Environment, migratory tendency, phylogeny and basal metabolic rate in birds

Basal metabolic rate (BMR) represents the minimum maintenance energy requirement of an endotherm and has far-reaching consequences for interactions between animals and their environments. Avian BMR exhibits considerable variation that is independent of body mass. Some long-distance migrants have been found to exhibit particularly high BMR, traditionally interpreted as being related to the energetic demands of long-distance migration. Here we use a global dataset to evaluate differences in BMR between migrants and non-migrants, and to examine the effects of environmental variables. The BMR of migrant species is significantly higher than that of non-migrants. Intriguingly, while the elevated BMR of migrants on their breeding grounds may reflect the metabolic machinery required for long-distance movements, an alternative (and statistically stronger) explanation is their occupation of predominantly cold high-latitude breeding areas. Among several environmental predictors, average annual temperature has the strongest effect on BMR, with a 50% reduction associated with a 20 degrees C gradient. The negative effects of temperature variables on BMR hold separately for migrants and non-migrants and are not due their different climatic associations. BMR in migrants shows a much lower degree of phylogenetic inertia. Our findings indicate that migratory tendency need not necessarily be invoked to explain the higher BMR of migrants. A weaker phylogenetic signal observed in migrants supports the notion of strong phenotypic flexibility in this group which facilitates migration-related BMR adjustments that occur above and beyond environmental conditions. In contrast to the findings of previous analyses of mammalian BMR, primary productivity, aridity or precipitation variability do not appear to be important environmental correlates of avian BMR. The strong effects of temperature-related variables and varying phylogenetic effects reiterate the importance of addressing both broad-scale and individual-scale variation for understanding the determinants of BMR.     

Thermoregulation and heterothermy in some of the smaller flying foxes (Megachiroptera) of New Guinea

Summary Body temperature, heterothermy, oxygen consumption, heart rate, and evaporative water loss were studied in four species of flying foxes (Megachiroptera), Dobsonia minor, Nyctimene major, Nyctimene albiventer, and Paranyctimene raptor, from the vicinity of Madang on the north coast of New Guinea.The thermoregulatory response of D. minor resembled that of most other placental mammals weighing 80 to 100 g. Body temperatures were relatively stable at ambient temperatures between 5 and 34°. The mean oxygen consumption at rest between 30 and 35° was 1.26 cc O₂ (g·hr)^–1. At ambient temperatures between 5 and 35° evaporative water loss averaged 4.5 mg (g·hr)^–1 and increased sharply at higher temperatures. When subjected to heat stress the animals panted, salivated, and licked the wings, belly, and uropatagium. At temperatures above 38° the ratio of heat lost through evaporation to heat production exceeded 1. Minimal heart rates in resting animals near thermal neutrality were approximately 275/min.In those parameters measured, N. major which weighed about 80 g resembled D. minor. Nyctimene albiventer and P. raptor weigh less than 30 g and are among the smallest of the flying foxes. Each shows both homeothermic and heterothermic patterns of response. At an ambient temperature of 35° the minimal oxygen consumption of homeothermic N. albiventer and P. raptor were 1.43 and 1.38 cc O₂ (g·hr)^–1, respectively. Oxygen consumption of homeothermic N. albiventer at 25°, 2.59 cc O₂ (g.hr)^–1, was almost quadruple that of torpid animals at the same temperature. During the daytime both N. albiventer and P. raptor characteristically allowed their body temperatures to fall to near 25°. Both readily aroused from the hypothermic state through physiological means. Heart rates of homeothermic N. albiventer resting at 35° ranged from 312 to 326/min while those of animals torpid at 25° were 88 to 96/min.The capacity for heterothermy has not previously been demonstrated in any members of the Megachiroptera, but our data indicate that it can occur on a daily basis in N. albiventer and P. raptor. This capacity appears to be related to size since it occurs in none of the larger flying foxes so far studied.The data presently available indicate that the relation of body weight to standard metabolism in the Megachiroptera is similar to that of the other placental mammals. In the species we studied, thermal conductances were higher, and heart rates, lower than predicted for mammals of their sizes.These studies were carried out during the 1969 Alpha Helix Expedition to New Guinea and were supported in part by grants GB-5139, GB-3656, and GB-8445 from the U. S. National Science Foundation.     

