Andrew E. McKechnie

AVIAN FACULTATIVE HYPOTHERMIC RESPONSES: A REVIEW

Abstract Recent evidence suggests that avian facultative hypothermic responses are more common, and occur in a wider variety of ecological contexts, than previously thought. The capacity for shallow hypothermia (rest-phase hypothermia) occurs throughout the avian phylogeny, but the capacity for pronounced hypothermia (torpor) appears to be restricted to certain taxa. Families in which torpor has been reported include the Todidae, Coliidae, Trochilidae, Apodidae, Caprimulgidae, and Columbidae. Facultative hypothermia occurs in species ranging in body mass (Mb) from <3 g to ca. 6500 g. Minimum body temperature (Tb) during hypothermia is continuously distributed from 4.3°C to ca. 38°C. The physiological distinction between torpor and rest-phase hypothermia is unclear. Whereas these two responses have traditionally been distinguished on the basis of Tb, we find little support for the biological reality of specific Tb limits. Instead, we argue that emphasis should be placed on understanding the relationship between metabolic and Tb reduction and the capacity to respond to external stimuli. Patterns of thermoregulation during avian hypothermic responses are relatively variable, and do not necessarily follow the entry–maintenance–arousal patterns that characterize mammalian responses. Avian hypothermic responses are determined by a suite of ecological and physiological determinants including food availability, ambient temperature, hormone levels, and breeding cycle. Respuestas Facultativas de la Hipotermia en Aves: Una Revisión Resumen. Evidencias recientes sugieren que las respuestas facultativas de la hipotermia aviar son más comunes y ocurren en una gran cantidad de contextos ecológicos, a diferencia de lo que anteriormente se pensaba. La capacidad de una hipotermia ligera (hipotermia de descanso) ocurre en toda la filogenia de las aves, pero la capacidad de mantener una hipotermia pronunciada (torpor) aparece sólo en ciertos taxones. El torpor ha sido reportado en las familias Todidae, Coliidae, Trochilidae, Apodidae, Caprimulgidae y Columbidae. La hipotermia facultativa ocurre en especies con un peso corporal (Mb) de <3 g hasta 6.5 kg. Durante la hipotermia, la temperatura mínima corporal (Tb) está distribuída contínuamente entre 4.3°C y 38°C. La diferencia fisiológica entre el torpor y la hipotermia de descanso no es clara. Tradicionalmente se ha reconocido que las dos respuestas se basan en la Tb. Sin embargo, nosotros encontramos pocas evidencias biológicas sobre límites específicos de la Tb. Por el contrario, nosotros argumentamos que el énfasis debe enfocarse en la relación entre la reducción metabólica y de Tb y la capacidad de responder a estímulos externos. Los patrones de termoregulación de las respuestas hipotérmicas de las aves son relativamente variables y no necesariamente siguen los patrones de entrada-mantenimiento-elevación que caracterizan estas respuestas en los mamíferos. Las respuestas de la hipotermia en aves están determinadas por la interacción entre factores ecológicos y fisiológicos como disponibilidad de alimentos, temperatura ambiental, niveles hormonales y ciclo reproductivo.

The Allometry of Avian Basal Metabolic Rate: Good Predictions Need Good Data

Basal metabolic rate (BMR) is often predicted by allometric interpolation, but such predictions are critically dependent on the quality of the data used to derive allometric equations relating BMR to body mass (Mb). An examination of the metabolic rates used to produce conventional and phylogenetically independent allometries for avian BMR in a recent analysis revealed that only 67 of 248 data unambiguously met the criteria for BMR and had sample sizes with n ≥ 3. The metabolic rates that represented BMR were significantly lower than those that did not meet the criteria for BMR or were measured under unspecified conditions. Moreover, our conventional allometric estimates of BMR (W; log BMR = −1.461 + 0.669log Mb) using a more constrained data set that met the conditions that define BMR and had n ≥ 3 were 10%–12% lower than those obtained in the earlier analysis. The inclusion of data that do not represent BMR results in the overestimation of predicted BMR and can potentially lead to incorrect conclusions concerning metabolic adaptation. Our analyses using a data set that included only BMR with n ≥ 3 were consistent with the conclusion that BMR does not differ between passerine and nonpasserine birds after taking phylogeny into account. With an increased focus on data mining and synthetic analyses, our study suggests that a thorough knowledge of how data sets are generated and the underlying constraints on their interpretation is a necessary prerequisite for such exercises.

Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review.

Comparative analyses of avian energetics often involve the implicit assumption that basal metabolic rate (BMR) is a fixed, taxon-specific trait. However, in most species that have been investigated, BMR exhibits phenotypic flexibility and can be reversibly adjusted over short time scales. Many non-migrants adjust BMR seasonally, with the winter BMR usually higher than the summer BMR. The data that are currently available do not, however, support the idea that the magnitude and direction of these adjustments varies consistently with body mass. Long-distance migrants often exhibit large intra-annual changes in BMR, reflecting the physiological adjustments associated with different stages of their migratory cycles. Phenotypic flexibility in BMR also represents an important component of short-term thermal acclimation under laboratory conditions, with captive birds increasing BMR when acclimated to low air temperatures and vice versa. The emerging view of avian BMR is of a highly flexible physiological trait that is continually adjusted in response to environmental factors such as temperature. The within-individual variation observed in avian BMR demands a critical re-examination of approaches used for comparisons across taxa. Several key questions concerning the shapes and other properties of avian BMR reaction norms urgently need to be addressed, and hypotheses concerning metabolic adaptation should explicitly account for phenotypic flexibility.

Phenotypic plasticity in the scaling of avian basal metabolic rate

Many birds exhibit short-term, reversible adjustments in basal metabolic rate (BMR), but the overall contribution of phenotypic plasticity to avian metabolic diversity remains unclear. The available BMR data include estimates from birds living in natural environments and captive-raised birds in more homogenous, artificial environments. All previous analyses of interspecific variation in BMR have pooled these data. We hypothesized that phenotypic plasticity is an important contributor to interspecific variation in avian BMR, and that captive-raised populations exhibit general differences in BMR compared to wild-caught populations. We tested this hypothesis by fitting general linear models to BMR data for 231 bird species, using the generalized least-squares approach to correct for phylogenetic relatedness when necessary. The scaling exponent relating BMR to body mass in captive-raised birds (0.670) was significantly shallower than in wild-caught birds (0.744). The differences in metabolic scaling between captive-raised and wild-caught birds persisted when migratory tendency and habitat aridity were controlled for. Our results reveal that phenotypic plasticity is a major contributor to avian interspecific metabolic variation. The finding that metabolic scaling in birds is partly determined by environmental factors provides further support for models that predict variation in scaling exponents, such as the allometric cascade model.

Phenotypic flexibility in the basal metabolic rate of laughing doves: responses to short-term thermal acclimation.

SUMMARY Many birds exhibit considerable phenotypic flexibility in maintenance energy requirements, and up- or downregulate basal metabolic rate (BMR) over time scales of days to weeks during thermal acclimation. However, the extent to which individual birds can reverse the direction of BMR adjustments over short time scales remains unknown. In this study, we examined metabolic responses to short-term thermal acclimation in laughing doves Streptopelia senegalensis. In 30 wild-caught doves (mean body mass=92.6 g) divided into three experimental groups of 10 birds each, initial BMR averaged 0.760±0.036 W. Thereafter, each group was acclimated to one of three acclimation air temperatures (Tacc=10, 22 or 35°C) for 21 days, during which time the doves were housed in individual cages. Following the first acclimation period (acclimation I), BMR (W) was significantly lower and was negatively and linearly related to Tacc [BMR=0.714-0.005Tacc]. Acclimation I BMR varied from 0.546±0.039 W in doves acclimated to Tacc=35°C to 0.665±0.058 W at Tacc=10°C. A second acclimation period of a further 21 days (acclimation II) revealed that the direction of BMR adjustments could be reversed within individuals, with acclimation II BMR again negatively and linearly related to Tacc. The slope of the relationship between BMR and Tacc following acclimation II was not significantly different to that following acclimation I. BMR exhibited consistent inter-individual variation, with a low but significant repeatability of 0.113. The within-individual BMR variation of up to 26% that we observed in laughing doves reveals that BMR is a highly flexible trait in this species, and reiterates the need to take phenotypic plasticity into account in comparative analyses of avian energetic parameters.

