Water and energy economy of an omnivorous bird: Population differences in the Rufous-collared Sparrow (Zonotrichia capensis)

Abstract

We investigated the intraspecific variation in basal metabolic rate (BMR) and total evaporative water loss (TEWL) in the omnivorous passerine Zonotrichia capensis from two populations inhabiting regions with different precipitation regimes and aridity indices. Values of TEWL in birds from the semi-arid region were significantly lower than those found in sparrows from the mesic region. TEWL in birds from the semi-arid site was 74% of the expectation based on body mass for passerines from mesic areas and similar to the allometric expectation for passerines from arid environments. In sparrows from the mesic area, TEWL was higher than predicted by their body mass for passerines from arid environments (133%), but very close (97%) to the expectation for passerines from mesic areas. BMR values were 25% lower in sparrows from the semi-arid region. The lower TEWL and BMR of birds from the semi-arid region may be a physiological adjustment that allows them to cope with fewer resources and/or water. We propose that the lower endogenous heat production in birds from the semi-arid environment may decrease their water requirements.

Full text

Water and energy economy of an omnivorous bird: Population differences in
the Rufous-collared Sparrow (Zonotrichia capensis)
Pablo Sabat
a,b,
⁎, Grisel Cavieres
a
, Claudio Veloso, Mauricio Canals
a
a
Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile
b
Center for Advanced Studies in Ecology and Biodiversity, Facultad de Ciencias Biológicas Pontificia Universidad Católica de Chile,
Casilla 114-D, Santiago, Chile
Abstract
We investigated the intraspecific variation in basal metabolic rate (BMR) and total evaporative water loss (TEWL) in the omnivorous passerine
Zonotrichia capensis from two populations inhabiting regions with different precipitation regimes and aridity indices. Values of TEWL in birds
from the semi-arid region were significantly lower than those found in sparrows from the mesic region. TEWL in birds from the semi-arid site was
74% of the expectation based on body mass for passerines from mesic areas and similar to the allometric expectation for passerines from arid
environments. In sparrows from the mesic area, TEWL was higher than predicted by their body mass for passerines from arid environments
(133%), but very close (97%) to the expectation for passerines from mesic areas. BMR values were 25% lower in sparrows from the semi-arid
region. The lower TEWL and BMR of birds from the semi-arid region may be a physiological adjustment that allows them to cope with fewer
resources and/or water. We propose that the lower endogenous heat production in birds from the semi-arid environment may decrease their water
requirements.
Keywords: BMR; Evaporative water loss; Heat; Population differences; Sparrows; Turbinates; Xeric environment; Zonotrichia capensis
1. Introduction
Organisms can survive and colonize xeric environments
through mechanisms acting at cellular, physiological, ecological
and/or behavioural levels (Cade et al., 1965; Casotti and Richard-
son, 1992; Tieleman et al., 1999; Haugen et al., 2003; Bozinovic
and Gallardo, 2006; Bozinovic et al., 2003).
Because of their diurnal habits, high mass-specific metabo-
lisms, and high body temperatures, passerines tend to have pro-
portionately high rates of water flux. For xeric-adapted birds, one
trait may be possessing low total evaporative water loss (TEWL)
rates. Such physiological traits would allow birds to conserve
water by reducing insensible water losses (Williams, 1996;
McNab, 2002; Tieleman et al., 2003; Vikelski et al., 2003). Some
authors have proposed that the low productivity of desert and
semi-desert environments selectively favours animals with lower
energy requirements. This hypothesis predicts that animals with a
low basal metabolic rate (BMR) are more likely to inhabit xeric
environments (Dawson and Bennett, 1973; Schleucher et al.,
1991). The scarcity of water in these environments may also be a
selective pressure favouring lower BMRs as lower endogenous
heat production may decrease water requirements for evaporative
cooling (Dawson, 1984).
Recent evidence has shown that energy and water requirements
not only vary among species from desert and non desert habitats
(see Withers and Williams, 1990; Hinsley et al., 1993; Williams
and Tieleman, 2000), but also along an aridity gradient (Tieleman
et al., 2004). This suggests that physiology is responsive to and
reflects small differences in water availability and temperature.
Several studies have examined water conservation in birds at the
interspecific level (see also Tieleman et al., 2002, 2003); however,
relatively few have sought to understand water conservation at
either the intraspecific level (Arieli et al., 2002; Williams and
⁎Corresponding author. Departamento de Ciencias Ecológicas, Facultad de
Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile. Tel.: +56 2
6787232; fax: +56 2 2727363.
E-mail address: psabat@uchile.cl (P. Sabat).

