Sheldon J. Cooper

Seasonal Acclimatization of Thermoregulation in the Black-Capped Chickadee

Black-capped Chickadees (Parus atricapillus) show behavioral adaptations (food caching, cavity roosting) and can undergo regulated bouts of nocturnal hypothermia, both of which reduce costs associated with wintering in temperate latitudes. These adjustments could reduce the need for the seasonal metabolic adjustments found in other small passerines that must deal with severe winter cold. We have examined this possibility by determining the extent of seasonal variation evident in chickadees concerning standard metabolic rate, metabolic response to temperature, cold resistance, and maximal thermogenic capacity (Vo2sum). Regression equations relating metabolism to air temperature below thermoneutrality did not differ significantly in either slope or Y-intercept between summer and winter, and neither did minimum thermal conductance for normothermic birds vary seasonally. Seasonal constancy in these parameters demonstrates the minor role that seasonal changes in insulation play in acclimatization in chickadees. However, winter birds tolerated cold stress far better than summer birds. This improved cold tolerance was associated with a significant increase in Vo2sum (36%) in winter relative to summer. Standard metabolic rates (SMR) were also significantly increased in winter birds compared to summer birds. Thus, Black-capped Chickadees show seasonal metabolic acclimatization similar to, or greater than, other temperate wintering passerines in addition to behavioral adaptations and nocturnal hypothermia.

Seasonal Metabolic Acclimatization in Mountain Chickadees and Juniper Titmice

Mountain chickadees and juniper titmice from northern Utah were examined to determine metabolic and body‐composition characteristics associated with seasonal acclimatization. These species use behavioral adaptations and nocturnal hypothermia, which reduce energetic costs. These adjustments could reduce the need for extensive metabolic adjustments typically found in small passerines that overwinter in cold regions. In addition, these species live at higher altitudes, which may also decrease metabolic acclimatization found in birds. Winter birds tolerated colder test temperatures than summer birds. This improved cold tolerance was associated with an increase in maximal thermogenic capacity or summit metabolism (Msum). Winter Msum exceeded summer Msum by 26.1% in chickadees and 16.2% in titmice. Basal metabolic rates (BMR) were also significantly higher in winter birds compared with summer birds. Pectoralis wet muscle mass increased 33.3% in chickadees and 24.1% in titmice in winter and paralleled the increased Msum and BMR. Dry mass of contour plumage increased in winter for both species and was associated with decreased thermal conductance in winter chickadees compared to summer chickadees. Chickadees and titmice show metabolic acclimatization similar to other temperate species.

The thermal and energetic significance of cavity roosting in Mountain Chickadees and Juniper Titmice

I examined the thermal and energetic benefits of cavity roosting in summer and winter-acclimatized Mountain Chickadees (Poecile gambeli) and Juniper Titmice (Baeolophus griseus). Reduction of wind speed inside the cavity increased standard operative temperature 2.5 to 5.9°C compared to the open sites in summer and 12.1 to 14.7°C in winter. Nocturnal energy savings ranged from 23.8 to 27.9% for summer birds and 25.1 to 37.6% for winter birds roosting in cavities. Wind speed was significantly lower inside cavities compared to open sites. These energy savings result in increased fasting endurance of 2.2 to 3 hr in summer and 5.7 to 7.3 hr in winter, which may be critically important for survival throughout the annual cycle for these two species.

The relationship of metabolic performance and distribution in black-capped and Carolina chickadees.

In endotherms, metabolic performance is associated with a wide array of ecological traits, including species distribution. Researchers have suggested that the northern boundaries of North American passerines are limited by their ability to sustain the high metabolic rates required for thermoregulation. Black‐capped chickadees (Poecile atricapillus; BC) are year‐round residents in most of Canada and the northern half of the United States, whereas Carolina chickadees (Poecile carolinensis; CA) are found exclusively in the southeastern United States. These species hybridize along a narrow contact zone that has been moving northward at a rate of about 1.6 km per decade, coincident with warming temperatures in Ohio. The location of the chickadee hybrid zone in Ohio closely matches air temperature isotherms, further suggesting that metabolic rate may correlate with distribution in these species. We tested the hypothesis that distribution patterns of chickadees are linked with their rate of metabolism. For populations of BC and CA chickadees, we measured basal metabolic rates (BMRs) and cold‐induced peak metabolic rates from areas that differ in winter temperatures and supplemented this information with data from other studies. Although our findings suggest a general relationship between lower air temperatures and higher metabolic rate among black‐capped chickadee populations, this trend was not robust across all locations. There was no significant relationship between lower air temperatures and metabolism in Carolina chickadees. Within Ohio, hybrids had a significantly higher mass‐corrected BMR than either parental species. We suggest that the mtDNA‐nDNA mismatch of hybrids may produce less efficient mitochondrial protein complexes, which in turn affects the efficiency of ATP production, thereby increasing rate of oxygen consumption to meet ATP demands.

