Metabolic response to wind of downy chicks of Arctic-breeding shorebirds (Scolopacidae)
1 Department of Life Sciences, Indiana State University, Terre Haute,
Indiana 47809, USA
2 Department of Evolution, Ecology and Organismal Biology, Ohio State
University, 1735 Niel Avenue, Columbus, Ohio 43210-1293, USA
3 Department of Biology, University of Missouri St Louis, 8001
Natural Bridge Road, St Louis, Missouri 63121-4499, USA
* Author for correspondence (e-mail: LSGSB{at}scifac.indstate.edu)
Accepted 12 August 2002
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Summary |
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Key words: shorebird, thermoregulation, wind speed, conductance, insulation, standard operative temperature, metabolism, evaporative water loss, down, least sandpiper, Calidris minutilla, short-billed dowitcher, Limnodromus griseus, whimbrel, Numenius phaeopus
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Introduction |
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Because downy chicks are poorly insulated compared to adults
(McNabb and McNabb, 1977;
Taylor, 1986
;
Visser, 1998
), foraging and
thermoregulation costs are high, accounting for 25-30% of the total energy
budget (Schekkerman and Visser,
2001
). Moreover, foraging requires physiological maturity of
muscle tissue for effective locomotion and thermoregulation, while rapid
growth is typically associated with physiological immaturity
(Ricklefs et al., 1994
;
Visser and Ricklefs, 1995
;
Starck and Ricklefs, 1998
;
Krijgsveld et al., 2001
). This
conflict limits the peak metabolic rate of young chicks.
Thus, foraging chicks often cannot, or at least do not, maintain a stable
body temperature (Tb). Chicks of some species can continue
foraging until Tb falls as low as 30°C
(Norton, 1973), but
nevertheless parental brooding eventually becomes necessary. Because brooding
prevents foraging by both the chicks and the brooding parent, adverse weather
can depress growth (Beintema and Visser,
1989a
; Schekkerman et al.,
1998
; Schekkerman and Visser,
2001
). To understand the behavior, physiology and energetics of
Arctic breeding one must therefore relate foraging time and thermoregulatory
costs to thermal conditions. Given the scarcity of shelter on the tundra, wind
is likely to be a significant factor in the cost of Arctic shorebird
thermoregulation (Piersma and Morrison,
1994
; Wiersma and Piersma,
1994
). Although some authors have remarked that down seems rather
sensitive to wind (Taylor,
1986
; Visser,
1998
), the effect of wind on downy chicks has received but limited
attention (Bakken et al.,
1999
), and no data are available on shorebird chicks.
We measured oxygen consumption in relation to temperature and wind speed in
downy scolopacid chicks of different ages varying in mass by an order of
magnitude. Chicks were from species with small, medium and large adults: least
sandpipers Calidris minutilla (approx. 20-30 g), shortbilled
dowitchers Limnodromus griseus (approx. 100-130 g) and whimbrels
Numenius phaeopus (approx. 300-400 g). Heat loss from the legs and
bill during cold stress is minimized by countercurrent heat exchange in a wide
range of species (Ederstrom and Brumleve,
1964; Steen and Steen,
1965
; Kilgore and
Schmidt-Nielsen, 1975
; Hagan
and Heath, 1980
;
Midtgård, 1980
).
Consequently, the variation in relative leg and bill length of growing
shorebird chicks of different species is probably unimportant. As their
morphology is otherwise similar, we describe thermoregulatory responses by a
single allometric model. We also use our data to define a standard operative
temperature (Tes) scale that may be useful in field
studies of shorebird chick behavior and energetics. Standard operative
temperature is the temperature of a standard respirometer with essentially no
wind, within which the same animal would have the same net heat production
(Bakken, 1976
,
1992
).
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Materials and methods |
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Experiments were begun when body mass was equal to or greater than 9 g (approx. 7 days post-hatching) for least sandpipers (N=4), 20 g (5 days) for dowitchers (N=8), and 63 g (7 days) for whimbrels (N=4). Studies were continued until contour feathers began to appear, at which time body mass was less than 18 g (14 days) for least sandpipers, 56 g (19 days) for dowitchers and 109 g (11 days) for whimbrels.