Personality and basal metabolic rate in a wild bird population

Personality and metabolic rate are predicted to show covariance on methodological and functional grounds, but empirical studies at the individual level are rare, especially in natural populations. Here we assess the relationship between exploration behaviour, an important axis of personality, and basal metabolic rate (BMR) for 680 free‐living great tits Parus major, studied over three years. We find that exploration behaviour is weakly negatively related to BMR among female, but not male, birds. Moreover, we find exploration behaviour to be independent of methodological aspects of BMR measurements (e.g. activity levels, time to acclimatize) which have been suggested to be indicative of personality‐related activity or stress levels during measurement. This suggests that the weak link between exploration behaviour and BMR found here is functional rather than methodological. We therefore test the hypothesis that selection favours covariance between exploration behaviour and metabolic rate, but find no evidence for correlational survival or fecundity selection. Our data therefore provide at best only very weak evidence for a functional link between personality and metabolic rate, and we suggest that studies of personality and metabolic strategies, or personality and daily energy expenditure, are required to further resolve the link between personality and metabolic rate.     

Food habits and the basal rate of metabolism in birds

Summary 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.     

Sample size and mass range effects on the allometric exponent of basal metabolic rate

The controversial relationship between body mass and basal metabolic rate in animals revolves around two questions: what is the allometric scaling exponent and what is the functional basis for it? For mammals, the first question could be resolved if measurements from all 4600 extant species were available, but this study shows that data for only 150 species, spanning three to four orders of magnitude variation in body mass, are sufficient to accurately determine the exponent. Because the currently available data set includes about 600 species that vary over five orders of magnitude in body size, further increases in sample size are unlikely to change the estimate of the scaling exponent.     

Testosterone effects on avian basal metabolic rate and aerobic performance: facts and artefacts

We examined the effects of cage size and testosterone (T) levels on basal and peak metabolic rates (BMR and PMR, respectively) and on pectoral and leg muscle masses of male house sparrows (Passer domesticus). Birds were housed either in small birdcages or in flight aviaries for at least 2 weeks prior to the initial metabolic evaluations. They were then implanted with either empty or T-filled silastic capsules and remeasured 5-6 weeks later. Birds treated with single T implants achieved breeding levels (4-6 ng/mL) and one group given double implants reached 10 ng/mL. There was no effect of T on BMR or PMR in any group studied, but there was an effect of caging. Caged birds showed significant reductions in PMR over the course of captivity, whereas PMR in aviary-housed birds were indistinguishable from their free-living counterparts. Testosterone treatment significantly increased leg muscle mass in caged birds, but had no effect on muscle mass in aviary-housed sparrows. We conclude that testosterone has no direct effect on sparrow metabolic rate or muscle mass, but may interact with cage conditions to produce indirect changes to these variables.     

Repeatability and individual correlates of basal metabolic rate and total evaporative water loss in birds: a case study in European stonechats

Basal metabolic rate (BMR) and total evaporative water loss (TEWL) are thought to have evolved in conjunction with life history traits and are often assumed to be characteristic features of an animal. Physiological traits can show large intraindividual variation at short and long timescales, yet natural selection can only act on a trait if it is a characteristic feature of an individual. The repeatability of a trait, a measure of the portion of variance that is caused by differences among individuals, indicates if it is a characteristic feature of an individual. We measured repeatability of BMR and TEWL of 18 captive European stonechats (Saxicola torquata rubicola) within the winter season. Repeatability was 0.56 for BMR and 0.60 for mass-specific BMR. Age and body mass had a significant effect on variation in BMR. Also after accounting for this variation, BMR remained repeatable. TEWL and mass-specific TEWL showed nonsignificant repeatabilities of 0.11 and 0.12, respectively. We conclude that BMR is a characteristic feature of an individual in our population of European stonechats, whereas TEWL is not. We discuss our results in the context of a review of currently available estimates of repeatability of BMR and TEWL for birds.     

A strong response to selection on mass-independent maximal metabolic rate without a correlated response in basal metabolic rate

Metabolic rates are correlated with many aspects of ecology, but how selection on different aspects of metabolic rates affects their mutual evolution is poorly understood. Using laboratory mice, we artificially selected for high maximal mass-independent metabolic rate (MMR) without direct selection on mass-independent basal metabolic rate (BMR). Then we tested for responses to selection in MMR and correlated responses to selection in BMR. In other lines, we antagonistically selected for mice with a combination of high mass-independent MMR and low mass-independent BMR. All selection protocols and data analyses included body mass as a covariate, so effects of selection on the metabolic rates are mass adjusted (that is, independent of effects of body mass). The selection lasted eight generations. Compared with controls, MMR was significantly higher (11.2%) in lines selected for increased MMR, and BMR was slightly, but not significantly, higher (2.5%). Compared with controls, MMR was significantly higher (5.3%) in antagonistically selected lines, and BMR was slightly, but not significantly, lower (4.2%). Analysis of breeding values revealed no positive genetic trend for elevated BMR in high-MMR lines. A weak positive genetic correlation was detected between MMR and BMR. That weak positive genetic correlation supports the aerobic capacity model for the evolution of endothermy in the sense that it fails to falsify a key model assumption. Overall, the results suggest that at least in these mice there is significant capacity for independent evolution of metabolic traits. Whether that is true in the ancestral animals that evolved endothermy remains an important but unanswered question.     

