The relative importance of intrinsic constraints imposed by evolved physiological trade-offs versus the proximate effects of temperature for interspecific variation in embryonic development time ...remains unclear. Understanding this distinction is important because slow development due to evolved trade-offs can yield phenotypic benefits, whereas slow development from low temperature can yield costs. We experimentally increased embryonic temperature in free-living tropical and north temperate songbird species to test these alternatives. Warmer temperatures consistently shortened development time without costs to embryo mass or metabolism. However, proximate effects of temperature played an increasingly stronger role than intrinsic constraints for development time among species with colder natural incubation temperatures. Long development times of tropical birds have been thought to primarily reflect evolved physiological trade-offs that facilitate their greater longevity. In contrast, our results indicate a much stronger role of temperature in embryonic development time than currently thought.
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IZUM, KILJ, NUK, PILJ, PNG, SAZU, UL, UM, UPUK
Human-induced climate change is increasing the frequency, duration, and intensity of heat waves and exposure to these extreme temperatures impacts individual physiology and performance (e.g., ...metabolism, water balance, and growth). These traits may be susceptible to thermal conditions experienced during embryonic development, but experiments focusing on post-natal development are scant. Documented effects of heat waves on whole-body metabolism may reflect changes in mitochondrial function, but most studies do not measure physiological traits at both the cellular and whole organism levels. Here, we exposed nests of zebra finches to experimentally simulated heat waves for 18 days after hatching and measured body mass, growth rate, whole-body metabolic rate, body temperature, wet thermal conductance, evaporative water loss, and relative water economy of chicks at three ages corresponding to ectothermic (day 5), poikilothermic (day 12), and homoeothermic (day 50) stages. Additionally, we measured mitochondrial bioenergetics of blood cells 80 days post-hatch. While early-life exposure to heat wave conditions did not impact whole body metabolic and hygric physiology, body temperature was lower for birds from heated compared with control nests at both 12 and 50 days of age. There was also an effect of nest heating at the cellular level, with mitochondria from heated birds having higher endogenous and proton-leak related respiration, although oxidative phosphorylation, maximum respiratory capacity, and coupling efficiency were not impacted. Our results suggest that early-life exposure to high ambient temperature induces programming effects on cellular-level and thermal physiology that may not be apparent for whole-animal metabolism.
Causes of interspecific variation in growth rates within and among geographic regions remain poorly understood. Passerine birds represent an intriguing case because differing theories yield the ...possibility of an antagonistic interaction between nest predation risk and food delivery rates on evolution of growth rates. We test this possibility among 64 Passerine species studied on three continents, including tropical and north and south temperate latitudes. Growth rates increased strongly with nestling predation rates within, but not between, sites. The importance of nest predation was further emphasized by revealing hidden allometric scaling effects. Nestling predation risk also was associated with reduced total feeding rates and per-nestling feeding rates within each site. Consequently, faster growth rates were associated with decreased per-nestling food delivery rates across species, both within and among regions. These relationships suggest that Passerines can evolve growth strategies in response to predation risk whereby food resources are not the primary limit on growth rate differences among species. In contrast, reaction norms of growth rate relative to brood size suggest that food may limit growth rates within species in temperate, but not tropical, regions. Results here provide new insight into evolution of growth strategies relative to predation risk and food within and among species.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK
Here we investigate possible carryover effects of experimentally increased incubation temperatures for postnatal growth, metabolism, and parental care within and among 6 north temperate and one ...tropical songbird species. Increased temperatures during embryonic development consistently caused higher postnatal resting metabolism compared to control nests, among but not within the 7 species studied. The effects of the experiment on growth were species specific and depended on the morphometric considered. Size before the fledge date was positively correlated with feeding rate, and metabolism was lower in larger broods. Our experiment did not elicit changes in parental food delivery rates or brooding effort during the postnatal stage, and higher brooding effort was associated with nestlings of smaller mass and faster metabolism independently from treatment. Consequently, parental care seemed unlikely to be the cause of the differences in growth rates between treatments. Instead, physiological mechanisms triggered by our heating treatment appear to be responsible for the observed variation in growth. These intrinsic changes unmatched