University of Groningen
Avian adaptation along an aridity gradient
Tieleman, Bernadine
IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to
cite from it. Please check the document version below.
Document Version
Publisher's PDF, also known as Version of record
Publication date:
2002
Link to publication in University of Groningen/UMCG research database
Citation for published version (APA):
Tieleman, B. I. (2002). Avian adaptation along an aridity gradient: Physiology, behavior, and life history
Groningen: s.n.
Copyright
Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the
author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).
Take-down policy
If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately
and investigate your claim.
Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the
number of authors shown on this cover page is limited to 10 maximum.
Download date: 14-06-2017
CHAPTER 2
Physiological ecology and
b e h a v i o r o f d e s e r t b i rd s
Joseph B. Williams and B. Irene Tieleman
Current Ornithology. Volume 16. Edited by V. Nolan Jr. and C. F. Thompson.
Kluwer Academics/Plenum Publishers, New York. Pp. 299-353. 2001.
ABSTRACT
We have reviewed the current literature on the
physiology and behavior of desert birds. A central
theme has been to examine the hypothesis that
desert birds do not possess unique physiological
adaptations to their environment. This timehonored view was originally formulated from
studies of species from the semi-arid deserts of
North America, which are probably 15,000 years
old. Since this view was promulgated nearly three
decades ago, research on the ecological physiology of desert birds has progressed slowly, in part
because fewer investigators are actively working
in this arena. We hope that our synthesis of the
work that has appeared in the last two decades
raises questions about the validity of this hypothesis. Using traditional least squares regression
analysis and regressions that employ phylogenetically independent contrasts, we have forged new
hypotheses that suggest that some desert birds
may have evolved physiological mechanisms that
promote low basal metabolic rates, low field metabolic rates, and low rates of evaporative water
loss. We hope that our views will stimulate colleagues to think about questions involving the
evolutionary and ecological physiology of desert
birds, and that challenges to the ideas in this
review will contribute to a resurgence of effort in
this area of physiological ecology.
ABSTRACT
BIRDS
DESERT
OF
BEHAVIOR
AND
ECOLOGY
PHYSIOLOGICAL
I n t ro d u c t i o n
Two major evolutionary events that shaped current vertebrate life forms were the
transition from water to land during the Carboniferous and the development of
endothermy during the Triassic (Freeman and Herron 1998). As a result of the
former, nascent terrestrial animals experienced new ecological opportunities,
while at the same time they confronted new physiological challenges such as
maintaining an aqueous internal milieu in a desiccating environment (Gordon
and Olson 1995). With the advent of endothermy, land animals presumably
increased their fitness, but their need for energy also rose by as much as an order
of magnitude compared to their ectothermic ancestors (Bennett and Dawson
1976; Bartholomew 1982). Endothermy also exacerbated problems of water loss
because high rates of metabolism were associated with elevated respiratory water
loss as well as increased water loss via urine and feces.
With low rainfall, low humidity, and high ambient temperatures (Ta), arid environments represent an extreme departure from the aqueous milieu in which vertebrate ancestors once lived. Because deserts differ markedly in climate, and
because species living in them are exposed to unique combinations of environmental parameters, the practice of collectively placing all species that reside in
these regions under the rubric “desert” limits the resolving power of comparative methods. In this review we use the term desert in the broadest sense to include all arid lands, but we also emphasize the dissimilarity of desert environments
by categorizing them as semi-arid, arid, or hyperarid (Meigs 1953). Despite the
desirability of making this distinction among desert environments, a paucity of
data has forced us in many of our analyses to classify species as desert or nondesert. We hope that future reviews will not be shackled by this impediment.
Birds that occupy arid environments face acute problems of energy and water
balance because of their high mass-specific water and energy requirements. A
lack of rain and consequent low primary productivity means that most deserts
provide scant food resources and little to no drinking water. Thus, only a few species of birds have evolved the capability to occupy desert environments, and the
ones that do should possess a number of adaptations that permit existence in
such extreme environments. Yet, numerous species of birds reside in deserts,
some during favorable periods, other permanently as residents.
Physiological ecologists have long been aware that organisms living in extreme
environments are likely to provide examples of evolutionary adaptation
(Bartholomew 1986). However, despite the fact that desert environments are
among the most extreme on earth, the current paradigm holds that desert birds
lack unique structural or physiological adaptations for contending with heat and
aridity (Maclean 1996). Bartholomew and Cade (1963) first promulgated this
view by saying “any bird which can satisfy its other habitat requirements in the
desert is a candidate for establishment there because it is likely to be as effective
21
physiologically as most birds already occupying this environment”. Maclean
(1996) espoused the same perspective: “what seems to be adaptive in birds to the
desert environment is in fact intrinsic to the avian condition”.
This chapter is a general review of the physiological mechanisms and behaviors
used by desert birds to survive in their environment. A central motif in our work
is to question some current thinking about whether birds in deserts have or have
not evolved physiological specializations that permit them to occupy desert environments. We develop our ideas around a tripartite conceptual model based on
mechanisms that influence energy balance, water balance, and thermoregulation
(Figure 1). First, we explore how energy expenditure may differ in desert birds
and ask whether basal metabolism and field metabolism are reduced in desert
birds. Second, we examine ways in which desert birds might cope without drinking water and ask whether they have evolved mechanisms that promote fluid
homeostasis with reduced water intake. Third, because some deserts have the
highest environmental temperatures on earth, we investigate behavioral and
physiological mechanisms employed by desert birds to maintain their body temperatures below lethal limits. Finally, we emphasize how linkages among energy,
water, and thermoregulation function in concert to allow birds to live in deserts.
Comparative Methods
Physiological ecologists seek to understand how organisms function in their
Figure 1. A conceptual model relating energy, water, and thermoregulation in desert birds.
22
BIRDS
DESERT
OF
BEHAVIOR
AND
ECOLOGY
PHYSIOLOGICAL
natural environment (Prosser 1986) and to acquire insights into the evolutionary forces, both past and present, that are responsible for the success of present day
phenotypes (Calow 1987; Bennett and Huey 1990). Allometry, the consequences of body size on function in organisms, has been a useful tool in many ecological, physiological, and evolutionary research programs (Calder 1984; SchmidtNielsen 1984a; Bradshaw 1986; Randall et al. 1997). Recently the use of traditional least-squares regression (LSR) in comparative analyses has been challenged
on the ground that species can not be considered as statistically independent
from each other because of their common evolutionary decent (Pagel and
Harvey 1988; Garland and Carter 1994). In effect, phylogenetic non-independence reduces the degrees of freedom permitted in hypothesis testing and affects
parameter estimation in statistical analyses (Grafen 1989; Martins and Garland
1991). To circumvent this problem, Felsenstein (1985a) designed a method
using phylogenetic independent contrasts (PIC) for phenotypic traits that
exhibit continuous variation; this method emerged as an often used technique
that ostensibly eliminates phylogenetic heritage in analyses (Martins and
Garland 1991; Garland and Carter 1994).
Because the incorporation of phylogenetic information into questions about evolutionary physiology is in its infancy, it comes as no surprise that disagreement
exists concerning the use of techniques that purportedly eliminate historical bias
(Miles and Dunham 1993; Westoby et al. 1995; Ricklefs and Starck 1996;
Björklund 1997). In truth, no matter whether LSR or PIC is used, problems exist
that hinder interpretations. Traditional LSR assumes instantaneous speciation of
the taxa being studied, i.e., a star phylogeny (Garland et al. 1992). Few biologists
would support the view that a star phylogeny accurately represents past evolutionary history. In contrast, PIC assumes a stochastic model of evolutionary
change, that of Brownian motion, which is a questionable assumption. Further,
PIC assumes that a phylogeny and its associated branch lengths are known; the
actual evolutionary descent of birds will likely never be completely resolved. In
using the PIC method, we have employed the phylogenetic tapestry of Sibley
and Ahlquist (1990), a hypothesis based on DNA-DNA hybridization. When
phylogenetic trees of avian descendancy are constructed using morphological
characters, or combinations of morphological characters and molecular evidence, the resulting relationships among taxa differ markedly from the Sibley and
Ahlquist tree (J. L. Cracraft, pers. comm.). When trait means are subtracted from
each other as in the PIC method, error variances are additive with the result that
the confidence one has in the estimation of slope and intercept values is weakened (Ricklefs and Starck 1996). Finally, in some situations contrasts may eliminate variation attributable to natural selection (Westoby et al. 1995; Starck
1998). It is this latter variation that we are attempting to identify in this review.
Because of these problems, we employ the conservative strategy of using both
23
conventional LSR and regressions based on PIC in our quest to understand the
evolutionary physiology of desert birds.
Deserts of the world
Definitions
Definitions of deserts abound, varying according to the author’s expertise and/or
purpose of enquiry, though regions delimited as deserts broadly overlap regardless
of which method is used to describe them (Köppen 1931; Shantz 1956;
McGinnies 1979; Shmida 1985; Thomas 1997). Noy-Meir (1973) described
deserts as “water-controlled ecosystems with unpredictable rainfall”, whereas ElBaz (1983) suggested that any region receiving less than 250 mm of rain per year
qualified as a desert. Some authors have characterized deserts by ascribing boundaries from criteria based solely on precipitation (Noy-Meir 1973; Grove 1977;
Shmida 1985). Hunt (1983) considered semi-arid, arid, and hyperarid deserts as
regions with an annual rainfall of 254-508 mm, 127-254 mm, and <127 mm,
respectively, but conceded that boundaries of deserts as delimited by moisture
shifted depending on such variables as Ta and seasonality of rainfall. We adopt
the classification system of Meigs (1953), who categorized deserts along a continuum from semi-arid, to arid, to hyperarid. Meigs based his system on
Thornthwaite’s (1948) index of moisture availability (Im), a complex parameter
incorporating rainfall, maximum air temperature (Ta) of the hottest month, and
minimum Ta of the coldest month. When evapotranspiration exceeds moisture
availability, as it does in deserts, Im obtains a negative value. In the Meigs’ scheme,
the Im of semi-arid, arid, and hyperarid regions is -20 to -40, -41 to -57, and < -57,
respectively. In addition, Meigs characterized as hyperarid only if there was one
documented occurrence of at least 12 consecutive months without rain.