黑线仓鼠繁殖输出与基础代谢率的关系

为了解黑线仓鼠繁殖输出与基础代谢率(BMR)的关系,阐明最大持续能量收支(SusMR)的限制水平, 揭示哺乳期能量收支对策,本文测定了哺乳期黑线仓鼠的体重、摄食量、BMR 和身体组成,以及哺乳期的胎仔数、胎仔重和泌乳能量支出(MEO)。结果显示,黑线仓鼠哺乳期体重降低了15.0 ± 0.8% , 摄食量显著增加, 哺乳高峰期平均摄食量为13.9 ± 0.3 g /d, 摄入能为222.1 ± 5.3 kJ/ d, 比哺乳初期增加121% , 比对照组高288% ;哺乳高峰期MEO 为62.4 ± 2.3 kJ/ d, 哺乳末期BMR 为49.7 ± 1.1 kJ/ d; 断乳时平均胎仔数4.7 ± 0.2、窝胎仔重50.5 ±1.6 g; 哺乳末期BMR 比对照组增加48% ,BMR 与消化系统各器官的相关性高于对照组; BMR 与胎仔数、胎仔重、乳腺重量和MEO 显著正相关。结果表明:初次繁殖的黑线仓鼠哺乳期SusMR 限制为4.47 ×BMR, 在自身维持和繁殖输出之间采取了“权衡分配”的原则,通过体重降低以减少BMR 的增加幅度, 从而有利于繁殖输出。     

The influence of heat increment of feeding on basal metabolic rate in Phyllotis darwini (Muridae)

One of the most important prerequisites for obtaining a reliable measure of basal metabolic rate (BMR) in endotherms is that the animal must be in a post-absorptive condition. However, because of the diversity of nutrition and digestion modes in vertebrates, it is not simple to generalize a standard procedure for BMR measurement. Thus, information in this regard must be experimentally obtained by measuring the heat increment of feeding (HIF). We used a repeated-measures design to test for the effects of HIF on BMR in Phyllotis darwini, a granivorous rodent. Our results suggest that, in this species, feeding induces an elevation in O(2) consumption that can persist up to 4 h after the last meal. In addition, and irrespective of the fasting period, measures made with less than 2 h of fasting yield BMR values that are significantly higher than measurements after longer fasting periods (i.e. 3 and 4 h).     

Testosterone effects on avian basal metabolic rate and aerobic performance: facts and artefacts.

We examined the effects of cage size and testosterone (T) levels on basal and peak metabolic rates (BMR and PMR, respectively) and on pectoral and leg muscle masses of male house sparrows (Passer domesticus). Birds were housed either in small birdcages or in flight aviaries for at least 2 weeks prior to the initial metabolic evaluations. They were then implanted with either empty or T-filled silastic capsules and remeasured 5-6 weeks later. Birds treated with single T implants achieved breeding levels (4-6 ng/mL) and one group given double implants reached 10 ng/mL. There was no effect of T on BMR or PMR in any group studied, but there was an effect of caging. Caged birds showed significant reductions in PMR over the course of captivity, whereas PMR in aviary-housed birds were indistinguishable from their free-living counterparts. Testosterone treatment significantly increased leg muscle mass in caged birds, but had no effect on muscle mass in aviary-housed sparrows. We conclude that testosterone has no direct effect on sparrow metabolic rate or muscle mass, but may interact with cage conditions to produce indirect changes to these variables.     

The effect of body fat on basal metabolic rate in adult harp seals (Phoca groenlandica)

Three adult harp seals (Phoca groenlandica) were fed different daily amounts of capelin (Mallotus villosus), and their body composition determined by use of the tritiated water method at different levels of fattening. Basal metabolic rate (BMR) was measured after 5 days of fasting by indirect calorimetry, and was on average 1.1 W.kg-1 when 45% of body mass (BM) was fat and 2.3 W.kg-1 when body fat was reduced to 13% of BM. This suggests that body fat contributes little to BMR in these animals. It follows, that predictions of BMR on the basis of BM is questionable in seals, in which body fat may change seasonally between 20 and 60% of BM.     

