources of mortality were predation, principally by mink (Mustela vison), and exposure to precipitation and cold temperature. For combined years, females had lower survival than males (P = 0.03). If the disparate survival between sexes of canvasbacks observed in this study is representative of canvasbacks in their breeding range, this phenomenon contributes to reduced reproductive potential and the male-biased sex ratio of the species.
Estimates of duckling survival are necessary to accurately assess recruitment of mallards (Anas platyrhynchos), yet few reliable estimates exist. During 1988-90, we estimated survival rates for 127 radio-marked mallard ducklings from 64 broods on Lower Klamath National Wildlife Refuge, California. In 1988, we restricted the survival estimate to the first 10 days post-hatch (Ŝ = 0.18, SE = 0.07). Survival from hatching to 50 days was 0.37 (SE = 0.09) in 1989 and 0.34 (SE = 0.07) in 1990. Total brood loss differed among years (P < 0.05); 81.2% in 1988 (n = 16), 36.8% in 1989 (n = 19), and 37.5% in 1990 (n = 24). Ninety-three percent of mortality occurred during the first 10 days of life. We detected no differences in the proportion of radio-marked ducklings fledged from early-hatched versus late-hatched nests (P = 0.74). During 1989-90, 16 females appeared to lose their entire brood; however, 3 radio-marked ducklings from 2 of these broods were fledged by other brood hens. Of 29 radio-marked ducklings that reached 44 days of life, 6 (20.7%) joined other broods. Habitat enhancement is the key to improving duckling survival because the large number of predator species that consume ducklings makes predator control difficult.
1.Heat production (HP) and body core temperature (CT) where measured in 1- to 10-day old Muscovy ducklings and turkey chick, incubated during the last week before hatching at a lower (34.5°C, LT-group) or at higher (38.5°C, HT-group), than the normal temperature of 37.5°C (control C-group).2.In Muscovy ducklings, on the 1st day post-hatching HP was affected by exposure to low Ta of 10°C Ta 28.2±3.9 Wkg−1 in the LT-group vs. 18.1±2.4Wkg−1 in normal controls. On the same day, CT was higher (39.5±1.1°C) in the HT- than in the CT-group (37.5±2.9°C).3.In turkeys, the relationships between Ta and HP could be described by parabola-like functions. Apart from the first day of life, the HP of the LT-group and the HT-group was higher than of the CT-group.4.The low prenatal temperature of incubation resulted in a decrease of the preferred temperature in the LH-group and in an increase in the HT-group.5.It is concluded that changes in incubation temperature at the end of embryonic development may induce an epigenetic temperature adaptation, which results in a long-lasting cold- and warm-adaptation in ducks but not in turkeys.
We examined sources of variation in incubation patterns among female Wood Ducks (Aix sponsa), and investigated the effect of female nest attentiveness on incubation period. Data were collected from 44 females (n = 911 days) using temperature data loggers to monitor nest attendance throughout incubation. Mean (± SE) incubation constancy was 86.9 ± 0.6% and incubation period averaged 30.9 ± 0.2 days. Females took an average of two bimodally-distributed recesses per day. Duration of recesses averaged 98.6 ± 3.4 min, but were shorter in the morning than in mid-day or late afternoon. Body mass of incubating females declined 0.68 ± 0.2 g day−1, but there was no relationship between constancy and early incubation body mass or weight change of females. Incubation constancy was not correlated with length of the incubation period. For most females, incubation constancy and recess frequency did not change as incubation progressed. The fact that incubating females only lost an average of 3% of body mass, and constancy was not related to either body mass or length of the incubation period, suggests that females were not constrained energetically. Finally, we propose that the combination of reduced predation risk and the need of neonates to be more functionally mature at hatching has selected for longer incubation periods in Wood Ducks and other cavity-nesting waterfowl.