Causes of aridity
24
Arid conditions occur when evapotranspiration from the earth’s surface exceeds
water influx, a situation attributable to one or a combination of four factors: high
pressure zones, continentality, rain shadows, and cold ocean currents (Bender
1982; Evenari 1985; Allan and Warren 1993; Thomas 1997). Most deserts lie
between 20° - 30° N and S latitude, in or near the sub-tropical zone, along a belt
of high pressure created by descending air masses below the sub-tropical jet stream
(Smith 1984). Near the equator, air is heated by a combination of intense solar
radiation and latent heat of condensation released into the atmosphere by cloud
formation. The heated air rises to the troposphere, where it begins to move
towards the poles in both hemispheres. Upon reaching the subtropical zone,
these large air masses descend, producing a belt of high pressure at the earth’s
surface. High pressure coupled with low relative humidity attributable to the
warming of the descending air mass, produces conditions unfavorable for cloud
formation. The Sahara in northern Africa, the Namib in southern Africa, the
Figure 2. Semi-arid (light grey), arid (grey), and hyperarid (black) regions of the world, based
on Meigs (1953).
PHYSIOLOGICAL
ECOLOGY
AND
BEHAVIOR
OF
DESERT
BIRDS
Arabian of the Middle East, the Atacama of South America, and the deserts of
Australia all lie juxtaposed to the Tropic of Cancer (23°30' N) or the Tropic of
Capricorn (23°30' S), within the sub-tropical zone (Figure 2).
Some arid regions are formed or their aridity is intensified because they are located in the interior of large continents far from sources of water. The Taklamakan
desert of Western China and the Gobi Desert of China and Mongolia are examples of deserts affected by continentality (Chao and Xing 1982).
When air masses that move across continents are forced to rise over mountains,
air cools, moisture condenses forming clouds, and orographic rain falls. As the
moisture-depleted air descends down the lee side of the mountains, it warms and
expands, resulting in a further diminution in relative humidity. Beyond the
mountains, dry winds extract moisture from the soils, enhancing the “rainshadow” effect. The semi-arid Great Basin in North America, situated on the lee
side of the Sierra Nevada and Cascade mountain ranges, and the Kalahari in
South Africa and Botswana, on the lee side of the Drakensberg mountains, owe
their existence largely to this process (Grayson 1993; Werger 1986).
Cold ocean currents that move from Antarctica towards the equator travel along
the western coasts of South America and Africa, where they cool the air layer
above sea and on adjacent land and effectively inhibit the penetration of warm,
moist air that potentially could bring rain (Meigs 1966; Walter 1986; Lancaster
1989). Some of the driest regions on earth, such as the Atacama (influenced by
the Peru or Humbolt Current) and the Namib (influenced by the Benguela
Current), occur along the western coast of continents (Figure 2).
25
Extant Deserts of the world
Of the approximately 149 million km2 of land surface on earth, deserts (semiarid, arid, and hyperarid) cover 52.9 million km2, 36.3% of the total (Meigs 1953;
Thomas 1997; Figure 2). Though all the regions highlighted in Figure 2 fall
under the rubric “desert”, they differ markedly in total area, temperature regime,
soils, and degree of aridity, factors of importance to birds because of their influence on food resources, water availability, and thermoregulatory demands
(Thornthwaite 1948; Bender 1982; Allan and Warren 1993).
The earth’s largest desert, the Sahara in northern Africa, occupies 9 million km2,
an expanse of land equivalent to the entire area of the continental United
States. Consisting of a hyperarid core circumscribed by semi-arid and arid areas,
the Sahara subsumes smaller deserts in eastern Africa, the Nubian Desert of
Sudan, the Ogaden Desert of Ethiopia and Somalia, and the Chalbi and Didi
Galgala Deserts of Kenya (Smith 1984; Allan and Warren 1993; Thomas 1997).
Birds residing in inland subtropical deserts, such as the central Sahara, the Rub’
Al Khali of Saudi Arabia, and the Australian deserts, must contend not only
with the highest Tas on earth, sometimes > 50 °C (Cloudsley-Thompson 1984;
Evenari 1985; Williams and Calaby 1985), but also must endure repeated exposure to these daily extremes, sometimes for several consecutive months
(Nuttonson 1958). Some species can not thermoregulate adequately at these
extreme Tas and suffer significant mortality when they occur (Serventy 1971;
Howell et al. 1974; Rauh 1985). Birds that live in cool, coastal deserts like the
Atacama and the Namib are less likely to encounter such extremes of heat.
Major areas of sand accumulation, known as sand seas, lie in the old world
deserts, the Sahara, the deserts of central Asia, Australia, and the Namib of
southern Africa (Lancaster 1989). Birds living in these areas rarely have access
to drinking water because rainwater quickly penetrates sand. Further, blowing
sand may cover food items, making foraging more problematic.
Differences in aridity affect not only the availability of drinking water but also
primary productivity, an indirect correlate of food supply for birds (Noy-Meir
1973; Louw and Seely 1982; Walter 1986). Regions with extremely low primary
production, such as the hyperarid regions of the world, include the central
Sahara, Rub’Al Khali, Taklamakan, Death Valley and portions of the Sonoran
Desert (Figure 2).
Some coastal deserts like the Atacama, Namib, portions of the Sonoran in Baja
California, and sections of the Sahara close to the Atlantic ocean, despite their
hyperarid status, receive moisture in the form of advective fog (Meigs 1966;
Rauh 1985; Lancaster 1989). When fog occurs, droplets of water develop on
vegetation and provide a temporary source of water for the fauna (Seely 1978).
Although absolute quantities are difficult to measure, estimates of fog precipitation in the Namib range from 30 mm to 150 mm per year (Lancaster et al. 1984).
26
At Gobabeb, a research station in the central Namib about 50 km from the
coast, fog occurs 1-4 days per month (Lancaster et al. 1984). The Namib and
other deserts near the ocean experience modest temperature fluctuations; mean
daily temperature at Gobabeb varies only 6-8 °C between summer and winter,
and the absolute maximum Ta rarely exceeds 40 °C.
Information about the existence of deserts during the Tertiary, when modern
birds diversified, is beyond the purview of this paper. For a general discussion of
the locations of paleodeserts, the reader should consult Van Devender and
Spaulding (1983), Dragàn and Airinei (1989), Zubakov and Borzenkova (1990),
and Frakes et al. (1992). However, we point out that deserts have been a part of
the landscape on earth for millions of years and that the Old World deserts are
DESERT
OF
BEHAVIOR
AND
ECOLOGY
Paleodeserts
PHYSIOLOGICAL
To gain an appreciation of the patterns and processes of adaptations of modernday birds to arid ecosystems, we need information about the time course of avian
evolution, about which taxa have evolved in deserts, and about the types of
paleoclimates that created part, at least, of the backdrop of selective pressures
ultimately responsible for the behavioral and physiological strategies that we
observe today. Unfortunately, the fossil record has remained silent with respect
to which groups of birds lived in desert ecosystems in the past.
The general plan of avian architecture, embodied by the signature fossil of avian
evolution, Archeopteryx, was formed by the mid-Jurassic period, 150 million years
before present (BP) (Feduccia 1996). Fossil discoveries from China and Spain
indicate that by the early Cretaceous period primitive birds were widely distributed with many distinct forms. Most belonged to the Enantiornithae, or “opposite” birds, named for the unique pattern of fusion of the metatarsal bones, proximal to distal, opposite to that of modern-day forms (Walker 1981; Hou and Zang
1993). At the end of the Cretaceous, 65 million years BP, an extinction event
occurred which eliminated entire assemblages of vertebrates including dinosaurs
and all Enantiornithine birds (Alvarez 1987; Chiappe 1995; Feduccia 1996).
Surviving species of birds, all members of the subclass Ornithurae, likely succeeded
because of their ability to live on scant and unpredictable resources, perhaps
seeds, or invertebrates that lived on detritus (Janzen 1995). The early Tertiary
period witnessed rapid diversification of avian species in a period of 5-10 million
years, during which almost all orders of birds except for the passerines evolved
(Daniels 1994). By the end of the Eocene, birds occupied all major ecosystems of
the world. During the mid-Tertiary another radiation occurred, during which
species of the order Passeriformes appeared (Feduccia 1996). Hence, all modern
orders of birds evolved during two radiation events, one in the early Tertiary, the
other in the mid-Tertiary.
BIRDS
Avian Evolution
27
geologically much older than those of the New World. As a result, one might
expect that species that reside in these Old World deserts would have finely
tuned physiological specializations to their environment. For example, the
deserts of northern Africa, the Middle East, and the Arabian Peninsula originated during the Miocene (25 million years BP), when a decline in global temperatures reduced evaporation from tropical oceans and strengthened the high
pressure zones in subtropical latitudes. These regions harbored arid to semi-arid
landscapes for over 20 million years (Miocene to Pliocene), although boundaries
apparently shifted several times during the Tertiary (Frakes 1979; Gerson 1982).
Most agree that by the late Miocene (10 million years BP) arid conditions prevailed throughout southern Africa (Namibia, Botswana, and South Africa) in
what is now the Namib and Kalahari deserts (Kennett 1980; Jones 1982).
In marked contrast to Old World deserts, the deserts of western North America,
now composed of the relatively cold Great Basin and of three warmer deserts, the
Mojave, Sonoran, and Chihuahuan, appeared less than 11,000 years ago
(Axelrod 1983; Van Devender and Spaulding 1983; Mead 1987). During the
early Tertiary a variety of forest types covered much of western North America,
but in the late Tertiary precipitation began to diminish, with the result that
savannah grassland and thorn-scrub assemblages dominated low-lying basins by
the Pliocene (Axelrod 1983). Until about 10,000 years ago, piñon pine-juniper
woodlands occurred over much of the area that is now semi-arid desert in the
southwestern United States (Wells et al. 1982).
E n e rg y
With their high rates of mass-specific metabolism and their existence in environments with low primary productivity, desert birds face the challenge of meeting daily energy requirements. Several authors have suggested that desert-dwelling birds have evolved mechanisms that reduce their energy expenditure as a
means of coping with low food availability (Dawson and Bennett 1973;
Schleucher et al. 1991). Scarcity of water in deserts may be another selective
pressure that favors low rates of metabolism, because the resultant low endogenous heat production may reduce water requirements for evaporative cooling
(Figure 1; Dawson 1984).
Basal metabolic rate
28
Physiological mechanisms that reduce the energy expenditure of free-living birds
are likely to be mirrored in a lower basal metabolic rate (BMR), as measured in
the darkened laboratory on inactive, post-absorptive birds at thermally neutral
temperatures during the rest-phase of their circadian cycle (Aschoff and Pohl
1970; King 1974). Several authors have suggested that desert birds have a reduced BMR (Dawson and Bennett 1973; Weathers 1979; Arad and Marder 1982;
Figure 3. Basal metabolic rate (BMR) as a function of body mass in desert and non-desert species. PIC = phylogenetic independent contrasts.