Body temperature
We measured Tb at 1 min intervals to within
±0.1°C with a 36AWG (0.13 mm conductors, 0.14 mmx0.69 mm
overall) Teflon®-insulated duplex thermocouple (type TT, Omega
Engineering, Stamford, CT, USA). We looped one full turn of the wire through
the thread holes of a clothing button, cemented it in place with the sensing
junction extending 1-2.5 cm beyond the button, and rounded the sensing
junction with a drop of epoxy cement. We matched button diameter and probe
length to the size of the chick. At the time of the experiment, we lubricated
the sensing junction with petroleum jelly, and inserted it into the cloaca. We
then secured the assembly by folding several nearby feathers over the button
and gluing them to the button with cyanoacrylate adhesive. At the end of the
experiment, the glue was dissolved with acetone to release the feathers so
that the thermocouple could be removed. Because some down was lost each time,
we limited body temperature measurements to approximately 40% of our runs to
avoid increasing normal rates of heat loss. We monitored
Tb during the first experiments in each size class to
avoid conditions leading to hypothermia. We also monitored
Tb on a random sample of chicks thereafter.
Experimental conditions
Our experimental conditions excluded solar radiation and simulated the
cold, windy conditions experienced by chicks during storms, heavy overcast
days, or the brief Arctic night. Our small-volume wind tunnel metabolism
chamber was limited to winds of speeds less than 3.5 ms-1
(Bakken et al., 1989). However,
this range of wind speed is sufficient to determine the quantitative trend of
wind effects. Further, wind speed varies logarithmically with height
(Campbell et al., 1980
), such
that wind measured at 10 cm height over tundra is only 20-35% of that measured
3 m above the surface (G.S.B., unpublished data from four tundra sites near
the Churchill Northern Studies Centre). Thus, our data can be used directly
with standard wind speeds up to 8-15 ms-1 (30-50 km
h-1). Finally, internal temperature gradients and peak metabolic
rates vary with body temperature, which complicates accurate measurements of
thermal conductance on cooling animals
(Eppley, 1994
;
O'Conner, 1999
). Consequently,
we used experimental air temperatures chosen such that chicks were
normothermic but below their lower critical temperature at all wind
speeds.
Gas exchange
We measured oxygen consumption and evaporative water loss at four wind
speeds (u; 0.1, 0.8, 1.8 and 3.0 ms-1) and at least two
air temperatures (Ta) between 15° and 30°C, the
exact value of Ta depending on the age and mass of the
chick. Procedures generally follow those detailed in earlier studies (Bakken
et al., 1991,
1996
), with some changes in
instrumentation. We measured oxygen consumption using an open-circuit system
supplied with dry, CO2-free, outdoor air at 1.11 min-1,
measured using a precision rotameter (Brooks Full View, Emerson Electric,
Hatfield, PA, USA) calibrated on-site against a bubble meter
(Levy, 1964
). We measured the
oxygen content of a dry, CO2-free subsample (200 ml
min-1) of chamber air with an electrochemical oxygen analyzer
(FC-1, Sable Systems, Henderson, NV, USA) and the water vapor density of a
separate subsample (200 ml min-1) using a dewpoint hygrometer (880,
EG&G, Waltham, MA, USA). We corrected all values to standard temperature
and pressure (STP) using an electronic readout barometric pressure transducer
(Model 2014-27/31.5, YSI Instruments, Yellow Springs, OH, USA). We calibrated
fan-shaft revs min-1, measured with a dedicated phototachometer,
against wind speed, measured with a Prandtl-design Pitot tube and electronic
hook gauge (Dwyer Instruments, Michigan City, IN, USA). We measured various
temperatures with copper-constantan thermocouples (type TT, Omega Engineering,
Stamford, CT, USA). A digital data logger (CR-21X, Campbell Scientific, Logan,
UT, USA) recorded Ta, Tb and rotameter
temperature, analyzer outputs and fan revs min-1. Control outputs
were used to automatically step through a predetermined randomized sequence of
wind speeds and switch a solenoid valve at 1 min intervals to alternate sample
and reference gas flow to the FC-1 for continuous baseline correction. The
FC-1 equilibrated within 40s of switching, including washout time for the
analyzer gas scrubbers. We used Z-transform methods to compute `instantaneous'
oxygen consumption and evaporative water loss for each 2 min sample interval
(Bartholomew et al., 1981
;
Bakken, 1991a
).
After weighing the chick, we installed the cloacal thermocouple and placed
it in the chamber, before allowing 30 min for it to recover from handling. We
then conducted measurements for 30 min at each wind speed. At the end of the
run, we removed the thermocouple, reweighed the chick, and returned it to its
box no more than 3.5 h after it was first removed. Because we needed to
maintain normal growth patterns while making maximum use of a limited number
of chicks, we made no attempt to ensure that chicks were post-absorptive.
