Torpor In Birds Research Articles

Daily Torpor in Birds and Mammals: Past, Present, and Future of the Field.

Torpor is an incredibly efficient energy-saving strategy that many endothermic birds and mammals use to save energy, by lowering their metabolic rates, heart rates, and typically body temperatures. Over the last few decades, the study of daily torpor-in which torpor is used for less than 24 hours per bout-has advanced rapidly. The papers in this issue cover the ecological and evolutionary drivers of torpor, as well as some of the mechanisms governing torpor use. We identified broad focus areas that need special attention: clearly defining the various parameters that indicate torpor use and identifying the genetic and neurological mechanisms regulating torpor. Recent studies on daily torpor and heterothermy, including the ones in this issue, have furthered the field immensely. We look forward to a period of immense growth in this field.

A heterothermic spectrum in hummingbirds.

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 temperature by 23-37°C, while others can only enter shallow torpor (e.g. pigeons, 3-10°C reduction). 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 whether 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.

Frequent nocturnal torpor in a free-ranging Australian honeyeater, the noisy miner.

Torpor in birds is considered to be far less common than in mammals. This is particularly true for passerine birds for which knowledge of torpor expression is scarce, although almost all are small, have high energy expenditure and could profit energetically from using torpor. To assess whether the extent and diversity of avian and especially passerine torpor expression and heterothermy may be currently underestimated because of limited long-term data on free-ranging birds, core body temperature fluctuations were quantified over ~ 4.3months in a medium-sized honeyeater, the noisy miner (Manorina melanocephala, ~ 75g), in an open woodland during the cold season in eastern Australia. Miners used shallow nocturnal torpor frequently (63% of days), torpor bouts lasted on average for 6.5h (maximum 13.5h) and, unlike during hypothermia, torpor was terminated by endogenous heat production for rewarming. Body temperatures (Tb) ranged from a maximum of 43.5°C to a minimum of 33.0°C, often fell by 7°C at night, and the overall mean Tb was 38.7 ± 0.7°C. The data show that yet another passerine bird, widely viewed to be homeothermic, expresses torpor in the wild for energy conservation. Considering the size of miners, it seems probable that many other, especially smaller birds, use a similar approach at least in winter to enhance the chance of survival in the face of high energy expenditure and low food availability.

Torpor in Birds: Taxonomy, Energetics, and Ecology

Recent reports on patterns and occurrence of torpor and other natural hypothermic states in birds have prompted a revision of many longstanding opinions. For instance, a larger assortment of birds covering a wider range of body mass than previously recognized uses energy-conserving mechanisms in the face of abundant food supplies. Thus, although acute energetic stress triggers the occurrence of hypometabolic states in many birds, energy deficits can no longer be regarded as the sole stimulus for avian torpor. Additionally, the phenology of this phenomenon (phases, duration, depth) shows more interspecific variation than previously appreciated, and traditional concepts of the phases of torpor are not always adequate. Hence, inclusive definitions of torpor based on physiological and/or behavioral criteria have become more difficult to formulate. However, average nighttime body temperature, which is highly consistent throughout the class Aves (38.54 degrees +/- 0.96 degrees C, n = 202), provides a convenient reference for detecting natural hypothermic states. Of the putative ecological factors associated with avian torpor, food specialization seems a prime candidate as an ultimate factor in the occurrence of this state in birds. With few exceptions, all of these animals capable of torpor are either frugivorous, nectarivorous, or insectivorous, suggesting a correlation between thermoregulatory pattern and predictability of food supply. To date, no clear answer exists as to whether the variety of thermoregulatory patterns evident in birds involves discrete mechanisms or merely steps in a physiological continuum. However, I suggest that the occurrence of differences in torpor patterns among closely related species (e.g., within families) favors the latter interpretation.

Evolution of daily torpor and hibernation in birds and mammals: importance of body size.

1. The evolution of hibernation and daily torpor in mammals and birds remains a controversial subject. The original view was that use of torpor reflects a primitive thermoregulation, as it occurs in ancestral groups of mammals. 2. This view is no longer widely supported. However, the interpretation of a polyphyletic derivation of torpor also has been challenged because of the astonishing similarity of torpor patterns among various orders and even the two classes. 3. A recent argument is that mutations required for torpor and hibernation are unlikely to occur simultaneously and that torpor must be plesiomorphic (ancestral), although it is not functionally primitive. Homeothermy is interpreted as a loss of the ability to enter torpor in those groups that could survive without the requirement of heterothermic periods for energy conservation. 4. Interestingly, while torpor in mammals occurs in the phylogenetically old groups, lending support to the hypothesis of an ancestral derivation of torpor, the opposite is the case for birds. Modern bird groups and ancestral mammal groups contain mainly small species that often rely on fluctuating food supply, whereas modern mammalian orders and ancient bird orders contain the largest species with low energy requirements for maintenance and thermoregulation. 5. It is, therefore, possible that not phylogenetic position but size and diet determine the occurrence of heterothermy. Moreover, because endothermy and torpor in birds has apparently evolved separately from that in mammals and because it is possible that daily torpor and hibernation represent two distinct torpor patterns that evolved separately, a convergent evolution of torpor in endotherms cannot be excluded.

Hibernation and Daily Torpor in Marsupials - a Review

Most heterothermic marsupials appear to display one of the two patterns of torpor that have been described in placental mammals. During shallow, daily torpor body temperature (T(b)) falls for several hours from about 35-degrees-C to values between 11 and 28-degrees-C, depending on the species, and metabolic rates fall to about 10-60% of the basal metabolic rate (BMR). In contrast during deep and prolonged torpor (hibernation), T(b) falls to about 1-5-degrees-C, metabolic rates to about 2-6% of BMR and torpor bouts last for 5-23 days. Shallow, daily torpor has been observed in the opossums (Didelphidae), the carnivorous marsupials (Dasyuridae) and the small possums (Petauridae). Daily torpor may also occur in the numbat (Myrmecobiidae) and the marsupial mole (Notoryctidae). Deep and prolonged torpor (hibernation) has been observed in the pygmy possums (Burramyidae), feathertail glider (Acrobatidae) and Dromiciops australis (Microbiotheriidae). The patterns of torpor in marsupials are paralleled by those of monotremes, placentals and even birds. These similarities in torpor patterns provide some support to the hypothesis that torpor may be plesiomorphic. However, as endothermy and torpor in birds apparently has evolved separately from that in mammals and as torpor occurrence in mammals can change within only a few generations it appears more likely that torpor in endotherms is convergent.