ALBERT

Description: Metabolism should drive demography by determining the rates of both biological work and resource demand. Long-standing “rules” for how metabolism should covary with demography permeate biology, from predicting the impacts of climate change to managing fisheries. Evidence for these rules is almost exclusively indirect and in the form of among-species comparisons, while direct evidence is exceptionally rare. In a manipulative field experiment on a sessile marine invertebrate, we created experimental populations that varied in population size (density) and metabolic rate, but not body size. We then tested key theoretical predictions regarding relationships between metabolism and demography by parameterizing population models with lifetime performance data from our field experiment. We found that populations with higher metabolisms had greater intrinsic rates of increase and lower carrying capacities, in qualitative accordance with classic theory. We also found important departures from theory—in particular, carrying capacity declined less steeply than predicted, such that energy use at equilibrium increased with metabolic rate, violating the long-standing axiom of energy equivalence. Theory holds that energy equivalence emerges because resource supply is assumed to be independent of metabolic rate. We find this assumption to be violated under real-world conditions, with potentially far-reaching consequences for the management of biological systems.

Description: Group living has been proposed to yield benefits that enhance fitness above the level that would be achieved through living as solitary individuals. Dominance hierarchies occur commonly in these social assemblages, and result, by definition, in resources not being evenly distributed between group members. Determinants of rank within a dominance hierarchy can be associated with morphological characteristics, previous experience of the individual, or personality traits such as exploration tendencies. The purpose of this study was to investigate whether greater exploration and positive responses to novel objects in homing pigeons ( Columba livia ) measured under laboratory conditions were associated with (i) greater initial exploration of the local area around the home loft during spontaneous exploration flights (SEF), (ii) faster and more efficient homing flights when released from further afield, and (iii) whether the traits of greater exploration and more positive responses to novel objects were more likely to be exhibited by the more dominant individuals within the group. There was no relationship between laboratory-based novel object exploration and position within the dominance hierarchy. Pigeons that were neophobic under laboratory conditions did not explore the local area during SEF opportunities. When released from sites further from home, neophobic pigeons took longer routes to home compared to those birds that had not exhibited neophobic traits under laboratory conditions, and had spontaneously explored to a greater extent. The lack of exploration in the neophobic birds is likely to have resulted in the increased costs of homing following release: unfamiliarity with the landscape likely led to the greater distances travelled and less efficient routes taken. Birds that demonstrated a lack of neophobia were not the dominant individuals inside the loft, and thus would have less access to resources such as food and potentially mates. However, a lack of neophobia makes the subordinate position possible, because subordinate birds that incur high travel costs would become calorie restricted and lose condition. Our results address emerging questions linking individual variation in behaviour with energetics and fitness consequences. This article is part of the themed issue ‘Physiological determinants of social behaviour in animals’.

Description: Dominance hierarchies confer benefits to group members by decreasing the incidences of physical conflict, but may result in certain lower ranked individuals consistently missing out on access to resources. Here, we report a linear dominance hierarchy remaining stable over time in a closed population of birds. We show that this stability can be disrupted, however, by the artificial mass loading of birds that typically comprise the bottom 50% of the hierarchy. Mass loading causes these low-ranked birds to immediately become more aggressive and rise-up the dominance hierarchy; however, this effect was only evident in males and was absent in females. Removal of the artificial mass causes the hierarchy to return to its previous structure. This interruption of a stable hierarchy implies a strong direct link between body mass and social behaviour and suggests that an individual's personality can be altered by the artificial manipulation of body mass.

Description: The discontinuous gas exchange cycle (DGC) is a breathing pattern displayed by many insects, characterized by periodic breath-holding and intermittently low tracheal O 2 levels. It has been hypothesized that the adaptive value of DGCs is to reduce oxidative damage, with low tracheal O 2 partial pressures ( P O 2 ∼2–5 kPa) occurring to reduce the production of oxygen free radicals. If this is so, insects displaying DGCs should continue to actively defend a low tracheal P O 2 even when breathing higher than atmospheric levels of oxygen (hyperoxia). This behaviour has been observed in moth pupae exposed to ambient P O 2 up to 50 kPa. To test this observation in adult insects, we implanted fibre-optic oxygen optodes within the tracheal systems of adult migratory locusts Locusta migratoria exposed to normoxia, hypoxia and hyperoxia. In normoxic and hypoxic atmospheres, the minimum tracheal P O 2 that occurred during DGCs varied between 3.4 and 1.2 kPa. In hyperoxia up to 40.5 kPa, the minimum tracheal P O 2 achieved during a DGC exceeded 30 kPa, increasing with ambient levels. These results are consistent with a respiratory control mechanism that functions to satisfy O 2 requirements by maintaining P O 2 above a critical level, not defend against high levels of O 2 .