Tieleman, 2000) or between populations of the same species that
inhabit both mesic and arid environments (Macmillen and Hinds,
1998). However, inter-populational differences in the energy and
water economy among birds may be widespread but it is not
universal. For example, Macmillen and Hinds (1998) compared
the water economy of coastal and desert populations of house
finches (Carpodacus mexicanus) and reported that birds from the
Mojave Desert are more economical in water use (ca. 40% lower
TEWL) rather than California coastal forms. By the other hand,
Thomas et al. (2001) found no evidence of local adaptation in
resting metabolic rates of blue tits (Parus caeruleus), in response
to hot climates. Intraspecific differences in the physiology of
geographically separated populations can provide insight into the
evolutionary processes that permit species to cope with environ-
mental variability. These studies are, therefore, important for
understanding the origin of physiological diversity and the evo-
lution of physiological tolerance (Garland and Adolph, 1991;
Spicer and Gaston, 1999).
To investigate intraspecific variability in energy and water
budgets, we measured BMR, TEWL, in the passerine bird, Rufous-
collared Sparrow (Zonotrichia capensis, Emberizidae). We made
these measurements in birds from two localities that varied in both
annual precipitation and temperature. We also assessed how the
nasal passages affected the capacity to recovery water from ex-
pelled air. Zonotrichia capensis is an omnivore distributed through-
out the neotropics (from southeast México to Cabo de Hornos;
Goodall et al., 1951). In Chile, it is nearly ubiquitous, inhabiting
areas as different as deserts and rain forests from 0 to more than
3600 m.a.s.l. (Araya, 1996). We predicted that animals from the
southern and wet area would have higher levels of energy pro-
duction (BMR) and water flux (TEWL), than those from the
northern xeric area.
2. Materials and methods
2.1. Animals and capture
Sparrows were collected during the austral winter of 2005 from
two localities in Chile: (1) La Serena (29° 54′S, 71° 15′W, n=6),
and (2) Quebrada de la Plata (33° 31′S, 70° 50′W, n=9). Our
study sites varied in mean annual rainfall: La Serena is semi-arid,
and receives 100 mm per year, whereas Quebrada de la Plata is
mesic and receives 367 mm per year, and their aridity scores using
the index of de Martone, (Martone index=P/(T+10), wherePis
annual precipitation in mm, and Tis mean annual temperature in
°C) are 5.13 for La Serena and 14.90 for Quebrada de la Plata (Di
Castri and Hajek, 1976; DGA, 2004).
2.2. BMR and TEWL
After capture, we transported the birds to the laboratory in
Santiago, Chile (33° 27′S, 70° 42′W) and housed them in
individual 35 × 35 × 35 cm plastic-mesh cages Temperature and
photoperiod were held at 22 ± 2 °C and 12 L:12 D respectively.
Birds had ad libitum access to mealworms, seeds and water.
After an initial laboratory habituation of two days, birds were
measured within the first week of capture. We measured rates of
oxygen consumption (V˙O
2
) and total evaporative water loss
(TEWL) in post absorptive (four hour fasted), resting birds in
the inactive phase, using standard flow-through respirometry
and hygrometry methods. Inside dark metabolic chambers (1 L),
birds perched on a wire-mesh grid that allowed excreta to fall
into a tray containing mineral oil, thus trapping the water from
this source. Oxygen consumption was measured using a com-
puterized, open-flow respirometry system (Sable Systems,
Henderson, NV, USA) calibrated with a known mix of oxygen
(20%) and nitrogen (80%) that were certified by chromatogra-
phy (INDURA, Chile). Measurements were made at ambient
temperatures (T
a
) of 25.0, 30.0, and 40.0 ± 0.5 °C at random. We
are confident that T
a
of 30.0 °C is within the thermo neutral zone
for this species (Novoa et al., 1990; Novoa, 1993) as we initially
measured V˙O
2
at temperatures ranging from 15 to 40 °C in four
individuals (Fig. 1). To estimate the contribution of turbinates in
the water economy of birds, we also determined V˙O
2
and
TEWL at 30 °C in birds with nares occluded by plastic dental
resin. We assumed that cutaneous evaporative water loss was
not affected by the treatment (see Tieleman et al., 1999). The
metabolic chamber received dried air at 500 mL min
−1
from a
mass flow controller and through Bev-A-Line tubing (Thermo-
plastic Processes Inc.). This flow ensured adequate mixing in
the chamber. The mass flow meter was calibrated monthly with
a volumetric (bubble) flow meter. The excurrent air passed
through a RH-200 relative humidity/dewpoint hygrometer
(Sable Systems) and through columns of Diedrite, CO
2
-absor-
bent granules of Baralyme, and Drierite before passing through
an O
2
-analyzer, model FC-10A (Sable System). The complete
V˙O
2
trial lasted 3 h. Output from the H
2
O (kPa) and oxygen
analyzers (%) was digitized using a Universal Interface II (Sable
Systems) and recorded on a personal computer using EXPE-
DATA data acquisition software (Sable Systems). Our sampling
interval was 5 s. Birds remained in the chamber for at least 3 h
and visual inspection of the recorded data allowed us to de-
termine when steady-state conditions had been achieved. We
averaged water vapour pressure and O
2
concentration of the
excurrent airstream over a 20 min period after steady-state was
Fig. 1. Profile of oxygen consumption as a function of ambient temperature in
Zonotrichia capensis from Central Chile. Data are reported as mean± SD.
