Seasonal effects on metabolism and thermoregulation abilities of the Red-winged Starling (Onychognathus morio)

Basal metabolic rate (BMR) of birds is beginning to be viewed as a highly flexible physiological trait influenced by environmental fluctuations, and in particular changes in ambient temperatures (T_a). Southern Africa is characterized by an unpredictable environment with daily and seasonal variation. This study sought to evaluate the effects of seasonal changes in T_a on mass-specific resting metabolic rate (RMR), BMR and body temperature (T_b) of Red-winged Starlings (Onychognathus morio). They have a broad distribution, from Ethiopia to the Cape in South Africa and are medium-sized frugivorous birds. Metabolic rate (VO₂) and T_b were measured in wild caught Red-winged Starlings after a period of summer and winter acclimatization in outdoor aviaries. RMR and BMR were significantly higher in winter than summer. Body mass of Starlings was significantly higher in winter compared with summer. The increased RMR and BMR in winter indicate improved ability to cope with cold and maintenance of a high T_b. These results show that the metabolism of Red-winged Starlings are not constant, but exhibit a pronounced seasonal phenotypic flexibility with maintenance of a high T_b.     

Seasonal effects on thermoregulatory abilities of the Wahlberg's epauletted fruit bat (Epomophorus wahlbergi) in KwaZulu-Natal,South Africa

Seasonal variations in ambient temperature (T_a) require changes in thermoregulatory responses of endotherms. These responses vary according to several factors including taxon and energy constraints. Despite a plethora of studies on chiropteran variations in thermoregulation, few have examined African species. In this study, we used the Wahlberg's epauletted fruit bat (Epomophorus wahlbergi, body mass≈115 g) to determine how the thermoregulatory abilities of an Afrotropical chiropteran respond to seasonal changes in T_a. Mass specific Resting Metabolic Rates (RMR_Ta) and basal metabolic rate (BMR) were significantly higher in winter than in summer. Furthermore, winter body mass was significantly higher than summer body mass. A broad thermoneutral zone (TNZ) was observed in winter (15–35 °C) compared with summer (25–30 °C). This species exhibited heterothermy (rectal and core body temperature) during the photophase (bats' rest-phase) particularly at lower T_as and had a low tolerance of high T_as. Overall, there was a significant seasonal variation in the thermoregulatory abilities of E. wahlbergi. The relative paucity of data relating to the seasonal thermoregulatory abilities of Afrotropical bats suggest further work is needed for comparison and possible effects of climate change, particularly extreme hot days.     

Seasonal variation in the metabolism-temperature relation of House Sparrows (Passer domesticus) in KwaZulu-Natal,South Africa

Many birds exhibit considerable phenotypic flexibility in metabolism to maintain thermoregulation or to conserve energy. This flexibility usually includes seasonal variation in metabolic rate. Seasonal changes in physiology and behavior of birds are considered to be a part of their adaptive strategy for survival and reproductive success. House Sparrows (Passer domesticus) are small passerines from Europe that have been successfully introduced to many parts of the world, and thus may be expected to exhibit high phenotypic flexibility in metabolic rate. Mass specific Resting Metabolic Rate (RMR) and Basal Metabolic Rate (BMR) were significantly higher in winter compared with summer, although there was no significant difference between body mass in summer and winter. A similar, narrow thermal neutral zone (25–28 °C) was observed in both seasons. Winter elevation of metabolic rate in House Sparrows was presumably related to metabolic or morphological adjustments to meet the extra energy demands of cold winters. Overall, House Sparrows showed seasonal metabolic acclimatization similar to other temperate wintering passerines. The improved cold tolerance was associated with a significant increase in VO₂ in winter relative to summer. In addition, some summer birds died at 5 °C, whereas winter birds did not, further showing seasonal variation in cold tolerance. The increase in BMR of 120% in winter, compared to summer, is by far the highest recorded seasonal change so far in birds.     