1The incubation-limitation hypothesis states that clutch size in shorebirds is constrained by the ability to incubate more than four eggs successfully. In order to test predictions from this hypothesis, clutches of northern lapwings (Vanellus vanellus) were here experimentally increased and reduced by one egg at the onset of incubation. Parental behaviour, incubation time, hatching synchrony, egg viability, hatching success and body condition of hatchlings was compared with unmanipulated clutches.2Nest desertion and egg breakage was not observed in any of the experimental nests, showing that clutch enlargement did not alter the parental behaviour adversely.3There were no differences among the experimental groups in male and female attentiveness, but the total nest attentiveness was lower in reduced clutches than in the other clutch sizes; nor did the parents’ frequency of nest visits differ between clutch sizes.4Enlarged clutches were incubated longer than controls and reduced clutches. There were, however, no significant differences among clutch sizes in partial or total clutch predation rates. Hatchability of the eggs (proportion of eggs hatching of those present in nests at the end of incubation) was marginally lower in the enlarged clutches (92·5% vs. 100% in the two other groups).5Contrary to predicted, hatching success was highest in enlarged clutches. The numbers of hatched eggs calculated from Mayfield estimates of daily nest and egg survival rates were 0·93, 2·10 and 3·14 in three-, four- and five-egg clutches, respectively.6When controlling for egg volume, mean body mass of newly hatched chicks was lower in clutches with five eggs than in other nests.7We suggest that the lowered body condition of chicks could outweigh the benefits of laying five instead of four eggs in northern lapwings. Future studies of the selective mechanisms of clutch size in shorebirds should not only focus on the number of young that hatch, but also their quality.
Summary • Maternal effects often explain a significant amount of variation in offspring phenotype, and can be important in the evolution of life histories. Incubation of eggs is an important maternal effect, and optimal growth and development of avian embryos takes place within a narrow range of incubation temperatures, but the effect of incubation microclimate on neonate phenotype remains relatively unexplored in birds. • In this study of Wood Ducks (Aix sponsa Linnaeus) we examined effects of incubation temperature on the length of incubation period and neonate quality. We monitored nest temperatures and incubation periods of naturally incubated Wood Duck nests and found a strong inverse relationship between incubation period and average nest temperature. • Next, we collected three unincubated eggs from each of 48 nests, and randomly assigned eggs from each nest to one of three incubation temperatures (34·6, 36·0 and 37·4 °C). Experimental incubation temperatures overlapped average nest temperatures of naturally incubated Wood Duck nests. • Hatching success varied with incubation temperature and was lowest for eggs incubated at the lowest temperature. Incubation period of experimental eggs decreased with increasing temperature but was not affected by fresh egg mass. • Wood Duck embryos catabolized an estimated 34–38% of egg lipids and 25–33% of egg protein during incubation. Percentage change of lipids increased with decreasing incubation temperature, but not significantly. Embryos incubated at lower temperatures used a greater percentage of protein than embryos incubated at higher temperatures. • In analyses using fresh egg mass as the covariate, we found that wet and dry mass of ducklings increased with increasing incubation temperature. Decreases in lipid content of Wood Duck neonates with decreasing incubation temperature were not significant, but eggs incubated at low temperatures produced ducklings that had reduced protein mass and that were structurally larger than ducklings from eggs incubated at high temperatures. • Our study illustrates the importance of incubation temperature on the development of Wood Duck embryos. Decisions made by incubating parents that influence egg temperature can modify incubation period and offspring phenotype. Investigations of incubation as a reproductive cost should consider how parental decisions influence both parents and offspring. Functional Ecology (2006) 20, 307–314 doi: 10.1111/j.1365-2435.2006.01108.x
There is a range of egg size phenotypes in Mallards (Anas platyrhynchos) that has a large genetic component. It was hypothesized that egg size variation could play an important role in survival of newly hatched ducklings during their first few days out of the nest when they are most susceptible to thermal stress and starvation. Precocial young must be physiologically capable of maintaining homeothermy in order to spend adequate time foraging. Duckling size at hatching was highly correlated with egg mass, and those hatching from heavier eggs were able to maintain homeothermy at colder environmental temperatures than those from lighter eggs. Heavy ducklings had significantly lower mass-specific cooling rates, but lower critical temperature did not vary significantly among ducklings of different size. Although insulation and energy reserves were not proportionally greater in larger ducklings, those hatching from heavier eggs can survive starvation longer than those from lighter eggs. The relative cold tolerance of young from light and heavy eggs will affect the ratio of time spent foraging to time spent being brooded by the female parent. Although there is no direct evidence that selection is acting on egg size, variation in this trait within a population could be maintained by fluctuating environmental conditions at hatch.