P. Sabat et al.

reached (following Tieleman et al., 2002). Because CO
2
was
scrubbed before entering the O
2
analyzer, oxygen consumption
was calculated as [Withers (1977: p 122)]: V˙O
2
= [FR * 60 * (F
i
O
2
−F
e
O
2
)] / (1 −F
i
O
2
), where FR is the flow rate in mL/min
after STP correction, F
i
and F
e
are the fractional concentrations
of O
2
entering and leaving the metabolic chamber, respectively.
TEWL was calculated as TEWL = [(V
e
ρ
out
−V
i
ρ
in
)] where
TEWL is in mg/mL. ρ
in
and ρ
out
are the absolute humidity in kg/
m
3
of the inlet air and the outlet air respectively, V
e
is the flow
rate of the air entering the chamber as given by the mass flow
controller (500 mL min
−1
after STP correction) and V
e
is the
flow of exiting air. V
e
was calculated following Williams and
Tieleman (2000) as V
e
=V
i
−[V˙O
2
(1 −RQ)] + VH
2
OV
i
, and
V˙O
2
(mL min
−1
) are known. We assumed a respiratory quotient
(RQ) as 0.71. Absolute humidity was calculated as ρ=P/
(T*R
w
), where Pis water vapour pressure of the air in Pascal, T
is the temperature of the dew-point hygrometer in Kelvin and
R
w
is the gas constant for water vapour (461.5 J/kg * Kelvin,
Lide, 2001). The P
in
was determining using the average value of
the vapour pressure of the air entering the empty chamber (i.e.,
the baseline period of 15 min) before and after each experiment.
Body mass was measured before the metabolic measurements
using an electronic balance (± 0.1 g) and cloacal body tem-
perature (T
b
) was recorded at the end of each measurement with
a Cole–Palmer copper–constantan thermocouple attached to an
Digi-Sense thermometer (Model 92800-15).
After metabolic experiments, birds were killed by exposure
to CO
2
and all animals were dissected abdominally. We ex-
tracted the large and small intestine, and then heart, lungs, liver
and kidneys. Organs were weighed immediately (±0.05 g).
2.3. Data analysis
Because our populations did not differ in body mass (m
b
)
(F
1,10
= 0.44, p= 0.52, Table 1), we analyzed data using a re-
peated measures ANOVA using individual measurements at
each T
a
(25, 30 and 40 °C) as repeated measures. Additionally,
since TEWL might be affected by oxygen consumption, we
performed linear regression analyses with TEWL as the depen-
dent variable and V˙O
2
consumption as the independent variable
in birds measured at each temperature. We estimated the me-
tabolic water production (MWP) of birds using equivalence:
0.567 mL H
2
O per liter O
2
consumed (Schmidt-Nielsen, 1997).
The ratio between MWP and TEWL was calculated and ana-
lyzed for population differences at different temperatures.
3. Results
Values of TEWL in birds from the semi-arid region of La
Serena were significantly lower than those found in sparrows
from Quebrada de la Plata, which is the mesic region (locality:
F
1,10
= 16.60, p= 0.002, Fig. 2). We also found that TEWL in-
creased with increasing T
a
(T
a
:F
2,22
= 268.4, pb0.001, Fig. 2).
BMR values were 25% lower (F
1,20
= 27.08, pb0.001, Table 1)
in sparrows from La Serena than those of birds from Quebrada
de la Plata. Coupled with the increase in TEWL, body tempe-
rature was also increased at 40 °C (T
a
:F
2,22
= 87.11, pb0.001)
In addition, the MWP/TEWL ratio decreased significantly with
T
a
(T
a
:F
2,20
= 162.3, pb0.001, Fig. 3) and ranged from ca. 65%
at 25 °C to 10% at 40 °C. No significant differences in MWP/
TEWL were found between localities (F
1,10
= 0.32, p= 0.58). A
Table 1
Body mass, organ masses, body temperature and basal metabolic rate (BMR) in
Zonotrichia capensis from two localities in central Chile
La Serena Quebrada de la Plata
Body mass (g) 20.06 ± 1.13 (6) 20.11± 1.17 (9)
Liver mass (g) 0.62 ± 0.08 (6) 0.73 ± 0.22 (9)
Kidney mass (g) 0.22 ± 0.02 (6) 0.24 ± 0.04 (9)
Intestine mass (g) 0.72 ± 0.11 (6) 0.81 ± 0.30 (9)
Heart mass (g) 0.25± 0.02 (6) 0.26± 0.03 (9)
Body temperature 40.26 ± 0.62 (6) 40.36± 0.54 (9)
BMR (mL O
2
h
−1
) 55.85 ± 4.84*(6) 73.08± 6.89 (9)
Asterisk denotes significant differences between localities and the number of
animals of each treatment is in parenthesis (see text for ANOVA results).
