Organisms use environmental cues to time annual cycles, fine-tune
breeding and make daily behavioral decisions. In the long term,
predictable changes in photoperiod, rainfall and temperature help
organisms correctly time life history transitions to maximize fitness.
In the short term, organisms use a broader array of cues for predicting
near-term weather. Here we focus on the latter class, asking whether
sparrows use declining barometric pressure as a cue to prepare for
Storms can profoundly affect foraging success, metabolic
requirements, body condition and parental behavior. For example,
heavy rains can flood nest sites and limit foraging opportunities,
and high winds can decrease foraging efficiency and increase heat
loss. Storms can also include low temperatures and snow. Cold
temperatures can increase metabolic costs of thermoregulation
and directly threaten survival. Snow can limit activity and cover
food resources. Are there predictable components to these rapid
abiotic changes? In principle, organisms could use storm-related
cues over several time scales. The most proximate are derived
from the storm itself – increasing cloud cover, high winds, falling
temperatures and heavy precipitation. However, cues in advance
of the storm may be more useful, because they potentially give
organisms more time to prepare by appropriately altering
physiology and behavior.
One well-known predictor of impending storms is falling
barometric pressure. As inclement weather approaches, barometric
pressure can decline by 2–12kPa over 24 to 72h [depending on the
severity of the storm (Saucier, 2003)]. This phenomenon is well
documented and could be a reliable cue used by vertebrates. Studies
from a variety of taxa indicate that animals use barometric pressure
to time behavioral transitions. Frogs may call more when barometric
pressure is low and rain is likely (Brooke et al., 2000; Oseen and
Wassersug, 2002); fish move into salt marshes (possibly to forage)
as barometric pressure declines (Crinall and Hindell, 2004); and
bats and birds can sense changes in barometric pressure (Kreithen
and Keeton, 1974; Lehner and Dennis, 1971; Paige, 1995), and may
alter migratory behavior to avoid poor weather (Blokpoel and
Richardson, 1978; Cryan and Brown, 2007; Maransky et al., 1997;
Matthews and Rodewald, 2010; Panuccio et al., 2010; Pyle et al.,
1993; Sapir et al., 2011; Shamoun-Baranes et al., 2006). The
majority of studies, however, examine correlations among behavioral
patterns and naturally varying barometric pressure. Direct
manipulation of barometric pressure itself is rare.
We also do not yet understand the mechanisms by which
vertebrates integrate pressure information into physiological and
behavioral responses. One likely candidate is the endocrine system,
especially the adrenocortical axis, which is a well-known integrator
of stress information in other contexts. Endocrine systems commonly
Severe storms can pose a grave challenge to the temperature and energy homeostasis of small endothermic vertebrates. Storms
are accompanied by lower temperatures and wind, increasing metabolic expenditure, and can inhibit foraging, thereby limiting
energy intake. To avoid these potential problems, most endotherms have mechanisms for offsetting the energetic risks posed by
storms. One possibility is to use cues to predict oncoming storms and to alter physiology and behavior in ways that make
survival more likely. Barometric pressure declines predictably before inclement weather, and several lines of evidence indicate
that animals alter behavior based on changes in ambient pressure. Here we examined the effects of declining barometric pressure
on physiology and behavior in the white-crowned sparrow, Zonotrichia leucophrys. Using field data from a long-term study, we
first evaluated the relationship between barometric pressure, storms and stress physiology in free-living white-crowned sparrows.
We then manipulated barometric pressure experimentally in the laboratory and determined how it affects activity, food intake,
metabolic rates and stress physiology. The field data showed declining barometric pressure in the 12–24h preceding
snowstorms, but we found no relationship between barometric pressure and stress physiology. The laboratory study showed that
declining barometric pressure stimulated food intake, but had no effect on metabolic rate or stress physiology. These data
suggest that white-crowned sparrows can sense and respond to declining barometric pressure, and we propose that such an
ability may be common in wild vertebrates, especially small ones for whom individual storms can be life-threatening events.
