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ORIGINAL RESEARCH
published: 02 August 2021
doi: 10.3389/fevo.2021.704676
Edited by:
Piotr Jablonski,
Seoul National University,
South Korea
Reviewed by:
Todd Jason McWhorter,
University of Adelaide, Australia
Piotr Matyjasiak,
Cardinal Stefan Wyszy ´
nski University,
Poland
*Correspondence:
Ivan Maggini
ivan.maggini@vetmeduni.ac.at
Specialty section:
This article was submitted to
Behavioral and Evolutionary Ecology,
a section of the journal
Frontiers in Ecology and Evolution
Received: 03 May 2021
Accepted: 12 July 2021
Published: 02 August 2021
Citation:
Paces B, Waringer BM, Domer A,
Burns D, Zvik Y, Wojciechowski MS,
Shochat E, Sapir N and Maggini I
(2021) Evaporative Water Loss
and Stopover Behavior in Three
Passerine Bird Species During
Autumn Migration.
Front. Ecol. Evol. 9:704676.
doi: 10.3389/fevo.2021.704676
Evaporative Water Loss and
Stopover Behavior in Three
Passerine Bird Species During
Autumn Migration
Bernhard Paces1, Barbara M. Waringer1, Adi Domer2, Darren Burns2, Yoram Zvik2,3,
Michał S. Wojciechowski4, Eyal Shochat2, Nir Sapir5and Ivan Maggini6*
1Division of Tropical Ecology and Animal Biodiversity, Department of Botany and Biodiversity Research, Faculty of Life
Sciences, University of Vienna, Vienna, Austria, 2Department of Life Sciences, Ben-Gurion University of the Negev,
Beersheba, Israel, 3Hoopoe Ornithology & Ecology Center, Yeroham, Israel, 4Department of Vertebrate Zoology
and Ecology, Faculty of Biological and Veterinary Sciences, Nicolaus Copernicus University, Toru ´
n, Poland, 5Department
of Evolutionary and Environmental Biology, and Institute of Evolution, University of Haifa, Haifa, Israel, 6Konrad-Lorenz
Institute of Ethology, University of Veterinary Medicine Vienna, Vienna, Austria
Migratory birds are often not specifically adapted to arid conditions, yet several species
travel across deserts during their journeys, and often have more or less short stopovers
there. We investigated whether differences in thermoregulatory mechanisms, specifically
evaporative cooling, explain the different behavior of three passerine species while
stopping over in the Negev desert, Israel. We measured cutaneous water loss (CWL)
under ambient conditions and the temperature of panting onset in an experimental
setup. In addition, we performed behavioral observations of birds at a stopover site
where we manipulated water availability. Blackcaps had slightly higher CWL at relatively
low temperatures than Willow Warblers and Lesser Whitethroats. When considered
relative to total body mass, however, Willow Warblers had the highest CWL of the
three species. Blackcaps started panting at lower ambient temperature than the other
two species. Taken together, these results suggest that Willow Warblers are the most
efficient in cooling their body, possibly with the cost of needing to regain water by
actively foraging during their staging. Lesser Whitethroats had a similar pattern, which
was reflected in their slightly higher levels of activity and drinking behavior when water
was available. However, in general the behavior of migratory species was not affected
by the availability of water, and they were observed drinking rather rarely. Our results
indicate that differences in thermoregulatory mechanisms might be at the basis of the
evolution of different stopover strategies of migratory birds while crossing arid areas
such as deserts.
Keywords: Negev, thermoregulation, panting, cutaneous water loss, water availability
INTRODUCTION
Thermoregulation in desert habitats is a challenge for endothermic animals. When ambient
temperatures (Ta) exceed body temperature (Tb), they need to dissipate excess heat produced
endogenously as well as gained from the environment to regulate Tb. Consequently, several
behavioral and physiological strategies have evolved among desert-living animals to cope with
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Paces et al. Thermoregulation of Migratory Birds
these conditions. Behavioral strategies include avoiding exposure
to excessive heat by e.g., living in burrows, or being active
when temperatures are not at their maximum (Yousef and Dill,
1971;Abáigar et al., 2018;Whitford and Duval, 2020). The
only way to dissipate body heat at Ta>Tbis to evaporate
water from body surfaces (Dawson, 1982), but since water is
scarce in the desert, several mechanisms have evolved in desert
species to reduce evaporative water loss and avoid dehydration
(King and Farner, 1961;Louw, 1993;Williams and Tieleman,
2005;Donald and Pannabecker, 2015). In birds, evaporative
cooling is primarily achieved through cutaneous water loss
(CWL) and respiratory water loss (RWL) (Whittow, 1986;
Williams and Tieleman, 2005;McKechnie and Wolf, 2019).
The proportion of CWL and RWL to total evaporative water
loss (TEWL) varies among species, but it is generally around
50% at moderate Ta’s (Wolf and Walsberg, 1996;Tieleman and
Williams, 2002;Ro and Williams, 2010). When Taapproaches
or exceeds Tb, birds increase both cutaneous and respiratory
water loss, but the latter to a greater extent (Wolf and Walsberg,
1996;Tieleman and Williams, 2002;Wojciechowski et al., 2021).
With the exception of Columbiforms (McKechnie and Wolf,
2004), respiratory water loss is the main avenue of water loss
when a bird is exposed to heat stress (Wolf and Walsberg,
1996;Tieleman and Williams, 2002;Wojciechowski et al., 2021).
