Does the New Zealand rockwren (Xenicus gilviventris) hibernate?

In this study, we examined the thermal physiology of the endangered New Zealand rockwren (Xenicus gilviventris), a member of the Acanthisittidae, a family unique to New Zealand. This family, derived from Gondwana, is thought to be the sister taxon to all other passerines. Rockwrens permanently reside above the climatic timberline at altitudes from 1000 to 2900 m in the mountains of South Island. They feed on invertebrates and in winter face ambient temperatures far below freezing and deep deposits of snow. Their body temperature and rate of metabolism are highly variable. The rockwrens in our study regulated their body temperature at ca. 36.4°C, which in one individual decreased to 33.1°C at an ambient temperature of 9.4°C; its rate of metabolism decreased by 30% and its body temperature then spontaneously returned to 36°C. The rate of metabolism in a second individual twice decreased by 35%, nearly to the basal rate expected from its mass without a decrease in body temperature. The New Zealand rockwren's food habits, entrance into torpor and continuous residence in a thermally demanding environment suggest that it may hibernate. However, for that conclusion to be accepted, evidence of its use of torpor for extended periods is required. Acanthisittids are distinguished from other passerines by the combination of their permanent temperate distribution, thermal flexibility and a propensity to evolve a flightless condition. These characteristics may principally reflect their geographical isolation in a temperate environment isolated from Gondwana for 82 million years in the absence of mammalian predators.

What determines the basal rate of metabolism?

The basal rate of metabolism (BMR) is the most reported estimate of energy expenditure in endotherms. Its principal determinant is body mass, but BMR also correlates with a variety of behavioral and ecological factors that do not determine basal rate: they are byproducts of the mechanisms that are its determinate. In mammals, mass-independent BMR increases when muscle mass is >40% of total body mass and BMR is then ≥100% of the value expected from body mass. Mammals with muscle masses <30% of body mass have lower BMRs, a diminished capacity to regulate body temperature and often have reduced activity levels. At muscle masses <42% of body mass, birds have body temperatures and basal rates higher than mammals with the same muscle mass. Their high basal rates derive from fast blood flow and increased mitochondrial density in their pectoral muscles. These enhancements also occur in the flight muscles of bats. Oxygen transport to the pectoral muscles of birds is facilitated by an increase in heart mass and hematocrit. This arrangement avoids transporting a large muscle mass to fuel flight, thereby reducing the cost of flight. Pectoral muscle masses <9% of body mass correlate with a flightless condition in kiwis, rails and ducks but some fruit pigeons have BMRs as low as those measured in kiwis, while remaining volant. The mass-independent BMRs of endotherms principally reflect changes of muscle activity and mass. An increase in muscle mass may have contributed to the evolution of endothermy.

The energetics of torpor in a temperate passerine endemic to New Zealand, the Rifleman (Acanthisitta chloris).

Compared to other birds, passerines, reflecting their small mass, have a narrow set of behavioral characteristics. One difference is that few enter torpor, especially in temperate environments. The few that do include swallows, none of which live throughout the year in cold-temperate environments, because their food, flying insects, is not available in winter and no passerine is known to hibernate. They seasonally migrate to warm-temperate and tropical environments. We present data on the energetics of the Rifleman (Acanthisitta chloris), a small, insectivorous member of the Acanthisittidae, a passerine family endemic to temperate New Zealand. This family is considered to be the sister taxon to all living passerines, which raises the question whether its physiological and behavioral characteristics reflect its evolutionary status in a manner that distinguishes it from other passerines. Only two of the eight known species in this family survive; four of the extinct species were flightless, a condition that evolved independently three times and is almost absent from other passerines. The Rifleman readily enters torpor, which is facilitated by its small mass. It enters torpor at ambient temperatures that are commonly encountered in its wet, cool-to-cold environment. As a result, its body temperature and rate of metabolism are highly variable. An estimate of the basal rate of metabolism is similar to that expected from body mass. Unlike some  torpor-prone birds, the Rifleman is a permanent resident in a temperate environment. This residency is possible, because the Rifleman gleans insect prey from surfaces, which does not require insects to have high body temperatures for activity. Its only living relative, the endangered, insectivorous Rock Wren (Xenicus gilviventris), is a permanent resident at altitudes from ca. 1000 to 2500 m in the mountains of South Island, New Zealand. There it faces severe winter conditions that are not avoided by descent to lower altitudes. Its response to these conditions may be an extended period of torpor. The repeated evolution of a flightless condition possibly reflects some distinctive property of the acanthisittids. The evolution of torpor and a flightless condition in acanthisittids may have facilitated their survival on a geographically isolated, temperate landmass, and these character states permitted by the absence of endemic mammalian predators.