Supplementary material available online at http://jeb.biologists.org/cgi/content/full/216/11/1982/DC1
Key words: activity, corticosterone, environmental cues, inclement weather, metabolic rate, stress.
Received 5 October 2012; Accepted 5 February 2013
The Journal of Experimental Biology 216, 1982-1990
© 2013. Published by The Company of Biologists Ltd
Environment, behavior and physiology: do birds use barometric pressure to
Creagh W. Breuner1,2,*, Rachel S. Sprague1,3, Stephen H. Patterson2and H. Arthur Woods2
1Wildlife Biology Program, The University of Montana, 32 Campus Drive, Missoula, MT 59812, USA,2Organismal Biology and
Ecology, The University of Montana, 32 Campus Drive, Missoula, MT 59812, USA and 3Pacific Islands Regional Office,
NOAA National Marine Fisheries Service, Honolulu Hawaii 96814, USA
*Author for correspondence (email@example.com)
THE JOURNAL OF EXPERIMENTAL BIOLOGY
1983 Storms, physiology and behavior in birds
translate environmental cues into organismal responses; for example,
elevated androgens promote migratory behavior in response to
longer days. Glucocorticoids are secreted from the adrenal gland,
and are thought to redirect physiology and behavior so that animals
can cope with deteriorating or unpredictable situations (Wingfield
and Sapolsky, 2003). From a life history perspective, glucocorticoids
are thought to redirect energy expenditures from reproduction to
self-maintenance, increasing the likelihood of survival during sub-
optimal conditions (Breuner et al., 2008; Wingfield et al., 1998).
Several lines of evidence suggest that corticosterone (CORT; the
primary avian glucocorticoid) regulates behavioral responses to
storms. Animals captured during snow and rainstorms can have
elevated CORT (Astheimer et al., 1995; Bize et al., 2010; Rogers
et al., 1993; Smith et al., 1994; Wingfield et al., 1983). Extreme
temperatures can increase circulating CORT (Bize et al., 2010; de
Bruijn and Romero, 2011; Dunlap and Wingfield, 1995; Tyrrell and
Cree, 1998). Glucocorticoids can increase activity in both laboratory
and field settings, and have been shown to increase food intake in
several vertebrates (e.g. Arvaniti et al., 1998; Astheimer et al., 1992;
Breuner et al., 1998; Breuner and Hahn, 2003; Crespi et al., 2004;
Nasir et al., 1999). And finally, glucocorticoid implants alter
responses to inclement weather in white-crowned sparrows (Breuner
and Hahn, 2003). Overall, these studies suggest that glucocorticoids
could become elevated as barometric pressure changes and storms
begin, and that rising glucocorticoids cause changes in physiology
and behavior that enable animals to withstand deteriorating
Here we examine the relationships between barometric pressure,
physiology and behavior in free-living and captive white-crowned
sparrows. In a field study of wild sparrows, we used a 7year data
set to evaluate both how much barometric pressure declines before
snowstorms, and the relationships between pressure and CORT
physiology. In a laboratory study, we exposed birds experimentally
to declining barometric pressure and evaluated changes in their
metabolic rates, foraging behavior, activity and stress physiology.
MATERIALS AND METHODS
White-crowned sparrows Zonotrichia leucophrys oriantha
Oberholser 1932 were sampled as part of a long-term field study
on stress physiology (Breuner and Hahn, 2003; Breuner et al., 2006;
Crino et al., 2011; Hahn et al., 2004; Lynn et al., 2007). White-
crowned sparrows are an ideal species to use for studies of
environment–physiology–behavior interactions. Four of the
subspecies (gambelii, oriantha, leucophrys and pugetensis) breed
in habitats where spring storms are common, and individual birds
often must redirect physiology and behavior to breed successfully
(Addis et al., 2011; Breuner and Hahn, 2003; Romero, 2002;