Intraspecific Correlations of Basal and Maximal Metabolic Rates in Birds and the Aerobic Capacity Model for the Evolution of Endothermy

The underlying assumption of the aerobic capacity model for the evolution of endothermy is that basal (BMR) and maximal aerobic metabolic rates are phenotypically linked. However, because BMR is largely a function of central organs whereas maximal metabolic output is largely a function of skeletal muscles, the mechanistic underpinnings for their linkage are not obvious. Interspecific studies in birds generally support a phenotypic correlation between BMR and maximal metabolic output. If the aerobic capacity model is valid, these phenotypic correlations should also extend to intraspecific comparisons. We measured BMR, Msum (maximum thermoregulatory metabolic rate) and MMR (maximum exercise metabolic rate in a hop-flutter chamber) in winter for dark-eyed juncos (Junco hyemalis), American goldfinches (Carduelis tristis; Msum and MMR only), and black-capped chickadees (Poecile atricapillus; BMR and Msum only) and examined correlations among these variables. We also measured BMR and Msum in individual house sparrows (Passer domesticus) in both summer, winter and spring. For both raw metabolic rates and residuals from allometric regressions, BMR was not significantly correlated with either Msum or MMR in juncos. Moreover, no significant correlation between Msum and MMR or their mass-independent residuals occurred for juncos or goldfinches. Raw BMR and Msum were significantly positively correlated for black-capped chickadees and house sparrows, but mass-independent residuals of BMR and Msum were not. These data suggest that central organ and exercise organ metabolic levels are not inextricably linked and that muscular capacities for exercise and shivering do not necessarily vary in tandem in individual birds. Why intraspecific and interspecific avian studies show differing results and the significance of these differences to the aerobic capacity model are unknown, and resolution of these questions will require additional studies of potential mechanistic links between minimal and maximal metabolic output.

DAILY AND SEASONAL VARIATION IN BODY MASS AND VISIBLE FAT IN MOUNTAIN CHICKADEES AND JUNIPER TITMICE

Abstract Diurnal variations in body mass and visible fat scores were measured for seasonally acclimatized Mountain Chickadees (Poecile gambeli) and Juniper Titmice (Baeolophus ridgwayi) to examine if they undergo winter fattening. Body mass varied with time of day and was highest in evening for both species in summer and winter. Body mass, expressed as percent mass increase from morning to evening, was 7.3% for summer chickadees, 7.6% for summer titmice, 9.1% for winter chickadees, and 6.1% for winter titmice. Body mass was not significantly higher in winter-acclimatized birds compared to summer-acclimatized birds. Visible fat scores were significantly elevated in winter-acclimatized Mountain Chickadees relative to summer. Mountain Chickadees and Juniper Titmice appear to have seasonally constant body mass rather than undergoing winter fattening. These data are similar to other North American species in the family Paridae but contrast with data on European parids.

SEASONAL AND DIURNAL VARIATION IN METABOLISM AND VENTILATION IN HOUSE SPARROWS

Abstract Passerines that are year-round residents in temperate climates undergo seasonal acclimatization that facilitates maintenance of thermoregulatory homeostasis. These changes in thermoregulatory metabolism must be supported by equivalent changes in oxygen transport. We measured the effects of ambient temperature and time of day on metabolism and ventilation in House Sparrows (Passer domesticus) in summer and winter. House Sparrows were exposed to ambient temperatures (Ta) ranging from −12°C to 15.5°C in summer and 17.5°C in winter. Open-circuit respirometry was used to measure oxygen consumption (V̇O2) and ventilation was recorded using whole-body plethysmography. In both summer and winter, V̇O2 increased with decreasing Ta. V̇O2 was significantly higher during the active phase compared to the resting phase of the daily cycle in both summer and winter. Thermal conductance was significantly lower in nighttime birds compared to daytime birds. With increased oxygen demands, minute volume (V̇I) increased in both summer and winter. In summer, only respiratory frequency (f) was significantly affected by time of day. In winter, active-phase birds had significantly higher respiratory frequency and minute volume (V̇I) than rest-phase birds. Winter birds in their rest phase had significantly higher oxygen extraction efficiency (EO2) than active-phase birds. Winter birds at rest phase also had significantly higher EO2 than summer birds. Variación Estacional y Diaria en el Metabolismo y la Ventilación en Passer domesticus Resumen. Las aves paserinas que residen a lo largo del año en climas de la zona templada pasan por un proceso de aclimatación estacional que facilita el mantenimiento de su homeostasis termorregulatoria. Estos cambios en el metabolismo termorregulatorio deben estar apoyados por cambios equivalentes en el transporte de oxígeno. En este estudio medimos los efectos de la temperatura del ambiente y la hora del día sobre el metabolismo y la ventilación en Passer domesticus en verano e invierno. Las aves fueron expuestas a temperaturas ambiente (Ta) en un rango de −12°C a 15.5°C en el verano, llegando a 17.5°C en el invierno. Empleamos respirometría de circuito abierto para medir el consumo de oxígeno (V̇O2) y registramos la ventilación usando pletismografía de cuerpo entero. Tanto en el verano como en el invierno, V̇O2 aumentó con disminuciones en Ta. V̇O2 fue significativamente mayor durante la fase activa en comparación con la fase de descanso del ciclo diario, tanto en verano como en invierno. La conductancia térmica fue significativamente menor en aves estudiadas en la noche que en aves estudiadas durante el día. Con incrementos en la demanda de oxígeno, el volumen minuto (V̇I) aumentó en verano y en invierno. En verano, sólo la frecuencia respiratoria (f) fue afectada por la hora del día. En invierno, la frecuencia respiratoria y el volumen minuto (V̇I) fueron significativamente mayores en las aves en fase activa que en las aves en fase de descanso. Las aves de invierno en su fase de descanso presentaron una eficiencia de extracción de oxígeno (EO2) siginificativamente mayor que la de las aves en fase activa. La EO2 de las aves de invierno en fase de descanso también fue significativamente mayor que la de las aves de verano.