Thermoregulatory responses in seasonally acclimatized captive Southern White-faced Scops-owls

Seasonal thermoregulatory responses that are associated with cold tolerance have been reported for many species that inhabit regions where winters are severe (e.g. Holarctic), but relatively few studies have focused on species from regions where the climate is more unpredictable (e.g. Southern Africa). In this study, metabolic rate (VO₂) and body temperature (T_b) was measured during summer and winter in captive Southern White-faced Scops-owl (Ptilopsis granti), to test for thermoregulatory responses representing energy conservation in winter. During winter the Southern White-faced Scops-owls increased resting metabolic rate (RMR) by 45% to regulate a set point T_b—a result similar to what had been shown in small passerines from the Holarctic region. Increased RMR and increased conductance at cold T_a's are suggestive of improved cold tolerance. Basal metabolic rate (BMR) was 0.60 mL O₂ g⁻¹ h⁻¹ and showed no seasonal flexibility. Thus, contrary to expectation, the Southern White-faced Scops-owls showed seasonal thermoregulatory responses that are unlikely to represent energy conservation which was expected for a medium-sized bird inhabiting unpredictable climates in Southern Africa.     

Thermoregulation in leopard tortoises in the Nama-Karoo: The importance of behaviour and core body temperatures

Despite being ectotherms, reptiles have an ability to thermoregulate which is enhanced by adopting a variety of behavioural mechanisms. Different behavioural postures, the use of retreat sites and selection of microhabitats enable reptiles to maintain their core body temperatures (T_b) above that of ambient temperatures (T_a) in winter or below T_a maximum in summer. This study describes the daily activity patterns of leopard tortoises (Stigmochelys pardalis) in relation to T_b and T_a, and the extent to which leopard tortoises can manipulate their T_b in response to seasonal changes in T_a. Ten and nine leopard tortoises were radio-tracked in 2002 and 2003, respectively and cloacal T_b and behaviours observed. Core T_bs were measured using Thermocron iButtons^™ surgically implanted into the body cavities of 4 and 5 adult telemetered tortoises for summer and winter 2003, respectively. There were seasonal differences in the extent to which certain behaviours were practiced and the time of day that these occurred. Leopard tortoises generally had unimodal activity patterns in winter and bimodal ones in summer. In winter tortoises were active at lower T_bs, and at lower T_a, than in summer. Tortoises maintained their core T_b well below T_a minimum profiles in summer and well above these in winter. Core T_b closely followed the increase in T_a minimum profiles in the mornings, however tortoises exhibited an extended thermal lag when T_a minimum profiles cooled overnight. By using different behavioural mechanisms in summer and winter, leopard tortoises maintained their core T_b at different levels compared with T_a minimum and maximum profiles. Consequently although they are ectotherms, they maintained their core T_b independent of T_a.     

The allometry of parrot BMR: seasonal data for the Greater Vasa Parrot, <Emphasis Type="Italic">Coracopsis vasa</Emphasis>, from Madagascar

In this study we examined the allometry of basal metabolic rate (BMR) of 31 parrot species. Unlike previous reports, we show that parrots per se do not display BMRs that are any different to other captive-raised birds of their body size. An ordinary least squares regression fitted the data best and body mass explained 95% of the variation in BMR. There was no phylogenetic signal in the BMR data. We also provide new data for the Greater Vasa Parrot (Coracopsis vasa) of Madagascar. We tested the hypotheses that C. vasa may, because of its insular existence, display conservative energetic traits (low BMR, use of adaptive heterothermy) similar to those observed in several Malagasy mammals. However, this was not the case. C. vasa had a higher BMR than other parrots, especially during summer, when BMR was up-regulated by 50.5% and was 95.7% higher than predicted from an ordinary least squares (OLS) allometry of parrots (BMR = 0.042M _b^0.649, BMR in Watts, M _b in grammes). Compared with BMR data for 94 captive-raised bird species, the winter and summer BMRs were, respectively, 45.5 and 117.8% higher than predicted by a phylogenetic generalised least squares (PGLS) allometry (BMR = 0.030M _b^0.687, BMR in Watts, M _b in grammes). The summer up-regulation of BMR is the highest recorded for a bird of any size to date. We suggest that the costs of a high summer BMR may be met by the unusual cooperative breeding system of C. vasa in which groups of males feed the female and share paternity. The potential breeding benefits of a high summer BMR are unknown.     

