The effect of food temperature on post-prandial metabolism in albatrosses

Heat generated by the specific dynamic action (SDA) associated with feeding is known to substitute for the thermoregulatory costs of cold-exposed endotherms; however, the effectiveness of this depends on food  temperature. When food is cooler than core body temperature, it is warmed by body heat and, consequently, imposes a thermoregulatory challenge to the animal. The degree to which this cost might be `paid' by SDA depends on the relative timing of food heating and the SDA response. We investigated this phenomenon in two genera of endotherms, Diomedea and Thalassarche albatrosses, by measuring postprandial metabolic rate following ingestion of food at body temperature (40°C) and cooler (0 and 20°C). This permitted us to estimate potential contributions to food warming by SDA-derived heat, and to observe the effect of cold food on metabolic rate. For meal sizes that were ~20% of body mass, SDA was 4.22±0.37% of assimilated food energy, and potentially contributed 17.9±1.0% and 13.2±2.2% of the required heating energy of food at 0°C for Diomedea and Thalassarche albatrosses, respectively, and proportionately greater quantities at higher food temperatures. Cold food increased the rate at which postprandial metabolic rate increased to 3.2–4.5 times that associated with food ingested at body temperature. We also found that albatrosses generated heat in excess by more than 50% of the estimated thermostatic heating demand of cold food, a probable consequence of time delays in physiological responses to afferent signals.

Thermoenergetics of pre-moulting and moulting kookaburras (Dacelo novaeguineae): they're laughing.

We examined the effect of temperature on resting metabolic rate in seven field-captured laughing kookaburras (Dacelo novaeguineae) during late winter and early spring. Basal metabolic rate averaged 201±3.4 ml O₂ h^–1 (0.603 ml O₂ g^–1 h^–1). Overall thermal conductance (K_o) declined with ambient temperature (T_a) and averaged 0.026 ml O₂ g^–1 h^–1 °C^–1 at T_as<10 °C. Day-night differences in body temperatures (2.6 °C) and in alpha-phase versus rho-phase minimum metabolic rates were much greater (33%) than predicted for 340-g nonpasserine birds and suggest that these animals operate as low-metabolic intensity animals in their rest phase, but normal-metabolic intensity animals during their active phase. Metabolic rate was measured in four of the same birds undergoing moult. Thermal conductance increased to 60% above pre-moult values about 6 weeks after moult began. Basal metabolic rate of moulting birds showing peak thermal conductance readings averaged 17 ml O₂ h^–1 higher than pre-moult measurements. Although this increase was not statistically significant, we believe the moult costs of kookaburras are too low to overcome the inherent variability of BMR determination. We suggest that moult costs of kookaburras are only somewhat higher than the measured costs of protein synthesis of other endotherms.

Physiological response to extreme fasting in subantarctic fur seal (Arctocephalus tropicalis) pups : metabolic rates, energy reserve utilization, and water fluxes

Physiological response to extreme fasting in subantarctic fur seal (Arctocephalus tropicalis) pups: metabolic rates, energy reserve utilization, and water fluxes. Am J Physiol Regul Integr Comp Physiol 297: R1582–R1592, 2009. First published September 23, 2009; doi:10.1152/ajpregu.90857.2008.— Surviving prolonged fasting requires various metabolic adaptations, such as energy and protein sparing, notably when animals are simultaneously engaged in energy-demanding processes such as growth. Due to the intermittent pattern of maternal attendance, subantarctic fur seal pups have to repeatedly endure exceptionally long fasting episodes throughout the 10-mo rearing period while preparing for nutritional independence. Their metabolic responses to natural prolonged fasting (33.4 ± 3.3 days) were investigated at 7 mo of age. Within 4–6 fasting days, pups shifted into a stage of metabolic economy characterized by a minimal rate of body mass loss (0.7%/day) and decreased resting metabolic rate  (5.9 ± 0.1 ml O₂ ·kg^-1·day^-1) that was only 10% above the level predicted for adult terrestrial mammals. Field metabolic rate (289 ± 10 kJ·kg^-1 ·day^-1) and water influx (7.9 ± 0.9 ml·kg^-1 ·day^-1) were also among the lowest reported for any young otariid, suggesting minimized energy allocation to behavioral activity and thermoregulation. Furthermore, lean tissue degradation was dramatically reduced. High initial adiposity (>48%) and predominant reliance on lipid catabolism likely contributed to the exceptional degree of protein sparing attained. Blood chemistry supported these findings and suggested utilization of alternative fuels, such as β-hydroxybutyrate and de novo synthesized glucose from fat-released glycerol. Regardless of sex and body condition, pups tended to adopt a convergent strategy of extreme energy and lean body mass conservation that appears highly adaptive for it allows some tissue growth during the repeated episodes of prolonged fasting they experience throughout their development.