PHYSIOLOGICAL
ECOLOGY
AND
BEHAVIOR
OF
DESERT
BIRDS
Withers and Williams 1990; Schleucher et al. 1991), but a formal comparative
analysis was performed only recently (Tieleman and Williams 2000). These authors
used traditional LSR and regressions employing PIC on 21 arid and 61 mesic
species from a wide range of geographic origins. They found that desert birds
have a BMR about 17% less than that of non-desert species (Figure 3). ANCOVA
disclosed that the slopes of the least squares regression equations for desert and
non-desert species were not significantly different (F1, 78 = 0.247, P = 0.62), but
that the intercepts differed (F1, 79 = 9.534, P = 0.003). The relationship between
BMR and body mass for birds from mesic habitats is
log BMR (kJ/d) = 0.584 + 0.644 log mass (g)
and for birds from arid areas is
log BMR (kJ/d) = 0.505 + 0.644 log mass (g).
The second approach consisted of calculating PICs (Felsenstein 1985a) and performing a stepwise multiple regression of the standardized contrasts for log BMR
as the dependent variable and log body mass and environment as the independent variables (Williams 1996). Results confirmed that birds from arid environments had a reduced BMR compared to their mesic counterparts. The equation
for BMR of desert birds generated from PICs was
log BMR = 0.304 + 0.702 log mass (g).
29
The physiological mechanisms responsible for a diminution in BMR of desert
birds are unknown, but may involve a reduction in the amount of metabolically
active tissue and/or lower rates of metabolism per unit tissue mass (Daan et al.
1990). The first alternative might be reflected in the size of organs such as the
heart, liver, and kidneys, which have been shown to contribute disproportionately to BMR compared to other tissues (Daan et al. 1990; Konarzewski and
Diamond 1995; Piersma et al. 1996; Kersten et al. 1998). The second explanation, tissues with lower metabolic intensity, might result from differences at the
cellular level, including reduced thyroxine secretion rate (Yousef and Johnson
1975; Scott et al. 1976; Merkt and Taylor 1994), fewer Na+-K+-pumps, or lower
mitochondrial density (Rolfe and Brown 1997).
We emphasize that the relationships between structural design features such as
organ sizes or tissue traits, physiological functions like metabolism, and characteristics of the desert environment such as high Tas or aridity are unresolved. We
do not know whether alterations in BMR are a phenotypic response to thermoregulatory demand, or whether they reflect modifications adapted to the environment (Dawson and O’Connor 1996). However, Hudson and Kimzey (1966)
found that House Sparrows (Passer domesticus) from Houston, Texas, had a significantly lower BMR than did individuals from more northerly latitudes. They
attributed this reduction in BMR to an adaptive modification for living in a hot
environment. Efforts to induce an increase in BMR by prolonged exposure to low
Tas in the laboratory were unsuccessful, indicating that a diminution in BMR in
this population may have been genetically programmed.
Although Tieleman and Williams have found a correlation between a reduction
in BMR and living in a desert environment, not all desert birds conform to this
pattern. The Dune Lark (Mirafra erythrochlamys), the only species that resides in
the Namib sand sea, one of the driest regions on earth, does not show a reduced
BMR, at least during the austral winter (Williams 1999). Williams hypothesized
that the BMR of Dune Larks is relatively high because of their thermoregulatory requirements, a result of a high lower critical temperature (Tlc = 27.9 °C) and
cool nighttime Tas. High thermoregulatory demands may necessitate maintenance of metabolic machinery for chemical heat production, which in turn may
elevate BMR.
Field metabolic rate
The finding of a reduced BMR in desert birds in the laboratory gains further evolutionary significance if it translates to a lower overall energy expenditure in the
field, thereby reducing energy and water requirements in the wild. Nagy (1987)
reported that the field metabolic rate (FMR) of four species of desert birds was
50% lower than that of non-desert species. Recently, Tieleman and Williams
(2000) used a larger data set to reevaluate the hypothesis that desert birds have
30
ECOLOGY
PHYSIOLOGICAL
Figure 4. Field metabolic rate (FMR) as a function of body mass in desert and non-desert species. PIC = phylogenetic independent contrasts.
AND
BEHAVIOR
OF
DESERT
BIRDS
a low FMR when compared to non-desert forms (Figure 4). They generated
equations using LSR for FMR of birds in each habitat category and performed an
ANCOVA. The slopes of these two equations were not significantly different (F1,
77 = 1.7, P < 0.20), but the intercept was significantly lower (F1, 78 = 49.6, P <
0.001). The relationship between FMR and body mass (n = 66) for non-desert
birds was described by
log FMR (kJ/d) = 1.035 + 0.704 log mass (g)
and for desert species (n = 15) by
log FMR (kJ/d) = 0.741 + 0.704 log mass (g).
The FMR of desert species was 49% lower than that of non-desert species.
Tieleman and Williams (2000) also calculated regression equations using PICs.
They performed a stepwise multiple regression forced through the origin, with
log FMR as the dependent variable and standardized contrasts of log body mass
and environment as independent variables. Results confirmed the finding that
FMRs of desert birds are lower than those of their non-desert counterparts (t =
2.11, P < 0.04). The equation for desert birds, generated by this method, was
log FMR (kJ/d) = 0.719 + 0.691 log mass (g).
31
Wa t e r
The hot conditions in many deserts, coupled with the scarcity of drinking water,
create the potential for physiological problems associated with inadequate hydration. These problems might be especially acute for birds, which have the highest mass-specific water loss rates of all terrestrial vertebrates. Selection pressures
to minimize water loss through excretion and evaporation may be counterbalanced
by short-term needs for effective evaporative cooling to prevent overheating
during episodes of heat stress (Figure 1). Therefore it is appropriate to inquire
whether desert species possess special mechanisms that minimize water loss in
the long run but that, when necessary, enable efficient cooling during short
bouts.
Water deprivation
For birds in deserts, the “struggle for existence” includes the task of maintaining
an adequate state of hydration, a necessary requisite for the manifold chemical
reactions that occur in living organisms. Many desert species rely on a combination of metabolic water formed during catabolism of energy substrates and on
preformed water in their diet to supply their entire water requirements. In the
laboratory when supplied with dry foods, most birds die within a few days unless
drinking water is provided (Bartholomew 1972). However, more than a dozen
species have been identified that at moderate temperatures can survive indefinitely in the laboratory solely on a diet of air-dried seeds (< 15% water)
(Bartholomew 1972; Dawson et al. 1979; Maclean 1996). This group includes
parrots from Australia, larks and finches from Africa, and sparrows from the New
World. With the exception of the salt marsh Savannah Sparrow (Passerculus
sandwichensis), all of them live in arid or semi-arid habitats, suggesting that these
environments may have selected for occupants that use water efficiently.
Many desert birds go through periods of water deprivation, when high Tas and
intense solar radiation force them to seek shade (Williams et al. 1995), when
strong winds and blowing sand prevent foraging, or when sources of water are
located far from feeding areas (Heim de Balsac 1936, Dawson 1976). In such circumstances these animals continue to lose water through evaporation, egestion,
and excretion. The loss of this fluid is accompanied by a loss of solids, both contributing to a substantial reduction in body mass. Tolerance of mass loss during
dehydration ranges widely, from less than 30% of initial mass in House Finches
(Carpodacus mexicanus; Bartholomew and Cade 1956), 35% in Brewer’s Sparrows
(Spizella breweri; Dawson et al. 1979), 37% in Mourning Doves (Zenaida macroura; Bartholomew and MacMillen 1960), to almost 50% in California Quail
(Callipepla californica; Bartholomew and MacMillen 1961). For Brewer’s
Sparrows, a species that breeds in semi-arid sage brush associations and winters
in the deserts of the southwestern United States, mass loss was a result of a reduc32
tion in body solids and water. Interestingly, in dehydrated individuals the percentage of body water (~ 67%) was similar to that of hydrated birds. Body composition rather than fluid volume appears to be the variable regulated during
water deprivation in birds, as is also the case for mammals (Chew 1951; Chew
1961; Dawson et al. 1979).
Metabolic water
Figure 5. A comparison, in four species, of the ratio of metabolic water production (MWP) to
total evaporative water loss (TEWL) as a function of ambient temperature.
PHYSIOLOGICAL
ECOLOGY
AND
BEHAVIOR
OF
DESERT
BIRDS
To understand avian water budgets it is useful to determine the extent to which
metabolic water production can replenish evaporative losses (Bartholomew and
Dawson 1953; MacMillen 1990; Williams 1999). In the catabolism of seeds (millet), 1 ml of oxygen consumed yields 0.62 mg metabolic water (Schmidt-Nielsen
1984b). Although an incomplete assessment of a bird’s water budget in its natural environment, the ratio of metabolic water production to total evaporative
water loss (TEWL) approaches ecological significance when one considers that
TEWL in small birds comprises > 70% of total water losses (Bartholomew 1972;
Dawson 1982; MacMillen and Baudinette 1993). A comparison of this ratio
among desert species (Figure 5; Williams 1999) shows that Dune Larks produce
more metabolic water than is lost by evaporation when Tas drop below ~ 20 oC.
Dune Larks may achieve a positive water balance when nighttime Ta falls and
draw upon this reserve during the daylight hours when Tas are higher. For this
species metabolic water production may play a significant role in its water economy. For other species metabolic water contributes less to TEWL. Australian
Zebra Finches (Poephilia guttata), which can live on air-dried seeds in the laboratory, achieve a positive ratio at ~15 °C. For the Inca Dove (Columbina inca) and
Black-throated Sparrow (Amphispiza bilineata), metabolic water production
33
equals TEWL only at very low Tas, indicating that these species are more dependent on preformed water in their diet.
Bartholomew (1972) reasoned that small birds have greater preformed water
requirements than do larger birds. He based his idea on the fact that the slope of
the allometric equation for TEWL scaled as M0.59 (Crawford and Lasiewski 1968)
whereas the slope for standard oxygen consumption was higher, M0.72 (Lasiewski
and Dawson 1967; Aschoff and Pohl 1970). Ratios of metabolic water production (MWP) to TEWL were thought to be positively related to body size.
Williams (1996) reassessed TEWL in birds and found that small birds have
slightly higher ratios (MWP/TEWL) than larger birds, at least at moderate temperatures. Because small birds do not have greater preformed water requirements,
there is no evidence that they are at a disadvantage in desert environments.
Renal structure and function
The avian kidney regulates the concentrations of electrolytes in body fluids,
including Na+, K+, HCO3-, and Cl-; eliminates potentially deleterious nitrogenous
end products, such as uric acid, and to a lesser extent NH3 and urea; and reabsorbs sugars, amino acids, and water from the filtrate. When one considers that
a 35-g bird filters 360 ml of water through its kidneys each day, 16 times its total
body water, the biological significance of water conservation becomes apparent.