The behavioral energetics of New Zealand's bats: Daily torpor and hibernation, a continuum.

We examine the impact of behavior on the short-term energy expenditures of the only terrestrial mammals endemic to New Zealand, two bats, the long-tailed (Chalinolobus tuberculatus, family Vespertilionidae), and the lesser short-tailed (Mystacina tuberculata, family Mystacinidae). Vespertilionidae has a world-wide distribution. Mystacinidae is restricted to New Zealand, although related to five neotropical families and one in Madagascar reflecting a shared Gondwanan origin of their Noctilionoidea superfamily. Both species have highly variable body temperatures and rates of metabolism. They feed on flying insects, which requires them to be torpid in shelters during cold, wet periods. In dry weather Mystacina is active in winter at ambient temperatures as low as -1.0 °C, foraging for terrestrial invertebrates in leaf litter, even in the presence of snow, and consuming fruit, nectar, and pollen from endemic plants that bloom in winter. The behavior of Mystacina expands its presence in a cool, wet, temperate forest in a manner unlike any other bat, another example of the distinctive characteristics of the endemic New Zealand fauna. The use of torpor generally depends on a series of factors, including body mass, ambient temperature, latitude, reproductive cycle, sociality, and fat deposits. These factors result in a diversity of responses that range along a continuum from short-term torpor to hibernation.

The difficulty with correlations: Energy expenditure and brain mass in bats.

Brain mass has been suggested to determine a mammal's energy expenditure. This potential dependence is examined in 48 species of bats. A correlation between characters may be direct or derived from shared correlations with intervening factors without a direct interaction. Basal rate of metabolism in these bats increases with brain mass: large brains are more expensive than small brains, and both brain mass and basal rate increase with body mass. Basal rate and brain mass also correlate with food habits in bats. Mass-independent basal rate weakly correlates with mass-independent brain mass, the correlation only accounting for 12% of the variation in basal rate, which disappears when the combined effects of body mass and food habits are deleted. The correlation between basal rate and brain mass seen in this and other studies usually accounts for <10% of the variation in basal rate and often <4%, even when statistically significant, a minimalist explanation for the level the basal rate. This correlation probably reflects the intermediacy of secondary factors, as occurred with food habits in bats. Most biological correlations are complicated and must be examined in detail before assurance can be given as to their bases.

Avian energetics: The passerine/non-passerine dichotomy.

Whether passerines collectively have a higher mean mass-independent basal rate of metabolism than the mean of other birds has been controversial. The conclusion that no difference exists was based on phylogenetic analyses. Higher basal rates, however, have been repeatedly seen in passerines and demonstrated by ANCOVA analyses. Several studies indicated that the mean mass-independent basal rate of passerines is >30% higher than the collective mean of other birds. Yet, at least three non-passerine orders of 25 have mean mass-independent basal rates equal to that of passerines. They are Anseriformes, Charadriiformes, and Procellariiformes, all characterized by an active lifestyle, including migratory and pelagic habits. In contrast, sedentary ducks endemic to islands have low basal rates. The high basal rates in temperate passerines correlate with migratory habits and life in cool to cold environments, the absence of these factors being partly responsible for the lower basal rates in most tropical passerines. The principal difference in energetics among non-passerines, between passerines and most non-passerines, and among passerines reflects the frequency of habits associated with high or low mass-independent energy expenditures, the habits correlating with body composition. The mean mass-independent basal rate in tropical passerines is slightly lower than in temperate passerines which implies that the collective mean in passerines would be somewhat lower if tropical passerines were included in proportion to their diversity. However, their inclusion will not eliminate the difference presently seen between passerines and other birds because the difference between tropical and temperate passerines is less than that between passerines and other birds.

Geographic and temporal correlations of mammalian size reconsidered: a resource rule.