Birds experiencing high rates of TEWL may have difficulties to
keep their body adequately hydrated while maintaining body
temperature below critical hyperthermia (Webster, 1991). Thus,
it becomes an obvious challenge, especially for diurnal birds, to
reduce TEWL while preventing lethal hyperthermia (McKechnie
and Wolf, 2010;Conradie et al., 2020). Tolerance of hyperthermia
is the primary physiological mechanism allowing for water
conservation in heat exposed birds (Calder and King, 1974;
Weathers, 1981;McKechnie and Wolf, 2019). It has been shown
that desert birds have a lower TEWL than species from mesic
areas (Williams, 1996). CWL is reduced through a specific lipid
composition of the skin’s stratum corneum, which makes it
less permeable to endogenous water (Tieleman and Williams,
2002;Haugen, 2003;Haugen et al., 2003;Muñoz-Garcia and
Williams, 2011;Champagne et al., 2012). A reduction of RWL
in desert birds as a mechanism of water conservation has been
discussed (Williams and Tieleman, 2005) and was observed in
zebra finches (Taeniopygia guttata) acclimated to limited water
availability (Wojciechowski et al., 2021). However, in the Kalahari
Desert, bird species relying on food as their only water source
started panting at a higher temperature and have overall higher
evaporative scope when compared with species that drink water
(Smit et al., 2016;Czenze et al., 2020). The ambient temperature
of panting onset potentially sets the time boundaries in which a
bird can remain active during the day in a desert environment,
while avoiding the excessive water loss induced by RWL for
thermoregulation at higher Ta(Weathers, 1981;Smit et al., 2016;
Pattinson et al., 2020).
Besides local desert specialists, many temperate-zone birds
stage in the desert for a relatively short time during migration.
In the European-African migration system, around 2.1 billion
passerine and near-passerine birds cross the Sahara Desert
during their autumn migration to reach their wintering grounds
(Moreau, 1972;Hahn et al., 2009). These birds presumably did
not evolve specific adaptations to the extremely arid climate
conditions of the desert, yet most songbirds do not overfly the
Sahara in one non-stop flight, but rather fly at night and stop
over during the day (Biebach, 1985;Bairlein, 1988;Schmaljohann
et al., 2007). Notably, many species avoid long stopovers in the
desert and prolong their flights as much as possible (Adamík
et al., 2016;Jiguet et al., 2019;Malmiga et al., 2021). Nonetheless,
these trans-Saharan migrants are known to perform longer
stopovers prior to the desert crossing during autumn (Yosef and
Chernetsov, 2005). Specifically, many migrating birds stop in the
Negev desert which is located at the northern edge of the Sahara
Desert (Moreau, 1972;Yosef and Chernetsov, 2005). Despite
being defined as an arid environment (Goldreich, 2012), the
Negev is the last potential stopover area before the Sahara Desert
crossing during autumn. Birds that stage at the desert edge are
staging for longer periods, accumulating large amounts of fat to
facilitate the cross-desert travel (Piersma, 1998;Schaub and Jenni,
2000;Wojciechowski et al., 2014). Observational studies showed
that the behavior at desert stopover sites varies among species
(Jenni-Eiermann et al., 2011;Arizaga et al., 2013;Hama et al.,
2013;Maggini et al., 2015). These differences are likely associated
with adaptations to arid habitats: while xerophilic species (e.g.,
many Mediterranean species) spend longer stopovers in the
desert and effectively refuel, mesophilic species usually avoid long
stopovers and spend rather short time on the ground resting in
the shade (Jenni-Eiermann et al., 2011).
The difference in stopover patterns between xerophilic and
mesophilic migratory species may result from differences in
their ability to maintain water balance. Foraging behavior and
fat accumulation of migratory Blackcaps (Sylvia atricapilla, a
mesophilic species) at a desert stopover site was influenced
by water availability, while this was not the case in Lesser
Whitethroats (Sylvia curruca, a xerophilic species) (Sapir et al.,
2004;Tsurim et al., 2008). In addition, Lesser Whitethroats were
able to accumulate energy stores in a similar fashion in a wide
range of habitats, while in Blackcaps this was restricted to a
habitat offering ideal feeding conditions, such as high amounts
of lipid-rich fruits (Sapir et al., 2004;Domer et al., 2018).
In this study, we aimed at understanding the physiological
mechanisms underlying the different behavior of birds at desert
stopovers in relation to water availability and their ability to
maintain water balance. We hypothesized that trans-Saharan
migratory songbird species adjust their stopover behavior in
the desert to minimize the risk of dehydration. We assumed
that species better adapted to arid conditions face lower risk
of dehydration. In particular, we predicted that species actively
refueling at a stopover in the Negev have a lower surface-specific
CWL and express a higher temperature threshold for panting
onset than species which spend their stopover resting in the
shade. We also predicted that an experimental manipulation
of water availability leads to a change in foraging behavior,
especially in species with low refueling rates, inducing an
increase in refueling when water was available. To test these
predictions, we quantified foraging and drinking behavior, CWL,
and temperature of panting onset in Blackcaps and Lesser
Whitethroats, taking advantage of the previous knowledge of
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their different stopover strategies during autumn migration in
Israel (Sapir et al., 2004;Tsurim et al., 2008). We also measured
CWL and panting onset in the Willow Warbler (Phylloscopus
trochilus). This species is regularly observed to actively forage
at desert stopover sites in spring (Jenni-Eiermann et al., 2011;
Maggini et al., 2015). If indeed differences in thermoregulatory
CWL underlie differences in stopover behavior among species,
Blackcaps should have a higher CWL and a lower temperature
of panting onset than the other two species. The augmented
availability of drinking water should increase foraging activity in
all species, but more so in Blackcaps.