Consequently, the respiratory exchange ratio may have varied during the run.
The order of wind speeds was randomized during each series to minimize any
resulting bias in our estimates of the effect of wind on heat loss. Total
chick metabolism included basal, thermoregulatory and active metabolism, the
heat increment of feeding (SDA) and growth. We assumed full thermoregulatory
substitution of all forms of metabolic heat production, which may or may not
be correct (Hart, 1952;
Paladino and King, 1984
;
Klaassen et al., 1989
;
Webster and Weathers, 1990
;
Zerba and Walsberg, 1992
;
Zerba et al., 1999
).
Data analysis
Data were converted to heat production M (W) and evaporative
cooling E (W), assuming 20.08 J ml-1 O2
consumed and 2427 J g-1 H2O evaporated. We discarded all
data from chicks that became hypothermic during the experiment
(Tb<37°C). Also, data points identified as outliers
(studentized residuals >3) in a preliminary multiple-regression model were
further scrutinized, and the entire run was discarded if there was evidence of
hyperactivity or abnormal experimental conditions during the measurements.
To allow comparison of thermoregulatory responses across the full range of
age and body mass, we computed overall thermal conductance,
Ko:
![]() | (1a) |
![]() | (1b) |
We used SYSTAT 7.0 (SPSS, Chicago, IL, USA) for all statistical analyses.
Because of the considerable inter- and intraspecific variation in mass, we
conducted allometric analyses using log10-transformed data when
appropriate to ensure homogeneity of variances. Homogeneity of variance was
then verified by examining residual plots. To allow statistical analysis, we
assumed that rapid growth justified treating each measurement as independent.
This assumption is not strictly correct, and consequently our results apply
only to the specific animals studied. In any event, the greatest source of
uncertainty in applying our data to wild chicks is systematic rather than
statistical, namely the effects of captive rearing. For example, captive
shorebird chicks may have lower total energy requirements and higher average
growth rates than wild ones (Beintema and
Visser, 1989b; Schekkerman and
Visser, 2001
).
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Results |
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Heat is stored or released when chick Tb changes, and
this needs to be included in the overall energy budget
(Eppley, 1994). We estimated
the maximum rate of heat storage or release as
cpm(
Tb/
t),
where m is body mass (g), cp is tissue heat
capacity (3.48 J g-1) and t is time (s). However, for the
Tb variation observed in our normothermic chicks, heat
storage was negligible relative to the average energy expended during a 30 min
interval.
Evaporative water loss
Evaporative water loss from shorebird chicks varied with mass and
Ta. The best-fit (adj. r2=0.76,
F2,117=188) model for evaporative cooling E (W)
was:
![]() | (2) |
|
Thermal conductance
Wind speed u affects both boundary layer convection processes,
which are proportional to u0.5, and dynamic processes
(wind displacement of and penetration among insulating fibers), which are
proportional to u2
(Bakken, 1991b). The net result
is that overall thermal conductance is related to u raised to an
intermediate exponent, the value reflecting the weighting of convective and
dynamic processes by the structure of the insulation. Therefore, we first
fitted a preliminary model of the form
a+buc+dmf to our data, where
a, b, c, d and f are fitted coefficients. The best-fit wind
speed exponents were c=1.04-1.09. The exact value of c was
not critical, and consequently u1.0 was used in the final
allometric models (Table
1).
|
We also plotted conductance as a function of body mass
(Fig. 2A,B), using LOWESS
(locally weighted scatterplot smoother) regressions
(Cleveland, 1985) to data at
each of the four wind speeds. The LOWESS lines suggest that the correlations
between both log10Ko and
log10Kow and log10m are
nonlinear, and that wind has a relatively greater effect on the smallest
chicks, a result expected from convective transport theory. LOWESS does not
assume a particular model, and thus cannot provide statistical information on
goodness-of-fit that might test the reality of, or hypotheses about, the
curvature. (Indeed, the goodness of fit is set a priori by the LOWESS
tension parameter). We tested polynomial regressions on body mass, as well as
regressions where each species was assigned a dummy variable equal to 1 if the
data applied to that species and 0 otherwise
(Draper and Smith, 1981
).