The tendency of mammals to increase or decrease body size with respect to geography or time depends on the abundance, availability, and size of resources. This dependency accounts for a change in mass with respect to geography, including latitude (Bergmann's rule), a desert existence, and life on oceanic islands (the island rule), as well as in a seasonal anticipation of winter (Dehnel's phenomenon) and a tendency for some lineages to increase in mass through time (Cope's rule). Such a generalized pattern could be called the "resource rule," reflecting the controlling effect of resource availability on body mass and energy expenditure. The correlation of mammalian size with geography and time reflects the impact of temperature, rainfall, and season on primary production, as well as the necessity in the case of some species to share resources with competitors. The inability of the constituent "rules" to account for all size trends often results from unique patterns of resource availability.

Resources and energetics determined dinosaur maximal size.

Some dinosaurs reached masses that were approximately 8 times those of the largest, ecologically equivalent terrestrial mammals. The factors most responsible for setting the maximal body size of vertebrates are resource quality and quantity, as modified by the mobility of the consumer, and the vertebrate's rate of energy expenditure. If the food intake of the largest herbivorous mammals defines the maximal rate at which plant resources can be consumed in terrestrial environments and if that limit applied to dinosaurs, then the large size of sauropods occurred because they expended energy in the field at rates extrapolated from those of varanid lizards, which are approximately 22% of the rates in mammals and 3.6 times the rates of other lizards of equal size. Of 2 species having the same energy income, the species that uses the most energy for mass-independent maintenance of necessity has a smaller size. The larger mass found in some marine mammals reflects a greater resource abundance in marine environments. The presumptively low energy expenditures of dinosaurs potentially permitted Mesozoic communities to support dinosaur biomasses that were up to 5 times those found in mammalian herbivores in Africa today. The maximal size of predatory theropods was approximately 8 tons, which if it reflected the maximal capacity to consume vertebrates in terrestrial environments, corresponds in predatory mammals to a maximal mass less than a ton, which is what is observed. Some coelurosaurs may have evolved endothermy in association with the evolution of feathered insulation and a small mass.

Seasonal energetics of northern phocid seals.

The metabolic rate of harp (Pagophilus groenlandicus), harbor (Phoca vitulina), and ringed seals (Pusa hispida) was measured at various temperatures in air and water to estimate basal metabolic rates (BMRs) in these species. The basal rate and body composition of three harp seals were also measured throughout the year to examine the extent to which they vary seasonally. Marine mammalian carnivores generally have BMRs that are over three times the rates expected from body mass in mammals generally, both as a response to a cold-water distribution and to carnivorous food habits with the basal rates of terrestrial carnivores averaging about 1.8 times the mean of mammals. Phocid seals, however, have basal rates of metabolism that are 30% lower than other marine carnivores. Captive seals undergo profound changes in body mass and food consumption throughout the year, and after accounting for changes in body mass, the lowest rate of food intake occurs in summer. Contrary to earlier observations, harp seals also have lower basal rates during summer than during winter, but the variation in BMR, relative to mass expectations, was not associated with changes in the size of fat deposits. The summer reduction in energy expenditure and food consumption correlated with a reduction in BMR. That is, changes in BMR account for a significant portion of the seasonal variation in energy expenditure in the harp seal. Changes in body mass of harp seals throughout the year were due not only to changes in the size of body fat deposits, but also to changes in lean body mass. These results suggest that bioenergetics models used to predict prey consumption by seals should include time-variant energy requirements.

Flightless rails endemic to islands have lower energy expenditures and clutch sizes than flighted rails on islands and continents.

Data are presented on the standard energetics of six flighted and five flightless species of rails (Aves: Rallidae). The factors influencing these data and those from three additional species available from the literature, one of which was flightless, are examined. Basal rate of metabolism correlates with body mass, residency on islands or continents, volant condition, pectoral muscle mass, and food habits, but not with climate. The greatest capacity (96.2%) to account for the variation in basal rate of metabolism in 15 populations that belong to the 14 species occurs when body mass, volant condition, and food habits are combined. Then flighted species have basal rates that average 1.38 times those of flightless species and herbivorous rails have basal rates that are 1.37 times those of omnivorous species, which means that, independent of body mass, flighted gallinules have basal rates that are 1.9 times those of flightless, omnivorous rails. Distribution, pectoral muscle mass, and flight ability cannot be combined in the same analysis because they code for similar information. The evolution of a flightless condition in rails requires the absence of eutherian predators, but has occurred in the presence of marsupial predators. Each of the six studied flightless rails independently evolved a flightless condition and a low basal rate, whereas the evolution of herbivory and an associated high basal rate evolved at least twice in these species. Flightless rails on islands have clutch sizes that are only about one-half those of flighted rails living on continents, the reduction in clutch size correlating with a reduction in basal rate of metabolism. Thermal conductance in rails is correlated with body mass and food habits: herbivorous rails had conductances that were 1.43 times those of omnivores, i.e., conductances are highest in species with the highest basal rates.