MATERIALS AND METHODS
Study Site
We collected data during the autumns of 2017 and 2018 at two
stopover sites in the Negev Desert, Israel (Figure 1). In 2017,
FIGURE 1 | The location of the two field sites in Israel. The study was conducted at Lake Yeruham in 2017, and at Midreshet Ben-Gurion in 2018.
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Paces et al. Thermoregulation of Migratory Birds
our study site was Lake Yeruham (30◦590N, 34◦530E), a
large artificial waterbody in the northern Negev. The vegetation
was dominated by Phragmites australis, Tamarix aphylla, and
Tamarix nilotica as well as Xanthium strumarium. At some
distance from the lakeshore, the most common plant species were
Acacia raddiana, Atriplex halimus, Morus sp., and P. australis.
During autumn 2018 we collected data at Midreshet Ben-Gurion
(30◦510N, 34◦460E), approximately 19 km south of the 2017 site.
This site includes an experimental mixed Pistacia tree plantation
(1.7 ha) which is populated mainly with two species, Pistacia
lentiscus and Pistacia chinensis, in addition to Acacia saligna and
A. halimus.
Study Species
We studied Blackcaps, Lesser Whitethroats and Willow Warblers.
These three species differ in body mass and size (Shirihai and
Svensson, 2018; own data in Table 1) and have similar breeding
origins (Yosef Kiat, Israeli Bird Ringing Center, unpubl. data).
Blackcaps and Willow Warblers winter mainly in forested areas,
although they are both highly flexible in their habitat selection
(Snow et al., 1997;Shirihai et al., 2001;Sapir et al., 2004;Baker,
2010). Even though both species use similar habitats, they have
different refueling strategies: migratory Blackcaps rely mainly
on pre-departure fattening rather than refueling in desert oases
especially during autumn migration (Izhaki and Maitav, 1998;
Sapir et al., 2004;Tsurim et al., 2008;Wojciechowski et al., 2014),
and Willow Warblers spend more time foraging en route and
carry relatively low fuel loads (Jenni-Eiermann et al., 2011;Haran
and Izhaki, 2013;Maggini et al., 2015). The preferred winter
habitats of Lesser Whitethroats are savannas with scattered trees
or thornbush savanna (Snow et al., 1997;Shirihai et al., 2001;
Sapir et al., 2004). The refueling strategy of Lesser Whitethroats
is not thoroughly studied, but they show positive refueling rates
in the region of our study (Sapir et al., 2004).
Field CWL Measurements
To quantify differences in evaporative water loss among bird
species we conducted CWL measurements at Midreshet Ben-
Gurion during autumn 2018. Birds were captured using mist nets.
Captures started at 5:30 AM and were stopped when ambient
temperature exceeded 30◦C. Captured birds were marked with
aluminum leg ring, after which the length of the folded wing
and body mass were measured using international standards
(Bairlein, 1995). Then, the birds were kept in a cotton bag
in a shaded location until CWL measurements were taken.
TABLE 1 | Mean body mass and wing length (mean ±1 SD) of the three species
measured in this study.
Species Body mass (g) Wing length (mm)
Blackcap (S. atricapilla,n= 205) 17.9±2.5 76.7±2.0
Lesser Whitethroat (S. curruca,n= 118) 12.7±1.7 67.0±2.1
Willow Warbler (P. trochilus,n= 134) 9.0±1.1 67.2±3.2
The sample size refers to all birds measured with respirometry in 2017 and with the
vapometer in 2018.
Sample sizes differ from later analyses because of the exclusion of birds showing
no changepoint in the analysis of panting onset.
At the beginning of each measurement, we recorded time, air
temperature, and air humidity using a mobile digital thermo-
hygrometer (NeKan EU). Relative humidity (RH, in %) was
transformed to absolute humidity (AH, in g H20 m−3) using
the formula AH = C ×Pw/T, where C is a constant of 2.16679
(gK J−1), Pwis the partial pressure of water vapor in Pa, and
T is the temperature in K. We calculated Pwas Pws (saturation
water vapor pressure in hPa) ×RH. Pws was obtained using the
formula Pws = A ×10 ˆ [m ×T/(T +Tn)], where A, m and
Tnare constants (respectively, 6.1164341, 7.591386, and 240.7263
for temperatures between −20◦C and +50◦C), and T was the
temperature in ◦C.
The measurement was made by an experimenter who exposed
at least 50 mm2of the lateral body apterium under the bird’s
left wing, while wearing latex gloves to avoid moistening of the
bird’s skin by human sweat. Then, five subsequent measurements
of surface-specific CWL were taken using a factory-calibrated
VapoMeterTM (Delfin Technologies, Ltd., Kuopio, Finland,
hereafter: vapometer; du Plessis et al., 2013). We used the small
adapter of the vapometer, which covers 16 mm2of skin (Muñoz-
Garcia and Williams, 2007;Muñoz-Garcia et al., 2012), and each
measurement took about 20–30 s. The whole procedure lasted
between 7 and 10 min, and immediately afterward the birds were
released at the site of capture. Visual fat score (Kaiser, 1993)
was assessed after the vapometer measurement to avoid blowing
moist air onto the bird’s skin.
Temperature of Panting Onset
This part of the study was conducted at Lake Yeruham during
autumn 2017. Birds were captured using mist nets from 5:30 AM
until at least five individuals of the study species were caught.
Captured birds were marked and measured as described above.
We used a flow-through respirometry protocol to measure
the temperature of panting onset. A bird was placed into a two-
compartment respirometry chamber (Wolf and Walsberg, 1996)
with which we intended to measure CWL and RWL separately.