Fig. 2. Total evaporative water loss in Zonotrichia capensis from two localities
in central Chile at three different temperatures. Letters denote significant
differences between temperatures. Data are reported as mean ± SD.
Fig. 3. The ratio between metabolic water production and total evaporative water
loss in Zonotrichia capensis from two localities in central Chile at three different
temperatures. Letters denote significant differences between temperatures. Data
are reported as mean ± SD.
P. Sabat et al.

significant effect of locality was found in the difference between
TEWL and the estimated MWP (locality: F
1,10
=14.19,
p= 0.003, Fig. 4). This difference was higher at Quebrada de
la Plata than at La Serena. We found a significant and positive
correlation between TEWL and oxygen consumption at 25 °C
(r= 0.76, p=0.001) and 30 °C (r= 0.57, p= 0.005), but not at
40 °C (r= 0.34, p= 0.28).
Birds with occluded nares had significantly greater TEWL
compared to birds whose nares were opened (t
4
=7.48, p=0.002
and t
9
=4.50, p=0.002 in La Serena and Quebrada de la Plata
populations, respectively). The ratios between TEWL of birds with
closed and open nares were 1.33± 0.09 and 1.56± 0.36 for birds
from La Serena and Quebrada de la Plata, respectively. Because
the oxygen consumption also increased when birds had their nares
occluded (t
4
=4.82, p= 0.008 and t
9
=5.66,pb0.001 for La Serena
and Quebrada de la Plata, respectively), to asses differences bet-
ween population in the capacity of recovering water from expired
air, we performed an ANCOVA analysis using the ratio of oc-
cluded/open TEWL as dependent variable and the ratio of oc-
cluded/open V˙O
2
as covariate (after a correction by the arcsine of
the square root of data). This analysis revealed a significant effect
of the ratio of V˙O
2
(r=0.66, F
1,11
=5.60, p= 0.0 3), but a non
significant effect of locality (F
1,11
=0.81, p= 0.39). In addition, an
MANOVA analysis revealed that any organ masses do not differ
between populations (Wilks lambda 0.79, p=0.78).
4. Discussion
In this paper we tested for intraspecific variability in energy
and water budgets, between populations of the passerine bird,
Rufous-collared Sparrow. The study of Tieleman et al. (2002)
account for interspecific differences in TEWL and BMR in an
aridity gradient. In this study, we confirm the effect of climate on
the water and energy economy of an granivorous bird at an inter
population level. Rufous-collared sparrows from both popula-
tions maintain low TEWL when exposed to 25 and 30 °C. How-
ever, when exposed to 40 °C, TEWL increases dramatically
(460%, Fig. 2). We compared our results obtained at 25 °C with
the expected values from the allometric equations for passerine
birds (see Tieleman et al., 2002). TEWL in birds from La Serena
was 74% of the expectation based on m
b
for passerines from mesic
areas and 101% of the allometric expectation for passerines from
arid environments. In birds from Quebrada de la Plata, TEWL was
higher than predicted by m
b
for passerines from arid environments
(133%), but very close (97%) to the expectation for passerines
from mesic areas. Although no differences were found in the ratio
of MWP and TEWL between localities at any temperature (Fig.
3), the total amount of water lost (i.e., the difference between
TEWL and MWP) was greater for birds from Quebrada de la Plata
(Fig. 4). This indicates that total water requirements (pre-formed
water in food and from freshwater drinking) are lower in sparrows
from xeric areas. Values of MWP/TEWL in Z. capensis are si-
milar to that found among similar size passerines, ca. 0.54–0.46
(Williams, 1996) but very low compared to that found in Carpo-
dacus mexicanum (ca. 1.0, Macmillen and Hinds, 1998).
However that value was measured at 5 °C, which probably raised
the metabolic rate in order to cope the thermoregulatory demands.
