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1. Proximate and evolutionary sources of variation in offspring energy expenditure in songbirds

   https://doi.org/10.1111/geb.13467  

   Mitchell, Adam E. ; Wolf, Blair O. ; Martin, Thomas E. ; Sheard, ed., Catherine ( February 2022 , Global Ecology and Biogeography)

   Understanding variation in offspring energy expenditure is important because energy is critical for growth and development. Weather may exert proximate effects on offspring energy expenditure, but in altricial species these might be masked by parental care and huddling with siblings. Such effects are particularly important to understand given changing global weather patterns, yet studies of wild offspring in the presence of parental care are lacking. Offspring energy expenditure may also vary among species due to evolved responses to environmental selection pressures, requiring studies at both proximate and ultimate levels.

   USA, South Africa, Malaysia.

   2016–2019.

   Songbirds.

   We used the doubly‐labelled water technique to estimate nestling daily energy expenditure of 54 songbird species across three continents. We used Bayesian phylogenetic mixed models to test proximate and evolutionary causes of variation in offspring energy expenditure while accounting for phylogeny and phylogenetic uncertainty.

   Offspring energy expenditure increased with more rainfall and colder air temperatures, but decreased among offspring in broods with more siblings. Across species, nestling and adult mortality, but not growth rate, were positively associated with offspring energy use.

   Weather had clear proximate effects on offspring energy expenditure and parents were either unable or unwilling to fully offset these effects. However, the decrease in offspring energy use when huddling with more siblings demonstrated a modulating effect of life history traits. For example, high nest predation rates favour reduced parental care and can force offspring to spend more energy coping with environmental conditions. Furthermore, reduced energy expenditure is thought to facilitate increased longevity, which is increasingly realized with lower extrinsic mortality rates, providing an explanation for the positive association between adult mortality and offspring energy expenditure. Ultimately, both proximate and evolutionary influences need to be considered to better understand causes of offspring energetics.

    

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2. White Paper: An Integrated Perspective on the Causes of Hypometric Metabolic Scaling in Animals

   https://doi.org/10.1093/icb/icac136  

   Harrison, Jon F. ; Biewener, Andrew ; Bernhardt, Joanna R. ; Burger, Joseph R. ; Brown, James H. ; Coto, Zach N. ; Duell, Meghan E. ; Lynch, Michael ; Moffett, Emma R. ; Norin, Tommy ; et al ( August 2022 , Integrative and Comparative Biology)

   Larger animals studied during ontogeny, across populations, or across species, usually have lower mass-specific metabolic rates than smaller animals (hypometric scaling). This pattern is usually observed regardless of physiological state (e.g., basal, resting, field, and maximally active). The scaling of metabolism is usually highly correlated with the scaling of many life-history traits, behaviors, physiological variables, and cellular/molecular properties, making determination of the causation of this pattern challenging. For across-species comparisons of resting and locomoting animals (but less so for across populations or during ontogeny), the mechanisms at the physiological and cellular level are becoming clear. Lower mass-specific metabolic rates of larger species at rest are due to (a) lower contents of expensive tissues (brains, liver, and kidneys), and (b) slower ion leak across membranes at least partially due to membrane composition, with lower ion pump ATPase activities. Lower mass-specific costs of larger species during locomotion are due to lower costs for lower-frequency muscle activity, with slower myosin and Ca++ ATPase activities, and likely more elastic energy storage. The evolutionary explanation(s) for hypometric scaling remain(s) highly controversial. One subset of evolutionary hypotheses relies on constraints on larger animals due to changes in geometry with size; for example, lower surface-to-volume ratios of exchange surfaces may constrain nutrient or heat exchange, or lower cross-sectional areas of muscles and tendons relative to body mass ratios would make larger animals more fragile without compensation. Another subset of hypotheses suggests that hypometric scaling arises from biotic interactions and correlated selection, with larger animals experiencing less selection for mass-specific growth or neurolocomotor performance. An additional third type of explanation comes from population genetics. Larger animals with their lower effective population sizes and subsequent less effective selection relative to drift may have more deleterious mutations, reducing maximal performance and metabolic rates. Resolving the evolutionary explanation for the hypometric scaling of metabolism and associated variables is a major challenge for organismal and evolutionary biology. To aid progress, we identify some variation in terminology use that has impeded cross-field conversations on scaling. We also suggest that promising directions for the field to move forward include (1) studies examining the linkages between ontogenetic, population-level, and cross-species allometries; (2) studies linking scaling to ecological or phylogenetic context; (3) studies that consider multiple, possibly interacting hypotheses; and (4) obtaining better field data for metabolic rates and the life history correlates of metabolic rate such as lifespan, growth rate, and reproduction.