The upper section of the chamber (head) was 8.75 l and the lower
section (body) was 11.25 l. Due to persistent baselining problems,
we failed to measure the absolute values for evaporative water
loss and O2consumption. However, the output allowed us to
record the temperature of panting onset using the sliding heating
protocol (see below). For this analysis we used data from the
upper section of the chamber (head compartment).
We performed the measurements using a sliding heating
protocol. The respirometry chamber with the bird was placed
inside a temperature-controlled box (35 l MobiCool G35). We
started the measurement with the flow rate through the chamber
set to 3.3 l min−1for 15 min to enable a quick washout of the
humidity accumulated in the chamber during the positioning of
the bird. After the washout period, we decreased the flow to 0.66 l
min−1and started the heating of the chamber. Temperature in
the temperature-controlled box was monitored continuously by
a custom-made temperature logger (precision: ±0.1◦C) attached
inside the respirometry chamber. The starting temperature of
the measurements was 31.0 ±3.4◦C and progressively increased
during the procedure at a rate of ∼0.3◦C min−1. We continued
the measurement for at least 5 min after noticing a sharp increase
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in excurrent air humidity in the upper chamber, which was a clear
indication of the onset of panting. On average, the measurement
of one bird took one hour and the average temperature at the end
of the experiment was 39.3 ±1.6◦C. The bird was immediately
released at the end of the trial, after being provided with water.
We did not perform visual observations of bird behavior during
these measurements.
Behavioral Responses to Changes in
Water Availability
We experimentally examined the effect of water availability on the
foraging and drinking behavior of staging birds at Midreshet Ben-
Gurion in 2018. We manipulated water availability at the same
study site in which bird captures with mist netting took place
(see CWL measurements). We created five drinking puddles of
water using plastic sheets and fresh tap water. The puddles were
placed in the shadow of large bushes 6–12 m from the closest
mist net, with the exception of one puddle which was directly
below a net. The plastic sheets were covered with soil before the
puddles were filled to achieve a more natural setting. The puddles
were filled and emptied alternately in a 5-day rhythm. The water
regime change was always conducted at 10 PM. In total, water was
provided on 13 days (two full 5-day periods and one truncated
period at the end of the season), while the puddles were dry on
11 days (two full 5-day periods and one day before the start of the
experiment). One additional artificial water body (150 ×70 cm)
was present at the site. It was built of concrete and had vertical
walls. This reservoir was most likely not a suitable drinking place
for birds, and none were ever observed to use it for drinking or
bathing. However, we covered it with wire mesh (0.5 cm mesh
size) when the experimental ponds were dry and uncovered when
water was provided at the experimental puddles.
We searched for Blackcaps and Lesser Whitethroats along a
transect in the plantation. One observer walked the transect each
day at 09:00, 11:00, 13:00, and 17:00 between September 5 and
September 29 (excluding September 10 and September 16). The
transect was approximately 1090 m long and its coverage took
45 min. The observer scanned vegetational structures (bushes
and trees) along a defined path for at least 2 min during
each round. When a bird was encountered, we classified its
behavior in one of the following four categories: (1) moving,
(2) foraging, (3) resting, and (4) grooming. We observed each
individual for 30–300 s and assigned a single behavior to each
bird. When more than one behavior was expressed, we chose
the behavior that lasted longer during the observation. Moving
was defined as occasions when the bird was jumping or flying
around. If during the movement the bird was seen pecking or
eating at least once during the observation, we classified its
behavior as foraging, because we assumed that movement could
be related to food-searching. Resting was defined as cases when
the bird just perched on a branch without undertaking any
other activity. Grooming was defined as the bird taking care
of its plumage during the observation time. It never occurred
that a bird was foraging and resting/grooming during one
observation sequence.
In addition to these observations, we set trail cameras
(Cuddeback Long Range IR) at 80–130 cm distance from the
edge of each artificial puddle. The cameras were attached to sticks
15–20 cm above the ground. They were set to take a picture and
start a video recording for 30 s following every movement trigger
and were active throughout the study period (including when
the puddles were dry). We analyzed all pictures and videos and
recorded all bird species present and the duration of their visit.
Time and date were also recorded.
DATA ANALYSIS
Field CWL Measurements
In a first step of the analysis, we explored the factors that
explained variation in CWL. We used a linear mixed-effects
model with the surface-specific CWL (g m−2h−1, measured with
the vapometer) as a dependent variable. We used the average
of the three lowest vapometer measurements as the response
variable because the measured values decreased gradually from
the first to the fifth measurement, reaching a plateau between
the third and fifth. Since ambient temperature as well as air
humidity influence CWL (Wolf and Walsberg, 1996;Tieleman
and Williams, 2002;Gerson et al., 2014;Champagne et al.,
2016), we included them as independent variables in the analysis,
together with water in the puddles (no/yes), ordinal date, waiting
time in the bag (CWL measurement time - extraction time
from the net), and size-corrected body mass. Size-corrected
body mass was calculated as: [(body mass/length of the folded
wing) ×(length of the folded wing)]. We used species as a
random intercept to be able to detect within-species variation in
CWL in relation to body mass. We eliminated non-significant
predictor variables in a stepwise backward procedure, checking
after every step that model deviance was not affected (Zuur et al.,
2009). We examined all combinations of predictor variables used
in the models for multicollinearity using scatterplot matrices and
correlation coefficients (Pearson’s r). All calculated |r| - values
were below 0.7, which is considered to be a suitable indicator
value above which multicollinearity severely distorts model
estimations (Dormann et al., 2013). The model was tested for
major violations of model assumptions by evaluating diagnostic
plots (Zuur et al., 2009). After identifying the most influential
parameter (which was Ta, see section “Results”), we tested for
interspecific differences using ANCOVA, with surface-specific
CWL as a dependent variable, Taas a continuous independent
variable, species as a categorical independent factor, and the
species ×Tainteraction. The assumptions for ANCOVA were
checked and met.