Wingfield et al., 1983; Wingfield and Ramenofsky, 2011). We have
studied behavioral and physiological response to spring storms in
Z. l. oriantha (the mountain white-crowned sparrow) since 1997.
Male Z. l. oriantha arrive at the high elevation breeding grounds
in early May. Females arrive ~2weeks later and often begin laying
eggs in early June (Morton, 2002). During this period, snow cover
recedes from 100 to ~50%, with frequent new snow. Birds were caught
at Tioga Pass Meadow, Inyo National Forest, CA, USA (37°54′53″N,
119°15′18″W, ~3000m elevation), with seed-baited potter traps. The
majority of blood samples were collected between early May (when
males first arrive at the breeding site) and mid-June (when nesting is
underway and we no longer use seed-baited trap lines to catch birds).
Blood was collected into heparinized capillary tubes from the alar
vein after puncture with a 26gauge needle, within 3min of disturbance
in the trap [sitting and eating in a potter trap does not alter baseline
or <30min CORT levels in white-crowned sparrows (Romero and
Romero, 2002)]. Birds were held in a cloth bag, and serial blood
samples were taken after 15 and 30min [termed a ‘stress series’ (e.g.
Wingfield, 1994)]. Blood was kept on ice until centrifuged (within
5h), and plasma was removed and frozen until assayed. CORT levels
were measured using enzyme immunoassay (EIA) as per Wada et al.
(Wada et al., 2007). All assays were completed in the Breuner
laboratory, using corticosterone EIA kits from Assay Designs (ADI-
901-097, Enzo Life Sciences, Farmingdale, NY, USA). The data
presented here are collated from over 8years of assays; on average
detectability levels were between 0.5 and 1.5ngml–1, average intra-
assay variation was 6.6%.
Barometric pressure was measured in Tuolumne Meadows,
Yosemite National Park (37.9°N, 119.4°W), by Dr Jessica Lundquist
(Department of Civil and Environmental Engineering, University
of Washington) as part of a long-term environmental study [~1km
from Tioga Pass Meadows (Lowry et al., 2010)]. Barometric
pressure was logged every 30min from 2001 to present.
To evaluate the barometric pressure change prior to snowfall, we
identified six storms from 2002 to 2008 when first snowfall was
detected at the meadow. We then graphed barometric pressure from
the previous 12+h.
To determine the relationship between barometric pressure and stress
physiology in free-living birds, we calculated the change in barometric
pressure over the 12h prior to each stress series sampled. Both baseline
CORT (endogenous level of CORT measured on capture, N=773),
and maximum CORT (highest CORT measured in response to
handling stress, N=452) were compared with the rate of barometric
pressure decline during the preceding 12h. This analysis evaluates
barometric pressure effects on both (1) resting levels of CORT and
(2) the animals’ ability to respond to subsequent stressors.
Barometric pressure versus mass and fat scores
If sparrows respond to approaching storms by eating more, they
may also gain mass or fat. However, it is also possible that the
declining environmental conditions would require greater energy
expenditure to maintain body temperature. We evaluated the
direction of the relationship between barometric pressure change
and mass or fat scores using linear mixed-effects (lme) models
(Pinheiro and Bates, 2000), with days before the first egg lay of the
season as a covariate, and individual ID as a random factor (R2.11.1,
White-crowned sparrows Zonotrichia leucophrys leucophrys
(Forster 1772) were caught in seed-baited potter traps at the Center
for Environmental Research at Hornsby Bend in Travis County, TX
(30°20′00″N, 97°48′00″W). Birds were captured during February
and March 2005 (N=6) for experiments completed in April and May
2005, and during February and March 2006 (N=8) for experiments
completed in April and May 2006. Birds were brought into captivity
and housed in individual cages (33×38×43cm) on an 8h:16h
light:dark cycle for at least 3weeks before the experiment began.
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