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Torpor and metabolism in hummingbirds
Abstract
1.1 Body temperature and diurnal cycle of energy metabolism at different ambient temperatures (+2 to +25°C) were tested for 18 different hummingbird species from different biotopes and of different body-masses (2.7–17.5 g).2.2. The level of resting metabolism (night time) reaches 30–70% of activity metabolism values (day time). The mean is almost exactly 50%.3.3. The mean metabolism-weight regression line of the night time values follows the equation M = 0.67 × W0.73 (M = energy metabolism in kJ/hr, W = body weight in g). That of the day time values is M = 0.83 × W0.53.4.4. Resting metabolic rate of the hummingbirds is considerably higher than the theoretically expected value for nonpasserine birds, even when torpor values are taken into account.5.5. All species tested show torpor during night time, independent of ambient temperature, feeding situation or the environment (biotope) of the species.6.6. In comparison to the resting metabolic rate, metabolism during torpor decreases by 60–90% to a relatively constant level. This level is not (linearly) temperature-dependent (m = 0.008. r = 0.22), nevertheless many species show a minimum at ca 15–20°C.7.7. During torpor, body temperature normally reaches the level of the ambient temperature but never falls below 18–20°C. The normal values during the daytime range from 38 to 40°C and during night time from 35 to 37°C.
... Hummingbirds (family Trochilidae) are well suited for exploring when and why endotherms use torpor. Because of their small body sizes and use of hovering flight, hummingbirds have some of the highest surface-area-to-volume ratios (Krüger et al. 1982) and mass-specific metabolic rates of any vertebrate (Suarez 1992). Small body size coupled with dependence on nectar, a spatiotemporally variable food resource, places hummingbirds regularly at risk of energetic deficit (Schleucher 2004), and many species undergo torpor frequently (Hainsworth and Wolf 1970;Krüger et al. 1982;Shankar et al. 2020;Spence and Tingley 2021). ...
... Because of their small body sizes and use of hovering flight, hummingbirds have some of the highest surface-area-to-volume ratios (Krüger et al. 1982) and mass-specific metabolic rates of any vertebrate (Suarez 1992). Small body size coupled with dependence on nectar, a spatiotemporally variable food resource, places hummingbirds regularly at risk of energetic deficit (Schleucher 2004), and many species undergo torpor frequently (Hainsworth and Wolf 1970;Krüger et al. 1982;Shankar et al. 2020;Spence and Tingley 2021). Previous studies have found that torpor use results in substantial energetic savings for most species (Shankar et al. 2020). ...
... Current understanding of hummingbird torpor use, however, has focused on north-temperate migrants (e.g., Carpenter and Hixon 1988;Hiebert 1993;Spence and Tingley 2021) or tropical montane species (e.g., Wolf et al. 2020), which regularly face cold temperatures and/or the energetic costs of migration. The lowland Neotropics are a center of global hummingbird diversity (McGuire et al. 2014), but we know relatively less about torpor use in species that occur in these relatively warm (i.e., ≥207C) and stable thermal environments (but see Krüger et al. 1982;Bech et al. 1997;Shankar et al. 2020). High, stable air temperature (T a ) may reduce torpor efficiency because hummingbirds can drop T b only as low as the local minimum T a . ...
Torpor, the temporary reduction of metabolic rate and body temperature, is a common energy-saving strategy in endotherms. Because of their small body size and energetically demanding life histories, hummingbirds have proven useful for understanding when and why endotherms use torpor. Previous studies of torpor in hummingbirds have been largely limited to tropical montane species or long-distance migrants that regularly experience challenging thermal conditions. Comparatively little is known, however, about the use of torpor in hummingbirds of the lowland tropics, where relatively high and stable year-round temperatures may at least partially negate the need for torpor. To fill this knowledge gap, we tested for the occurrence of torpor in tropical lowland hummingbirds (n=37 individuals of six species) from central Panama. In controlled experimental conditions simulating the local temperature regime, all six species used torpor to varying degrees and entered torpor at high ambient temperatures (i.e., ≥28°C), indicating that hummingbirds from the thermally stable lowland tropics regularly use torpor. Torpor reduced overnight mass loss, with individuals that spent more time in torpor losing less body mass during temperature experiments. Body mass was the best predictor of torpor depth and duration among and within species-smaller species and individuals tended to use torpor more frequently and enter deeper torpor. Average mass loss in our experiments (∼8%-10%) was greater than that reported in studies of hummingbirds from higher elevation sites (∼4%). We therefore posit that the energetic benefits accrued from torpor may be limited by relatively high nighttime temperatures in the lowland tropics, although further studies are needed to test this hypothesis.