To determine the variability in total CWL in the three
species, we modeled the slopes and intercepts for each species
as obtained from the ANCOVA model. We obtained hourly
ambient temperature data from the Israel Meteorology Service
station located in Kibbutz Sde-Boker, approximately 3 km north-
east of the Midreshet Ben-Gurion site. In both years September
temperatures ranged between 14.0 and 36.5◦C, which overlaps
with the range of temperatures at which bird CWL was measured.
Using the equations describing the relationship between CWL
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and Ta, we calculated changes in total CWL (g H2O h−1).
Body surface area was calculated as As (cm2) = 10 body mass
(g)0.667 (Walsberg and King, 1978). To simplify the approach, we
assumed that CWL changes during the day only in relation to
changes in Ta. We do realize that this approach is very simplistic,
yet it provides information on the ecologically relevant species
differences in CWL. Daily CWL was obtained by integrating the
total CWL over a given day. Finally, we simulated changes in
CWL using ambient temperature for days in September 2017
and 2018. Integrated total CWL was compared between species
using a repeated ANOVA on ranks. We then compared CWL
as a percentage of total body mass lost during the day in the
three study species.
Temperature of Panting Onset
We used the absolute humidity values from the upper chamber as
a proxy for RWL. We matched the temperature measurements in
the temperature-controlled box with the humidity measurements
from the upper chamber such that our dataset included data
for every minute. We excluded the first 25 min (15 min
washout +10 min equilibrium establishment) from the analysis.
We used breakpoint analysis to identify the temperature at which
a sharp increase in chamber humidity, an indication of panting,
took place. We determined the breakpoint in the curve between
the 26th minute of the measurement procedure and its end
using the “segmented” function provided by the “segmented”
package in R (Muggeo, 2009) and used this breakpoint as the
temperature of panting onset for every individual. Sometimes
the linear increase in RWL after the onset of panting became
exponential toward the end of the measurements. We removed
such points prior to the calculation of the segmented regression
due to their high leverage on the estimate. Birds failing to
show a clear breakpoint were not included in the analysis
(12 out of 88; 3 blackcaps, 4 lesser whitethroats, and 5
willow warblers). We compared the temperatures of panting
onset between species using a one-way ANOVA after we
ascertained that the normality assumption was met, as was the
homogeneity of variances between the samples (Levene’s Test
from medians: F2,73 = 0.473, p= 0.625). We used a Tukey HSD
post hoc test to examine species-specific differences at a 95%
confidence level.
Behavioral Responses to Changes in
Water Availability
The probability of finding moving or foraging birds is
consistently higher than for resting birds. To deal with this
bias, we analyzed the relationship between daily captured and
observed individuals in Blackcaps and Lesser Whitethroats. We
ran a generalized linear model (GLM) with a Poisson error family,
with the number of birds observed as a dependent variable, and
the number of birds captured and the species as independent
variables. The model fit was checked by visually inspecting
diagnostic plots (Faraway, 2016). We cannot exclude that we
observed some individuals multiple times, but we considered
these observations as independent since we were not able to
differentiate among individuals.
All analyses were performed with R 4.0.2 (R Core Team, 2020)
within the RStudio IDE (version 1.4.1717).
RESULTS
Field CWL Measurements
We obtained 360 CWL measurements from the three study
species (Blackcap: n= 165, Lesser Whitethroat: n= 89, Willow
Warbler: n= 108). The results of the mixed-effects model are
shown in Table 2. The variables retained in the model were
Ta, AH, date, water in the puddles, and size-corrected body
mass. The effect sizes of AH and date were small and were
considered irrelevant, and in addition, the low t-value (<2)
for AH indicated that this effect was not significant. Tahad a
positive effect on surface-specific CWL, while the availability of
water and size-corrected body mass were negatively correlated
to surface-specific CWL (Table 2 and Figure 2). The ANCOVA
confirmed the positive effect of Taon surface-specific CWL
(Table 3). There were also significant differences between species,
with Blackcaps having higher surface-specific CWL than Lesser
Whitethroats and Willow Warblers (Table 3). This was mostly
due to higher values at low temperatures, as confirmed by the
significant difference in the slope of surface-specific CWL in
relation to Ta(Table 3 and Figure 3).
Daily absolute CWL simulated by our model equaled:
2.025 ±0.085 g H2O day−1in Blackcaps, 1.520 ±0.083 g
H2O day−1in Lesser Whitethroats, and 1.230 ±0.072 g H2O
day−1in Willow Warblers. Expressed as a percentage of body
mass, Blackcaps would lose 11.31 ±0.47%, Lesser Whitethroats
11.96 ±0.65%, and Willow Warblers 13.71 ±0.80% of body mass
daily by cutaneous evaporation only (Figure 4). These differences
among species were statistically significant (rm ANOVA on
ranks, χ2= 120, df =2,p<0.001).
Temperature of Panting Onset
We estimated the temperature of panting onset of 76 birds
(Blackcap: n= 30, Lesser Whitethroat: n= 25, Willow Warbler:
n= 21). It differed significantly between the three study
TABLE 2 | Results of a linear mixed-effects model with surface-specific CWL as
dependent variable.
Fixed effects:
Estimate Std. error t-value
Intercept −4.066 3.888 −1.046
Ta0.416 0.023 17.844
Ambient humidity 0.046 0.042 1.106
Date 0.028 0.013 2.123
Water (yes) −0.487 0.188 −2.590
Size-corrected body mass −0.135 0.044 −3.098
Random effects:
Variance Std. dev.