These models explained significantly more variance than the linear model,
indicating the relation is indeed nonlinear. However, we cannot discriminate
between phylogenetic and mass-related physical effects such as convection
because mass and taxon are confounded.
|
Standard operative temperature scale
Standard operative temperature Tes is the temperature
defined by an enclosure with free-convection conditions (u0)
in which the animal with the same body temperature Tb
would have the same net heat loss as it does in its actual environment
(Bakken, 1976
,
1992
). We defined a standard
operative temperature (Tes) scale appropriate for use in
the absence of thermally significant visible radiation. For this case,
operative temperature Te equals air temperature
Ta, and:
![]() | (3a) |
![]() | (3b) |
![]() | (3c) |
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Discussion |
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![]() | (4) |
A suitable published Tes scale for adult birds with
contour feathers is not available, so we reanalyzed data on dark-eyed juncos
from Bakken et al. (1991). The
best-fit relation had conductance vary as u0.7. The
corresponding Tes scale is:
![]() | (5) |
For downy chicks that respond to u1.0, we used
Equations 3a and 3b, plus a Tes scale developed for
1-day-old mallard ducklings (equations 4 and 5 in
Bakken et al., 1999). The
junco and mallard Tes scales involve recursive relations,
and were solved numerically (Bakken et al.,
1991
).
Because these Tes scales have different mathematical
forms, they are best compared graphically
(Fig. 3). Comparisons assume
the average conditions of the present study, Ta=20°C
and u=0-3 m s-1. The importance of wind is evident, as
even at room temperature, a wind speed of 3 m s-1 decreases
Tes by 7-8°C and increases heat loss by 40-50%. The
overall effect of wind, and thus the effect of differences in wind response
among temperature scales, is greater at lower Ta values.
While the relative effect of wind on Tes is similar among
the downy chicks and adult passerines, the effect on required heat production
also depends on the baseline conductance at low wind speed:
![]() | (6) |
|
The only clear conclusion about the effect of different wind speed
exponents is that the correlation using u is too
sensitive to wind speeds from 0.5 to 1.5 m s-1, and that the
discrepancy is most significant for downy chicks. Otherwise, the shorebird
chick scales based on wet and dry thermal conductance bracket the mallard
scale and overlap the junco scale. These differences are within experimental
error.
Evaporative water loss
During the experiments, humidity was generally higher than has been
recommended for making standardized evaporative water loss measurements
(Lasiewski et al., 1966). The
high chamber humidities were unexpected, as we were examining the response of
animals below their lower critical temperature, where evaporative water loss
is generally low. The dewpoint increased significantly (P<0.001)
with the size of the bird. Consequently, the E of small birds may be
exaggerated compared to the larger ones, and this may account for the
shallower slope of the shorebird chick regression compared to the adult
correlation (Fig. 1). High
chamber humidity should have decreased evaporation, but nevertheless our
measured values of evaporative water loss from shorebird chicks, adjusted to
Ta=25°C using Equation 2
(Fig. 1), are substantially
higher than comparable values for adult birds under thermally neutral
conditions (Williams,
1996
).
Calder and King (1974)
suggested that, to a first approximation, the ratio E/M should be
mass-independent. Briefly, they argued that metabolism is proportional to
respiratory minute volume, as is respiratory water loss. Further, metabolism
is proportional to mass, as is surface area, and cutaneous water loss is
proportional to surface area. Indeed, their review of published data
demonstrated that, at a given temperature, E/M had a consistent
relationship to ambient temperature, across a wide range of body mass. It is
particularly interesting that while E and M are positively
correlated with each other and with mass at one temperature, they are
negatively correlated across temperatures, such that
E/M=0.05+0.0148exp(0.087Ta). Bartholomew
(1972
) suggested that the
remarkable ability of birds to decrease E when M, and thus
minute volume, was increasing was because colder inspired air chilled the
respiratory tract, and thus water condensed on the respiratory passages when
exhaled. Respiratory passages were increasingly chilled as ambient air
temperature decreased, and consequently the temperature of exhaled air
decreased, and therefore its water content. This mechanism is not affected by
wind, and E should thus remain constant or even increase when
convective cooling increases M. Consequently, one expects
E/M should track Ta as in Calder and King's
equation, and perhaps even increase when wind increased M at a given
Ta.
In shorebird chicks, we found that M and E are correlated
with each other (r=0.66, P<0.00001), and with body mass.
However, we were unable to fit Calder and King's exponential to our data.
Using a linear model, we found E/M increased with
Ta (P<0.00001) as expected, but contrary to
expectation, E/M decreased rather than increased with wind speed
u (P<0.00001):
![]() | (7) |
![]() | (8) |
|
We suggest that reduced skin temperature and relatively high cutaneous evaporative water loss may account for the wind effect. Because down is relatively poor thermal insulation, a significant part of the overall resistance to heat loss is provided by tissue. Thus, a wind-induced increase in heat loss reduces skin temperature with no change in air temperature. Reduced skin temperature may reduce E via two mechanisms unrelated to M, and thus decrease E/M: (1) a low skin temperature causes vasoconstriction and reduces water movement to the skin by increasing the diffusion distance for liquid water; (2) the vapor pressure of the water that does reach the stratum corneum decreases with air temperature.
