Birds in the Cold BIOL 433 Environmental Physiology

Birds in the Cold BIOL 433: Environmental Physiology of Animals

The Problem • In temperate-zone or arctic climates: · Climatic conditions and environmental resources favorable in summer · Deteriorate in winter • Birds respond by two general patterns: · Migration · Permanent Residency

Winter Thermoregulation • • Cold temperatures Short days foraging Forced fast through long nights Relative scarcity of food How do birds respond to these conditions?

Cold Adaptation in Birds • Types of Adjustments – Physical – Physiological – Behavioral

Endothermic Response to Temperature Metabolic Rate Msum TNZ LCT Temperature UCT

Conductance = 1/insulation Conductance minimized at LCT

Physical Adjustments • Feathers (Insulation) – Plumage generally thicker in winter (and at higher latitudes), but plumage replaced at molt and shows wear thereafter – Not great seasonal differences, particularly for small birds – Temperature differential between skin and outside may be substantial (up to 40°C in Black-capped Chickadee)

Physical Adjustments • Subcutaneous Fat – Forms insulatory layer in only a few birds (e. g. , penguins, grouse) – Most store fat only in furcular and abdominal regions – Most small birds (esp. ground-foragers) store more fat in winter – Serve as fuel store and don’t contribute much to insulation

Furcular Fat Pectoralis Muscle Abdominal Fat

Physical Adjustments • Regional Hypothermia and Peripheral Circulation – Regions of body maintained at lower temperatures than body core – Peripheral vasoconstriction shunts blood away from body surface – Countercurrent heat exchange = closely opposed vessels allow heat exchange to keep warm blood near core (see figure) – Changes in peripheral circulation can heat loss markedly (by up to 90% through legs and feet)

Countercurrent Heat Exchange back

Physiological Adjustments • Some birds show winter increases in BMR, but others don’t. • Elevated BMR may indicate cost associated with maintaining metabolic machinery, rather than being directly adaptive.

2 BMR (ml O 2 min -1) Summer Winter 1 0 BCCH WBNU DOWO

Physiological Adjustments • Increased Summit MR and Shivering Endurance - occurs in most winter acclimatized small birds (precise mechanisms unknown) • Summit MR correlated with shivering endurance • Provides higher total capacity for heat production (4 -8 X BMR), although rarely if ever do birds reach Msum in nature.

American Goldfinch 7 6 2 0 -2 -4 5 4 3 -6 -8 -10 2 1 0 6 4 Winter April Summer -12 -14 Tcl ( C) O 2 Consumption (ml. O 2 min-1) Msum and Cold Tolerance

Msum and Thermogenic Endurance 60 Junco: R 2 = 0. 54 (P < 0. 001) Time hypo Residuals 40 20 0 -20 -40 -0. 08 -0. 04 0. 00 log M sum Residuals 0. 04 0. 08

Physiological Adjustments • How is winter increase in Msum accomplished? • Because HP in birds is mainly by shivering, changes occur in muscles. • 2 options: Increase cellular aerobic capacity or get bigger muscles – Enhanced fat catabolism capacities – Bigger muscles for shivering

All 3 muscles SCC & leg Citrate Synthase * *

* * * Pectoralis SCC Leg * HOAD

Leg PFK * * *

Wintering Birds (Pectoralis) • American Goldfinch (Marsh and Dawson 1982, Marsh et al. 1990) – CS - stable, HOAD - increase, PFK increase • House Finch (Marsh et al. 1984, Carey et al. 1989, O’Connor 1995) – CS - stable, HOAD - stable

Fatty Acid Binding Protein in Passerine Birds Pectoralis and Supracoideus Muscles H-FABP ~ 14 k. D WESA HW 3 W BW 2 S WW 9 W SDS-Page Western Blot

FABP Modulation and Seasonal Acclimatization: Results 94% P<0. 03 14 % Cytosolic Protein 12 5 5 10 8 4 4 6 4 2 0 w pect s pect w scc s scc Increased: Pectoralis