Geographical variation in bill size across bird species provides evidence for Allen's rule

Allen’s rule proposes that the appendages of endotherms are smaller, relative to body size, in colder climates, in order to reduce heat loss. Empirical support for Allen’s rule is mainly derived from occasional reports of geographical clines in extremity size of individual species. Interspecific evidence is restricted to two studies of leg proportions in seabirds and shorebirds. We used phylogenetic comparative analyses of 214 bird species to examine whether bird bills, significant sites of heat exchange, conform to Allen’s rule. The species comprised eight diverse taxonomic groups—toucans, African barbets, Australian parrots, estrildid finches, Canadian galliforms, penguins, gulls, and terns. Across all species, there were strongly significant relationships between bill length and both latitude and environmental temperature, with species in colder climates having significantly shorter bills. Patterns supporting Allen’s rule in relation to latitudinal or altitudinal distribution held within all groups except the finches. Evidence for a direct association with temperature was found within four groups (parrots, galliforms, penguins, and gulls). Support for Allen’s rule in leg elements was weaker, suggesting that bird bills may be more susceptible to thermoregulatory constraints generally. Our results provide the strongest comparative support yet published for Allen’s rule and demonstrate that thermoregulation has been an important factor in shaping the evolution of bird bills.

Physiological responses of elite junior Australian Rules footballers during match-play

Australian Football (AF) is Australia's major football code. Despite research in other football codes, to date, no data has been published on the physiological responses of AF players during match play. Fifteen athletes (17.28 ± 0.76 yrs) participated in four pre-season matches, sanctioned by Australian Football League (AFL) Victoria, investigating Heart Rate (HR), Blood Lactate (BLa), Core Temperature (Tcore), and Hydration status. Match HR was measured continuously using HR monitors. BLa was measured via finger prick lancet at the end of each quarter of play. Tcore was measured by use of ingestible temperature sensor and measured wirelessly at the end of each quarter of play. Hydration status was measured using refractometry, measuring urine specific gravity, and body weight pre and post-match. Environmental conditions were measured continuously during matches. Results of HR responses showed a high exertion of players in the 85-95% maximum HR range. Elevated mean BLa levels, compared to rest, were observed in all players over the duration of the matches (p = 0.007). Mean Tcore rose 0.68 °C between start and end of matches. Mean USG increased between 0.008 g/ml (p = 0.001) with mean body weight decreasing 1.88 kg (p = 0.001). This study illustrates physiological responses in junior AF players playing in the heat as well as providing physiological data for consideration by AF coaching staff when developing specific training programs. Continued research should consider physiological measurements under varying environments, and at all playing levels of AF, to ascertain full physiological responses during AF matches.

An increase in minimum metabolic rate and not activity explains field metabolic rate changes in a breeding seabird

The field metabolic rate (FMR) of a free-ranging animal can be considered as the sum of its maintenance costs (minimum metabolic rate, MMR) and additional costs associated with thermoregulation, digestion, production and activity. However, the relationships between FMR and BMR and how they relate to behaviour and extrinsic influences is not clear. In seabirds, FMR has been shown to increase during the breeding season. This is presumed to be the result of an increase in foraging activity, stimulated by increased food demands from growing chicks, but few studies have investigated in detail the factors that underlie these increases. We studied free-ranging Australasian gannets (Morus serrator) throughout their 5 month breeding season, and evaluated FMR, MMR and activity-related metabolic costs on a daily basis using the heart rate method. In addition, we simultaneously recorded behaviour (flying and diving) in the same individuals. FMR increased steadily throughout the breeding season, increasing by 11% from the incubation period to the long chick-brooding period. However, this was not accompanied by either an increase in flying or diving behaviour, or an increase in the energetic costs of activity. Instead, the changes in FMR could be explained exclusively by a progressive increase in MMR. Seasonal changes in MMR could be due to a change in body composition or a decrease in body condition associated with changing the allocation of resources between provisioning adults and growing chicks. Our study highlights the importance of measuring physiological parameters continuously in free-ranging animals in order to understand fully the mechanisms underpinning seasonal changes in physiology and behaviour.