This wind effect on E/M was not seen in a study of adult juncos
(Bakken et al., 1991), possibly
because they are better insulated so that skin temperature is less affected by
wind (thermal conductance of shorebird chicks is 30-60% greater than that of
juncos of similar mass).
Down versus contour feathers as insulation
Wind has a substantial effect on thermal conductance. For a 25 g bird (the
approximate geometric mean for our study), increasing wind speed from 0.1 to 3
m s-1 increased Ko by 50% and
Kow by 30%. Data from heated taxidermic mounts
(Bakken, 1991b) indicated that
the thermal conductance of contour feather insulation increases with wind
speed as u0.7u0.8. Fur is more
affected by dynamic processes and responds as u1.0, with
some very soft furs on strongly curved surfaces responding as
u1.5. The best exponent for downy shorebird chicks was
1.04-1.09, which indicates a fur-like response to wind matching the fur-like
appearance of down.
Because the chicks of Arctic-breeding shorebirds are often exposed to cold,
one might expect their down to provide unusually effective insulation. In
Fig. 2, we compare our data
with other chicks and regressions to data on adult birds with contour
feathers. The downy insulation of shorebird chicks was slightly better than
that of day-old mallard ducklings (Anas platyrhynchos), but inferior
to the extremely dense down of notably cold-hardy capercaillie (Tetrao
urogallus; Pis, 2002) and
Xantus' murrelet (Synthliboramphus hypoleucus;
Eppley, 1984
) chicks. The down
of the latter two approaches the insulating value of summer adult plumages
(Fig. 2B). Comparison with
various regressions for adults indicates that shorebird chicks are rather
poorly insulated compared to adults. The regression coefficients for published
adult regression models as well as a regression that we constructed from
published data for adult shorebirds
(Kendeigh et al., 1977
;
Kersten and Piersma, 1987
) are
listed in Table 1.
Energetic considerations are probably paramount in determining the use of
down rather than contour feathers in chicks. The mass of contour feathers
needed to give the same amount of insulation is approximately 3 times the mass
of down (McNabb and McNabb,
1977), and the cost of synthesizing feathers appears to be
considerably greater than for other proteins
(Lindstrom et al., 1993
).
Apparently, the selective tradeoff between the thermal benefits of improved
insulation and the cost of synthesizing contour feathers and keeping them
properly preened favors the use of down by chicks.
Shorebird versus duckling insulation
Some data are available to compare the overall thermal conductance
Ko of downy shorebirds to that of ducklings breeding in
the same area. In another study at Churchill, we measured three long-tailed
(oldsquaw) 4-day-old ducklings (Clangula hyemalis) averaging about 35
g, using the same equipment and protocol. These long-tailed ducklings had an
average Ko=0.040 W °C-1, increasing by 13%
to 0.045 W °C-1 at u=1 m s-1. The
conductance of shorebird chicks with the same body mass as the ducklings, 35
g, is similar, Ko=0.039 W °C-1, increasing
by 14% to 0.045 W °C-1 at u=1 m s-1
(Table 1).
Mallards (Anas platyrhynchos) typically breed at lower latitudes
and have higher thermal conductance than Arctic-breeding shorebirds
(Fig. 2). However, 1- to
2-day-old mallard ducklings are physiologically more mature, having greater
thermogenic capacity than 1- to 2-week-old shorebirds of similar size
(Visser and Ricklefs, 1995).
Consequently, they are able to tolerate Ta values at least
as low as 10°C for over an hour
(Koskimies and Lahti, 1964
;
Bakken et al., 1999
).
In conclusion, the insulation of Arctic-breeding shorebird chicks thus appears somewhat, but not greatly, better than that of many other downy chicks. However, shorebird chicks are considerably less well insulated than capercaillie or Xantus' murrelet chicks of similar mass. Wind can increase heat loss and metabolic rate by 30-50% under windy conditions (30-50 km h-1). Thus, the success of Arctic breeding shorebirds depends on efficient parental care, the ability to use stored heat to enable foraging with falling body temperature, and perhaps behavioral adjustments such as foraging in such sheltered areas as may be available.
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Acknowledgments |
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