Eric T. Liknes

A comparative analysis of thermogenic capacity and cold tolerance in small birds

SUMMARY Small birds showing marked seasonal changes in cold tolerance also exhibit winter increases in summit metabolic rate (Msum=maximum cold-induced thermogenesis or thermogenic capacity) relative to summer birds. However, some birds show modest seasonal changes in cold tolerance without winter increases in Msum and others exhibit large seasonal changes in cold tolerance with only minor changes in Msum. Thus, the degree of correlation between cold tolerance and Msum is uncertain and no interspecific study has directly addressed this question. In this study, we measured cold tolerance and Msum in summer- (21 species) and winter- (11 species) acclimatized birds from southeastern South Dakota. Msum was measured as the maximum oxygen consumption attained during exposure of individual birds to a declining series of temperatures in 79% helium/21% oxygen (helox). Cold tolerance was measured as the temperature at cold limit (TCL), which is the helox temperature that induced hypothermia in individual birds. Residuals from allometric regressions of logMsum and logTCL were significantly and negatively related for summer (R2=0.34, P=0.006) and winter (R2=0.40, P=0.037) birds. Data were also subjected to a comparative analyses with phylogenetically independent contrasts to remove potential confounding effects of phylogeny, and results were similar to the non-phylogenetic analyses, with significant negative correlations in both summer (R2=0.47, P<0.001) and winter (R2=0.40, P=0.049). Thus, birds with high Msum tended to show reduced TCL (i.e. high cold tolerance), suggesting that cold tolerance and summit metabolism are phenotypically linked in small birds.

Seasonal variation in cold tolerance, basal metabolic rate, and maximal capacity for thermogenesis in White-breasted Nuthatches Sitta carolinensis and Downy Woodpeckers Picoides pubescens, two unrelated arboreal temperate residents

White-breasted Nuthatches Sitta carolinensis and Downy Woodpeckers Picoides pubescens are permanent residents in areas with cold temperate climates and are ecologically similar, but belong to different taxonomic orders. We measured basal metabolic rate (BMR) and peak metabolic rate (PMR = peak rate of cold-induced thermogenesis) for wild, free-living summer and winter acclimatised White-breasted Nuthatches and Downy Woodpeckers to determine seasonal and interspecific variation in cold tolerance and thermogenic ability. Both species were more cold tolerant and had significantly higher BMR and PMR in winter than in summer. Furthermore, during midsummer (early July to mid-August), nuthatches exhibited a significant decrement in cold tolerance and PMR relative to other seasons. A winter increment of metabolism, coupled with only minor seasonal variation in body mass and fat scores in both species, indicates that both species rely more on metabolic adjustments than gross morphological adjustments for winter acclimatisation. Woodpeckers and nuthatches exhibited roughly similar BMR and PMR at both seasons. The only significant interspecific differences in metabolic rates involved per-bird PMR in winter and midsummer, per-bird BMR in winter and summer (woodpeckers > nuthatches in both cases), and mass-specific PMR in summer (early/ late summer nuthatches > summer woodpeckers). Interspecific differences in cold tolerance and metabolic rates are probably explained, at least in part, by differences in body mass, as woodpeckers were significantly larger than nuthatches at all seasons. These data indicate that White-breasted Nuthatches and Downy Woodpeckers exhibit similar thermogenic performance and major phylogenetic effects on thermoregulation are not apparent.

SEASONAL ACCLIMATIZATION IN THE AMERICAN GOLDFINCH REVISITED: TO WHAT EXTENT DO METABOLIC RATES VARY SEASONALLY?