... Moreover, the use of torpor appears to be distributed along a continuum [18,25,26], and subtle modifications in the frequency of torpor and bout duration are crucial to birds' ability to save energy [15,27]. As a consequence, the use of torpor varies across species [15,[27][28][29], within species [19,25,27,30], and even within individuals (e.g. [28,31]). ...
... As a consequence, the use of torpor varies across species [15,[27][28][29], within species [19,25,27,30], and even within individuals (e.g. [28,31]). Broadly speaking, meta-analytic perspectives suggest that body mass explains some interspecific variation in how torpor is used across species [18,19,32], as does shared ancestry: in hummingbirds, some characteristics of torpor are similar among close relatives and show phylogenetic signal [15]. ...
Daily torpor allows endotherms to save energy during energetically stressful (e.g. cold) conditions. Although studies on avian torpor have mostly been conducted under laboratory conditions, information on the usage of torpor in the wild is limited to few, predominantly temperate-zone species. We studied torpor under seminatural conditions from 249 individuals from 29 hummingbird species across a 1920 m elevational gradient in the western Andes of Colombia using cloacal thermistors. Small birds were more likely to use torpor than large birds, but only at low ambient temperatures, where torpor was prolonged. We also found effects of proxy variables for body condition and energy expenditure on the use of torpor, its characteristics, and impacts. Our results suggest that context-dependency and phylogenetic variation in the probability of deploying torpor can help understand clade-wide patterns of elevational distribution in Andean hummingbirds.
... This body temperature is between 35 and 42˚C, which is 10-15˚C higher than the typical body temperature of ectothermic vertebrates [35]. We have therefore looked at ADAR1 and ADAR2 orthologs from five species-two mammals and two birds, and one ectotherm invertebrate, that inhabit different environmental niches: (1) Human (Homo sapiens), whose ADARs are commonly used in base editing research [32,36,37]; (2) Squid (Loligo opalescens), an ectotherm invertebrate living in diverse temperatures, which was shown to have extraordinarily high levels of A-to-I editing in coding sequences [38][39][40]; (3) The marine mammal, Orca whale (Orcinus orca), with core body temperature of~38˚C [41]; (4,5) Hummingbird (Calypte anna) and Mallard duck (Anas platyrhynchos), two birds with relatively high core body temperatures of~40˚C and~42˚C respectively, the warm end of the endothermic spectrum [42,43]. ...
The most abundant form of RNA editing in metazoa is the deamination of adenosines into inosines (A-to-I), catalyzed by ADAR enzymes. Inosines are read as guanosines by the translation machinery, and thus A-to-I may lead to protein recoding. The ability of ADARs to recode at the mRNA level makes them attractive therapeutic tools. Several approaches for Site-Directed RNA Editing (SDRE) are currently under development. A major challenge in this field is achieving high on-target editing efficiency, and thus it is of much interest to identify highly potent ADARs. To address this, we used the baker yeast Saccharomyces cerevisiae as an editing-naïve system. We exogenously expressed a range of heterologous ADARs and identified the hummingbird and primarily mallard-duck ADARs, which evolved at 40-42°C, as two exceptionally potent editors. ADARs bind to double-stranded RNA structures (dsRNAs), which in turn are temperature sensitive. Our results indicate that species evolved to live with higher core body temperatures have developed ADAR enzymes that target weaker dsRNA structures and would therefore be more effective than other ADARs. Further studies may use this approach to isolate additional ADARs with an editing profile of choice to meet specific requirements, thus broadening the applicability of SDRE.
... To cope with such nighttime energy limitations and challenges, hummingbirds can use heterothermy to decrease their nocturnal energy expenditure by reducing their metabolic rate and body temperature by varying amounts (Hainsworth et al., 1977;Krüger et al., 1982;Lasiewski, 1963;Shankar et al., 2020). In addition to deep torpor where they drop almost to air temperature, hummingbirds can also use shallow torpor, maintaining intermediate a body temperature and metabolism, to achieve moderate energy savings (Shankar et al., 2022). ...