Effects of metabolic level on the body size scaling of metabolic rate in birds and mammals

Metabolic rate is traditionally assumed to scale with body mass to the 3/4-power, but significant deviations from the '3/4-power law' have been observed for several different taxa of animals and plants, and for different physiological states. The recently proposed 'metabolic-level boundaries hypothesis' represents one of the attempts to explain this variation. It predicts that the power (log-log slope) of metabolic scaling relationships should vary between 2/3 and 1, in a systematic way with metabolic level. Here, this hypothesis is tested using data from birds and mammals. As predicted, in both of these independently evolved endothermic taxa, the scaling slope approaches 1 at the lowest and highest metabolic levels (as observed during torpor and strenuous exercise, respectively), whereas it is near 2/3 at intermediate resting and cold-induced metabolic levels. Remarkably, both taxa show similar, approximately U-shaped relationships between the scaling slope and the metabolic (activity) level. These predictable patterns strongly support the view that variation of the scaling slope is not merely noise obscuring the signal of a universal scaling law, but rather is the result of multiple physical constraints whose relative influence depends on the metabolic state of the organisms being analysed.     

Effects of dietary quality on basal metabolic rate and internal morphology of European starlings (Sturnus vulgaris)

European starlings (Sturnus vulgaris) were fed either a low- or high-quality diet to test the effects of dietary quality on basal metabolic rate (BMR) and internal morphology. Basal metabolic rate did not differ significantly between the two dietary groups, but internal morphology differed greatly. Starlings fed the low-quality diet had heavier gastrointestinal tracts, gizzards, and livers. Starlings fed the high-quality diet had heavier breast muscles. Starlings on the low-quality diet maintained mass, while starlings on the high-quality diet gained mass. Dry matter digestibility and energy digestibility were lower for starlings fed the low-quality diet, and their food and water intake were greater than starlings on the high-quality diet. The lack of dietary effect on BMR may be the result of increased energy expenditure of digestive organs paralleling a reduction of energy expenditure of organs and tissues not related to digestion (i.e., skeletal muscle). This trade-off in energy allocation among organs suggests a mechanism by which organisms may alter BMR in response to a change in seasonal variation in food availability.     

Seasonality in basal metabolic rate and thermal conductance in a long-distance migrant shorebird,the knot (Calidris canutus)

Knots Calidris canutus live highly seasonal lives, breeding solitarily on high arctic tundra and spending the non-breeding season in large social flocks in temperate to tropical estuaries. Their reproductive activities and physiological preparations for long flights are reflected in pronounced plumage and body mass changes, even in long-term captives of the islandica subspecies (breeding in north Greenland and northeast Canada and wintering in western Europe) studied in outdoor aviaries. The three to four fattening episodes in April-July in connection with the flights to and from the high arctic breeding grounds by free-living birds, are represented by a single period of high body mass, peaking between late May and early July in a sample of ten captive islandica knots studied over four years. There are consistent and synchronized annual variations in basal metabolic rate and thermal conductance in three islandica knots. Basal metabolic rate was highest during the summer body mass peak. Within the examined individuals, basal metabolic rate scales on body mass with an exponent of about 1.4, probably reflecting a general hypertrophy of metabolically expensive muscles and organs. Any potential effect of moult on basal metabolic rate was obscured by the large seasonal mass-associated variations. In breeding plumage, insulation (the inverse of thermal conductance) was a factor of 1.35 lower than in winter plumage. This was paralleled by the dry mass of contour feathers being a factor of 1.17 lower. In this subspecies the breeding season is indeed the period during which the costs of thermoregulation are lowest. In captive knots seasonal changes in basal metabolic rate and thermal conductance likely reflect an anticipatory programme adaptive to the variable demands made by the environment at different times of the year.     

The relationship between basal metabolic rate (BMR) and concentrations of plasma thyroid hormones in fasting cockerels

A correlation between the Basal Metabolic Rate (BMR) and the level of rT3, and occasionally between BMR and T3 or T4 was found in 12 month fasting cockerels. The birds were fasted for 48 hrs and BMR was measured eight times (before fasting, at 6, 12, 24, 30, 36, and 48 hrs of fasting, and 4 hours after fasting). Blood samples for plasma collection were taken immediately after measuring the BMR. During starvation a decrease in BMR was observed. After refeeding BMR returned to the starting level. The decrease in BMR was accompanied by an increase in rT3 and T4 plasma levels. Between BMR and levels of T4 and rT3 negative coefficients of correlation were observed (r = -0.20 and r = -0.42, respectively). Contrary to this, the T3 level declined and was correlated with BMR (r = 0.62). After refeeding, the T3 level rapidly increased against the control value. Moreover, a high coefficient of correlation (r = -0.39) was found between the level of T3 and rT3. The data show that the reduction in plasma T3 level and increase in the rT3 one during starvation may be due to inhibition of deiodination of T4 to T3, since rT3 is a competitive inhibitor of this reaction. The presented results support the suggestion that in birds T3 is the metabolically active thyroid hormone, and rT3 antagonizes this effect.