Seasonal variations in basal metabolic rate, lower critical temperature and responses to temporary starvation in the arctic fox (Alopex lagopus) from Svalbard

Metabolic rates of four resting, post-absorptive male adult summer- and winter-adapted captive arctic foxes (Alopex lagopus) were recorded. Basal metabolic rates (BMR) varied seasonally with a 36% increase from winter to summer, while body mass was reduced by 17% in the same period. The lower critical temperature (T _1c) of the winter-adapted arctic fox was estimated to −7°C, whereas T _lc during summer was 5°C. The similarity of these values, which are much higher than hitherto assumed (e.g. Scholander et al. 1950b), is mainly due to a significantly (P<0.05) lower BMR in winter than in summer. Body core (stomach) temperature was stable, even at ambient temperatures as low as −45°C, but showed a significant (P<0.05) seasonal variation, being lower in winter (39.3±0.33°C) than in summer (39.8±0.16°C). The thermal conductivity of arctic fox fur was the same during both seasons, whereas the thermal conductance in winter was lower than in summer. This was reflected in an increase in fur thickness of 140% from summer to winter, and in a reduced metabolic response to ambient temperatures below T _lc in winter. Another four arctic foxes were exposed to three periods of forced starvation, each lasting 8 days during winter, when body mass is in decline. No significant reduction in mass specific BMR was observed during the exposure to starvation, and respiratory quotient was unchanged at 0.73±0.02 during the first 5 days, but dropped significantly (P<0.05) to 0.69±0.03 at day 7. Locomotor activity and body core (intraperitoneal) temperature was unaltered throughout the starvation period, but body mass was reduced by 18.5±2.1% during these periods. Upon re-feeding, locomotor activity was significantly (P<0.05) reduced for about 6 days. Energy intake was almost doubled, but stabilised at normal levels after 11 days. Body mass increased, but not to the level before the starvation episodes. Instead, body mass increased until it reached the reduced body mass of ad libitum fed control animals. This indicates that body mass in the arctic fox is regulated according to a seasonally changing set point.     

Seasonality of torpor and thermoregulation in three dasyurid marsupials

Summary Seasonal variation in the pattern of torpor and temperature regulation was investigated in the closely related arid zone dasyurid marsupialsSminthopsis crassicaudata (17 g),S. macroura (24 g), andDasyuroides byrnei (120 g). The tendency to enter torpor was greater, torpor commenced earlier, torpor duration was longer, and body temperatures (T _b) were lower inSminthopsis spp. than inD. byrnei. The minimum mass-specific rate of oxygen consumption ( ) of torpid animals was similar among the three species despite the differences in minimumT _b. The mass-specific oxygen consumption of normothermic animals was reduced during winter when compared with the summer values in all species, but there was no seasonal variation in normothermicT _b in any species. The tendency to enter torpor was incrased during winter. TorpidSminthopsis spp. had lower values ofT _b and during winter than during summer;D. byrnei did not show seasonal changes in these variables. These results suggest that seasonal changes in the pattern of thermoregulation and torpor in small dasyurids may be more distinct than in larger species.Abbreviations RMR resting metabolic rate - BMR basal metabolic rate     

Seasonal effects on the thermoregulation of invasive rose-ringed parakeets (Psittacula krameri)

Invasive species are a major threat to global biodiversity. Rose-ringed parakeets Psittacula krameri are widely established outside their native range and are successful invaders in many countries, including South Africa. Physiological and behavioral responses to environmental conditions are considered to be major factors that influence the abundance and distribution of birds. As rose-ringed parakeets are able to tolerate wide varieties of climatic conditions as invaders, it is important to understand their physiological responses to these. This study examined the effects of seasonal changes in ambient temperatures (T_a) on metabolic rate and body temperature (T_b) of captive-bred rose-ringed parakeets. Resting metabolic rate at various T_a and basal metabolic rate were significantly lower in winter compared to summer, and the thermo-neutral zone was broader in winter than in summer. There was no significant difference in body mass (M_b) between seasons. These parakeets showed seasonal thermoregulatory responses that represented energy conservation as expected, rather than cold tolerance. They were relatively tolerant of low T_a and showed no hypothermia at 5 °C. Our results suggest that this species is physiologically and behaviorally equipped to cope with a range of climatic situations and this partly explains their global success as an invader species.     