Differences in metabolic rate at the inter-population level for Z.
capensis are comparable to that found at an interspecific levels in
birds. Several studies have shown that field metabolic rate and
BMR of bird species depend of environmental temperature and
rainfall. This has been interpreted as an adaptive feature to cope
with low levels of productivity (Tieleman et al., 2004). Generally,
increased rainfall increases both the productivity of terrestrial
habitats (Lieth, 1978; Polis and Hurd, 1996) and, presumably, the
availability of resources (i.e., invertebrates, seeds). For instance,
Tieleman et al. (2002) reported that desert and mesic larks (Al-
audidae) differ in 43% in BMR, being lower in desert larks. Our
results revealed a difference of a 24% inBMR between La Serena
and Quebrada de la Plata. The lower difference between our
sparrow populations probably reflects the lower gradient in tem-
perature and rainfall between Chilean localities.
The mechanism we suggest that Z. capensis has evolved to
cope with semi-arid environments by reducing TEWL remains to
be tested. Yet, several studies have reported that the morphology
of the nasal passages in birds can contribute to a decrease in
evaporative water loss through a countercurrent heat exchange
mechanism present in the turbinates (Geist, 2000). Our findings
support the hypothesis that nasal passages can reduce evaporative
water loss. Birds with occluded nares exhibited an elevated TEWL
(33–56%), which is in accord with Tieleman et al. (1999) who
found that TEWL was elevated by 27% in Crested larks (Galerida
cristatta) with occluded nares at 15 °C, but the effects of the
turbinate disappears at elevated temperatures (e.g., 40 °C) when
birds were panting. Interestingly, these authors did not found any
effect of nasal passages on TEWL in the Desert lark Ammomanes
deserti. Contrary to the results of Tieleman et al. (1999),wefound
the increase in V˙O
2
consumption in birds with occluded nares was
significant. The significant and positive correlation between the
increment of TEWL and the increment of V˙O
2
we report in this
study revealed that roughly 44% of the variation in TEWL is
explained by the increment in V˙O
2
. The remaining 56% of va-
riation may be explained by the condensation of the exhaled air
stream on the cooled membranes of the nasopharynx (Schmidt-
Nielsen et al., 1970). This is also supported by our finding that the
Fig. 4. The difference between total evaporative water loss and metabolic water
production in Zonotrichia capensis from two localities in central Chile at three
different temperatures. Letters denote significant differences between tempera-
tures. Data are reported as mean± SD.
P. Sabat et al.

ratio between the MWP/TEWL was higher in birds with open
nares (Fig. 3). However, because there was no difference in the
ability of the two populations to recover water from expired air,
our findings suggest that the structure of nasal passages is similar
between them. This observation is consistent with results of in-
vestigation in several bird species that demonstrated no main
differences in turbinate-mediated water savings (Geist, 2000). In
addition, our regression analysis indicates that oxygen consump-
tion may explain 30% to 56% of water loss at moderate tem-
peratures. Therefore, one factor influencing TEWL between our
populations appears to be energy expenditure. Besides, Haugen et
al. (2003) demonstrated that adjustments in ratios of lipids in the
skin are associated with changes in cutaneous water loss (see also
Muñoz-Garcia and Williams, 2005; Williams and Tieleman,
2005). Hence, additional tests are needed to determine whether
populations of Z. capensis show differences in skin permeability
and what the relative contributions of respiratory and cutaneous
water losses are to TEWL.
The physiological mechanisms responsible for differences in
BMR of birds from both populations are unknown. Several al-
ternatives has been proposed to explain a reduction in BMR, in-
cluding a reduction in the amount of metabolically active tissue and
lower rates of metabolism of specific tissues (Daan et al., 1990;
Konarzewski and Diamond, 1995; Piersma and Lindström, 1997;
Kersten et al., 1998; Merkt and Taylor, 1994, but see Burnes et al.,
2005). In addition, it has been demonstrated that birds may ac-
climate their organ masses. For example Klaassen et al. (2004)
found differences in organ masses and BMR in cold- and warm-
acclimated garden warblers (Sylvia borin). Our results do not sup-
port the first alternative, i.e., a reduction in the size of organs as
heart, liver, and kidneys (Table 1).The second alternative appears as
plausible but further efforts are needed to evaluate this hypothesis
in Z. capensis.