Reclamation of this water is especially relevant to birds living in water-limited
environments (Williams et al. 1991a). One might expect that natural selection
has endowed arid-adapted species with unique features in their osmoregulatory
system, allowing them to eliminate nitrogenous wastes and excess ions in a smaller volume of water than is required by species from more mesic environments
(Dantzler 1970).
Kidney structure
34
The architectural design of the avian kidney and its blood supply have been
detailed by Braun and Dantzler (1972), Skadhauge (1981), and Braun (1985
1993). Though both birds and mammals have the capacity to excrete a hyperosmotic urine relative to blood plasma, there are major differences between the
structure and function of their osmoregulatory systems. In birds most nephrons
are loopless, whereas in mammals all nephrons have loops of Henle, albeit of
varying lengths. When birds experience dehydration, they reduce their glomerular filtration rate (GFR), primarily by reducing filtration of the loopless nephrons
(Braun and Dantzler 1972; Williams et al. 1991a), but mammals increase tubular reabsorption of fluids to conserve water (Valtin 1983). Rather than reducing
GFR during dehydration, as many other birds do, the chicken (Gallus domesticus)
increases tubular reabsorption to conserve water (Stallone and Braun 1985). The
mammalian kidney is divided into two discrete regions, the cortex, which contains the glomeruli, Bowman’s capsules, and proximal tubules, and the medulla,
the location of the vasa recta, loops of Henle, and collecting ducts (Valtin 1983;
Koeppen and Stanton 1997). Because in birds these latter three structures, along
with collecting ducts from loopless nephrons, are encapsulated in the medullary
cone, the division of the avian kidney into cortex and medulla is less clear.
DESERT
OF
BEHAVIOR
AND
ECOLOGY
PHYSIOLOGICAL
To compare renal structure among mammals of different size, Sperber (1944) calculated relative medullary thickness, i.e., the longest axis of the medullary region
times 10, divided by the cube root of the three linear dimensions of the kidney
(height x width x depth). He noticed that this ratio was larger in species from
arid habitats than in species from more mesic areas. Subsequent studies on small
mammals supported Sperber’s findings and buoyed the notion that renal structure is different in desert mammals (Schmidt-Nielsen and O’Dell 1961; Heisinger
and Breitenbach 1969). The assumption underlying these findings was that
selection had fashioned a large medullary mass relative to total kidney mass in
species from deserts, and, more importantly, relatively long loops of Henle, and
as a result arid-adapted species excreted a more concentrated urine. Presumably,
the increase in medullary thickness allows a steeper osmotic gradient to be formed by the counter-current multiplier system.
Searching for a similar relationship between kidney structure and function in
birds, Johnson (1974) constructed a measure of relative medullary cone length,
calculated as the mean length of the medullary cones times 10, divided by the
cube root of kidney volume. He found that the medullary cone length of birds
from semi-arid and arid habitats, such as Brewer’s Sparrows, Black-throated
Sparrows, Zebra Finches, and Verdins (Auriparus flaviceps), is greater than that of
more mesic species. Johnson and Skadhauge (1975) extended these observations
by showing that relative medullary cone length was positively related to urine
concentrating ability. Unfortunately, these authors measured concentrations in
cloacally voided urine, now known to differ from ureteral urine as a result of
modification in the lower gastrointestinal tract. Using more modern methods,
Goldstein and Braun (1989) quantified ureteral urine osmolalities of dehydrated
birds and related those measurements to relative medullary cone length. They
found no association between relative cone length and maximal ureteral urine
concentration (Umax), nor did their data suggest that birds from arid habitats
could concentrate their urine more than non-desert species. However, their
sample size was only seven species, two of which were seabirds with salt glands;
birds with salt glands have larger kidneys than other species, which may complicate
comparisons (Calder and Braun 1983). Goldstein and Braun (1989) suggested
that small species could concentrate urine more than larger species, regardless of
habitat affinity, and that Umax and the length of Henle’s loop was negatively correlated in birds. Such a relationship also occurs in mammals and has been
BIRDS
Adaptive significance of renal structure
35
explained, at least in part, by a decline in mass-specific metabolism as body size
increases (Greenwald and Stetson 1988; Beuchat 1990).
The absence of a positive association between Umax and loop length in interspecific comparisons among mammals prompted Greenwald and Stetson (1988) to
suggest that Umax is influenced by transport capacities of the tissues of the thick
ascending limb. They believed that transport capacity is directly related to massspecific metabolic rate, but inversely correlated with body mass. Thus, the relatively lower metabolic rate in larger mammals may be attributable to fewer ion
pumps in renal tissues. Although this hypothesis is largely untested for birds, the
idea that the level of metabolism influences kidney structure may have interesting implications for desert birds. If the desert environment has selected inhabitants for a reduced FMR, then total metabolic waste that needs to be eliminated
by the kidney may be less in these species than in those from mesic environments, evaluated on a mass-specific basis. This suggests that Umax may generally
scale with mass-adjusted rates of field metabolism.
Another ramification of a relationship between level of metabolism and kidney
structure is that kidney tissue has a high rate of oxygen consumption relative to
other body tissues (Daan et al. 1990; Konarzewski and Diamond 1995). Selective
pressures to conserve water may increase the size of the kidney, or the density of
transport enzymes in the tubule epithelia, but also may have to be optimized
against antagonistic pressures to maintain a low BMR.
Urine concentration and habitat
The capability of mammals from desert environments, particularly small rodents,
to produce a more highly concentrated urine than species from more mesic habitats embodies a familiar example of environmental adaptation (Schmidt-Nielsen
1964; Beuchat 1990; Schmidt-Nielsen 1997). Some small rodents that live in
deserts concentrate their urine to ~7,000-9,000 mOsm when deprived of water.
Another way of looking at the functional capacity of kidneys is the examination
of the ratio between the osmolalities of urine and plasma, the U:P ratio, which
ranges from about 20 to 30 among small desert rodents when they are dehydrated. Exceptional water conservation by reabsorption of water in the kidneys may
explain, in part, how desert rodents can live solely on dry food in the laboratory
(Schmidt-Nielsen 1964; Chew 1965).
U:P ratios in water-deprived arid-zone birds, which rarely exceed 2.5, pale in
comparison to values for desert rodents. Some colleagues assert that birds have
not evolved special renal mechanisms in response to arid conditions (Goldstein
and Braun 1989), and some have noted that the ability of birds to fly to distant
water sources in deserts mitigates their need to conserve water (Maclean 1996).
We think that comparisons of renal concentrating ability, specifically of U:P
ratios, between mammals and birds are potentially misleading; we recommend
36
BIRDS
DESERT
OF
BEHAVIOR
AND
ECOLOGY
PHYSIOLOGICAL
caution when using them for three reasons. First, birds excrete primarily uric
acid, a molecule with four nitrogen atoms, which contributes little to the osmotic activity of avian urine (Anderson 1980; Wright 1995). In contrast, mammals
synthesize urea, a highly soluble molecule with only two nitrogen atoms, which
contributes significantly to the osmotic gradient in the medulla and the osmotic
concentration of the urine. Second, spherical, colloidal precipitates of urate in
avian urine sequester electrolytes, removing them from the liquid phase and eliminating them as a contributor to osmotic pressure (Braun 1993). Third, the
denominator of the U:P ratio, plasma osmolality, remains relatively stable in
mammals, whereas in water-deprived birds plasma osmolality can vary by 50-80
mOsm over normal hydration states (Ramsay and Thrasher 1984; Williams et al.
1991a).
Comparisons of renal concentrating ability among birds are few. McNabb (1969)
compared U:P ratios among three species of quail, Bobwhite (Colinus virgianus),
California Quail, and Gambel’s Quail (Callipepla gambelii), whose respective
habitats increase in aridity. Gambel’s Quail, the most xeric species, tended to
produce the most concentrated urine as determined by measurements of cloacally voided urine during periods of water deprivation. Bobwhite quail excreted
urine with the lowest concentration. However, scrutiny of McNabb’s paper reveals that none of these trends was statistically significant. Moreover, the concentrations of electrolytes in the precipitated urate fraction were not measured in
this study and could vary among species. Hence, support for the idea that quail
from arid environments concentrate their urine more than species from more
mesic environments is inconclusive.
An alternative way to evaluate the concentrating ability of the avian kidney,
which can be used for comparisons among birds and for interclass contrasts, is to
compare the moles of nitrogen relative to the moles of water excreted under different regimes of hydration. Kangaroo Rats (36 g), often regarded as the quintessential desert mammal, produce a maximally concentrated urine that contains
7.7 mmoles nitrogen per ml water lost (Schmidt-Nielsen 1964). Desert quail
(150 g), when hydrated, produce 0.71 mmole urate per ml water lost as urine, or
2.9 mmole nitrogen from urates per ml (Anderson and Braun 1985). If 25% of
the total nitrogen lost is in a form other than urate (McNabb and McNabb 1975;
McNabb et al. 1980), then total nitrogen loss is 3.9 mmole N per ml water lost
in urine. Assuming that dehydrated birds produce the same amount of nitrogenous metabolites, and that they concentrate their urine 2.5 fold (Williams et al.
1991a; Braun 1993), these birds would lose 7.7 mmole of nitrogen per ml water
in urine. Similar treatment of data from Pigeons (500 g; Columba livia; McNabb
and Poulson 1970), which occupy both mesic and arid environments, indicates
that at the maximum they excrete 13.6 mmoles N per ml water lost. While we
acknowledge that these calculations, along with their assumptions, are specula-
37
tive, the necessary data required to assess nitrogen loss for any species of waterdeprived bird are not available. Still, these speculations suggest that arid-zone
birds may be as efficient at eliminating catabolic end products as are desert
rodents. An assessment of nitrogen loss by an array of water-deprived individuals from species from both arid and mesic environments would make a meaningful contribution toward our understanding of the selective forces responsible for
systems of avian osmoregulation.
The foregoing discussion does not include the contribution of the lower intestinal tract to water reclamation in birds. Ureters convey urine to the cloaca,
where it is moved by retrograde peristalsis into the rectum (Akester et al. 1967;
Brummermann and Braun 1994). Here the epithelial tissues actively transport
Na+-ions from the intestinal lumen into the extracellular fluid, and water passively follows, a process that potentially reduces water loss in urine when it is finally voided (Skadhauge 1981; Anderson and Braun 1985). Solute-linked water
transport functions to recover water up to luminal osmotic concentrations of 200
mOsm above plasma concentrations (Bindslev and Skadhauge 1971). This integration of kidney function and intestinal water recovery should be included in
calculations of water conservation. During periods of severe dehydration, when
urine osmolalities reach maximum values, waves of reverse peristalsis slow, apparently because the high concentration of urine inhibits water recovery
(Brummermann and Braun 1994).