The relationship among flow rate, chamber volume and calculated rate of metabolism in vertebrate respirometry.

A relationship exists among the calculated rate of metabolism of an animal enclosed in a chamber, chamber volume and air flow rate. A "critical" flow rate, defined as the minimal flow rate that produces a complete mixture of chamber gases, characterizes each chamber/animal combination. At flow rates below the critical flow rate, calculated rates of metabolism decrease with flow rate and approach zero as flow rate approaches zero. These calculated rates are unreliable estimates of rate of metabolism. At flow rates greater than the critical flow rate, calculated rates of metabolism are independent of flow rate because a reciprocal relationship exists between flow rate and the differential in oxygen content found between the air entering and exiting the chamber; they represent an accurate estimate of the animal's rate of metabolism under the conditions to which the animal is exposed. The critical flow rate increases with chamber volume, the animal's rate of metabolism and with any factor that increases rate of metabolism, including body mass, activity and in endotherms ambient temperatures below thermoneutrality, although chamber volume is its single most important determinant. Some evasions of the critical flow rate are discussed.

The energetics of reproduction in endotherms and its implication for their conservation.

The energy expenditure of endotherms, through its impact on the rate of reproduction, affects their ability to withstand competition, to tolerate environmental disturbances, and to endure predation. The fecundity of eutherian mammals increases with rate of metabolism because the post-natal growth rate increases and the gestation and conception-to-weaning periods decrease with a mass-independent increase in basal rate of metabolism. These correlations account for the observation that species that have large population fluctuations have high rates of metabolism and reproduction. Species with high rates of metabolism out-compete species with low rates when using resources that permit consumers to have high rates of metabolism, which explains why eutherian carnivores replace marsupial carnivores, none of which have high basal rates as a result of their form of reproduction. Fecundity in birds also appears to correlate with energy expenditure, which may account for the huge die-off of birds endemic to oceanic islands after the invasion of humans: island endemics, many of which have low rates of metabolism, are unable to increase fecundity in response to a human-based increase in mortality. The long-term protection for endotherms characterized by low rates of energy expenditure requires their isolation from high levels of predation and competition, conditions that are likely to occur only on islands free from eutherian predators and with low species diversity. Such endotherms may survive on continents if they are ecologically isolated from the general fauna.

Food habits and the evolution of energetics in birds of paradise (Paradisaeidae).

Basal rates of metabolism, minimal thermal conductances, and body temperatures are reported for 13 species of birds of paradise that belong to nine genera. Body mass alone accounts for 91.7% of the variation in their basal rates. Basal rate in this family also correlates with food habits and the altitudinal limits to distribution. Species that feed almost exclusively on fruit have basal rates that average 79.4% of species in which >10% of the diet is insects, and species restricted to altitudes <1,000 m have basal rates that are 90.6% of those found at higher altitudes. The combination of body mass, food habits, and altitudinal distribution accounts for 99.0% of the variation in basal rate in the species studied. The application of food habits to a cladogram of the studied Paradisaeidae implies that frugivory and low basal rate were plesiomorphic in this family. The evolution of omnivory, defined as including >10% of the diet as insects, appears to have occurred at least twice, and in each case was associated with an increase in basal rate of metabolism. Basal rate increased at least thrice with a movement into the highlands. Basal rate, however, does not correlate with plumage dimorphism or with reproductive behavior. The basal rates of metabolism in manakins and birds of paradise, i.e., passerine frugivores, are greater than those found in nonpasserine frugivores. Thermal conductance correlates with body mass, which accounts for 85.8% of its variation in this family. Body temperature in paradisaeids, the mean of which was 40.2 degrees C, may correlate with basal rate of metabolism.