Abstract We evaluated seasonal changes in cold tolerance, basal metabolic rate (BMR), and summit metabolic rate (Msum) for American Goldfinches (Carduelis tristis) from southeastern South Dakota to determine if goldfinches differ in pattern of metabolic acclimatization from other species of small birds. Goldfinches were captured in winter (January–February), spring (April), and summer (June–August) and tested on the day of capture. Cold exposure tests involved subjecting individual birds to a decreasing series of temperatures in an atmosphere of 79% helium to 21% oxygen (helox) concurrent with open-circuit respirometry. The helox temperature eliciting hypothermia was designated the cold limit (Tcl). Whole-animal metabolic rates were analyzed. Winter goldfinches demonstrated significantly higher BMR (46%) and Msum (31%) and significantly lower Tcl (−9.5°C vs. 1.3°C) than their summer counterparts. Spring goldfinches also showed significantly higher Msum (21%) and significantly lower Tcl (−5.3°C) than summer birds. Winter birds had higher BMR (23%) and Msum (8%) than spring birds. In winter birds, Tcl was also significantly lower than in spring birds. These data support the view that prominent winter increases in Msum and BMR are components of winter acclimatization in American Goldfinches from South Dakota and that seasonal changes in metabolism in goldfinches are similar to those for other small temperate-wintering birds. La Aclimatación Estacional en Carduelis tristis Revisitada: ¿En qué Grado Varían Estacionalmente las Tasas Metabólicas? Resumen. Evaluamos los cambios estacionales en la tolerancia al frío, la tasa metabólica basal (TMB) y la tasa metabólica pico (Mpico) en individuos de Carduelis tristis del sudeste de South Dakota para determinar si esta especie difiere de otras aves pequeñas en el patrón de aclimatación metabólica. Las aves fueron capturadas en invierno (enero–febrero), primavera (abril) y verano (junio–agosto) y sometidas a exámenes el día de captura. Los exámenes de tolerancia al frío consistieron en someter a las aves a una serie decreciente de temperaturas en una atmósfera de 79% helio y 21% oxígeno (helox) al mismo tiempo que se practicaba respirometría de circuito abierto. La temperatura que provocó hipotermia se designó como el límite de tolerancia al frío (Tfr). Se analizaron tasas metabólicas de animales completos. Las aves capturadas en el invierno presentaron TMB y Mpico significativamente mayores (46% y 31%, respectivamente) y Tfr significativamente menor (−9.5°C vs. 1.3°C) que las capturadas en el verano. Las aves de primavera también presentaron Mpico significativamente mayor (21%) y Tfr significativamente menor (−5.3°C) que las aves de verano. Las aves de invierno tuvieron mayores TMB (23%) y Mpico (8%) que las de primavera. En aves de invierno, Tfr también fue significativamente menor que en las aves de primavera. Estos datos apoyan la idea de que los incrementos invernales prominentes en Mpico y TMB son componentes de la aclimatación de invierno de C. tristis de South Dakota y que los cambios estacionales del metabolismo en esta especie son similares a los de otras aves que inviernan en la zona templada.

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.

Abundance and Richness of Neotropical Migrants During Stopover at Farmstead Woodlots and Associated Habitats in Southeastern South Dakota

Abstract Woodland habitats are scarce in the northern Great Plains and were historically concentrated along river corridors. Over the past century, riparian habitats in this area have been much reduced, but new woodland habitats in the form of farmstead woodlots and shelterbelts have appeared. We used mist net sampling and point counts to document richness and abundance of Neotropical migrant birds in farmstead woodlot habitats during spring and fall migrations (1996–1997) in southeastern South Dakota. A total of 668 individuals of 30 Neotropical migrant species (excluding the taxa Coccyzus, Troglodytes, Mimidae, Icterus and Pheucticus, in which migratory and non-migratory individuals were difficult to distinguish) was captured in 4342 net hours (using 9-m, rather than the standard 12-m mist nets) in spring. The corresponding fall totals (again using 9-m nets) were 3250 net h, 231 individuals and 29 species. If fall captures in a ragweed (Ambrosia trifida) patch occurring within the woodlot are included, however, the fall totals were 5107 net h, 1211 individuals and 29 species. Overall densities of Neotropical migrants from point counts were 1302 birds · km−2 in spring and 898 birds · km−2 in fall. Capture and point count data followed similar phenologies, with peak abundance during mid-May in spring and late August-early September in fall. Both methods indicated seasonal abundance differences for some species, with Swainsons thrush (Catharus ustulatus) and blackpoll warbler (Dendroica striata) more abundant in spring. Orange-crowned (Vermivora celata), Nashville (V. ruficapilla) and Wilsons (Wilsonia pusilla) warblers were more abundant in fall. Captures within the woodlot were evenly distributed among different microhabitats during spring migration, but fall captures occurred disproportionately in scrubby edge-related microhabitats, especially in ragweed, suggesting that seasonal shifts in microhabitat selection may occur within woodlots. Density and capture rate data were similar to previously reported values for riparian habitats in this area. Thus, a diverse assemblage of Neotropical migrants occurs in woodlots during migration, suggesting that woodlots are regularly used as stopover sites and supplement available natural woodland habitats along river corridors.

Phenotypic flexibility in passerine birds: seasonal variation in fuel storage, mobilization and transport.

Winter acclimatization in small birds living in cold climates produces a winter phenotype characterized by upregulation of metabolic rates to meet enhanced thermoregulatory demands. We measured several key aspects of fuel storage, mobilization and transport in summer and winter to determine whether black-capped chickadees (Poecile atricapillus), white-breasted nuthatches (Sitta carolinensis), and house sparrows (Passer domesticus) seasonally modulate these attributes to meet enhanced winter thermoregulatory demands. In addition, we exposed birds to thermoneutral (control) and severe cold exposure treatments to determine whether acute cold exposure influenced fuel storage, mobilization or transport. Carcass lipid mass and pectoralis intramuscular lipid did not vary significantly between seasons or temperature treatments for any of the study species. Muscle glycogen varied significantly seasonally only for chickadee supracoracoideus and leg muscles, and did not vary among warm or cold treatments for any species. Pectoralis fatty acid binding protein (FABPc) was significantly elevated in winter for chickadees and nuthatches, but not for sparrows. Plasma metabolites showed little consistent variation in response to season or acute cold exposure. Thus, fuel storage and mobilization do not appear to be major targets of adjustment associated with seasonal metabolic flexibility in these species, but modulation of intracellular lipid transport by FABPc may be an important contributor to seasonal phenotypes in some species of small birds.