Reproduction entails a trade-off between short-term energetic costs and long-term fitness benefits. This is especially apparent in small endotherms that exhibit high mass-specific metabolic rates and live in unpredictable environments. Many of these animals use torpor, substantially reducing their metabolic rate and often body temperature to cope with high energetic demands during non-foraging periods. In birds, when the incubating parent uses torpor, the lowered temperatures that thermally sensitive offspring experience could delay development or increase mortality risk. We used thermal imaging to noninvasively explore how nesting female hummingbirds sustain their own energy balance while effectively incubating their offspring. We located 67 active Allen's hummingbird (Selasphorus sasin) nests in Los Angeles, California and recorded nightly time-lapse thermal images at 14 of these nests for 108 nights using thermal cameras. We found that nesting females usually avoided entering torpor, with one bird entering deep torpor on two nights (2% of nights), and two other birds possibly using shallow torpor on three nights (3% of nights). We also modeled nightly energetic requirements of a bird experiencing nest temperatures vs. ambient temperature and using torpor or remaining normothermic, using data from similarly-sized broad-billed hummingbirds. Overall, we suggest that the warm environment of the nest, and possibly shallow torpor, help brooding female hummingbirds reduce their own energy requirements while prioritizing the energetic demands of their offspring.
... In this state several homeostatic mechanisms including internal energy regulation are ceased. Thereby birds are able to save a substantial amount of energy: an increase of 60% of the normal usage [32]. ...
Dynamical stabilization processes (homeostasis) are ubiquitous in nature, but the needed energetic resources for their existence have not been studied systematically. Here, we undertake such a study using the famous model of Kapitza’s pendulum, which has attracted attention in the context of classical and quantum control. This model is generalized and rendered autonomous, and we show that friction and stored energy stabilize the upper (normally unstable) state of the pendulum. The upper state can be rendered asymptotically stable, yet it does not cost any constant dissipation of energy, and only a transient energy dissipation is needed. Asymptotic stability under a single perturbation does not imply stability with respect to multiple perturbations. For a range of pendulum–controller interactions, there is also a regime where constant energy dissipation is needed for stabilization. Several mechanisms are studied for the decay of dynamically stabilized states.
... In this state several homeostatic mechanisms-including internal energy regulation-are ceased. Thereby birds are able to save a substantial amount of energy: up ≃ 60% of the normal usage [24]. ...
Homeostasis is an active, self-regulating process by which an unstable state is stabilized against external perturbations. Such processes are ubiquitous in nature, but energetic resources needed for their existence were not studied systematically. Here we undertake such a study using the mechanical model of inverted pendulum, where its upper (normally unstable) state is stabilized due to a fast controlling degree of freedom and due to friction. It is shown that the stabilization itself does not need constant dissipation of energy. There is only a transient dissipation of energy related to the relaxation to the stable state. The stabilization is achieved not due to a constant dissipation of energy, but due to the energy initially stored in the controlling degree of freedom. In particular, the stored energy is needed for ensuring stability against multiple perturbations, a notion of stability that differs from the usual asymptotic stability against a single perturbation.
... Although once commonly associated with mammals from seasonally cold climates to save energy, it is now apparent that many mammals and birds from subtropical and tropical latitudes also employ heterothermy on a regular basis (Genoud, 1993;Geiser and Brigham, 2012;Geiser, 2020;Reher and Dausmann, 2021). Among birds, members of Apodiformes and Caprimulgiformes readily enter torpor in response to energy or water shortages in the wild (Krüger et al., 1982;Smit et al., 2011;Brigham et al., 2012;Wolf et al., 2020). However, there is limited evidence that captive caprimulgids mirror the thermoregulatory patterns of their wild counterparts although birds in general appear less likely to employ heterothermy under captive conditions compared to mammals . ...
