Functional Ecology
Appendix S1. Calibration of Skin and Core Body Temperatures in song sparrows
(Melospiza melodia)
Experimental Methods and Statistical Analysis
To determine whether a song sparrow’s skin temperature accurately predicts its
core body temperature, and thus fever, we performed an experiment in aviaries exposed
to natural variations in ambient temperature. Three adult male song sparrows were
captured near Princeton, NJ during December of 2008 and housed in individual cages
(55x25x25cm), which were placed in outdoor aviaries at Princeton University. Aviaries
were exposed to natural ambient temperatures, but sheltered from sun and rain, and
sheltered from wind on three sides.
After one week of acclimation to captivity, each bird was fitted with an external
temperature sensing radio transmitter (model # LB-2NT, 0.51g, Holohil Systems, Ltd.,
Carp, Ontario, Canada), as described in the main methods section. In addition, each bird
was implanted with an internal temperature sensing radio transmitter (model # BD2NTH, 0.61g, Holohil Systems, Ltd., Carp, Ontario, Canada) using the methods of
Clemens (1989), with slight modification. Briefly, birds were anesthetized using
isoflurane mixed with air and restrained with rubber bands to a small wooden board.
Then, following a procedure similar to that for laparotomy (Wingfield & Farner 1976), a
small (ca. 1cm) incision was made into the lateral abdominal wall, exposing the
peritoneum (Reinertsen 1982; Clemens 1989; Waite 1991). The activated internal
transmitter was then placed inside the peritoneum and the wound closed using Vetbond
surgical adhesive (3M, St. Paul, MN, USA). Birds were allowed to recover for one day
before any data collection.
Adelman et al. Radio telemetry reveals variation in fever and sickness behaviours with
latitude in a free-living passerine.
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To determine the correlation between core and skin temperature in the shade, we
monitored both transmitters remotely using an automated receiver (model # 10-1000,
Sparrow Systems, Champaign-Urbana, IL) and a directional, 4-element Yagi-Uda
antenna over one or two consecutive days and nights. The receiver recorded 3 data points
per minute. To asses the effect of direct sunlight on this correlation, we placed all three
cages outside of the aviary in direct sunlight for two hours and monitored temperature in
the same manner. Ambient temperature was recorded in the shade using temperature
loggers (model # H08-004-02, Onset Computer Corp., Bourne, MA, USA). During shade
observations, ambient temperatures ranged from -1.1˚C to 21.7˚C. During direct sunlight
observations, ambient temperatures measured in the shade ranged from 9.0˚C to 12.2˚C.
As in the main methods section, we omitted any data points where the signal strength of
the transmitter came within 2dB of the background noise level (ca. -123dB).
We assessed the relationship between skin and core temperature when birds were
housed in the shade and in direct sunlight using linear mixed effects models in R version
2.7.1 (R Development Core Team, Vienna, Austria) (Pinheiro & Bates 2000). We used
maximum likelihood estimators, Treatment contrasts, and included random effects for
each bird and each day on which that individual bird was sampled. Interactions among
fixed effects were removed by backwards elimination as in the main paper. First, we
asked whether the slope of the relationship between skin and core temperature differed
among individuals. To do this we compared models using core temperature as the
dependent variable and skin temperature as the independent variable with and without
random effects for the slope of this relationship for each bird. Additional fixed effects in
the model included the following two binary variables and their 2-way interactions with
Adelman et al. Radio telemetry reveals variation in fever and sickness behaviours with
latitude in a free-living passerine.
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skin temperature: sun (sunny or shady) and overall temperature (whether ambient
temperature was always above 10C or always below 10C for the sampling day/night).
To further assess whether the slope of the relationship between core and skin
temperature changed with ambient temperature, we ran a separate linear mixed effects
model using the ratio of skin temperature:core temperature as the dependent variable and
ambient temperature as the independent variable. Additional fixed effects in this model
were (sunny or shady), overall temperature (whether ambient temperature was always
above 10C or always below 10C for the sampling day/night), and their 2-way interactions
with ambient temperature. Interactions among fixed effects terms were removed by
backwards elimination as above. To control for auto-correlation with respect to time, we
used only one data point every 30 minutes and incorporated an exponential correlation
structure with no nugget effect into our models. This correlation structure was chosen
using AIC values in the same manner as in the main methods.
Results
When housed in the shade, birds showed a tight correlation between temperature
measured at the skin and core (Fig. S1). A linear mixed effects model shows that core
temperature increased by 1.08°C for every 1°C increase in skin temperature when birds
were housed in the shade (Table S1). A comparison of models with and without random
effects for slope showed that the slope of this relationship did not differ among
individuals or sampling days (Log-likelihood ratio = 3.09x10-8, P > 0.99). Intercepts did,
however, differ significantly among birds (comparison of models with and without
random effects for intercept: Log-likelihood ratio = 43.10, P < 0.001). The marginally
Adelman et al. Radio telemetry reveals variation in fever and sickness behaviours with
latitude in a free-living passerine.