In a study of 12 species of birds, some inhabitants of the Kara-Kum desert of central Asia and others from more mesic regions in Eurasia, Amanova (1984) reported that lumen contents of the lower intestine in desert birds had a 15% lower
water content than lumen contents of non-desert species. Amanova proposed
that desert species have a greater capacity for absorbing water in their lower
intestine against an osmotic gradient. Because few data were presented to evaluate this assertion, the hypothesis needs further testing.
Evaporative water loss
Total evaporative water loss
Total evaporative water loss, the sum of evaporative water losses through the skin
and from the respiratory passages, is the major avenue of water efflux in birds,
especially for small species in which TEWL is five time greater than urinary-fecal
water loss (Bartholomew 1972; Dawson 1982). Given the central importance of
water balance in the survivorship of arid-zone birds, one might expect adaptations that reduce TEWL in these species. In an early study, Bartholomew and
Dawson (1953) examined the TEWL of 13 North American species from both
mesic and arid habitats and concluded that TEWL did not differ between the
two groups. Williams (1996) tested this hypothesis on a larger data set and
showed that the TEWL of arid-adapted species at a Ta of 25 °C is lower, the dimi38
DESERT
OF
BEHAVIOR
AND
Early investigators assumed that almost all evaporative cooling took place in the
respiratory passages and that cutaneous water loss (CWL) was unimportant in
the process of thermoregulation (Rawles 1960; Bartholomew and Cade 1963;
Mount 1979). More recent work has shown that CWL can equal or exceed evaporation from the respiratory passages at moderate Tas, at least at temperatures
below body temperature (Tb) (Bernstein 1971; Dawson 1982; Webster and King
1987; Wolf and Walsberg 1996b). Few studies have investigated CWL at high
Tas when Tb must be regulated below lethal limits solely by evaporative water
loss (Marder and Ben-Asher 1983; Wolf and Walsberg 1996b). From the data
available, two patterns have emerged (Table 1): some species, especially members of the Columbiformes, rely primarily on CWL to regulate Tb when Ta
ECOLOGY
3.4.2. Cutaneous Water Loss
PHYSIOLOGICAL
nution amounting to as much as 33% (Figure 6). He first used LSR to determine the relationship between TEWL and body mass. For birds from mesic areas
(n = 64),
log TEWL (g/d) = -0.438 + 0.661 log mass (g)
and for birds from arid regions (n = 38),
log TEWL (g/d) = -0.754 + 0.75 log mass (g).
The slopes of these two equations were significantly different (Fslope = 4.0, P <
0.05). His second approach involved PICs and confirmed that birds from arid
regions had a reduced TEWL. Natural selection has apparently reduced evaporative water losses in desert species, but the mechanism(s) that produce this
result are unknown.
BIRDS
Figure 6. Total evaporative water loss (TEWL) as a function of body mass in desert and nondesert species.
39
TA B L E I . Cutaneous water loss (CWL) among species of birds.
Species
Verdin
Habitata
Body Mass
(g)
CWL
(g H2 O/d)
Ta
Source
d
7
12.5
30
40
45
50
30
Wolf and Walsberg 1996
d
0.55
0.87
1.22
1.73
1.68
d
31.6
4.02
30
Bernstein 1971
d
43.2
3.11
35
Lasiewski et al. 1971
d
89
5.45
25
Withers and Williams 1990
d?
112
260
d
d
269
274
472
d
480
20
40
45
52
27
42
45
51
30
35
20
36
40
45
22
Marder and Ben-Asher 1983
d
8.60
25.81
28.76
30.64
15.6
133.53
172.22
164.11
9.04
9.86
9.29
6.46
22.31
23.67
25.46
d
40000
758.4
45
Maloney and Dawson 1998
d
95400
595.3
25
Withers 1983
m
27
1.43
20
Robinson et al. 1976
m
42.3
2.13
30
Bernstein 1971
m
42.6
3.47
30
Bernstein 1971
m,d
109.4
4.41
25
Webster and Bernstein 1987
m
118
146.3
20
36
40
45
21
Marder and Ben-Asher 1983
m
7.6
2.26
8.21
7.36
3.26
m
168
285
20
45
52
20
36
40
45
52
25
30
40
25
43
Ben-Asher 1983
m,d
11.41
44.75
68.94
14.29
13.47
49.93
74.55
114.22
49.94
54.84
64.63
273.48
619.2
Auriparus flaviceps
Zebra Finch
Bernstein 1971
Taeniopygia guttata
Budgerigar
Meloposittacus undulatus
Common Poor-will
Phalaenoptilus nuttallii
Spinifex Pigeon
Geophaps plumifera
Laughing Dove
Streptopelia senegalensis
Spotted Sandgrouse
Pterocles senegallus
Greater Roadrunner
Geococcyx californianus
Chukar Partridge
Alectoris chukar
White-necked Raven
Marder et al. 1986
Lasiewski et al. 1971
Marder and Ben-Asher 1983
Bernstein 1981
Corvus albicollis
Emu
Dromaius novaehollandiae
Ostrich
Struthio camelus
White-crowned Sparrow
Zonotrichia leucophrys
Painted Quail
Coturnix chinensis
Village Weaver
Ploceus cucullatus
Mourning Dove
Zenaida macroura
Japanese Quail
Coturnix japonica
Ringed Turtle Dove
Appleyard 1979
Streptopelia decaocto
Collared Dove
Streptopelia decipiens
Rock Dove
Columba livia
Domestic Fowl
m
2040
m
21500
Gallus gallus
Rhea
Rhea americana
40
a
d = birds from desert habitats; m = birds from mesic habitats.
Marder and Ben-Asher 1983
Richards 1976
Taylor et al. 1971
BIRDS
DESERT
OF
BEHAVIOR
AND
ECOLOGY
PHYSIOLOGICAL
exceeds Tb. Other species, members of the Galliformes and Passeriformes,
employ a combination of CWL and respiratory evaporative water loss (REWL),
the latter facilitated by panting or gular flutter (Bouverot et al. 1974; Wolf and
Walsberg 1996b; Tieleman et al. 1999). However, because only a few observations have been made at high Tas, our understanding of CWL and REWL and of
how these variables are partitioned remains rudimentary
A model that describes CWL is
CWL (g H2O m-2 s-1) = (ρs - ρa)/rv ,
where ρs is the water vapor density (g m-3) at the surface of the skin (assumed to
be saturated at skin temperature), ρa is the water vapor density of external air,
and rv (s m-1) is the total resistance to vapor diffusion (Tracy 1982; Marder and
Ben-Asher 1983; Webster et al. 1985). Mautz (1982) described some of the
important underlying assumptions of this model. Although this equation is rather simple, a number of factors that affect the variables, and as a result the magnitude of CWL, should be borne in mind. Changes in the vapor density gradient
(ρs - ρa), attributable to either an alteration of ρs or of ρa, affect CWL. During
periods of heat stress, CWL may increase because skin temperature increases, and
ρs is a function of skin temperature. However, birds can reduce their CWL by
selecting microsites in which ρa is higher than in the general environment.
The conductance of water vapor, CWL/ (ρs - ρa) (in m s-1), across the skin, feathers, and boundary layer can be visualized as the slope of the equation that relates
CWL (g H2O m-2 s-1) to the vapor density gradient (g H2O m-3) (Appleyard
1979). If this conductance is thought of as the velocity of water vapor movement
from skin to air per unit of gradient, then the reciprocal of this value provides
information about the time required for water to move across a unit of space, a
parameter called resistance. Values of resistance are preferred over measures of conductance because they can be used in calculations involving parallel resistances,
analogous to resistances in electrical circuits. Total resistance varies interspecifically from ~ 25 to 250 s m-1, depending on skin temperature, the degree to which
feathers are fluffed, and species; but the mechanisms that drive this variation are
largely unexplored (Campbell 1977; Webster et al. 1985; Wolf and Walsberg
1996b). Components of rv include resistance to water vapor diffusion across skin
(rs), feathers (rf), and boundary layer (rb); rs accounts for 75 - 90% of rv, at least
at moderate Tas (Appleyard 1979; Webster et al. 1985). Resistances across plumage and boundary layers become larger components of the total rv as Ta increases and rs decreases. Birds often compress their feathers when exposed to high
Tas, which presumably minimizes rf (McFarland and Baher 1968; Appleyard
1979; Withers and Williams 1990).
Avian skin is composed of an epidermis and a well vascularized dermal layer
(Lucas and Stettenheim 1972). For rs to change, birds must vary the diffusion
path length or alter the permeability of the skin to water vapor. During heat
41
stress, birds can increase CWL by vasodilation of the dermal capillary bed, effectively reducing the diffusion path length (Peltonen et al. 1998). Rock Doves
under heat stress not only dilate capillaries but also alter the permeability of skin
to water vapor. As skin temperature increases, the level of hydration in the epidermal cells also increases (Smith 1969; Arieli et al. 1995). In response to high
Tas or dehydration, changes in epidermal lipid conformation within the stratum
corneum may reduce rs by reducing the permeability of the skin to water vapor,
although there are few data to support this idea (Webster et al. 1985; Menon et
al. 1988; Menon et al. 1989; Menon et al. 1996). We suggest that natural selection may have elevated rs in species that occupy hot, dry environments in which
water conservation is of paramount importance.
Cutaneous water loss at thermal neutral temperatures
To test the hypothesis that rs in arid-zone species is higher, and thus CWL lower,
we collated data on CWL (Table 1). The variety of methods used to evaluate
CWL may add significant variation to the data. We adjusted the values for CWL
reported by Marder and Ben-Asher (1983) because they used estimates of external
surface area (SAe) as given by the equation SAe (cm2) = 8.11 mass (g)0.667 rather than
predictions for skin surface (SAs) area from Meeh’s equation SAs (cm2) = 10 mass
(g)0.667 (Walsberg and King 1978).
CWL at moderate Tas (20 - 25 °C) has been reported for 16 species equally divided between occupants of arid and mesic environments (Figure 7). A comparison of slopes and intercepts of regression lines from these two subsets revealed no
significant difference (slope: F1,14 = 0.14; P > 0.5; intercept: F1,14 = 1.9; P > 0.2).
Figure 7. Cutaneous water loss (CWL) as a function of body mass in desert and non-desert species.
42
With data combined, log CWL (g H2O/d) = -0.74 + 0.73 log mass (g). Although
the result is no support for the hypothesis that CWL is reduced in desert birds,
the data are few and hence conclusions tentative. Some species listed in Table 1,
even though assigned to the desert category, were raised in captivity at moderate
Tas with food and water provided ad libitum, conditions which may have altered
properties of the skin that influence resistance. With the exception of the
Verdin, CWL has not been measured in species from hyperarid regions where
selection for water conservation mechanisms is perhaps most intense.