Intraspecific allometry of standard metabolic rate in green iguanas, Iguana iguana.

To study the allometric relationship between standard metabolic rate and body mass (mass range 16-3627 g) in green iguanas, Iguana iguana (n=32), we measured rates of oxygen consumption (V(O(2))) at 30 degrees C during scotophase. The relationship could be described as: V(O(2))(ml h(-1))=0.478W(0.734). The resulting mass exponent was similar to the 3/4 power commonly used in interspecific curves (P>0.05), but differed from a proposed intraspecific value of 2/3 (P<0.05). The mass exponents of male (n=8) and female (n=11) iguanas did not differ (P>0.05). The mass adjusted V(O(2)) was higher than predicted from generalized squamate curves. The mean mass exponent of intra-individual allometric equations of iguanas (n=7) at varying masses during ontogeny did not differ from that of the pooled equation, indicating that scaling of V(O(2)) is similar for both between and within individuals. Thermal acclimation, compensatory changes in V(O(2)) with prolonged exposure to a constant temperature, was not observed in juvenile iguanas (n=11) between 1 and 5 weeks of acclimation at 30 degrees C.

The energetics of New Zealand's ducks.

Measurements on rates of metabolism and temperature regulation are presented from nine populations of seven species of ducks resident in New Zealand. An analysis of these data and those from 18 additional species obtained from the literature indicates that basal rate of metabolism in anatids correlates with body mass and restriction to the Australian-New Zealand region: these 'southern' species have basal rates that average 70% of those from the Northern Hemisphere. The low basal rates of southern anatids may reflect reduced pectoral muscle masses in association with the absence of migratory habits and/or life on land masses without eutherian predators. New Zealand flightless teal (Anas aucklandica nesiotis, Anas aucklandica aucklandica) do not have mass-independent basal rates that differ from those found in flighted ducks living in the same region, although flightless teal have lower total basal rates than most ducks as a result of small masses. Minimal thermal conductance in this sample is determined by body mass alone. Regulated body temperature is negatively correlated with body mass.

Standard energetics of phyllostomid bats: the inadequacies of phylogenetic-contrast analyses.

The basal rates of metabolism (BMR) of bats belonging to the family Phyllostomidae are re-examined after an earlier correlation with food habits was rejected because it did not take phylogeny into consideration. This rejection was based on an erroneous attribution of food habits and on an analytical method, phylogenetic contrasts, that ignores interactions that occur among character states and preferentially attributes responsibility for character states to phylogeny. The re-examination made here was based on analysis of covariance, which makes no a priori assumptions on the relative impact of factors that influence character states and permits factor interactions to be identified. A resulting model, based on variation in body mass, food habits, occurrence with respect to elevation, and residence on islands or continents, accounts for 99.4% of the variation in the BMR of 30 species of phyllostomids. Basal rate is also correlated with subfamily, but only if food habits are excluded because they are correlated with subfamily affiliation, as is residence on islands and continents, two examples of factor interaction. The preference to assign the effects of food habits and island residence on basal rate to subfamily affiliation (and phylogeny) is not justified. The concept that quantitative physiological characters can be transmitted via phylogeny without regard to the habits of animals and the characteristics of their environments cannot be defended. Phylogeny is the historical context in which the evolution of character states occurs, not the 'cause' of their evolution.

Food habits and the basal rate of metabolism in birds.

The correlation of basal rate of metabolism with various factors is examined in birds. Chief among these is body mass. As in mammals, much of the remaining variation in basal rate among birds is associated with food habits. Birds other than passerines that feed on grass, nectar, flying insects, or vertebrates generally have basal rates that are similar to mammals of the same mass and food habits. In contrast, most invertebrate-eating birds that weigh over 100 g have higher basal rates than equally-sized, invertebrate-eating mammals. The high basal rates of small passerines equal those of small mammals that do not enter torpor and represent the minimal cost of continuous endothermy. Large passerines and small procellariiforms, charadriiforms, and psittaciforms generally have higher basal rates than mammals with the same mass and food habits. The high basal rates of passerines (in combination with altricial habits) may have significance in permitting high post-natal growth rates and the exploitation of seasonally abundant resources. These interrelations may contribute to the predominance of passerines in temperate land environments.