A global heterothermic continuum in mammals

Aim: The ability of endotherms to physiologically regulate body temperature (Tb) is presumed to be important in the adaptive radiation of birds and mammals. Recently, attention has shifted towards determining the extent and energetic significance of Tb variation documented in an ever-expanding list of species. Thus, we provide the first global synthesis of ecological and evolutionary correlates of variation in mammalian Tb. Location: World-wide Methods: We conducted a phylogenetically informed analysis of Tb variation using two complementary metrics, namely Thermoregulatory Scope (TS) and Heterothermy Index (HI), that treat Tb variation as a continuous variable. We included morphological (e.g. body mass), ecological (e.g. food habits) and environmental (e.g. latitude) correlates in the analysis. Results: Among 560 mammal species included in the TS analysis, Tb relates most strongly to body mass (included in all models), season (relative parameter weight: 0.95), absolute latitude (0.80) and hoarding behavior (0.72), with small-bodied, high latitude and non-hoarding species expressing the most Tb variation. Small-bodied and high latitude species also express a greater range of thermoregulatory patterns than large-bodied and low latitude species. Results were generally similar in HI analysis, but in summer the extent of heterothermy decreases with latitude. Main conclusions: Mammalian heterothermy is related to evolutionary history, climate conditions constraining minimum Tb, resource conditions mediating energy supply for maintaining high Tb, and latitudinal variation in the nature of seasonality. Our analysis further shows that traditional classification of mammals as hibernators, daily heterotherms or homeotherms is clouded or possibly misleading.

Stress-induced rise in body temperature is repeatable in free-ranging Eastern chipmunks (Tamias striatus)

In response to handling or other acute stressors, most mammals, including humans, experience a temporary rise in body temperature (T b). Although this stress-induced rise in T b has been extensively studied on model organisms under controlled environments, individual variation in this interesting phenomenon has not been examined in the field. We investigated the stress-induced rise in T b in free-ranging eastern chipmunks (Tamias striatus) to determine first if it is repeatable. We predicted that the stress-induced rise in T b should be positively correlated to factors affecting heat production and heat dissipation, including ambient temperature (T a), body mass (M b), and field metabolic rate (FMR). Over two summers, we recorded both T b within the first minute of handling time (T b1) and after 5 min of handling time (T b5) 294 times on 140 individuals. The mean ∆T b (T b5 – T b1) during this short interval was 0.30 ± 0.02°C, confirming that the stress-induced rise in T b occurs in chipmunks. Consistent differences among individuals accounted for 40% of the total variation in ∆T b (i.e. the stress-induced rise in T b is significantly repeatable). We also found that the stress-induced rise in T b was positively correlated to T a, M b, and mass-adjusted FMR. These results confirm that individuals consistently differ in their expression of the stress-induced rise in T b and that the extent of its expression is affected by factors related to heat production and dissipation. We highlight some research constraints and opportunities related to the integration of this laboratory paradigm into physiological and evolutionary ecology.

Heat for nothing or activity for free? Evidence and implications of activity-thermoregulatory heat substitution