Species Intercept 0.752 0.867
Residual 2.964 1.722
N = 360 observations of three species.
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FIGURE 2 | Relationship between body mass and surface-specific CWL in the three study species. In all three species, there is a negative relationship between body
mass and CWL.
species (one-way ANOVA: F2,73 = 5.137, p= 0.008, Figure 5).
Blackcaps started panting at a lower temperature (mean ±1
SD: 36.5◦C±1.6◦C) than Lesser Whitethroats (37.6◦C±1.5◦C;
Tukey HSD post hoc Test: adj. p= 0.048) and Willow Warblers
(37.9◦C±1.8◦C; Tukey HSD post hoc Test: adj. p= 0.020).
Lesser Whitethroats and Willow Warblers did not differ in their
temperature of panting onset (adj. p= 0.804).
Behavioral Responses to Water
During autumn 2018 we captured 181 Blackcaps, 89 Lesser
Whitethroats and 133 Willow Warblers. During 90 transects
(45 min each, totaling 67.5 h) we observed 26 Blackcaps and 83
Lesser Whitethroats. The number of birds observed increased
on average by 0.12 ±0.04 with every captured bird (GLM:
z= 3.02, p= 0.003), and the slope of the increase was not
TABLE 3 | Results of the ANCOVA with surface-specific CWL as a
dependent variable.
Coefficients
Estimate Std. error tvalue p
Intercept 0.637 0.998 0.638 0.524
Ta0.461 0.041 11.162 <0.001
Species (Blackcap) 3.386 1.310 2.585 0.010
Species (L. Whitethr.) 0.726 1.472 0.493 0.622
Ta×Species (Blackcap) −0.119 0.052 −2.268 0.024
Ta×species (L. Whitethr.) −0.041 0.060 −0.680 0.497
Residual standard error was 1.757 on 356 degrees of freedom.
Adj. R2= 0.505, F5,356 = 74.68, p <0.001.
In this table, the Willow Warbler is used as a reference category for the
effects of species.
different between species (GLM, interaction term species ×birds
captured: estimate = 0.01 ±0.06, z= 0.14, p= 0.888). Significantly
more Lesser Whitethroats were observed along the transects than
Blackcaps (GLM, main effect of species: estimate = 1.69 ±0.51,
z= 3.29, p= 0.001).
Most birds were observed moving or foraging in the vegetation
(Blackcap: 92.6%; Lesser Whitethroat: 95.1%). The remaining
birds were resting (Figure 6). The proportion of foraging and
moving birds did not differ significantly between days with water
availability and days with no water (Chi-square test: χ2= 0.050,
df = 1, p= 0.822). Comfort behavior and resting were excluded
from the test due to small sample sizes or lack thereof.
In 2018 we recorded 143 individuals from 13 bird species
at the artificial puddles. The most abundant were resident bird
species, while only a few migratory birds occurred at the ponds
for drinking. Of our focal species, four Blackcaps, nine Lesser
Whitethroats and four Willow Warblers were observed at the
puddles. Mean duration of stay at the puddle did not differ
among the three species (one-way ANOVA: F2,13 = 0.342,
p= 0.717, Table 4).
DISCUSSION
We found partial support to our prediction that our three study
species would have different adaptations to arid conditions.
Blackcaps had slightly higher surface-specific CWL than Lesser
Whitethroats and Willow Warblers, but this difference was
mostly due to higher CWL at Ta’s well below Tb. When
extrapolated over the whole body surface, the species with the
highest overall CWL were also the ones showing higher activity
levels, which is against our expectations. However, as predicted,
the onset of panting occurred at lower Tain Blackcaps compared
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FIGURE 3 | Relationship between Taand surface-specific CWL in the three study species. Blackcaps (green) had significantly higher overall CWL than the other two
species, as a result of higher values at low Ta.
to the other two species. The availability of water did not seem
to influence the birds’ activity. Taken together, these results do
not support the hypothesis that the activity of birds at a stopover
site would be associated with the risk of dehydration. However,
physiological constraints related to water can help explain the
birds’ behavior.
The measured maximum CWL ranged between 34 and 36 mg
H2O cm−2day−1, and were within the range of 12 temperate
zone passerine bird species (21.8–35.8 mg H2O cm−2day−1)
FIGURE 4 | Daily CWL of the three study species as simulated from our
empirical data. Each point represents a single day in September 2017 (red
dots) and 2018 (gray dots). The values are given as percentage of body mass
(taking the average body mass for each species as estimated in this project,
Table 1). Different letters indicate significant difference between medians
(Tukey test: p<0.001).
measured in dry conditions (Ro and Williams, 2010). Our
simulated data show that this represents a daily CWL of 11–13%
of the total body mass of the focal species. Though we have no
data on RWL, we can assume that this would have similar values,
because in passerines, at Ta’s below the panting threshold, there
is an approximate 50:50 ratio of CWL and RWL (Tieleman and
Williams, 2002;Muñoz-Garcia and Williams, 2005). Therefore,
assuming that a bird would sit completely still in a shaded
area during a whole day, its TEWL would be in the range of
20–26% of body mass, depending on the species. This by far
exceeds the 11% dehydration threshold for the maintenance of
coordination in small passerines (Wolf and Walsberg, 1996). In
the bird species measured so far, total body water in healthy
individuals is about 60–65% of body mass (Hughes et al., 1987;
Ellis and Jehl, 1991;Speakman, 1997). Our predicted water loss is
therefore in the range of 31–43% of the total body water. This
implies that birds must replenish their water reserves to avoid
death by dehydration. Foraging activity might expose the animals
to higher Taand, possibly, direct sunlight. This, together with
an increase in metabolic heat production due to muscular work
would sharpen the need for evaporative cooling and result in even
higher water loss.