Free-ranging tawny frogmouths ( Podargus strigoides ) typically defend body temperature ( T b ) between 38 and 40°C during activity and allow it to fall to 29°C during cold evenings. However, this pattern of nightly T b decline has not been elicited in captivity during short-term respirometry measurements. We used implanted T b loggers to record the T b of two captive tawny frogmouths from 24 September to 24 December 2019 to determine if the conditions in captivity would elicit similar T b patterns to those measured in the wild. We recorded an average T b of 34.8 ± 1.1 and 35.6 ± 1.0°C for the two birds and minimum T b of 31.0 and 32.0°C. Minimum daily T b was correlated between the two individuals, and the minimum T b of both individuals was correlated with minimum daily T a . Our results highlight the need to keep birds under appropriate captive conditions to perform physiological research that produces results which mirror responses by individuals in the wild.
... If these trade-offs are similar in birds, it might be beneficial for birds that use the deepest possible form of torpor to sometimes use a shallower form, to allow moderate energy savings while minimizing some of the potential costs of deep torpor (Boyles et al., 2013). Yet, in contrast to mammals, bird species have been observed to use either shallow or deep torpor, but usually not both (Berger, 1984;Brigham et al., 2000;Hainsworth and Wolf, 1978;Hiebert, 1990;Kruger et al., 1982;McKechnie and Lovegrove, 2002;Ruf and Geiser, 2015). One mousebird species has been described to use both shallow and deep torpor when starved over several days, with their depth of torpor deepening as their energy stores were depleted (McKechnie and Lovegrove, 2000;Prinzinger et al., 1992). ...
Many endotherms use torpor, saving energy by a controlled reduction of their body temperature and metabolic rate. Some species (e.g., arctic ground squirrels, hummingbirds) enter deep torpor, dropping their body temperatures by 23-37°C, while others can only enter shallow torpor (e.g., pigeons, 3-10°C reductions). However, deep torpor in mammals can increase predation risk (unless animals are in burrows or caves), inhibit immune function, and result in sleep deprivation, so even for species that can enter deep torpor, facultative shallow torpor might help balance energy savings with these potential costs. Deep torpor occurs in three avian orders, but the trade-offs of deep torpor in birds are unknown. Although the literature hints that some bird species (mousebirds and perhaps hummingbirds) can use both shallow and deep torpor, little empirical evidence of such an avian heterothermy spectrum within species exists. We infrared imaged three hummingbird species that are known to use deep torpor, under natural temperature and light cycles, to test if they were also capable of shallow torpor. All three species used both deep and shallow torpor, often on the same night. Depending on the species, they used shallow torpor for 5-35% of the night. The presence of a heterothermic spectrum in these bird species indicates a capacity for fine-scale physiological and genetic regulation of avian torpid metabolism.
Thermal physiological research in Germany over the past 70 years has endeavoured to “illuminate” normal homoeothermic temperature regulation—and fever, hyperthermia, and hypothermia as abnormal states—“at all levels of biological organisation”. The topics of this research have ranged from humans and whole animal models to their organismic, cellular, and molecular levels. The approaches of comparative and behavioural physiology have been used extensively to elucidate the principles underlying the functional cytoarchitecture of central nervous control of body temperature. Studies of the ontogeny of homoeothermic temperature regulation have assisted in clarifying the principles of temperature regulation as a hierarchically organised system of multiple sensors, controllers, and effectors. The inherent redundancy of the system accounts for the high degree of stability of homoeothermic temperature regulation in the face of disturbances of thermal homoeostasis in conditions in which competing demands are imposed on its effectors by nervous and endocrine control of non-thermoregulatory systems essential for body homoeostasis. Perhaps a suitable summary of thermoregulatory research in Germany might be a slight modification of the name of one of the sections, which we often cite, of the American Journal of Physiology, viz., Regulatory, Integrative and Comparative Physiology of Temperature Regulation!
Trait databases have become important resources for large-scale comparative studies in ecology and evolution. Here we introduce the AnimalTraits database, a curated database of body mass, metabolic rate and brain size, in standardised units, for terrestrial animals. The database has broad taxonomic breadth, including tetrapods, arthropods, molluscs and annelids from almost 2000 species and 1000 genera. All data recorded in the database are sourced from their original empirical publication, and the original metrics and measurements are included with each record. This allows for subsequent data transformations as required. We have included rich metadata to allow users to filter the dataset. The additional R scripts we provide will assist researchers with aggregating standardised observations into species-level trait values. Our goals are to provide this resource without restrictions, to keep the AnimalTraits database current, and to grow the number of relevant traits in the future.