Thermal relations of large crocodiles,Crocodylus porosus,free-ranging in a naturalistic situation

We monitored behaviour and environmental and body temperatures (T_b) in summer and winter in 11 salt-water crocodiles (Crocodylus porosus), of body mass 32 to 1010kg, free-ranging in naturalistic captivity in northern Australia. We found pronounced daily cycles in air and water temperatures in both winter (16 to 33 degrees C and 20 to 31degrees C, respectively) and summer (21 to 45 degrees C and 24 to 36 degrees C, respectively). In winter, crocodiles exposed themselves to the sun during the day and stayed in the water at night. In summer, they remained in the water during the day and emerged onto land at night. Body temperature showed a daily cycle the amplitude of which decreased with increasing mass, from 3.5 degrees C (mass 32kg) to 1.0 degrees C (660kg) in summer, and from 3.5 degrees C (42kg) to 1.4 degrees C (1010kg) in winter. Underlying the daily cycles in T_b were intermediate (10 to 13 day, tidal?) and seasonal cycles. Overall, values of modal T_b ranged from 25.1 to 28.7 degrees C in winter and from 28.4 to 33.6 degrees C in summer, trending upwards with body size. This pattern of continuous oscillations in T_b, with no daily plateau, is conspicuously different from that seen in crocodilians of small sizes and from the pattern usually regarded as typical of reptiles in general.     

Body temperature variation of South African antelopes in two climatically contrasting environments

To understand the adaptive capacity of a species in response to rapid habitat destruction and climate change, we investigated variation in body temperature (T_b) of three species of antelope, namely eland, blue wildebeest and impala, using abdominally-implanted temperature data loggers. The study was conducted at two climatically contrasting environments in South Africa, one with a less seasonal and mild winter (Mapungubwe National Park) and the other with a more seasonal, long and cold winter (Asante Sana Game Reserve). Since the habitat with long and cold winters would be suboptimal for these African antelopes, which evolved in less seasonal and hot environments, antelopes in Asante Sana were expected to exhibit a larger amplitude in T_b and a lower minimum body temperature (Min T_b) during winter to reduce T_b and the ambient temperature (T_b−T_a) gradient to save energy. In both eland and impala, 24-h body temperature amplitude did not differ between the study sites, regardless of season. Conversely, wildebeest in Mapungubwe showed a higher variability in the 24-h amplitude of body temperature and also a lower Min T_b during winter and spring than the wildebeest in Asante Sana. This variation in T_b among Mapungubwe wildebeest was influenced by both the amplitude of ambient temperature (positive) and cumulative rainfall (negative), which was not the case for wildebeest in Asante Sana. We propose that the low Min T_b of wildebeest in Mapungubwe was the result of nutritional stress during winter and spring; an evident response even during a year of average rainfall. Therefore, these wildebeest apparently live in a physiologically stressful environment. With the predicted increase in the frequency and intensity of drought periods in southern Africa, wildebeest and other grazers, will likely experience greater nutritional stress in the future.     

Seasonal variations in metabolism and thermoregulation in the striped hamster (Cricetulus barabensis)

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Metabolic rate (MR), thermal neutral zone (TNZ), body temperature (T_b), and thermal conductance were measured in striped hamsters (Cricetulus barabensis) that were live-trapped in winter and summer.     

Metabolic and ventilatory acclimatization to cold stress in house sparrows (Passer domesticus)

Passerines that overwinter in temperate climates undergo seasonal acclimatization that is characterized by metabolic adjustments that may include increased basal metabolic rate (BMR) and cold-induced summit metabolism (M(sum)) in winter relative to summer. Metabolic changes must be supported by equivalent changes in oxygen transport. While much is known about the morphology of the avian respiratory system, little is known about respiratory function under extreme cold stress. We examined seasonal variation in BMR, M(sum), and ventilation in seasonally acclimatized house sparrows from Wisconsin. BMR and M(sum) increased significantly in winter compared with summer. In winter, BMR increased 64%, and M(sum) increased 29% over summer values. The 64% increase in winter BMR is the highest recorded for birds. Metabolic expansibility (M(sum)/BMR) was 9.0 in summer and 6.9 in winter birds. The metabolic expansibility of 9.0 in summer is the highest yet recorded for birds. Ventilatory accommodation under helox cold stress was due to changes in breathing frequency (f), tidal volume, and oxygen extraction efficiency in both seasons. However, the only significant difference between summer and winter ventilation measures in helox cold stress was f. Mean f in helox cold stress for winter birds was 1.23 times summer values.     