While part of the lost body water might be produced
metabolically (Morrison, 1953), the main avenue for obtaining
additional water for most bird species is food, especially when
no drinking water is available. Some species are even known
not to drink when surface water is available (Smit et al., 2016;
Czenze et al., 2020), and for these species it is imperative to
obtain their water through foraging. Despite the percentage of
active birds observed was similar for Lesser Whitethroats and
Blackcaps, the proportion of observed to trapped birds was
much higher for Lesser Whitethroats. This suggests that inactive
Blackcaps were likely underrepresented in our observation study,
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FIGURE 5 | Temperature of panting onset in the three study species. Species marked with the same letters (a, b) were not significantly different. Willow Warbler
(orange): n= 21; Blackcap (green): n= 30; Lesser Whitethroat (blue): n= 25.
FIGURE 6 | Behavior of Blackcaps and Lesser Whitethroats at Midreshet Ben-Gurion in September 2018. Behavioral observations were not performed on Willow
Warblers. Blackcap: n= 26; Lesser Whitethroat: n= 83. In Lesser Whitethroats, values for resting and grooming behavior were 3.6 and 1.2%, respectively.
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TABLE 4 | Number of birds recorded and mean duration of stay (±SD, only for
species with N>3) at the artificial puddles during the study in 2018.
Species Water Total
captures
Mean duration
(sec)
Yes No
European Turtle Dove Streptopelia
turtur
2 2 1
Red-backed Shrike Lanius collurio 1 0 18
White-spectacled Bulbul
Pycnonotus xanthopygos*
51 0 13 24.4±7.9
Willow Warbler Phylloscopus
trochilus
4 0 122 12.3 ±10.9
Blackcap Sylvia atricapilla 4 0 143 18.5 ±8.6
Common Whitethroat Sylvia
communis
5 0 10 21.0±6.7
Eastern Orphean Warbler Sylvia
crassirostris
1 0 12
Lesser Whitethroat Sylvia
curruca
9 0 89 15.3 ±11.4
Arabian Babbler Turdoides
squamiceps*
14 1 0 16.7±9.6
Spotted Flycatcher Muscicapa
striata
1 0 11
Rufous-tailed Scrub Robin
Cercotrichas galactotes
30 17 3 22.1±9.5
Ortolan Bunting Emberiza hortulana 1 0 1
Target species are outlined in bold and resident species are marked with *.
The total number of captures refers to the period 05.09.2018–27.09.2018 and is
given as a proxy for the abundance of the species.
However, species of large size might be underrepresented because mist nets are
not designed for capture of these species.
because of lower detectability. This suggests that, overall, Lesser
Whitethroats are more active than Blackcaps, which can be
associated with the higher percentage of body water that they
lose through CWL. Unfortunately, we have no data on the
activity of Willow Warblers, but previous studies conducted in
the Sahara Desert showed that they are also actively foraging
during stopovers (Jenni-Eiermann et al., 2011;Maggini et al.,
2015). Intriguingly, these differences do not seem to have arisen
by different adaptations of the skin membranes among species
(as shown e.g., in larks and sparrows, Tieleman and Williams,
2002;Muñoz-Garcia et al., 2012), since the surface-specific rate
of CWL was fairly comparable among species. It is possible that
a difference would be observable during spring migration, since
Blackcaps spend the winter in more mesic habitats than Lesser
Whitethroats (Snow et al., 1997;Shirihai et al., 2001) and their
skin membranes might be accordingly flexibly adjusted to the arid
conditions at the wintering grounds (Muñoz-Garcia et al., 2008).
The higher percentage of water loss in the Willow Warbler could
be an indication of higher evaporative cooling efficiency (the rate
of heat loss over heat production). As a result, this species may
afford higher activity and exposure to higher Ta, provided that
the amount of water lost does not exceed a threshold above which
dehydration would pose a death threat (Albright et al., 2017;
Conradie et al., 2020).
The main behavioral and physiological indication of the risk of
dehydration at high ambient temperatures is the onset of panting
(Pattinson et al., 2020). The results of this study confirmed the
prediction that Blackcaps have a lower temperature of panting
onset than Willow Warblers and Lesser Whitethroats. The mean
values we measured in the three species (Blackcap: 36.5◦C,
Lesser Whitethroat: 37.6◦C, Willow Warbler: 37.9◦C) were in the
range of temperatures (31.3◦C–46◦C, mean: 39.3◦C) at which
50% of the individuals from 33 different Kalahari Desert bird
species were observed to begin panting (Smit et al., 2016). This
result provides a promising avenue to explain the evolution
of the different use of stopover sites in migratory species.
It also indicates that behavioral characteristics of response to
heat could be relevant for sites outside the desert as well.
It has to be noted that larger species usually initiate heat
dissipation behaviors (e.g., panting and wing drooping) at lower
temperatures than smaller species due to their smaller surface
to volume-ratio (Weathers, 1981;Smit et al., 2016;Pattinson
et al., 2020). This could be an explanation for the observation
in our study. In addition, different adaptations to optimize heat
loss in arid conditions, such as the ability to tolerate high body
temperatures during facultative hyperthermia (Tieleman and
Williams, 1999;Smit et al., 2013, 2016;Nilsson et al., 2016),
the dependence on wing-drooping as alternative heat dissipation
behavior (Smit et al., 2016;Wojciechowski et al., 2021) or
the reduction of metabolic rate (Williams and Tieleman, 2005;
Wojciechowski et al., 2021) may also influence the temperature
of panting onset. These factors clearly indicate new avenues for
further research investigating the response of different species to
dehydrating conditions.