Recent research in birds has demonstrated that incubation temperature influences a suite of traits important for hatchling development and survival. We explored a possible mechanism for the effects on hatchling quality by determining whether incubation temperature influences embryonic energy expenditure of wood ducks (Aix sponsa). Because avian embryos are ectothermic, we hypothesized that eggs incubated at higher temperatures would have greater energy expenditure at any given day of incubation. However, because eggs incubated at lower temperatures take longer to hatch than embryos incubated at higher temperatures, we hypothesized that the former would expend more energy during incubation. We incubated eggs at three temperatures (35.0°, 35.9°, and 37.0°C) that fall within the range of temperatures of naturally incubated wood duck nests. We then measured the respiration of embryos every 3 d during incubation, immediately after ducks externally pipped, and immediately after hatching. As predicted, embryos incubated at the highest temperature had the highest metabolic rates on most days of incubation, and they exhibited faster rates of development. Yet, because of greater energy expended during the hatching process, embryos incubated at the lowest temperature expended 20%-37% more energy during incubation than did embryos incubated at the higher temperatures. Slower developmental rates and greater embryonic energy expenditure of embryos incubated at the lowest temperature could contribute to their poor physiological performance as ducklings compared with ducklings that hatch from eggs incubated at higher temperatures.
Incubation temperature is an important maternal effect in birds that can influence numerous offspring traits. For example, ducklings from eggs incubated at lower temperatures have lower growth rates, protein content, and are in poorer body condition than ducklings from eggs incubated at higher temperatures. Based on these observations, we predicted that incubation temperature would indirectly influence performance through its direct effects on body size. Wood duck (Aix sponsa) eggs were incubated at three ecologically relevant temperatures (35, 35.9, 37°C). After hatching, all ducklings were housed under identical conditions and were subjected to aquatic and terrestrial racing trials at 15 and 20 days posthatch (dph). Contrary to our prediction, incubation temperature did not influence most duckling body size parameters at 15 or 20 dph. However, incubation temperature did have a strong influence on locomotor performance independent of body size and body condition. Ducklings hatched from eggs incubated at the lowest temperature had significantly reduced maximum aquatic swim velocity than ducklings from higher temperatures. Maximum terrestrial sprint velocity followed a similar pattern, but did not differ statistically among incubation treatments. To our knowledge, this is the first study to demonstrate that slight changes in incubation temperature can directly affect locomotor performance in avian offspring and thus provide a significant source of phenotypic variation in natural wood duck populations.
As is the case with any metaphor, parental effects mean different things to different biologists--from developmental induction of novel phenotypic variation to an evolved adaptation, and from epigenetic transference of essential developmental resources to a stage of inheritance and ecological succession. Such a diversity of perspectives illustrates the composite nature of parental effects that, depending on the stage of their expression and whether they are considered a pattern or a process, combine the elements of developmental induction, homeostasis, natural selection, epigenetic inheritance and historical persistence. Here, we suggest that by emphasizing the complexity of causes and influences in developmental systems and by making explicit the links between development, natural selection and inheritance, the study of parental effects enables deeper understanding of developmental dynamics of life cycles and provides a unique opportunity to explicitly integrate development and evolution. We highlight these perspectives by placing parental effects in a wider evolutionary framework and suggest that far from being only an evolved static outcome of natural selection, a distinct channel of transmission between parents and offspring, or a statistical abstraction, parental effects on development enable evolution by natural selection by reliably transferring developmental resources needed to reconstruct, maintain and modify genetically inherited components of the phenotype. The view of parental effects as an essential and dynamic part of an evolutionary continuum unifies mechanisms behind the origination, modification and historical persistence of organismal form and function, and thus brings us closer to a more realistic understanding of life's complexity and diversity.
Estimating energy costs by respirometry is fundamental to many studies of the ecology, behavior and evolution of reptiles. However, traditional respirometry procedures seldom incorporate objective techniques for removal of outliers from estimates of metabolic parameters. We demonstrate how computer-automated respirometry equipment, which records many respiratory measurements over short intervals, can be coupled with mathematical procedures to produce robust estimates of pre- and post-prandial metabolism in banded water snakes (Nerodia fasciata fasciata). Standard metabolic rate of N. f. fasciata was estimated to be 1.21 ml O2/h (mass = 30.21 +/- 0.74 g) at 25 degrees C. After ingestion of a fish equaling 20% of their body mass, snakes exhibited a fivefold increase in metabolic rate with peak O2 consumption rate (VO2) reaching 6.5 ml O2/h. Total cost of digestion was 5.44 kJ, equivalent to approximately 21% of the energy in the meal. Repeated measurements of metabolism in the same individuals revealed that our methods yielded similar results, even when individuals exhibited different patterns of VO2 variation between respiratory trials. Our results underscore the importance of obtaining many VO2 measurements, coupled with objective removal of outlier values from estimates of metabolic rate, especially when metabolic values are to be interpreted in a comparative context.