Rates of O₂ consumption () and respiratory parameters, breathing rate (), tidal volume (), and respiratory minute volume (), were measured for poorwills and hummingbirds during torpor cycles. The of euthermic poorwills and hummingbirds at an ambient temperature of 20 C were 1.06 ± 0.16 and 0.817 ± 0.04 ml g⁻¹ h⁻¹, respectively, with of 30.0 ± 3.5 and 45.7 ± 3.1 ml air min⁻¹. Oxygen extraction of euthermic poorwills and hummingbirds was 4.0% and 1.8%, respectively. During torpor cycles, of poorwills and hummingbirds decreased to <0.05 and 0.053 ± 0.007 ml O₂ g⁻¹ h⁻¹, respectively, with of <2.8 and 1.98 ± 0.46 ml air min⁻¹. Oxygen extraction of torpid poorwills and hummingbirds was 3% and 2.9%, respectively. The and showed a considerable hysteresis during entry into and arousal from torpor, but and were strongly correlated, except at the terminal stages of entry into torpor and the initial stages of arousal. Mass specific thermal conductance was greater during entry into torpor than for euthermic, cold-stressed poorwills, thus facilitating heat loss; and conductance was less during arousal, facilitating heat retention. The increase in conductance during entry into torpor probably reflects altered ptilo-erection and peripheral blood-flow patterns, whereas the diminished conductance during arousal most probably indicates additional insulative value of the colder extremities and abdomen.
1.1. Body temperature (Tb) and metabolism (M) of red-backed mousebirds (Colius castanotus) fed ad libitum are in the same range as reported for other bird species of similar size (69 g).2.2. The interrelation between M (J/g-hr) and ambient temperature (Ta) can be described by the formula M = 78.7− 1.63 Ta. The thermal conductance varies from 2.1 to 2.5 J/g·hr·°C (predicted value 2.44).3.3. Sub-maintenance feeding leads to a gradual decrease of Tb and M following the loss of body mass (b.m.). The corresponding regression lines are: Tb = −12.7 + 0.83 b.m. and M = −98.1 + 2.4 b.m. respectively. The thermal conductance decreased to more favourable values between 1.9 and 2.1 J/g-hr-°C due to a smaller difference of Tb − Ta.4.4. The relation between Tb and M (Q10) was determined as 2.04–2.77 indicating that the decline in M closely follows physico-chemical conditions.5.5. After a long period of food deprivation and a loss of body mass of about 35%, the birds enter a state of torpidity. M of torpid birds may fall to less than 1/3 (on average) of basal levels depending on the actual Tb reached after cooling. Tb approximates Ta with a critical level of about 18°C, below which no spontaneous arousal is possible and the birds fall in uncontrolled hypothermia.
Der Umsatz nchterner, im Dunkeln sitzender Vgel hat einen ausgeprgten Tagesgang; die Sauerstoffaufnahme liegt in der Aktivittszeit () rund 25% hher als in der Ruhezeit (). Eine Aufarbeitung der in der Literatur mitgeteilten Meergebnisse zeigt, da es, zumindest bei Vgeln, mglich und sinnvoll ist, fr die Abhngigkeit des Umsatzes vom Krpergewicht zwei nach - und -Werten getrennte Regressionsgeraden zu berechnen. Es bleibt eine Frage der bereinkunft, ob man im Hinblick auf die Streuungsunterschiede zwischen - und -Werten und im Wunsch nach Minimal-Werten knftig zur Angabe des wahren Ruheumsatzes (Grundumsatzes) nur solche Werte zult, die in gemessen sind.The metabolism of starving birds sitting motionless in the dark, has a profound diurnal rhythm; oxygen uptake during activity-time () is about 25 percent higher than during rest-time () (Fig. 1). A re-examination of data published in the literature, together with our results, reveals that the well known allometric equation expressing the relationship between metabolic rate and body weight should be computed separately for - and for -values. At least in birds, the typical regression line will than be replaced by two parallel lines (Fig. 2). It remains a matter of agreement whether only -values will be accepted as representing the basal or true resting metabolism.
4 species of European white-toothed shrews enter torpor with extremely low metabolic rate. Newborn shrews (Crocidura russula) react as homeotherms during their first week before they develop the ability of torpor.