Thermoregulation and the energetic significance of clustering behavior in the white-backed mousebird (Colius colius).

Thermoregulation and the energetic significance of clustering behavior were assessed in the white‐backed mousebird Colius colius. Basal metabolic rate was 40% below the predicted allometric values. Rest‐phase body temperature (Tb) was highly labile and as low as 26°C. Rest‐phase Tb was not regulated with respect to a constant set point temperature, as occurs typically in endotherms. Rather, we observed periods of linear decreases in rest‐phase Tb at a rate dependent on ambient temperature (Ta) and the number of individuals in a cluster. The apparent inability of individual mousebirds to maintain rest‐phase homeothermy suggests that clustering behavior is obligatory in the defense of a rest‐phase set point Tb. The low rest‐phase body temperatures exhibited by single C. colius hence appear to represent a normothermic state rather than typical avian facultative hypothermia. The birds were able to make significant energy savings by means of clustering behavior. These energy savings were dependent on Ta and the number of birds in the cluster. At a Ta of 15°C, the mean energy expenditure of each bird in a cluster of six was 50% of that of a single bird. The metabolic traits of C. colius are likely be adaptive in the arid habitats that this species inhabits.

A New Comparative Metric for Estimating Heterothermy in Endotherms

A major focus in the study of endothermic thermoregulation has been the description of thermoregulatory patterns used by various species and/or populations. Compared with ectotherms, relatively few attempts have been made to study the thermoregulation of endotherms in an adaptive framework. We believe that one of the main factors limiting this area of research has been the lack of an appropriate metric to directly compare body temperature (Tb) variation across all endothermic species. Thus, we present a simple comparative metric, the heterothermy index (HI), to quantify the expression of heterothermy by endotherms during a given time frame. Key advantages of HI are that (1) it represents a new analytical technique that has different strengths than the metrics commonly used to describe variation in Tb, (2) it allows for evaluation of nonenergetic costs and benefits that affect the expression of heterothermy, and (3) it has the potential to unify research on homeotherms and heterotherms through quantitative comparative analyses that examine the entire continuum of thermoregulatory patterns. In short, we suggest that our metric provides a means to overcome one of the hurdles presently slowing the advancement of research on endothermic thermoregulation beyond the simple description of thermoregulatory patterns.

Partitioning of evaporative water loss in white-winged doves: plasticity in response to short-term thermal acclimation

SUMMARY We investigated changes in the relative contributions of respiratory evaporative water loss (REWL) and cutaneous evaporative water loss (CEWL) to total evaporative water loss (TEWL) in response to short-term thermal acclimation in western white-winged doves Zenaida asiatica mearnsii. We measured REWL, CEWL, oxygen consumption and carbon dioxide production in a partitioned chamber using flow-through respirometry. In doves housed for 2-4 weeks in a room heated to ca. 43°C during the day, TEWL increased from 5.5±1.3 mg g-1 h-1 at an air temperature (Ta) of 35°C to 19.3±2.5 mg g-1 h-1 at Ta=45°C. In doves housed at room temperature for the same period, TEWL increased from 4.6±1.1 mg g-1 h-1 at Ta=35°C to 16.1±4.6 mg g-1 h-1 at Ta=45°C. The CEWL of heat-acclimated doves increased from 3.6±1.2 mg g-1 h-1 (64% of TEWL) at 35°C to 15.0±2.1 mg g-1 h-1 (78% of TEWL) at Ta=45°C. Cool-acclimated doves exhibited more modest increases in CEWL, from 2.7±0.7 mg g-1 h-1 at Ta=35°C to 7.8±3.4 mg g-1 h-1 at Ta=45°C, with the contribution of CEWL to TEWL averaging 53% over this Ta range. Cool-acclimated doves became mildly hyperthermic (body temperature Tb=42.9±0.4°C) and expended 35% more energy relative to heat-acclimated doves (Tb=41.9±0.6°C) at Ta=45°C, even though TEWL in the two groups was similar. In each of the two groups, metabolic rate did not vary with Ta, and averaged 7.1±0.5 mW g-1 in cool-acclimated doves and 6.3±0.8 mW g-1 in heat-acclimated doves. The differences in TEWL partitioning we observed between the two experimental groups resulted from a consistently lower skin water vapour diffusion resistance (rv) in the heat-acclimated doves. At Ta=45°C, rv in the cool-acclimated doves was 120±81 s cm-1, whereas rv in the heat-acclimated doves was 38±8 s cm-1. Our data reveal that in Z. a. mearnsii, TEWL partitioning varies in response to short-term thermal acclimation.