by adjustments in parental effort may contribute to longer-term consequences for individual quality and survival that deserve further attention. LAY SUMMARY Temperatures experienced during incubation can have later influences on the growth and metabolism of chicks. Temperatures additionally impact the energy balance of parents and therefore their ability to allocate resources for feeding themselves and their brood after hatching. This evidence suggests that early temperature conditions during the egg stage can have downstream effects on nestling growth that can be fully understood only by integrating physiological and parental contributions. After experimentally heating nests of 7 different species of songbirds, we measured nestling metabolism and growth, together with parental rates of feeding and brooding. Our results show that nestlings from heated eggs had increased metabolism and some species changed their growth trajectories, but this was not associated with different rates of parental brooding and feeding. These results are important because higher ambient temperatures are forecasted all over the world and may influence thermal conditions during incubation. However, growth sustained by higher food availability is considered beneficial, though when associated with accelerated metabolism is considered detrimental for individual quality. Aquí investigamos los posibles efectos de arrastre del aumento experimental de las temperaturas de incubación para el crecimiento posnatal, el metabolismo y el cuidado parental dentro y entre seis especies de aves canoras de zonas templadas del norte y una tropical. El aumento de las temperaturas durante el desarrollo embrionario provocó consistentemente un mayor metabolismo en reposo posnatal en comparación con los nidos de control, entre las siete especies estudiadas, pero no dentro de ellas. Los efectos del experimento sobre el crecimiento fueron específicos de cada especie y dependieron de la morfometría considerada. El tamaño antes de la fecha del emplumamiento se correlacionó positivamente con la tasa de alimentación y el metabolismo fue menor en las crías más grandes. Nuestro experimento no provocó cambios en las tasas de entrega de alimentos de los padres ni en el esfuerzo de crianza durante la etapa posnatal, y el esfuerzo de crianza se asoció con polluelos de mayor masa y metabolismo más rápido independientemente del tratamiento. En consecuencia, parecía poco probable que el cuidado de los padres fuera la causa de las diferencias en las tasas de crecimiento entre los tratamientos. En cambio, los mecanismos fisiológicos desencadenados por nuestro tratamiento térmico parecen ser responsables de la variación observada en el crecimiento. Estos cambios intrínsecos, que no se pueden comparar con ajustes en el esfuerzo de los padres, pueden contribuir a consecuencias a más largo plazo para la calidad y la supervivencia individual que merecen mayor atención.
Heat waves are predicted to be detrimental for organismal physiology with costs for survival that could be reflected in markers of biological state such as telomeres. Changes in early life telomere ...dynamics driven by thermal stress are of particular interest during the early post‐natal stages of altricial birds because nestlings quickly shift from being ectothermic to endothermic after hatching. Telomeres of ectothermic and endothermic organisms respond differently to environmental temperature, but few investigations within species that transition from ectothermy to endothermy are available. Also, ambient temperature influences parental brooding behaviour, which will alter the temperature experienced by offspring and thereby, potentially, their telomeres. We exposed zebra finch nestlings to experimental heat waves and compared their telomere dynamics to that of a control group at 5, 12 and 80 days of age that encapsulate the transition from the ectothermic to the endothermic thermoregulatory stage; we also recorded parental brooding, offspring sex, mass, growth rates, brood size and hatch order. Nestling mass showed an inverse relationship with telomere length, and nestlings exposed to heat waves showed lower telomere attrition during their first 12 days of life (ectothermic stage) compared to controls. Additionally, parents of heated broods reduced the time they spent brooding offspring (at 5 days old) compared to controls. Our results indicate that the effect of heat waves on telomere dynamics likely varies depending on age and thermoregulatory stage of the offspring in combination with parental brooding behaviour during growth.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Metabolism is thought to mediate the connection between environmental selection pressures and a broad array of life history tradeoffs, but tests are needed. High juvenile predation correlates with ...fast growth, which may be achieved via fast juvenile metabolism. Fast offspring metabolism and growth can create physiological costs later in life that should be minimized in species with low adult mortality. Yet, relationships between juvenile metabolism and mortality at offspring versus adult stages are unexplored. We found that post-natal metabolism was positively correlated with adult mortality but not nest predation rates among 43 songbird species on three continents. Nest predation, but not adult mortality, explained additional variation in growth rates beyond metabolism. Our results suggest that metabolism may not be the mechanism underlying the relationships between growth and mortality at different life stages.