    

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3. Size-Dependent Scaling of Stingless Bee Flight Metabolism Reveals an Energetic Benefit to Small Body Size

   https://doi.org/10.1093/icb/icac131  

   Duell, Meghan E. ; Klok, C. Jaco ; Roubik, David W. ; Harrison, Jon F. ( September 2022 , Integrative and Comparative Biology)

   Understanding the effect of body size on flight costs is critical for the development of models of aerodynamics and animal energetics. Prior scaling studies that have shown that flight costs scale hypometrically have focused primarily on larger (>100 mg) insects and birds, but most flying species are smaller. We studied the flight physiology of 13 stingless bee species over a large range of body sizes (1–115 mg). Metabolic rate during hovering scaled hypermetrically (scaling slope = 2.11). Larger bees had warm thoraxes, while small bees were nearly ecothermic; however, even controlling for body temperature variation, flight metabolic rate scaled hypermetrically across this clade. Despite having a lower mass-specific metabolic rate during flight, smaller bees could carry the same proportional load. Wingbeat frequency did not vary with body size, in contrast to most studies that find wingbeat frequency increases as body size decreases. Smaller stingless bees have a greater relative forewing surface area, which may help them reduce the energy requirements needed to fly. Further, we hypothesize that the relatively larger heads of smaller species may change their body pitch in flight. Synthesizing across all flying insects, we demonstrate that the scaling of flight metabolic rate changes from hypermetric to hypometric at ∼58 mg body mass with hypermetic scaling below (slope = 1.2) and hypometric scaling (slope = 0.67) >58 mg in body mass. The reduced cost of flight likely provides selective advantages for the evolution of small body size in insects. The biphasic scaling of flight metabolic rates and wingbeat frequencies in insects supports the hypothesis that the scaling of metabolic rate is closely related to the power requirements of locomotion and cycle frequencies.

    

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4. Carry‐over effects of larval food stress on adult energetics and life history in a nectar‐feeding butterfly

   https://doi.org/10.1111/een.13124  

   Niitepõld, Kristjan ; Boggs, Carol L. ( January 2022 , Ecological Entomology)

   Stressful juvenile developmental conditions can affect performance and fitness later in life. In holometabolous insects such as butterflies, development under stressful conditions may lead to smaller adult size, lower reproductive output, and shorter lifespan. However, how larval developmental stress affects energy intake and expenditure in adult individuals is poorly understood.

   We subjected last‐instar larvae ofSpeyeria mormoniaEdwards (Lepidoptera: Nymphalidae) to periodic dietary restriction (DR) to examine the allocation of energy and nutrients among different life history processes. We measured adult food intake, resting metabolic rate (RMR), metabolic flight capacity, lifespan, and reproductive output. Consistent with pressure to disperse from a poor environment while maintaining offspring number, we predicted that stressed individuals would have increased adult food intake and higher flight capacity.

   Adult body size was strongly reduced. Contrary to predictions, we found no compensatory adult feeding. Mass‐adjusted flight metabolic rate was reduced, suggesting poor dispersal capacity. Larval DR did not affect adult lifespan, nor did the rate of metabolic senescence change. Larval DR did affect RMR, as stressed females had a steeper slope between RMR and body mass, which may reflect differences in physiological activity due to condition.

   Fecundity decreased less than predicted based on body mass. Instead of investing in flight capacity, females increased relative allocation to reproduction, which may partly buffer against poor environmental conditions.

   Understanding the interplay of energy acquisition and allocation to life history traits across the life cycle is vital for predicting responses to environmental change.

    

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5. The Pace of Life: Metabolic Energy, Biological Time, and Life History

   https://doi.org/10.1093/icb/icac058  

   Brown, James H ; Burger, Joseph R ; Hou, Chen ; Hall, Charles A ( July 2022 , Integrative and Comparative Biology)

   Synopsis New biophysical theory and electronic databases raise the prospect of deriving fundamental rules of life, a conceptual framework for how the structures and functions of molecules, cells, and individual organisms give rise to emergent patterns and processes of ecology, evolution, and biodiversity. This framework is very general, applying across taxa of animals from 10–10 g protists to 108 g whales, and across environments from deserts and abyssal depths to rain forests and coral reefs. It has several hallmarks: (1) Energy is the ultimate limiting resource for organisms and the currency of biological fitness. (2) Most organisms are nearly equally fit, because in each generation at steady state they transfer an equal quantity of energy (˜22.4 kJ/g) and biomass (˜1 g/g) to surviving offspring. This is the equal fitness paradigm (EFP). (3) The enormous diversity of life histories is due largely to variation in metabolic rates (e.g., energy uptake and expenditure via assimilation, respiration, and production) and biological times (e.g., generation time). As in standard allometric and metabolic theory, most physiological and life history traits scale approximately as quarter-power functions of body mass, m (rates as ∼m–1/4 and times as ∼m1/4), and as exponential functions of temperature. (4) Time is the fourth dimension of life. Generation time is the pace of life. (5) There is, however, considerable variation not accounted for by the above scalings and existing theories. Much of this “unexplained” variation is due to natural selection on life history traits to adapt the biological times of generations to the clock times of geochronological environmental cycles. (6) Most work on biological scaling and metabolic ecology has focused on respiration rate. The emerging synthesis applies conceptual foundations of energetics and the EFP to shift the focus to production rate and generation time. 

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