Seasonal torpor and normothermic energy metabolism in the Eastern chipmunk (Tamias striatus)

To assess the changes in thermoregulatory characteristics that accompany the seasonal expression of torpor we measured seasonal differences in body mass adjustments, body temperature (T _b) and metabolic rate (MR) in both summer- and winter-acclimated individuals from a species of food-storing hibernator, the Eastern chipmunk (Tamias striatus). Torpor occurred only in the winter and was associated with lower normothermic T _b, during inter-bout arousal periods than in the summer. Chipmunks increased body mass before the initiation of torpor in winter, and steadily lost mass as the hibernation season progressed. Torpor expression was correlated to initial mass gain, with the individuals who showed the largest mass increase in the fall showing the highest degree of torpor. Acclimation to winter-like conditions produced a decline in normothermic MR at all ambient temperatures examined. The findings indicate that torpor expression is accompanied by a decrease in T _b and MR during normothermy, indicating that a conservation of energy metabolism occurs, not only in torpor, but also during the inter-bout arousal periods.     

Seasonal acclimatization of metabolism in Eurasian tree sparrows (Passer montanus)

Acclimatization to winter conditions is an essential prerequisite for survival of small passerines of the northern temperate zone. Changes in photoperiod, ambient temperature and food availability trigger seasonal acclimatization in physiology and behavior of many birds. In the present study, seasonal adjustments in several physiological, hormonal, and biochemical markers were examined in wild-captured Eurasian tree sparrows (Passer montanus) from the Heilongjiang Province in China. In winter sparrows had higher body mass and basal metabolic rate (BMR). Consistently, the dry mass of liver, heart, gizzard, small intestine, large intestine and total digestive tract were higher in winter than in that in summer. The contents of mitochondrial protein in liver, and state-4 respiration and cytochrome c oxidase (COX) activity in liver and muscle increased significantly in winter. Circulating level of serum triiodothyronine (T₃) was significantly higher in winter than in summer. Together, these data suggest that tree sparrows mainly coped with cold by enhancing thermogenic capacities through increased organ masses and heightened activity of respiratory enzymes activities. The results support the view that prominent winter increases in BMR are manifestations of winter acclimatization in tree sparrows and that seasonal variation in metabolism in sparrows is similar to that in other small temperate-wintering birds.     

Acclimation to temperature in Actinia equina L.: Effects of season and shore level on aquatic oxygen consumption

Effect of seasonal and experimental acclimation to temperature upon aquatic oxygen consumption of the sea anemone Actinia equina L. has been studied in animals from two shore levels during the summer of 1981 and the winter of 1982. A clear influence of both season and shore level on the weight exponent is registered, higher values occurring during the summer. Seasonally acclimated animals from the upper shore showed perfect winter-summer compensation with lateral translation to the right of the R-T curve in response to warm acclimation while this pattern was coupled with clockwise rotation and partial compensation in specimens collected from the low shore. Experimental acclimation during the summer resulted in partial compensation at T_a 15°C and no acclimation was found at T_a 25°C; during the winter, only high shore specimens exhibited compensatory responses. A significant increase in oxygen consumption, regardless of shore level, occurs in winter in both seasonally and experimentally acclimated animals.     

Does fear beget fear? Risk-mediated habitat selection triggers predator avoidance at lower trophic levels

Seasonal changes in weather and food availability differentially impact energy budgets of small mammals such as bats. While most thermal physiological research has focused on species that experience extreme seasonal temperature variations, knowledge is lacking from less variable temperate to subtropical climates. We quantified ambient temperature (T _a) and skin temperature (T _sk) responses by individuals from a population of New Zealand lesser short-tailed bats (Mystacina tuberculata) during summer and winter using temperature telemetry. During summer, communal roosts were more thermally stable than T _a. During winter, solitary roosts were warmer than T _a indicating significant thermal buffering. Communal roost trees were used on 83 % of observation days during summer, and individuals occupying them rarely entered torpor. Solitary roosts were occupied on 93 % of observation days during winter, and 100 % of individuals occupying them used torpor. During summer and winter, bats employed torpor on 11 and 95 % of observation days, respectively. Maximum torpor bout duration was 120.8 h and winter torpor bout duration correlated negatively with mean T _a. Torpor bout duration did not differ between sexes, although female minimum T _sk was significantly lower than males. The summer Heterothermy Index varied, and was also significantly affected by T _a. Mean arousal time was correlated with sunset time and arousals occurred most frequently on significantly warmer evenings, which are likely associated with an increased probability of foraging success. We provide the first evidence that torpor is used flexibly throughout the year by M. tuberculata, demonstrating that roost choice and season impact torpor patterns. Our results add to the growing knowledge that even small changes in seasonal climate can have large effects on the energy balance of small mammals.     