Chronic increases in stress hormones such as glucocorticoids are maladaptive, yet studies demonstrating a causal relationship among chronic stress, increases in glucocorticoid concentrations, and subsequent fitness costs in free-living animals are lacking. We experimentally induced chronic psychological stress in female European starlings (Sturnus vulgaris) by subjecting half of the females at our study site to a chronic stress protocol consisting of 4, 30 min stressors (loud radio, predator calls, a novel object, or predator decoys including a snake, rat, and owl) administered in random order daily for 8 days after clutch completion. Experimental females were captured at the end of the chronic stress protocol (9 days after the onset of the chronic stress protocol), and unstressed control females were captured at the same stage of the nesting cycle. Chronically stressed females had lower baseline corticosterone (CORT, the avian glucocorticoid) concentrations and lower reproductive success than unstressed females. Furthermore, surviving nestlings in experimentally stressed broods showed sensitization of the CORT response to acute stress, which is a physiological change that could persist to adulthood. Attenuation of baseline CORT concentrations in adult females is contrary to the general assumption that elevated CORT concentrations indicate stress, suggesting that more research is necessary before CORT concentrations can be used to accurately assess chronic stress in field studies.
Theory predicts shorter embryonic periods in species with greater embryo mortality risk and smaller body size. Field studies of 80 passerine species on three continents yielded data that largely conflicted with theory; incubation (embryonic) periods were longer rather than shorter in smaller species, and egg (embryo) mortality risk explained some variation within regions, but did not explain larger differences in incubation periods among geographic regions. Incubation behavior of parents seems to explain these discrepancies. Bird embryos are effectively ectothermic and depend on warmth provided by parents sitting on the eggs to attain proper temperatures for development. Parents of smaller species, plus tropical and southern hemisphere species, commonly exhibited lower nest attentiveness (percent of time spent on the nest incubating) than larger and northern hemisphere species. Lower nest attentiveness produced cooler minimum and average embryonic temperatures that were correlated with longer incubation periods independent of nest predation risk or body size. We experimentally tested this correlation by swapping eggs of species with cool incubation temperatures with eggs of species with warm incubation temperatures and similar egg mass. Incubation periods changed (shortened or lengthened) as expected and verified the importance of egg temperature on development rate. Slower development resulting from cooler temperatures may simply be a cost imposed on embryos by parents and may not enhance offspring quality. At the same time, incubation periods of transferred eggs did not match host species and reflect intrinsic differences among species that may result from nest predation and other selection pressures. Thus, geographic variation in embryonic development may reflect more complex interactions than previously recognized.
Species with “slow” life history strategies (long life, low fecundity) are thought to produce high-quality offspring by investing in larger, but fewer, young. Larger eggs are indeed associated with fewer eggs across taxa and can yield higher-quality offspring. Tropical passerines appear to follow theory because they commonly exhibit slow life history strategies and produce larger, but fewer, eggs compared with northern species. Yet, I show here that relative egg mass (corrected for adult mass) varies extensively in the tropics and subtropics for the same clutch size, and this variation is unexplained. I propose a hypothesis to explain egg size variation both within the tropics and between latitudes: Relative egg mass increases in species with cooler egg temperatures and longer embryonic periods to offset associated increases in energetic requirements of embryos. Egg temperatures of birds are determined by parental incubation behavior and are often cooler among tropical passerines because of reduced parental attentiveness of eggs. Here, I show that cooler egg temperatures and longer embryonic periods explained the enigmatic variation in egg mass within and among regions, based on field studies in tropical Venezuela (36 species), subtropical Argentina (16 species), and north temperate Arizona (20 species). Alternative explanations are not supported. Thus, large egg sizes may reflect compensation for increased energetic requirements of cool egg temperatures and long embryonic periods that result from reduced parental attentiveness in tropical birds.
• clutch size
• incubation
• life history
• passerines
Ecology and Management of the Wood Duck Season and latitudinal trends in clutch size: thermal constraints during laying and incubation
- F C Bellrose
- D J Holm
- Stackpole Books
- Mechanicsburg
- C B Cooper
- W M Hochachka
- G Butcher
- A Dhondt
Bellrose, F.C. & Holm, D.J. (1994) Ecology and Management of the Wood Duck. Stackpole Books, Mechanicsburg. Cooper, C.B., Hochachka, W.M., Butcher, G. & Dhondt, A. (2005) Season and latitudinal trends in clutch size: thermal constraints during laying and incubation. Ecology, 86, 2018–2031.