In summary, the lower TEWL and energy expenditures in
sparrows from the semi-arid locale could be interpreted as an
adaptive feature to cope with fewer resources and/or water (Wil-
liams and Tieleman, 2005). However, as pointed out by Garland
and Adolph (1994) that the “two species comparison”approach is
limiting, the two-population comparisons can only be used with
caution to infer adaptation. It is probably that two populations (or
species) may differ in several physiological or morphological
traits just because they are different populations (Garland and
Adolf, 1994). Besides, physiological adjustments to climatic
conditions may be the result of phenotypic plasticity (the modi-
fication of phenotype according to environmental cues; see Pig-
liucci, 2001; Hammond et al., 2001). Physiological and
morphological features related to water economy in birds may
be modified by acclimation (i.e., phenotypic flexibility; see Wil-
liams and Tieleman, 2000; Haugen et al., 2003; Tieleman et al.,
2003) and by the exposition to different environments during
early development (or developmental plasticity sensu Piersma
and Drent, 2003; McKechnie et al., 2006). For example, Hudson
and Kimzey (1966) found that the sparrow (Passer domesticus)
from Houston, Texas, had a lower BMR than sparrows from more
mesic latitudes. Authors attribute the reduction in BMR in the
Houston form to an adaptive feature to cope with warm climates.
However, the efforts to obtain increases in BMR by cold accli-
mation in this species have been unsuccessful; suggesting that
lower BMR in this population may be genetically programmed. It
seems that Z.capensis can be considered as a physiologically
flexible bird. For example, Castro and Wunder (1991) reported
differences in BMR of cold acclimated and warm acclimated Z.
capensis from Peru; Sabat et al. (2004) and Sabat et al. (1998)
found a morphological and biochemical responses in kidney and
gut traits when fed on different diets, and Novoa et al. (1994)
found seasonal adjustments in thermal conductance of Z. capensis
of a population from a seasonal locality of central Chile. It is likely
that Z. capensis populations can adjust their physiology to meet
different environmental conditions. Chronic temperature accli-
mation during the development of birds (i.e., months) and mea-
surements of TEWL, are needed to evaluate these hypotheses.
Besides, as many authors suggest, plasticity of physiological and
morphological traits may be constrained in specialist individuals,
and might have an adaptive value in those that experience larger
temporal variation in their physical and biotic environment (Sch-
lichting and Pigliucci, 1998). For example the White-browed
scrubwrens (Sericornis frontalis) from Australian deserts (which
exhibits more temporal variation than mesic habitats) reduced
BMR during summer, but a population in a more mesic area did
not show such seasonal adjustment (Ambrose and Bradshaw,
1988). However, Tieleman et al. (2003) found no evidence for the
hypothesis that species from desert environments display larger
phenotypic flexibility than those from mesic areas. In this sense,
Z. capensis dwell in a great range of habitats with a broad seasonal
variation. Hence, some potential variation in the availability of
water and temperature regime that individuals experience is ex-
pected through time. To what extent the ability to modify me-
tabolic capacities and water fluxes depends on the ecological
habits of species or populations are a question yet to be assessed.
Acknowledgements
We thank Bradley Bakken for their useful comments on a
previous version of our manuscript. Sandra Gonzales and Andres
Sazo provided invaluable assistance in the field and in the la-
boratory. Funded by Fondecyt 1050196 to PS.
References
Ambrose,S.J., Bradshaw, S.D., 1988.Seasonal changesin standard metabolic rates
in the white-browed scrubwren Sericornis frontalis (Acanthizidae) from arid,
semi-arid and mesic environments. Comp. Biochem. Physiol., A 89, 79–83.
Araya, M.B., 1996. Guía De Campo De las aves de Chile. Editorial Universitaria,
Santiago.
Arieli, Y., Peltonen, L., Ophir, E., 2002. Cooling by cutaneous water evaporation in
the heat-acclimated rock pigeon (Columba livia). Comp. Biochem. Physiol., A
131, 497–504.
Bozinovic, F., Gallardo, P., 2006. The water economy of South American desert
rodents: from integrativeto molecular physiological ecology. Comp. Biochem.
Physiol., C 142, 163–172.
Bozinovic, F., Gallardo, P.A., Visser, R.H., Cortés, A., 2003. Seasonal accli-
matization in water flux rate, urine osmolality and kidney water channels in
free-living degus: molecular mechanisms, physiological processes and
ecological implications. J. Exp. Biol. 206, 2959–2966.
Burnes, G., Chardine, J.W., Darveau, C.A., 2005. Flight muscle enzyme activities
do not differ between pelagic and near-shore foraging seabirds species. Comp.
Biochem Physiol., A 140, 53–58.
P. Sabat et al.

Cade, T.J., Tobin, C.A., Gold, A., 1965. Water economy and metabolism of two
estrildine finches. Physiol. Zool. 38, 9–33.
Casotti, G., Richardson, K.C., 1992. A stereological analysis of kidney structure
of honeyeater birds (Meliphagidae) inhabiting either arid or wet environ-
ments. J. Anat. 180, 281–288.
Castro, G., Wunder, B.A., 1991. Cold adaptations in the rufous-collared sparrow
Zonotrichia capensis. Comp. Biochem. Physiol., A 98, 101–102.