Description: For free-ranging animals, field metabolic rate (FMR) is the sum of their energy expenditure over a specified period. This quantity is a key component of ecological processes at every biological level. We applied a phylogenetically informed meta-analytical approach to identify the large-scale determinants of FMR in seabirds during the breeding season. Using data from 64 studies of energetics in 47 species, we created a model to estimate FMR for any seabird population. We found that FMR was positively influenced by body mass and colony latitude and that it increased throughout the breeding season from incubation to brood to crèche. FMR was not impacted by colony-relative predation pressure or species average brood size. Based on this model, we present an app through which users can generate estimates of FMR for any population of breeding seabird. We encourage the use of this app to complement behavioural studies and increase understanding of how energetic demands influence the role of seabirds as driving components of marine systems.

Description: Hypertrophy of the flight muscles is regularly observed in birds prior to long-distance migrations. We tested the hypothesis that a large migratory bird would increase flight behaviour prior to migration, in order to cause hypertrophy of the flight muscles, and upregulate key components of the aerobic metabolic pathways. Implantable data loggers were used to record year-round heart rate in six wild barnacle geese ( Branta leucopsis ), and the amount of time spent in flight each day was identified. Time in flight per day did not significantly increase prior to either the spring or the autumn migration, both between time periods prior to migration (5, 10 and 15 days), or when compared with a control period of low activity during winter. The lack of significant increase in flight prior to migration suggests that approximately 22 min per day is sufficient to maintain the flight muscles in condition for prolonged long-distance flight. This apparent lack of a requirement for increased flight activity prior to migration may be attributable to pre-migratory mass gains in the geese increasing workload during short flights, potentially prompting hypertrophy of the flight muscles.

Description: Cormorants hunt both benthic (sedentary) and pelagic (motile) prey but it is not known if the energy costs of foraging on these prey differ. We used respirometry to measure the costs of diving in double-crested cormorants ( Phalacrocorax auritus ) foraging either for sedentary (fish pieces) or motile (juvenile salmon) prey in a deep dive tank. Short dives for sedentary prey were more expensive than dives of similar duration for motile prey (e.g. 20% higher for a 10 s dive) whereas the reverse was true for long dives (i.e. long dives for motile prey were more expensive than for sedentary prey). Across dives of all durations, the foraging phase of the dive was more expensive when the birds hunted motile prey, presumably due to pursuit costs. The period of descent in all the dives undertaken appears to have been more expensive when the birds foraged on sedentary prey, probably due to a higher swimming speed during this period.

Description: Waterfowl undergo an annual simultaneous flight-feather moult that renders them flightless for the duration of the regrowth of the flight feathers. In the wild, this period of flightlessness could restrict the capacity of moulting birds to forage and escape predation. Selection might therefore favour a short moult, but feather growth is constrained and presumably energetically demanding. We therefore tested the hypothesis that for birds that undergo a simultaneous flight-feather moult, this would be the period in the annual cycle with the highest minimum daily heart rates, reflecting these increased energetic demands. Implantable heart rate data loggers were used to record year-round heart rate in six wild barnacle geese ( Branta leucopsis ), a species that undergoes a simultaneous flight-feather moult. The mean minimum daily heart rate was calculated for each individual bird over an 11-month period, and the annual cycle was divided into seasons based on the life-history of the birds. Mean minimum daily heart rate varied significantly between seasons and was significantly elevated during wing moult, to 200 ± 32 beats min −1 , compared to all other seasons of the annual cycle, including both the spring and autumn migrations. The increase in minimum daily heart rate during moult is likely due to feather synthesis, thermoregulation and the reallocation of minerals and protein.

Description: Body size and temperature are primary determinants of metabolic rate, and the standard metabolic rate (SMR) of animals ranging in size from unicells to mammals has been thought to be proportional to body mass ( M ) raised to the power of three-quarters for over 40 years. However, recent evidence from rigorously selected datasets suggests that this is not the case for birds and mammals. To determine whether the influence of body mass on the metabolic rate of vertebrates is indeed universal, we compiled SMR measurements for 938 species spanning six orders of magnitude variation in mass. When normalized to a common temperature of 38 °C, the SMR scaling exponents of fish, amphibians, reptiles, birds and mammals are significantly heterogeneous. This suggests both that there is no universal metabolic allometry and that models that attempt to explain only quarter-power scaling of metabolic rate are unlikely to succeed.

Description: Previously, it has been suggested that insect gas exchange cycle frequency (fC) is mass independent, making insects different from most other animals where periods typically scale as mass−0.25. However, the claim for insects is based on studies of only a few closely related taxa encompassing a relatively small size range. Moreover, it is not known whether the type of gas exchange pattern (discontinuous versus cyclic) influences thefC–mass scaling relationship. Here, we analyse a large database to examine interspecificfC–mass scaling. In addition, we investigate the effect of mode of gas exchange on thefC–scaling relationship using both conventional and phylogenetically independent approaches. Cycle frequency is scaled as mass−0.280(when accounting for phylogeneticnon-independence and gas exchange pattern), which did not differ significantly from mass−0.25. The slope of thefC–mass relationship was shallower with a significantly lower intercept for the species showing discontinuous gas exchange than for those showing the cyclic pattern, probably due to lower metabolic rates in the former. Insects therefore appear no different from other animals insofar as the scaling of gas exchangefCis concerned, although gas exchangefCmay scale in distinct ways for different patterns.