FABP Modulation and Seasonal Acclimatization: Results 6 % Cytosolic Protein 5 5 5 4 5 5 3 2 1 0 w pect s pect w scc s scc Increased: None

FABP Modulation and Seasonal Acclimatization: Results 46% P=0. 06 5 % Cytosolic Protein 4 4 5 3 2 1 0 w pect s pect w scc s scc Increased: Pectoralis

Summary: Cellular aerobic capacity changes • Intracellular lipid transport often modified • Pectoralis FABPC ↑ in 2 of 3 species tested • Cellular aerobic enzyme capacity sometimes changes • Not a consistent contributor • HOAD does ↑ in several species

Percent Winter Increase Msum Pectoralis Wet Mass 40 30 20 10 0 DEJU HOFI MOCH JUTI BCCH

Physiological Adjustments • How is winter increase in pectoralis mass accomplished? • Myostatin = A potent autocrineparacrine inhibitor of muscle growth in mammals, appears to have similar functions in birds • Our Study: Does gene expression of myostatin (and activators) vary seasonally in house sparrows?

Control vs. Myostatin Knockout Mice Belgian Blue Bull – double muscling phenotype from mutation in myostatin gene Lee (2004) Annu. Rev. Cell Devel. Biol. 20: 61 -86.

Fig. 2. Myostatin processing and receptor activation. (A) Di-sulphide bonds cause dimerisation of Myostatin. Mature region cleaved from Propeptide region. Propeptide portion forms non-covalent link to mature region. (B) Inactive Myostatin is secreted by muscle cells. (C) Proteases on muscle cells release propeptide from mature region. (D) Mature region binds type II Activin receptor. (E) Transphorylation leads to activation of type I receptor. (F) Type I receptor phosphorylates Smad 3 which facilitates translocation into nucleus where it initiates gene transcription. Patel and Amthor (2005)

Summary - House Sparrows • Msum and cold tolerance increase in winter • Pectoralis muscle mass increases in winter • Myostatin and TLL-1 gene expression decrease in winter • Consistent with a role for myostatin in regulating winter increase in muscle mass and thermogenic capacity • Regulator of muscle mass changes in other portions of annual cycle?

Physiological Adjustments • Regulated Hypothermia and Torpor – Tb normally drops 2 -3°C at night – Some birds (e. g. , chickadees) allow Tb to drop 10 -12°C below daytime levels, yet remain responsive to external stimuli (= Regulated Hypothermia) – Torpor = state of dormancy, usually occurs on a daily basis in birds, Tb may drop to temperatures near ambient (down to 5°C in some birds). Regulated at lower Tb.

Euthermic MR Torpid Tb Ambient Temperature

Physiological Adjustments • Hypothermia and torpor allow great energy savings because metabolic rate is much reduced. May reduce overnight energy expenditures by 1/3. • Torpor occurs in hummingbirds, nightjars, swifts, mousebirds, bee-eaters. • Formerly thought to be used only in cases of emergency (low food availability coupled with low temperatures), but may be more common (e. g. , saving fat for migration).

Behavioral Adjustments • Posture - decrease exposed surface area; tuck legs and bills into feathers, orient perpendicular to sun to receive maximum solar radiation • Microclimate Selection - choose roost sites that protect from the elements (cavities in trees, thick brush, subnivean space). Can reduce energy expenditure by up to 50% compared to open areas.

Plumage differences for thermoregulation during sleep

Behavioral Adjustments • Huddling - documented for several bird species. Reduces heat loss by decreasing surface area of each individual bird exposed to air (see figure). • Feeding Intensity - show greater feeding intensities during colder times of year; arctic birds active at lower light levels in winter than in summer

Behavioral Thermoregulation in Starlings back

Behavioral Adjustments • Food Caching - storing food in specific locations. – Provides a readily available food source for times when energy expenditures are high – Birds that cache generally store less fat than those that don’t (decreases flight costs) – Occurs in Acorn Woodpecker, nuthatches, corvids, chickadees and titmice