Seasonal variation in thermal energetics of the Australian owlet-nightjar (Aegotheles cristatus)

Many birds living in regions with seasonal fluctuations in ambient temperatures (T_a) typically respond to cold by increasing insulation and adjusting metabolic rate. Seasonal variation in thermal physiology has not been studied for the Caprimulgiformes, an order of birds that generally have basal metabolic rates (BMR) lower than predicted for their body mass. We measured the metabolic rate and thermal conductance of Australian owlet-nightjars (Aegotheles cristatus) during summer and winter using open-flow respirometry. Within the thermoneutral zone (TNZ; 31.3 to 34.8 °C), there was no seasonal difference in BMR or thermal conductance (C), but body temperature was higher in summer- (38.2 ± 0.3 °C) than winter-acclimatized (37.1 ± 0.5 °C) birds. Below the TNZ, resting metabolic rate (RMR) increased linearly with decreasing T_a, and RMR and C were higher for summer- than winter-acclimatized birds. The mean mass-specific BMR of owlet-nightjars (1.27 mL O₂ g^− 1 h^− 1) was close to the allometrically predicted value for a 45 g Caprimulgiformes, but well below that predicted for birds overall. These results suggest that owlet-nightjars increase plumage insulation to cope with low winter T_a, which is reflected in the seasonal difference in RMR and C below the TNZ, rather than adjusting BMR.     

Seasonal variation in body composition in an Afrotropical passerine bird: increases in pectoral muscle mass are,unexpectedly, associated with lower thermogenic capacity

Phenotypic flexibility in avian metabolic rates and body composition have been well-studied in high-latitude species, which typically increase basal metabolic rate (BMR) and summit metabolism (M_sum) when acclimatized to winter conditions. Patterns of seasonal metabolic acclimatization are more variable in lower-latitude birds that experience milder winters, with fewer studies investigating adjustments in avian organ and muscle masses in the context of metabolic flexibility in these regions. We quantified seasonal variation (summer vs winter) in the masses of organs and muscles frequently associated with changes in BMR (gizzard, intestines and liver) and M_sum (heart and pectoral muscles), in white-browed sparrow-weavers (Plocepasser mahali). We also measured pectoral muscle thickness using a portable ultrasound system to determine whether we could non-lethally estimate muscle size. A concurrent study measured seasonal changes in BMR and M_sum in the same population of sparrow-weavers, but different individuals. There was no seasonal variation in the dry masses of the gizzard, intestines or liver of sparrow-weavers, and during the same period, BMR did not vary seasonally. We found significantly higher heart (~ 18% higher) and pectoral muscle (~ 9% higher) dry mass during winter, although ultrasound measurements did not detect seasonal changes in pectoral muscle size. Despite winter increases in pectoral muscle mass, M_sum was ~ 26% lower in winter compared to summer. To the best of our knowledge, this is the first study to report an increase in avian pectoral muscle mass but a concomitant decrease in thermogenic capacity.

     

Intra-Seasonal Flexibility in Avian Metabolic Performance Highlights the Uncoupling of Basal Metabolic Rate and Thermogenic Capacity

Stochastic winter weather events are predicted to increase in occurrence and amplitude at northern latitudes and organisms are expected to cope through phenotypic flexibility. Small avian species wintering in these environments show acclimatization where basal metabolic rate (BMR) and maximal thermogenic capacity (M_SUM) are typically elevated. However, little is known on intra-seasonal variation in metabolic performance and on how population trends truly reflect individual flexibility. Here we report intra-seasonal variation in metabolic parameters measured at the population and individual levels in black-capped chickadees ( Poecile atricapillus ). Results confirmed that population patterns indeed reflect flexibility at the individual level. They showed the expected increase in BMR (6%) and M_SUM (34%) in winter relative to summer but also, and most importantly, that these parameters changed differently through time. BMR began its seasonal increase in November, while M_SUM had already achieved more than 20% of its inter-seasonal increase by October, and declined to its starting level by March, while M_SUM remained high. Although both parameters co-vary on a yearly scale, this mismatch in the timing of variation in winter BMR and M_SUM likely reflects different constraints acting on different physiological components and therefore suggests a lack of functional link between these parameters.