Interestingly, surface-specific CWL was negatively correlated
with body mass in all three species studied. Since body mass is
largely affected by fat stores in migratory birds, this provides an
indication that subcutaneous fat may be directly or indirectly
related to cutaneous evaporation. However, the mechanistic
processes involved are still unknown yet. Surface-specific CWL
values were also lower when water was available in the puddles.
This difference was relatively small (∼0.5 g m−2h−1) but
statistically significant. This may suggest that birds with slightly
lower CWL were more likely to be captured on days where
water was available. This is somewhat counterintuitive, because
we would have expected birds with higher water losses to be
more motivated to replenish their water content by drinking or
foraging more actively. A possible explanation might include a
combination of the effects of body condition (heavier birds –
the ones with lower CWL – could be the ones that are more
active when water is available) and diet. Birds that consume
drier food are more affected by the lack of water (Mizrahy et al.,
2011). These birds might be taking advantage of the availability
of surface water.
Our study integrates physiological and behavioral data for
better explaining differences in stopover ecology among three
migratory species that were about to cross a wide ecological
barrier, the Sahara Desert, on their way from the temperate
breeding areas to their sub-Saharan over-wintering grounds.
Our comparison between captured and observed birds showed
that Lesser Whitethroats are observed far more often than
Blackcaps at the study site, despite the lower number of captures.
This confirms that Blackcaps spend more time resting in deep
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foliage than Lesser Whitethroats at this autumn stopover site
in Israel. Despite simulating Sapir et al.’s (2004) study closely,
our data do not suggest that the availability of drinking water
would affect the behavior of Blackcaps by inducing increased
foraging as they were only observed drinking at the artificial
puddles rarely, and proportionally less than Lesser Whitethroats.
However, Midreshet Ben-Gurion was recently found to act as an
unordinary stopover site. While many passerines during autumn
migration are attracted to it, most of them abandon it during
their first morning (Domer et al., 2018). Given this information,
the behavioral part of this study should be treated accordingly,
as birds will actively forage only a few days after landing
once they fully restored their digestive capacity (Gannes, 2002;
McWilliams and Karasov, 2005).
The results of this study suggest that evaporative water loss
provides an important physiological background that might have
played a crucial role in the evolution of different desert-crossing
strategies in small trans-Saharan migrants. While some species
rely on en route refueling to cross the Sahara, others gain the
necessary amounts of fat prior to the desert crossing (Jenni-
Eiermann et al., 2011;Arizaga et al., 2013;Hama et al., 2013).
Both strategies are successful and enable billions of birds to cross
this large ecological barrier twice a year (Moreau, 1972;Hahn
et al., 2009). However, the populations of many migratory bird
species of the Old World are declining, and especially trans-
Saharan migrants do so to a greater extent than resident or
short-distance migrants (Vickery et al., 2014). Climate change
leads to more arid conditions for the whole African continent
(Nicholson et al., 2018), potentially imposing constraints on
birds that use both refueling strategies before, during and after
crossing the desert. While species which rely on pre-departure
fattening might be confronted with the energetic challenge of
carrying even higher fat loads in order to be able to cross an
enlarged desert barrier, species which refuel en route might
experience more difficulties to find suitable oases for efficient
fat accumulation.
This study provides a first step toward identifying potential
physiological mechanisms that constrain the birds’ behavior
during a challenging phase of their migration. However, many
open questions on the physiological mechanisms involved in
the evolution of different refueling strategies and their species-
specific consequences for the entire migration process remain to
be addressed. We argue that explaining the behavior of migratory
birds through physiological adaptations should be addressed
through a mechanistic approach by applying comparative and
experimental studies.
DATA AVAILABILITY STATEMENT
The datasets presented in this study can be found in online
repositories. The names of the repository/repositories and
accession number(s) can be found below: https://phaidra.
vetmeduni.ac.at/o:669.
ETHICS STATEMENT
The animal study was reviewed and approved by Israel Nature
and National Parks Authority.
AUTHOR CONTRIBUTIONS
IM, ES, and NS conceived the study. BP, BW, DB, and YZ
performed fieldwork. BP, BW, MW, and IM performed data
analysis. BP, BW, AD, MW, and IM wrote the manuscript. YZ,
ES, and NS provided logistical support. All authors read and
approved the final version of the manuscript.
FUNDING
This study was supported by a start-up grant (Profillinien) of the
University of Veterinary Medicine Vienna to IM. The University
of Vienna supported BP with a Grant Abroad (KWA) as well as
a Needs-based Scholarship (Förderstipendium), and BW with a
Needs-based Scholarship (Förderstipendium). NS was supported
by the Israel Science Foundation (Grant 702/17), and MW
was supported by the Polish National Science Centre (Grant
2017/25/B/NZ8/00541).
ACKNOWLEDGMENTS
We thank Ofer Ovadia for allowing us to work at the
Ben-Gurion University of the Negev. We also thank Finja
Strehmann, Sarah Degenhart, and Ron Efrat for their help
during fieldwork. Benjamin Seaman proofread a previous version
of the manuscript. Yosef Kiat from the Israeli Bird Ringing
Center (IBRC), Israel Ornithological Center of the Society for the
Protection of Nature in Israel provided unpublished data of ring
recoveries, the Israel Meteorology Service provided data used in
this work, and Christian Schulze provided the camera traps.
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