HEAT PRODUCTION FROM FORAGING ACTIVITY CONTRIBUTES TO THERMOREGULATION IN BLACK-CAPPED CHICKADEES

Abstract We measured metabolic heat production (H ˙m) of perching and foraging Black-capped Chickadees (Poecile atricapillus) to determine if the heat produced during foraging activity, or exercise thermogenesis, could replace thermoregulatory heat production requirements. H ˙m and activity of chickadees in winter were measured at ambient temperatures (Ta) ranging from −11.5° to 15.5°C. Mean activity amplitude recorded with an activity detector was significantly higher in foraging birds than perching birds. H ˙m did not vary significantly between perching and foraging birds, indicating that heat produced during foraging does substitute for heat produced by shivering for thermoregulation. Evaporative water loss and dry thermal conductance did not vary significantly between perching and foraging chickadees. These results suggest that heat produced from locomotor muscles during foraging activity substitutes for thermoregulatory requirements in glean-and-hang foraging species, such as chickadees, as well as in ground-foraging birds.

THERMOREGULATION AND HABITAT PREFERENCE IN MOUNTAIN CHICKADEES AND JUNIPER TITMICE

Abstract The Mountain Chickadee (Poecile gambeli) and the Juniper Titmouse (Baeolophus ridgwayi) are closely related, ecologically similar passerines sympatric in portions of their range. However, Mountain Chickadees prefer higher altitude, cooler habitats than Juniper Titmice. We measured oxygen consumption, evaporative water loss, body temperature, and thermal conductance on seasonally acclimatized individuals to determine if thermoregulatory differences correlate with habitat preference. The Mountain Chickadees lower critical temperature was 4.2°C lower than the Juniper Titmouses in summer and 2.4°C lower in winter. Thermal conductance decreased significantly in winter relative to summer in Mountain Chickadees but not in Juniper Titmice. The Mountain Chickadees upper critical temperature was 4.2°C lower than the Juniper Titmouses in summer. Also in summer, Mountain Chickadees had significantly higher body temperature above the upper critical temperature than Juniper Titmice, indicating less heat tolerance. The overall metabolic response to temperature in these two species suggests that physiology plays a role in maintaining their habitat segregation. Termo-regulación y preferencia de hábitat en Poecile gambeli y Baeolophus ridgwayi Resumen. Las aves paserinas Poecile gambeli y Baeolophus ridgwayi, cercanamente emparentadas y ecológicamente similares, se distribuyen de modo simpátrico en partes de sus rangos. Sin embrago, P. gambeli prefiere ambientes más elevados y frescos que B. ridgwayi. Medimos el consumo de oxígeno, la pérdida de agua por evaporación, la temperatura corporal y la conductancia térmica en individuos aclimatados estacionalmente para determinar si las diferencias en termo-regulación se correlacionan con la preferencia de hábitat. La temperatura crítica menor de P. gambeli fue 4.2°C más baja que la de B. ridgwayi en el verano y 2.4°C más baja en el invierno. La conductancia térmica disminuyó significativamente en el invierno en relación al verano en P. gambeli pero no en B. ridgwayi. La temperatura crítica mayor de P. gambeli fue 4.2°C más baja que la de B. ridgwayi en el verano. También en el verano, P. gambeli tuvo una temperatura corporal significativamente mayor, por arriba del límite superior de temperatura crítica, que la de B. ridgwayi, indicando menor tolerancia al calor. La respuesta metabólica global a la temperatura en estas dos especies sugiere que la fisiología juega un rol importante en mantener la segregación de sus ambientes.

Resting Metabolic Rates of Adult Northern Shrikes (Lanius excubitor) Wintering in Northern Wisconsin

ABSTRACT Resting metabolic rate (RMR) represents a significant component of an animal’s energy budget and is correlated with ecological, physiological, and life-history parameters. We measured resting metabolic rates of 14 adult Northern Shrikes (Lanius excubitor) wintering in northern Wisconsin (Ashland and Bayfield Counties) over a 2-year period (Jan–Apr 2008 and 2009). The average (±SE) RMR was 3.09 ± 0.45 ml O2/g/hr (range 2.46–3.83) from the first reported RMR values for adults of this species from the Neartic. Our RMR values were 50% higher than RMRs gathered from summer adult Northern Shrikes in the Paleartic. These data suggest Northern Shrikes exhibit seasonal variation in their RMR as a potential means of winter acclimatization.