If heat generated through activity can substitute for heat required for thermoregulation, then activity in cold environments may be energetically free for endotherms. Although the possibility of activity-thermoregulatory heat substitution has been long recognized, its empirical generality and ecological implications remain unclear. We combine a review of the literature and a model of heat exchange to explore the generality of activity-thermoregulatory heat substitution, to assess the extent to which substitution is likely to vary with body size and ambient temperature, and to examine some potential macroecological implications. A majority of the 51 studies we located showed evidence of activity-thermoregulatory heat substitution (35 of 51 studies), with 28 of 32 species examined characterized by substitution in one or more study. Among studies that did detect substitution, the average magnitude of substitution was 57%, but its occurrence and extent varied taxonomically, allometrically, and with ambient temperature. Modeling of heat production and dissipation suggests that large birds and mammals, engaged in intense activity and exposed to relatively warm conditions, have more scope for substitution than do smaller endotherms engaged in less intense activity and experiencing cooler conditions. However, ambient temperature has to be less than the lower critical temperature (the lower bound of the thermal neutral zone) for activity-thermoregulatory heat substitution to occur and this threshold is lower in large endotherms than in small endotherms. Thus, in nature, substitution is most likely to be observed in intermediate-sized birds and mammals experiencing intermediate ambient temperatures. Activity-thermoregulatory heat substitution may be an important determinant of the activity patterns and metabolic ecology of endotherms. For example, a pattern of widely varying field metabolic rates (FMR) at low latitudes that converges to higher and less variable FMR at high latitudes has been interpreted as suggesting that warm environments at low latitudes allow a greater variety of feasible metabolic niches than do cool, high-latitude environments. However, activity-thermoregulatory heat substitution will generate this pattern of latitudinal FMR variation even if endotherms from cold and warm climates are metabolically and behaviorally identical, because the metabolic rates of resting and active animals are more similar in cold than in warm environments. Activity-thermoregulatory heat substitution is an understudied aspect of endotherm thermal biology that is apt to be a major influence on the physiological, behavioral and ecological responses of free-ranging endotherms to variation in temperature.

When surfacers do not dive : multiple significance of extended surface times in marine turtles

Marine turtles spend more than 90% of their life underwater and have been termed surfacers as opposed to divers. Nonetheless turtles have been reported occasionally to float motionless at the surface but the reasons for this behaviour are not clear. We investigated the location, timing and duration of extended surface times (ESTs) in 10 free-ranging loggerhead turtles (Caretta caretta) and the possible relationship to water temperature and diving activity recorded via satellite relay data loggers for 101–450 days. For one turtle that dived only in offshore areas, ESTs contributed 12% of the time whereas for the other turtles ESTs contributed 0.4–1.8% of the time. ESTs lasted on average 90 min but were mostly infrequent and irregular, excluding the involvement of a fundamental regulatory function. However, 82% of the ESTs occurred during daylight, mostly around noon, suggesting a dependence on solar radiation. For three turtles, there was an appreciable (7°C to 10.5°C) temperature decrease with depth for dives during periods when ESTs occurred frequently, suggesting a re-warming function of EST to compensate for decreased body temperatures, possibly to enhance digestive efficiency. A positive correlation between body mass and EST duration supported this explanation. By contrast, night-active turtles that exceeded their calculated aerobic dive limits in 7.6–16% of the dives engaged in nocturnal ESTs, probably for lactate clearance. This is the first evidence that loggerhead turtles may refrain from diving for at least two reasons, either to absorb solar radiation or to recover from anaerobic activity.

The role of infrequent and extraordinary deep dives in leatherback turtles (Dermochelys coriacea)

Infrequent and exceptional behaviours can provide insight into the ecology and physiology of a particular species. Here we examined extraordinarily deep (300–1250 m) and protracted (>1h) dives made by critically endangered leatherback turtles (Dermochelys coriacea) in the context of three previously suggested hypotheses: predator evasion, thermoregulation and exploration for gelatinous prey. Data were obtained via satellite relay data loggers attached to adult turtles at nesting beaches (N=11) and temperate foraging grounds (N=2), constituting a combined tracking period of 9.6 years (N=26,146 dives) and spanning the entire North Atlantic Ocean. Of the dives, 99.6% (N=26,051) were to depths <300 m with only 0.4% (N=95) extending to greater depths (subsequently termed `deep dives'). Analysis suggested that deep dives: (1) were normally distributed around midday; (2) may exceed the inferred aerobic dive limit for the species; (3) displayed slow vertical descent rates and protracted durations; (4) were much deeper than the thermocline; and (5) occurred predominantly during transit, yet ceased once seasonal residence on foraging grounds began. These findings support the hypothesis that deep dives are periodically employed to survey the water column for diurnally descending gelatinous prey. If a suitable patch is encountered then the turtle may cease transit and remain within that area, waiting for prey to approach the surface at night. If unsuccessful, then migration may continue until a more suitable site is encountered. Additional studies using a meta-analytical approach are nonetheless recommended to further resolve this matter.