Understanding the consequences of heat exposure on mitochondrial function is crucial as mitochondria lie at the core of metabolic processes, also affecting population dynamics. In adults, ...mitochondrial metabolism varies with temperature but can also depend on thermal conditions experienced during development. We exposed zebra finches to two alternative heat treatments during early development: “constant”, maintained birds at ambient 35 °C from parental pair formation to fledglings’ independence, while “periodic” heated broods at 40 °C, 6 h daily at nestling stage. Two years later, we acclimated birds from both experiments at 25 °C for 21 days, before exposing them to artificial heat (40 °C, 5 h daily for 10 days). After both conditions, we measured red blood cells’ mitochondrial metabolism using a high-resolution respirometer. We found significantly decreased mitochondrial metabolism for Routine, Oxidative Phosphorylation (OxPhos) and Electron Transport System maximum capacity (ETS) after the heat treatments. In addition, the birds exposed to “constant” heat in early life showed lower oxygen consumption at the Proton Leak (Leak) stage after the heat treatment as adults. Females showed higher mitochondrial respiration for Routine, ETS and Leak independent of the treatments, while this pattern was reversed for OxPhos coupling efficiency (OxCE). Our results show that short-term acclimation involved reduced mitochondrial respiration, and that the reaction of adult birds to heat depends on the intensity, pattern and duration of temperature conditions experienced at early-life stages. Our study provides insight into the complexity underlying variation in mitochondrial metabolism and raises questions on the adaptive value of long-lasting physiological adjustments triggered by the early-life thermal environment.
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EMUNI, FIS, FZAB, GEOZS, GIS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
Summary
Variation in post‐natal growth rates is substantial among organisms and especially strong among latitudes because tropical and south temperate species typically have slower growth than north ...temperate relatives. Metabolic rate is thought to be a critical mechanism underlying growth rates after accounting for allometric effects of body mass. However, comparative tests on a large spatial scale are lacking, and the importance of metabolism for growth rates remains unclear both within and particularly across latitudes.
Songbirds exhibit strong interspecific variation in growth rates across geographic space, although within latitudes an association between metabolic rate and growth rate has not always been observed. Moreover, the hypothesis that differences in growth rates across latitudes reflect underlying differences in metabolism is untested. Here, we investigate these possibilities across north temperate, south temperate and tropical study sites.
Phylogenetic analyses showed that, for a given body mass, metabolic rates of north temperate nestlings were higher than tropical and south temperate species. Metabolic rates controlled for body mass correlated with post‐natal growth rates both within and among latitudes. Offspring body mass explained substantial residual variation in growth rates as expected under classic allometric theory.
Our results suggest that variation in metabolic rates has an important influence on broad patterns of avian growth rates at a global scale. We suggest further studies that address the ecological and physiological costs and consequences of variation in metabolism and growth rates.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK
Our understanding of connections between human and animal health has advanced substantially since the canary was introduced as a sentinel of toxic conditions in coal mines. Nonetheless, the ...development of wildlife sentinels for monitoring human exposure to toxins has been limited. Here, we capitalized on a three-decade long child blood lead monitoring program to demonstrate that the globally ubiquitous and human commensal house sparrow (Passer domesticus) can be used as a sentinel of human health risks in urban environments impacted by lead mining. We showed that sparrows are a viable proxy for the measurement of blood lead levels in children at a neighborhood scale (0.28 km2). In support of the generalizability of this approach, the blood lead relationship established in our focal mining city enabled us to accurately predict elevated blood lead levels in children from another mining city using only sparrows from the second location. Using lead concentrations and lead isotopic compositions from environmental and biological matrices, we identified shared sources and pathways of lead exposure in sparrows and children, with strong links to contamination from local mining emissions. Our findings showed how human commensal species can be used to identify and predict human health risks over time and space.
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IJS, KILJ, NUK, PNG, UL, UM
Telomere length and DNA methylation (DNAm) are two promising biomarkers of biological age. Environmental factors and life history traits are known to affect variation in both these biomarkers, ...especially during early life, yet surprisingly little is known about their reciprocal association, especially in natural populations. Here, we explore how variation in DNAm, growth rate, and early‐life conditions are associated with telomere length changes during development. We tested these associations by collecting data from wild, nestling zebra finches in the Australian desert. We found that increases in the level of DNAm were negatively correlated with telomere length changes across early life. We also confirm previously documented effects of post hatch growth rate and clutch size on telomere length in a natural ecological context for a species that has been extensively studied in the laboratory. However, we did not detect any effect of ambient temperature during developmental on telomere length dynamics. We also found that the absolute telomere length of wild zebra finches, measured using the in‐gel TRF method, was similar to that of captive birds. Our findings highlight exciting new opportunities to link and disentangle potential relationships between DNA based biomarkers of ageing, and of physiological reactions to environmental change.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
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