Response of avian nectarivores to the flowering of Aloe marlothii: a nectar oasis during dry South African winters

In southern Africa, Aloe marlothii flowers during the dry winter season and offers copious dilute nectar to a variety of birds. Avian abundance and community composition were monitored at an A. marlothii forest at Suikerbosrand Nature Reserve, South Africa. Sampling occurred during two summer months (February–March) when no flowers were present, and six months (May–October) that spanned the winter flowering. We hypothesized that an influx of occasional nectarivores to the A. marlothii forest during flowering would lead to significant changes in the avian community. Overall bird abundance increased 2–3 fold at the peak of nectar availability (August). We recorded 38 bird species, of 83 species detected during transects, feeding on A. marlothii nectar; this diverse assemblage of birds belonged to 19 families, including Lybiidae, Coliidae, Pycnonotidae, Sylviidae, Cisticolidae, Muscicapidae, Sturnidae, Ploceidae and Fringillidae. Surprisingly, only two species of sunbird (Nectariniidae) were observed feeding on A. marlothii nectar, and both occurred in low abundance. We predicted that competition for nectar resources would be high, but few aggressive inter- and intra-specific interactions occurred between birds while feeding on inflorescences. During peak flowering, insect feeders (insectivores, omnivores, nectarivores) fed on nectar during the cold morning when insect activity was low, whilst non-insect feeders (frugivores and granivores) fed on nectar in the middle of the day. Our study highlights the importance of A. marlothii nectar as a seasonal food and water source for a diverse assemblage of occasional nectarivores.

The impact of humidity on evaporative cooling in small desert birds exposed to high air temperatures.

Environmental temperatures that exceed body temperature (Tb) force endothermic animals to rely solely on evaporative cooling to dissipate heat. However, evaporative heat dissipation can be drastically reduced by environmental humidity, imposing a thermoregulatory challenge. The goal of this study was to investigate the effects of humidity on the thermoregulation of desert birds and to compare the sensitivity of cutaneous and respiratory evaporation to reduced vapor density gradients. Rates of evaporative water loss, metabolic rate, and Tb were measured in birds exposed to humidities ranging from ∼2 to 30 g H2O m−3 (0%–100% relative humidity at 30°C) at air temperatures between 44° and 56°C. In sociable weavers, a species that dissipates heat primarily through panting, rates of evaporative water loss were inhibited by as much as 36% by high humidity at 48°C, and these birds showed a high degree of hyperthermia. At lower temperatures (40°–44°C), evaporative water loss was largely unaffected by humidity in this species. In Namaqua doves, which primarily use cutaneous evaporation, increasing humidity reduced rates of evaporative water loss, but overall rates of water loss were lower than those observed in sociable weavers. Our data suggest that cutaneous evaporation is more efficient than panting, requiring less water to maintain Tb at a given temperature, but panting appears less sensitive to humidity over the air temperature range investigated here.