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significant Warm Day / Cold Day term in Table S1A suggests that the difference in
intercepts among birds may be partially explained by whether or not the ambient
temperature was always above 10°C. When birds are housed in the sun, the slope of the
relationship between skin and core temperatures is no longer near 1, but rather near 0
(Skin Temperature x Sun/Shade term in Table S1A). Taken together, these results
suggest that while skin temperature does not necessarily predict absolute core
temperature, changes in skin temperature very accurately reflect changes in core
temperature when individuals are in the shade (or after sunset).
Furthermore, the model predicting the ratio between skin and core temperature
shows that within each sampling day, ambient temperature does not change the
relationship between skin and core temperature when birds are housed in the shade (Fig.
S1B, Table S1B). As with the models above, a comparison of models with and without
random effects for slope showed that this the slope of this relationship does not differ
among individuals or sampling days (Log-likelihood ratio = 0.74, P > 0.86). Again,
however, intercepts did differ significantly among birds (comparison of models with and
without random effects for intercept: Log-likelihood ratio = 45.48, P < 0.001). The nonsignificant contribution of the Warm Day / Cold Day term to the model suggests that this
difference in intercept among birds was not explained by differences in ambient
temperature. Differences in intercepts may reflect differences in the final position of
internal transmitters, as these may have migrated closer to or further from the skin
surface in different individuals.
Adelman et al. Radio telemetry reveals variation in fever and sickness behaviours with
latitude in a free-living passerine.
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References
Clemens, D.T. (1989) Nocturnal hypothermia in rosy finches. The Condor 91, 739-741.
Pinheiro, J.C. & Bates, D.M. (2000) Mixed-effects models in S and S-PLUS. Springer,
Berlin.
R Development Core Team (2008) R: A Language and Environment for Statistical
Computing, version 2.7.1. Vienna, Austria. http://www.R-project.org.
Reinertsen, R.E. (1982) Radio telemetry measurements of deep body temperature of
small birds. Ornis Scandinavica 13, 11-16.
Waite, T.A. (1991) Nocturnal hypothermia in gray jays Perisoreus canadensis wintering
in interior Alaska. Ornis Scandinavica 22, 107-110.
Wingfield, J.C. & Farner, D.S. (1976) Avian endocrinology: Field investigations and
methods. Condor 78, 570-573.
Adelman et al. Radio telemetry reveals variation in fever and sickness behaviours with
latitude in a free-living passerine.
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Table S1. Fixed effects parameters from the best-fit linear mixed models describing the
relationship between skin temperature and core temperature every half hour among
captive song sparrows housed outside. A total of three birds were monitored, all for at
least one day and night in the shade and one separate morning in the sun. One bird was
monitored for two days and nights in the shade.
A. Dependent Variable: Core Temperature
Parameter
Estimate
SE
Df
t
P -value
Intercept
0.48
0.80
194
0.59
0.55
Skin Temperature
1.08
0.19
194
58.0
<0.001 *
Sun/Shade
46.77
3.91
2
11.96
0.007 *
Warm/Cold Day
-1.50
0.47
2
-3.17
0.09
Skin Temperature x Sun/Shade
-1.11
0.094
194
-11.84
<0.001 *
B. Dependent Variable: Skin Temperature / Core Temperature
Parameter
Estimate
SE
Df
t
P -value
Intercept
0.93
9.4x10-3
194
98.04
<0.001 *
Ambient Temperature
-2.8x10-4
2.8x10-4
194
0.99
0.32
Sun/Shade
0.10
0.015
2
6.58
0.02 *
Warm/Cold Day
0.02
8.2x10-3
2
2.44
0.13
Skin Temperature x Sun/Shade
-0.01
1.2x10-4
194
-8.13
<0.001 *
Adelman et al. Radio telemetry reveals variation in fever and sickness behaviours with
latitude in a free-living passerine.
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Figure S1. The relationship between skin and core body temperature in song sparrows.
A. Core body temperature varies directly with skin temperature in the shade, but not
sunlight for song sparrows housed outside in individual cages. Intercepts differ in the
shade, showing that skin temperature does not accurately predict absolute core
temperature differences among birds. However, because slopes from a linear mixed
effects model (LME) do not vary among birds in the shade, changes in skin temperature
accurately predict changes in core temperature in the shade. B. Similarly, the relationship
between skin temperature and core body temperature (skin/core) remains constant
regardless of ambient temperature in the shade, but is less predictable in direct sunlight.
Adelman et al. Radio telemetry reveals variation in fever and sickness behaviours with
latitude in a free-living passerine.
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