Cutaneous water loss at 45 °C
One can imagine a selective advantage to species that can significantly increase
CWL during bouts of heat stress. Unfortunately measurements of CWL at 45 °C
are available for only five desert species and three non-desert species (Table 1),
too few to make reliable comparisons. For the data combined, log CWL (g/d) =
-0.16 + 0.71 log mass (g). CWL at 45 °C is about 3.5 times higher than values
at thermal neutral temperatures, but the data are inadequate to address the
question whether differences in CWL exist between species that have evolved in
different habitats.
DESERT
OF
BEHAVIOR
AND
ECOLOGY
PHYSIOLOGICAL
Respiratory evaporative water loss (REWL), a parameter influenced by both physiological and environmental variables, can be measured directly or calculated as
REWL = V (ρe - ρi),
where ρe and ρi are the water vapor densities (g m-3) of expired and inspired air,
respectively, and V is respiratory ventilation volume, a product of breathing frequency and tidal volume (Welch and Tracy 1977; Tieleman and Williams 1999).
In most studies, exhaled air is assumed to be saturated, although some authors
question this assumption (Withers et al. 1981; Kaiser and Bucher 1985).
Condensation of water vapor from the exhaled air stream, as it courses over previously cooled membranes of the nasopharynx, is thought to reduce REWL in
birds and mammals (Jackson and Schmidt-Nielsen 1964; Murrish 1973;
Hillenius 1992). When air is inhaled, its temperature rises to that of Tb, and the
air becomes saturated with water vapor from the respiratory passages and the
lungs. Convective heat exchange and evaporation of water in the nasal passages
during inhalation presumably cool the associated membranes, and upon exhalation the air is cooled by these nasal surfaces with the result that water condenses
on them. Schmidt-Nielsen (1981) proposed that counter-current heat exchange
in the nasal passages is an adaptation to arid environments and that desert animals should have more complex nasal turbinates that allow cooling of exhaled
air to temperatures below those of non-desert species, resulting in a larger reduction in REWL in desert species.
Working in the Negev Desert of Israel on Crested Larks (Galerida cristata, 33 g),
BIRDS
Respiratory water loss
43
a widely distributed mesic to semi-arid species typically found near water, and on
Desert Larks (Ammomanes deserti, 19 g), a species restricted to much drier habitats, Tieleman et al. (1999) tested the hypothesis that water recovery in the nasal
passages diminished REWL (and as a result, TEWL) more in Desert Larks than
in Crested Larks. With the nares of Crested Larks occluded, experimental birds
lost from 27% to 0% more evaporative water than did controls over a Ta range
of 15 to 45 °C. Blocking the nares of Desert Larks did not affect their TEWL over
the same Ta range. This study, the only direct test to date of water recovery from
the exhaled airstream in birds, indicates that some birds reduce REWL by recovery of water in the nose, at least at moderate to low Tas, but that others do not.
At high Tas, water recovery in the nares is apparently insignificant.
Tieleman et al. (1999) also examined Schmidt-Nielsen’s (1981) suggestion that
the temperature of exhaled air (Tex) is lower as a result of passage over previously cooled nasal membranes. They compared Tex taken from the nares of Crested
Larks and Tex taken from the open mouth when the nares were occluded. If air
flow through the nasal passages was prevented, nasal membranes would not function as a heat exchanger and Tex should be higher. At moderate Tas, measurements of Tex with the nares blocked gave values 1 - 4 °C higher than those with
the nares open, indicating some cooling of the air stream, but at 35 °C differences were insignificant. They proposed that Tex which probably closely tracks Ta
instead of being determined by evaporation of water on the nasal membranes, is
determined primarily by the temperature of the bill and surrounding tissue.
Effect of hyperthermia on evaporative water loss
The high Tb of birds, around 41 °C (Prinzinger et al. 1991), may “preadapt” them
to desert life because it results in an more favorable thermal gradient between
environment and animal (Bartholomew 1964; Dawson and Schmidt-Nielsen
1964; Dawson 1984; Maclean 1996). Several authors have proposed that tolerance of Tb 2-3°C above normal (hyperthermia) could decrease the amount of
water required for evaporative cooling (Calder and King 1974; Weathers 1981;
Dawson 1984; Withers and Williams 1990). However, Tieleman and Williams
(1999) suggested that the amount of water saved by hyperthermia is a function
of body size and of the duration of the hyperthermic bout, and they pointed out
that gaps in our knowledge of hyperthermia prevent a complete understanding
of its effects on water savings.
Discussions about the potential benefits of hyperthermia have focused on two
factors. First, an increase in the gradient between Tb and Ta causes an increase in
the dry heat flux (Calder and King 1974). If Ta exceeds Tb, the rate of heat gain
from the environment will be reduced. Second, heat stored and dissipated later
when the environment has cooled saves water that otherwise would be used for
evaporative cooling (Schmidt-Nielsen 1964; Dawson and Bartholomew 1968;
Calder and King 1974). Few have considered features of hyperthermia that may
44
increase water loss, such as the augmentation of REWL as a result of greater
water vapor pressures in the lungs when Tb is elevated (Tieleman and Williams
1999). When Tb increases, exhaled air temperature will increase, as does the
amount of water vapor exhaled. In addition, ventilation patterns vary markedly
with Tb, and elevated Tb potentially results in increased ventilation volumes.
The combination of higher water vapor density and increased volume of exhaled air negates some of the hypothesized advantages of hyperthermia
(Tieleman and Williams 1999).
Exploring the combined effects of an improved thermal gradient, heat storage,
and altered respiratory variables in reducing or augmenting water loss in hyperthermic birds, Tieleman and Williams (1999) calculated that during acute (1
hour) exposure to high Ta, birds over a size range of 10-1000 g save about 50%
of their total evaporative water loss by elevating their Tb 3 °C. For chronic (5
hour) episodes of hyperthermia, small birds again save about 50% of their
TEWL, but larger birds save far less. A 1000-g bird may actually lose more water
as a consequence of its elevated Tb than it does if it remains normothermic for 5
hours. These results suggest the hypothesis that, when exposed to high Tas, small
birds should always regulate their Tb at higher levels, but that under some circumstances larger species should not become hyperthermic. This analysis considers only water balance. Hyperthermia also has an impact on a suite of other factors, like energy balance (Seymour 1972), protein stability, and tissue function
(Marder et al. 1989), and this should be kept in view when thinking about optimal levels of Tb of desert birds (Tieleman and Williams 1999).
DESERT
OF
BEHAVIOR
AND
ECOLOGY
PHYSIOLOGICAL
Nagy and Peterson (1988) reported that field water flux of desert forms is lower
than that of species from mesic environments. Their analysis included 18 data
points derived from five desert species; such multiple measurements on individual species inflate degrees of freedom and adds bias to estimates of slope and
intercept in the regression analysis (Pagel and Harvey 1988). Recently, Tieleman
and Williams (2000) collated field water flux rates for 17 desert and 41 nondesert species, and employed two comparative techniques to reevaluate the
hypothesis that desert birds have lower water flux rates than more mesic species
(Figure 8). ANCOVA revealed no significant difference between the slopes of
regression lines for desert and non-desert species, but disclosed a lower intercept
for the equation for desert birds. The relationship between water flux and body
mass in desert birds was described by
log water flux (ml/day) = - 0.126 + 0.724 log mass (g)
and in species from mesic areas by
log water flux (ml/day) = 0.263 + 0.724 log mass (g).
The water flux rates of desert birds amounted to 41% of values for non-desert
species.
BIRDS
Field water flux
45
Tieleman and Williams’ regressions using PICs indicated that water flux rates did
not differ significantly between birds from arid and mesic environments, despite
the wide variety of taxa. Comparisons using PICs and LSR usually yield similar
conclusions when the data are phylogenetically diverse (Weathers and Siegel
1995; Ricklefs and Starck 1996). Given the lack of agreement between these two
comparative approaches, a definitive answer to the question whether desert birds
have a reduced field water flux cannot be given.
The effectiveness of mechanisms that conserve water is often expressed as the
water economy index (WEI; ml water kJ-1), calculated as the ratio of water flux
to FMR (Nagy and Peterson 1988). Nagy and Peterson (1988) tested the hypo-
Figure 8. Water flux rate as a function of body mass for desert (dashed line) and non-desert (solid
line) species; LSR = least squares regression.
thesis that desert birds conserve water more effectively than their mesic relatives
as judged by lower WEI values, but found no statistical support. Utilizing a larger data set, Tieleman and Williams (2000) showed that the average WEI for
desert birds was 0.16 ± 0.06 (n = 14), whereas for non-desert species it was 0.20
± 0.09 (n = 40), values which differ significantly (P = 0.05).
However, inferences about water-conserving mechanisms based on WEI values
should be interpreted with caution because water flux values in the field do not
necessarily reflect minimum water requirements. Animals that take in large
amounts of dietary and/or drinking water could have large values for WEI, whereas animals that do not drink and that consume food with a low water content may
be characterized by low WEI values. Therefore, relatively low WEI in desert birds
46
DESERT
OF
BEHAVIOR
AND
The patterns of thermoregulatory responses of birds to Ta do not differ between
desert and non-desert forms (Scholander et al. 1950; Calder and King 1974;
Dawson 1982, 1984). However, some desert birds have remarkable thermal tolerance, withstanding higher Tas than reported for any non-desert species. Most
species have a thermal neutral zone (TNZ), a range of Tas in which metabolism
is minimal and the requirements for evaporative cooling are generally low. At Tas
below the TNZ, metabolism increases owing to regulatory thermogenesis, while
ECOLOGY
Responses to high T a
Metabolism and evaporation
PHYSIOLOGICAL
T h e r m o re g u l a t i o n
Adult birds maintain their Tb within a few degrees of the upper lethal limit, 4647 °C (Dawson and Schmidt-Nielsen 1964; Calder and King 1974). Controlling
Tb within narrow limits requires a balance of heat gain from metabolic heat production and from the environment and heat loss from radiation, evaporation,
conduction, and convection (Figure 1). Desert environments pose complex challenges to the heat balance of birds. Solar radiation and high Tas during the day
mandate an efficient cooling system and behaviors that reduce thermal loading,
whereas, in some deserts, nighttime Tas may require a high capacity for regulatory thermogenesis. Anecdotal evidence indicates that the capabilities of birds to
regulate their Tb can be exceeded. Periods of extreme heat, with Tas exceeding
50 °C, have caused significant mortality among populations of desert birds
(McGilp 1932; Miller 1963; Serventy 1971). One can imagine that events like
these have selected for behavioral and physiological adaptations to regulate Tb
below upper lethal limits.