Daan, S., Masman, D., Groenewold, A., 1990. Avian basal metabolic rates: their
association with body composition and energy expenditure in nature. Am.
J. Physiol. 259, R333–R340.
Dawson, W.R., 1984. Physiological studies of desert birds: present and future
considerations. J. Arid Environ. 7, 133–155.
Dawson, W.R., Bennett, A.F., 1973. Roles of metabolic level and temperature
regulation in the adjustment of western plumed pigeons to desert conditions.
Comp. Biochem. Physiol., A 44, 249–266.
DGA (Dirección General de Aguas), 2004. Listado de datos de estaciones
meteorológicas de Chile. Ministerio de Obras Públicas de Chile.
Di Castri, F., Hajek, E.R., 1976. Bioclimatología de Chile. Ediciones Uni-
versidad Católica de Chile.
Garland Jr., T., Adolph, S.C., 1991. Physiological differentiation of vertebrate
populations. Ann. Rev. Ecolog. Syst. 22, 193–228.
Garland Jr., T., Adolph, S.C., 1994. Why not to do two-species comparative
studies: limitations on inferring adaptation. Physiol. Zool. 67, 797–828.
Geist, N.R., 2000. Nasal turbinate function in birds. Physiol. Biochem. Zool. 73,
581–589.
Goodall, J.D., Jonson, A.W., Philippi, R.A., 1951. Las aves de Chile, su
conocimiento y sus costumbres, vol. II. Platt Establecimientos Gráficos, Buenos
Aires, Argentina.
Hammond, K., Szewczak, J., Krol, E., 2001. Effects of altitude and temperature
on organ phenotypic plasticity along an altitudinal gradient. J. Exp. Biol.
204, 1991–2000.
Haugen, M.J., Tieleman, B.E., Williams, J.B., 2003. Phenotypic flexibility in
cutaneous water loss and lipids of the stratum corneum. J. Exp. Biol. 206,
3581–3588.
Hinsley, S.A., Ferns, P.N., Thomas, D.H., Pinshow, B., 1993. Black-bellied
Sandgrouse (Prerocles orientalis) and Pin-tailed Sandgrouse (Pterocles nol-
chata): closely related species with differing bioenergetic adaptations to arid
zones. Physiol. Zool. 66, 20–42.
Hudson, J.W., Kimzey, S.L., 1966. Temperature regulation and metabolic
rhythms in populations of the House Sparrow, Passer domesticus. Comp.
Biochem. Physiol. 17, 203–217.
Kersten,M.,Bruinzeel,L.W.,Wiersma,P.,Piersma,T.,1998.Reducedbasal
metabolic rate of migratory waders wintering in coastal Africa. Ardea 86, 71–80.
Klaassen, M., Oltrogge, M., Trost, L., 2004.Basal metabolic rate, food intake, and
body mass in cold- and warm-acclimated Garden Warblers. Comp. Biochem.
Physiol., A 137, 639–647.
Konarzewski, M., Diamond, J., 1995. Evolution of basal metabolic rate and
organ masses in laboratory mice. Evolution 49, 1239–1248.
Lide, D.R., 2001. Handbook of Chemistry and Physics. CRC Press, Boca Raton.
Lieth, H., 1978. Primaryproductivity inecosystems: comparative analysis of global
patterns. In: Leith, H. (Ed.), Patterns of primary productivity in the biosphere.
Hutchinson & Ross, Stroudsburg, Pennsylvania, USA, pp. 301–321.
Macmillen, R.E., Hinds, D.S., 1998. Water economy of granivorous birds: Cali-
fornian House Finches. Condor 100, 493–504.
Merkt, J.R., Taylor, C.R., 1994. “Metabolic switch”for desert survival. Proc. Natl.
Acad.Sci.U.S.A.91,12313–12316.
McKechnie, A.E., Freckleton, R.P., Jetz, W., 2006. Phenotypic plasticity in the
scaling of avian basal metabolic rate. Proc. R. Soc. B 273, 931–937.
McNab, B.K., 2002. The physiological ecology of vertebrates. A view from
energetics. Cornell University press, Cornell.
Muñoz-Garcia, S., Williams, J.B., 2005. Cutaneous water loss and lipids of the
stratum corneum in house sparrows Passer domesticus from arid and mesic
environments. J. Exp. Biol. 208, 3689–3700.
Novoa, F.F., 1993, Ecofisiología de Zonotrichia capensis: cambios estacionales
en el gasto y la adquisición de energía. Tesis Doctoral. Facultad de Ciencias,
Universidad de Chile, Santiago. Xx+125 pp.