In this section we focus on physiological and behavioral thermoregulation under
hot conditions (Figure 1). We only briefly review data on heat balance during
cold nights and their consequences for energy expenditure. We survey several
laboratory studies that provide insights into physiological thermoregulation in
response to Ta, wind, and solar radiation. Finally, we consider microhabitat selection and how it plays a role in balancing thermoregulatory requirements with
water and energy availability (Williams et al. 1999).
BIRDS
may simply reflect the fact that animals outside desert environments take in
excessive amounts of water, exceeding their minimum requirements. Because
birds living in deserts may lose substantial amounts of water used for cooling and
may have low FMRs, one may not expect unusually low values of WEI. The combination of a reduced FMR and a low WEI in desert birds suggests that these species exploit non-evaporative pathways for heat loss, reducing the amount of
water required for cooling, or that they compensate for large quantities of evaporative water loss by a small loss of water through excretion.
47
evaporative water loss is relatively constant. Above the TNZ evaporative water
loss increases exponentially, whereas metabolism increases linearly.
Because few studies have reported thermoregulatory responses of birds exposed to
Tas above 45 °C, it is difficult to detect patterns of heat tolerance that may have
adaptive significance (Tieleman and Williams 1999). When raised as nestlings at
high Tas, Rock Doves, a species found in both mesic and xeric habitats, can withstand Tas exceeding 60 °C for more than 2 hours. These birds maintained their
Tb between 41.2 and 42.0 °C by elevating evaporative heat loss to 304% of metabolic heat production (Marder and Arieli 1988). Spinifex Pigeons (Geophaps
plumifera), birds that inhabit the hot, dry interior of Australia, tolerated a Ta of
50 °C for 1 hour in the laboratory. Their Tb increased to 43.4 °C, and the ratio
of total evaporative heat loss to metabolic heat production varied between 200
and 350% (Withers and Williams 1990). When exposed to 55 °C for 2 hours,
Houbara Bustards (Chlamydotis undulata macqueenii), birds from deserts in North
Africa and the Middle East, maintained Tb at 42.4 °C by elevating their evaporative heat loss to 214% of metabolic heat production (pers. obs.). Responses to
extreme heat among these three species include a relatively low metabolic heat
production, increased resistance of the feather layer to heat flux, high rates of
evaporative cooling compared to metabolic heat production, and increased contribution of cutaneous water loss to total evaporative water loss. In addition,
Rock Doves and Houbara Bustards, two species that can tolerate Tas greater than
50 °C for several hours, maintain Tb at levels close to normal when exposed to
high Tas and do not become hyperthermic.
Body temperature at high T a
Tolerance of hyperthermia may enable birds to inhabit hot environments, presumably because tolerance reduces requirements for evaporative cooling by
improving the thermal gradient between the environment and the animal
(Bartholomew 1964; Dawson and Schmidt-Nielsen 1964; Dawson 1984;
Maclean 1996; Tieleman and Williams 1999). We have already discussed the
influence of hyperthermia on rates of evaporative water loss. Here we consider
whether desert species regulate their Tb at higher levels than non-desert species,
a result that one might expect if hyperthermia is advantageous for birds living
under hot conditions. Unfortunately, data on Tbs of birds in the field are unavailable, forcing us to resort to measurements from the laboratory. Various desert
and non-desert species increase their Tb within and above the TNZ (Weathers
and Schoenbaechler 1976; Weathers 1981; Tieleman and Williams 1999). In an
analysis of 23 species, ranging in body mass from 6.4 g to 412 g, Tieleman and
Williams (1999) found that Tbs were on average 3.3 ± 1.28 °C (SD) higher at a
Ta of 45 °C than at the lower critical temperature. The mean elevation in Tb of
desert species was not significantly different from that of non-desert birds.
48
Hence, the idea that desert species regulate their Tb differently than non-desert
forms at high Tas finds no support (Tieleman and Williams 1999).
Dry heat transfer coefficient
When exposed to Tas >50 °C, Rock Doves, Spinifex Pigeons and Houbara
Bustards assume a compact body posture and erect their feathers, presumably to
minimize surface area and to improve the insulation of their integument (Marder
et al. 1989; Withers and Williams 1990). This suggests that birds minimize dry
heat gain from the environment when Ta exceeds Tb. An integrated measure of
dry heat transfer, including specific heat transfer coefficients for conduction,
convection, and radiation, is provided by the dry heat-transfer coefficient (h).
As a property of the bird, h is influenced by characteristics of insulation, vasodilation, body size, and surface to volume ratios. Calculation of h using the
equation
M - E - C(dTb/dt)
DESERT
OF
BEHAVIOR
AND
ECOLOGY
requires information about metabolic heat production (M; J h-1), evaporative
heat loss (E; J h-1), rate of heat gain in or loss from body tissue (C(dTb/dt); J h-1),
Tb and Ta (Birkebak 1966; Porter and Gates 1969; Calder and King 1974;
Tieleman and Williams 1999).
Below the TNZ, h is often assumed to be minimal (but see McNab 1980). As Ta
increases within the TNZ, birds dissipate metabolic heat by dry heat loss over a
decreasing thermal gradient. Therefore, one might expect that birds continuously adjust the thickness of their feather layer and blood supply to the skin, such
that h increases (Tieleman and Williams 1999). At Tas above Ta = Tb, where the
direction of heat flow is reversed and the bird gains heat from its environment,
one might predict a decrease to minimal h. A review of values reported for h at
Tas above Ta = Tb shows considerable variation (Tieleman and Williams 1999).
Some studies suggest a decrease to a minimal value, while others show no apparent trend (Hinds and Calder 1973; Weathers and Caccamise 1975; Weathers
and Schoenbaechler 1976; Dmi’el and Tel Tzur 1985; Withers and Williams
1990). Tieleman and Williams (1999) point out that some of the variation in h
results from the fact that none of these studies took into account the rate of heat
gain C(dTb/dt), despite the significant contribution of this factor to the heat
balance at high Tas. Calculations of h near Ta = Tb have frequently been problematical because small errors in measurements of the variables in the equation
in the preceding paragraph can translate into large errors in h. The error in h
should be reduced by including C(dTb/dt) in the calculations.
BIRDS
Tb - Ta
PHYSIOLOGICAL
h =
49
In the past, h has not been calculated at Ta = Tb because both numerator and
denominator are zero. Despite the fact that heat transfer (J h-1) is zero at Ta=Tb,
the heat transfer coefficient (J h-1 °C-1), which is a property of the bird, does not
become zero. Tieleman and Williams (1999) describe a method of calculating h
at Ta = Tb using l'Hôpital's rule (Apostol 1967), a differentiation technique that
provides a polynomial approximation of h when both numerator and denominator are zero.
Incorporating C(dTb/dt) and applying l'Hôpital's rule to calculations of h at Ta =
Tb, Tieleman and Williams (1999) found that 22 species of birds (6 - 412 g) did
not reduce h when Ta > Tb, a result in contrast to expectations. Most species
were measured at 45 °C, a Ta only slightly higher than Tb. These authors compared this result with results from Rock Doves (Marder and Arieli 1988) and
Houbara Bustards (unpubl. data), which tolerate Tas above 50 °C. These heattolerant species decreased h at Tas exceeding Tb, which supports the hypothesis
that behaviors which reduce surface area and increase insulation minimize dry
heat uptake at high Tas.
Macroclimate
Wind
Wind decreases the thickness of the boundary layer and disturbs the air layer
within the feathers, which increases convective heat transfer between the animal
and its environment. At Tas below body-surface temperature, birds must increase
their metabolism in response to increasing wind speeds to maintain a constant
Tb. Most studies have focused on energetic costs of exposure to wind at low Tas,
and only a few investigators have extended their measurements to Tas in and
above the TNZ (Gessaman 1972; Robinson et al. 1976; Goldstein 1983; Webster
and Weathers 1988; Bakken 1990; Bakken et al. 1991; Wolf and Walsberg
1996a). In several studies, metabolic rate increases linearly with the square root
of wind speed (Robinson et al. 1976; Webster and Weathers 1988; Bakken 1990;
Bakken et al. 1991; but see Goldstein 1983). The increase in metabolism as a
function of wind speed depends on mass and Ta (Goldstein 1983; Webster and
Weathers 1988). As body mass increases, surface to volume ratio decreases and
mass-specific heat loss at a given wind speed falls. Further, the effect of convective heat loss on metabolic rate increases as Ta decreases (Goldstein 1983;
Webster and Weathers 1988). Changes in the thermal conductance and in the
temperature difference that drives heat flux between the bird’s body and the
environment explain this finding (Campbell 1977; Goldstein 1983; Webster and
Weathers 1988). In wintering Verdins, the additional thermoregulatory costs due
to a moderate increase in mean daily wind speed has been estimated to comprise
20-30% of their daily energy expenditure (Webster and Weathers 1988).
The effect of wind on metabolic rate at Tas around the lower critical tempera50
ture, Tlc, is not well understood (Goldstein 1983; Bakken et al. 1991). Tlc is higher
in wind than under free convection conditions, such as in metabolic chambers, but
the magnitude of the shift remains to be quantified (Goldstein 1983). If a given
wind velocity increased thermal conductance by a constant amount, one could
estimate the shift in Tlc. However, the only study on this issue found an abrupt
onset of wind sensitivity around the Tlc and a discontinuity between metabolic
rate in and below the TNZ in the presence of wind (Bakken et al. 1991).
Knowledge of the effect of wind on the upper critical temperature, Tuc, on metabolism, and on water loss at Tas above the TNZ could yield important information about thermoregulatory consequences of microclimate selection by desert
birds. If Tuc does not exceed Tb, increased convective heat loss due to wind may
elevate Tuc, and extend the TNZ. At Tas above Tb, wind might increase convective heat flux from the environment to the bird, elevating the internal heat load
and the requirements for evaporative cooling. Gambel’s Quail became frantic
when placed in wind at high Tas (Goldstein 1984), a possible indication that
convection increases heat stress owing to increased heat flow to the animal.