Novoa, F.F., Bozinovic, F., Rosenmann, M., 1990. Maximum metabolic rate and
temperature regulation in the Rufous-collared sparrow, Zonotrichia capensis,
from central Chile. Comp. Biochem. Physiol., A 95, 181–183.
Novoa, F.F., Bozinovic, F., Rosenmann, M., 1994. Seasonal changes of thermal
conductance in Zonotrichia capensis (Emberizidae) from central Chile: the
role of plumage. Comp. Biochem. Physiol., A 107, 297–300.
Piersma, T., Drent, J., 2003. Phenotypic flexibility and the evolution of organismal
design. Trends Ecol. Evol. 18, 228–233.
Piersma, T., Lindström, A., 1997. Rapid reversible changes in organ size as a
component of adaptive behaviour. Trends Ecol. Evol. 12, 134–138.
Pigliucci, M., 2001. Phenotypic Plasticity: Beyond Nature and Nurture. Johns
Hopkins University, Baltimore, MD.
Polis, G.A., Hurd, S.D., 1996. Linking marine and terrestrial food webs: al-
lochthonous input from the ocean supports high secondary productivity on
small islands and coastal land communities. Am. Nat. 147, 396–423.
Sabat, P., Novoa, F.F., Bozinovic, F., Martinez del Río, C., 1998. Dietary flexibility
and intestinal plasticity in birds: a field and laboratory study. Physiol. Zool. 71,
226–236.
Sabat, P., Sepúlveda-Kattan, E., Maldonado, K., 2004. Physiological and bio-
chemical responses to dietary protein in the omnivore passerine Zonotrichia
capensis (Emberizidae). Comp. Biochem. Physiol., A 137, 391–396.
Schleucher, E., Prinzinger, R., Withers, P.C., 1991. Life in extreme environ-
ments: investigations on the ecophysiology of a desert bird, the Australian
diamond dove (Geopelia cuneata Latham). Oecologia 88, 72–76.
Schlichting, C.D., Pigliucci, M., 1998. Phenotypic Evolution. Sinauer Associates
Inc, Sunderland.
Schmidt-Nielsen, K., 1997. Animal Physiology. Cambridge University Press,
Cambridge, UK.
Schmidt-Nielsen, K., Hainsworth, F.R., Murrish, D.E., 1970. Counter-current heat
exchange in the respiratory passages: effect of on water and heat balance.
Respir. Physiol. 9, 263–276.
Spicer, J.I., Gaston, K.J., 1999. Physiological diversity and its ecological im-
plications. Blackwell Science, Malden.
Thomas, D.W.,Blondel, J., Perr et,P., 2001. Physiological ecology of Mediterranean
Blue Tits (Parus caeruleus) I. A test for inter-population differences in resting
metabolic rate and thermal conductance as a response to hot climates. Zoology
104, 33–40.
Tieleman, B.I., Williams, J.B., Michaeli, G., Pinshow, B., 1999. The role of the nasal
passages in the water economy of crested larks and desert larks. Physiol.
Biochem. Zool. 72, 219–226.
Tieleman, B.I., Williams, J.B., Bloomer, P., 2002. Adaptation of metabolism and
evaporative water loss along an aridity gradient. Proc. R. Soc. Lond. 270,
207–214.
Tieleman, B.I., Williams, J.B., Buschur, M.B., Brown, K., 2003. Phenotypic
variation of larks along an aridity gradient: are desert birds more flexible?
Ecology 84, 1800–1815.
Tieleman, B.I., Williams, J.B., Visser, G.H., 2004. Energy and water budgets of
larks in a life history perspective: parental effort varies with aridity. Ecology
95, 1399–1410.
Vikelski, M., Spinney, L., Schelski, W., Scheuerlinn, A., Gwinner, E., 2003.
Slow pace of life in tropical sedentary birds: a common garden experiment
on four stonechat populations from different latitudes. Proc. R. Soc. Lond.
270, 2383–2388.
Williams, J.B., 1996. A phylogenetic perspective of evaporative water loss in
birds. Auk 113, 457–472.
Williams, J.B., Tieleman, B.I., 2000. Flexibility in basal metabolic rate and
evaporative water loss among hoopoe larks exposed to different environ-
mental temperatures. J. Exp. Biol. 203, 3153–3159.
Williams, J.B., Tieleman, B.I., 2005. Physiological adaptation in desert birds.
Bioscience 55, 416–425.
Withers, P.C., 1977. Measurements of metabolic rate, VCO
2
, and evaporative
water loss with flow through mask. J. App. Physiol. 42, 120–123.
Withers, P.C., Williams, J.B., 1990. Metabolic rate and respiratory physiology of
an arid-adapted Australian birds, the Spinifex Pigeon. Condor 92, 961–969.
P. Sabat et al.