The temperature of the ground surface, tree bark, or any other substrate that is
in contact with or close to a bird contributes to its microclimate through conduction and radiation. Heat transfer by conductance between a substrate and an
animal is a function of the temperature gradient, the area of contact surface, and
the conductance between the substrate and the animal. The heat that birds gain
DESERT
OF
BEHAVIOR
AND
ECOLOGY
Substrate temperature
PHYSIOLOGICAL
Solar radiation has a large impact on the water and energy budgets of birds
(Lustick 1969; Lustick et al. 1970; Ohmart and Lasiewski 1971; De Jong 1976;
Wolf and Walsberg 1996a). Sunlight is absorbed by feathers and at low Tas this
decreases the thermal gradient from the skin to the feather surface, which reduces conductive heat loss (Lustick 1969). Below the TNZ, absorption of solar
radiation substantially reduces energy expenditure (Lustick 1969; Ohmart and
Lasiewski 1971; De Jong 1976). Insolation can decrease Tlc and Tuc by as much
as 15 °C (De Jong 1976). At high Tas, solar radiation increases the temperature
of the feather layer and heat flow to the animal, augmenting heat stress and
requirements for evaporative cooling (De Jong 1976). In a study of Verdins (7 g),
Wolf and Walsberg (1996a) measured the decrease in metabolic heat production
at 15 °C as a function of simulated solar radiation and wind speed. Exposure to
radiation significantly reduced metabolic rate at wind speeds of 0.4 - 1.7 m s-1, but
not at 3.0 m s-1. The effects of insolation on the water and energy budgets of birds
are influenced by the intensity of solar radiation, Ta, and wind (Lustick 1969; De
Jong 1976; Wolf and Walsberg 1996a), but the precise relationships between
these parameters await further study.
BIRDS
Solar radiation
51
by radiation from the substrate depends on its temperature and on the emissivity of the substrate surface.
The thermoregulatory consequences of avoiding or seeking specific substrates
have not been explicitly studied, even though behavioral observations suggest
that they have a prominent role in the heat balance of desert birds. Ground foraging desert birds often run from shade spot to shade spot when foraging during
the middle part of the day (pers. obs.). This strategy minimizes not only time
exposed to direct solar radiation, but also time spent on the hot ground surface,
where temperatures can exceed 65 °C. When the soil surface becomes too hot,
some species (e.g. chats and larks) interrupt their movements to perch on small
shrubs or grasses, elevated above the ground, to avoid contact with the hot surface (Willoughby 1971). Desert birds sometimes press the body against the cool
surface of shaded soil, tree bark, or moist plants to conduct away heat during the
hottest part of the day (Wolf et al. 1996; Shobrak 1998; Williams et al. 1999).
Microclimate
Effect of body size
Most desert birds are diurnal, do not dig burrows, and thus are directly confronted with the extremes of their environment (Dawson and Bartholomew 1968;
Wolf et al. 1996; Williams et al. 1999). Thermoregulatory requirements under
hot conditions vary with body size. Large species have a low mass-specific heat
production and a low surface to volume ratio, resulting in slower heat gain when
Tas are elevated. In addition, large birds benefit from greater thermal inertia and
increased capacity to store energy and water. In contrast, smaller species, as result
of their relatively high mass-specific metabolism, higher surface to volume ratio,
and lower thermal inertia, gain heat from the environment more rapidly and
require relatively large amounts of evaporative water for thermoregulation under
hot conditions. On the other hand, small birds benefit from small-scale spatial
variation in microhabitats and may be able to find favorable locations that are
unaccessible to larger birds.
Integrated measures of microclimate: T e and T es
52
Microclimates created by spatial variation in microhabitat result from the interplay of Ta, wind, solar radiation, substrate temperature, and humidity. Although
water vapor pressure may vary among microsites and may influence water loss in
birds, few field measurements have been made. Knowledge of the effect of variation in water vapor pressure on rates of evaporative water loss comes only from
laboratory studies (Lasiewski et al. 1966).
Descriptions of microclimates have improved with the use of integrated measures, such as operative environmental temperature (Te) and standard operative
environmental temperature (Tes) (Bakken and Gates 1975; Bakken 1976). Te
reflects the temperature of a model that duplicates all external conductive, con-
BIRDS
DESERT
OF
BEHAVIOR
AND
ECOLOGY
PHYSIOLOGICAL
vective and radiative properties of the focal animal in thermodynamic equilibrium with its environment, but without heat produced by metabolism or lost by
evaporation (Bakken and Gates 1975; Bakken 1976). Tes is defined as the temperature of a standard environment in which an animal with a constant Tb requires
the same effective net metabolic heat production (metabolic heat production
minus evaporative heat loss) to maintain Tb as it does in the natural environment (Bakken 1976). The latter concept permits data obtained in laboratories to
be translated directly to field situations. Unheated and heated taxidermic
mounts have proved useful to measure Te and Tes (Bakken 1976; Bakken 1980;
Bakken et al. 1981; Chappell and Bartholomew 1981; Salzman 1982; Goldstein
1984; Chappell et al. 1984; Wolf et al. 1996), although Walsberg and Wolf
(1996) for some species questioned the accuracy of data obtained with taxidermic mounts. They compared responses of heated and unheated mounts to those
of live animals. For models of two mammal species, predictions of Tes based on
unheated mounts deviated up to 28.5 °C from actual values when body thermal
resistance was unknown, and up to 7.6 °C when it was known. Predictions of Tes
from Verdin models were within 1.8 °C of actual values when thermal resistance between animal surface and environment and body thermal resistance were
known (Walsberg and Wolf 1996). Larochelle (1998) identified problems with
Walsberg and Wolf’s study and concluded that their data were insufficient to
cast doubt on the ability of mounts to yield reliable measures of Te and Tes. Most
studies that have used taxidermic mounts have been carried out in cold environments; their application in hot environments deserves further attention.
No studies on desert birds have applied heated mounts to measure Tes. Some workers have employed unheated mounts to determine Te under hot conditions, but
none of these reported calibration data at high Tas or provided information about
the amount of variation between individual mounts (Salzman 1982; Chappell et
al. 1984; Goldstein 1984; Williams et al. 1995). Walsberg and Wolf (1996) measured Te using mounts of Verdins exposed to combinations of wind and solar
radiation and found that estimates of Tes varied by 2-3 °C among mounts. These
results indicate the importance of using several mounts simultaneously to provide
estimates of Te and Tes. Some investigators have calibrated heated taxidermic
mounts in a wind tunnel (following Bakken et al. 1981) to determine the ratio
of the thermal conductance in the general environment to that in the laboratory and used this information to calculate Tes from Te (Goldstein 1984; Williams
et al. 1995). Unfortunately these calibrations were performed over Tas of 6-25 °C
(Goldstein 1984) and 0-36 °C (Williams et al. 1995) and in the absence of solar
radiation. Field measurements of Te in these studies far exceeded 40 °C, and estimates of Tes required extrapolation beyond empirically derived values. Calculation
of Tes based on Te at temperatures in and above the TNZ, and especially at Tas
> Tb, has not been validated. Estimates of Tes at high Tes should therefore be
53
regarded with caution, because they require untested assumptions about conductance (Goldstein 1984). Changes in conductance of live birds at high Tas under
laboratory conditions are poorly understood (Tieleman and Williams 1999), and
values for conductance at high Tas in the presence of wind and solar radiation
are lacking. In addition to the problem of translating Te to Tes, measurement of
Te itself is sometimes problematic. When conductance of an animal and a mount
differ greatly, as is the case when an extensive part of a live animal’s body touches
a substrate, Te as measured with mounts may deviate significantly from actual Te
(Bakken 1976)
Microsites providing protection from cold
Selection of microsites by desert birds depends on either energy or water balance
and may vary during the course of the day or seasons. To minimize energy
requirements for heat production under cold conditions, especially during winter
nights, some species, e.g. Phainopepla (Phainopepla nitens) and Black-tailed
Gnatcatcher (Polioptila melanura), occupy roost nests (Walsberg 1986; Walsberg
1990). Hoopoe Larks (Alaemon alaudipes) and Crested Larks in Arabia spend the
night sitting in small depressions that they dig in sand (pers. obs.). For most
desert species nocturnal roost sites are unknown.
Microsites providing protection from heat
54
Birds select favorable microsites under hot conditions to avoid excessive heat
gain and to minimize evaporative water loss. As Ta increases during the day,
small ground-foraging species like Gray’s Larks (Ammomanes grayi), Spike-heeled Larks (Chersomanes albofasciata) (Willoughby 1971), Dune Larks, Dunn’s
Larks (Eremalauda dunni), and Hoopoe Larks (Shobrak 1998; pers. obs.) perch on
stones or vegetation above the ground surface, with wings held away from the
body to expose thinly feathered areas under the wings. These birds can be exposed to direct sunlight, and convective heat loss apparently exceeds solar heat
gain under these circumstances. To avoid high Tas close to the ground, raptors
soar during the middle part of the day (Madsen 1930; Dawson 1976). When the
intensity of solar radiation increases, many other species choose shade created by
rocks, vegetation, or burrows that are dug by rodents or lizards (Ricklefs and
Hainsworth 1968; Willoughby 1971; Cox 1983; Hinsley 1994; Wolf et al. 1996;
Shobrak 1998; Williams et al. 1999).
During hot days some desert species press the ventral parts of the body against
cool substrates to conduct away heat without excessive loss of water for evaporation. Black-tailed Gnatcatchers (Wolf et al. 1996), larks, and shrikes (pers. obs.)
lie prostrate in sandy spots that are shaded by vegetation. Hoopoe Larks and
Dunn’s Larks fashion small cups in the sand against tufts of grass that provide
shade, pressing their ventral surface against the cool substrate. Occasionally
Hoopoe Larks lie with their wings spread on the mat-like plant Corchorus depres-
sus, apparently benefitting from the relatively cool, damp foliage (Shobrak
1998). Black-tailed Gnatcatchers and Verdins seek cool substrates on the bark of
Paloverde trees (Cercidium floridum), where they spend the hottest part of the
afternoon (Wolf et al. 1996). Finally, during hot summer days in the Arabian
Desert Hoopoe Larks, Dunn’s larks, Bar-tailed Desert Larks (Ammomanes cincturus), and Black-crowned Finch Larks (Eremopterix nigriceps) use burrows of the
large herbivorous lizard Uromastyx aegypticus as thermal refugia (Williams et al.
1999).
DESERT
OF
BEHAVIOR
AND
ECOLOGY
PHYSIOLOGICAL
The energetic cost of thermoregulation has been defined as either the sum of
thermostatic costs plus basal metabolic rate, i.e. maintenance metabolism, or as
the sum of thermostatic costs alone (Dawson and O’Connor 1996). Estimates of
avian maintenance metabolism vary from nil to 90% (Dawson and O’Connor
1996), but generally constitute 40-60% of field metabolic rates (Walsberg 1983).
Dawson and O’Connor (1996) review data on energetic costs of thermoregulation in birds inhabiting hot environments and conclude that these costs comprise a lower proportion of field metabolic rate than those for species in cold climates. Studies that report costs of thermoregulation usually focus on energetic
costs and often fail to estimate evaporative water loss, despite the high rates of
evaporation measured on birds in the laboratory at high Tas (Walsberg 1983;
Dawson and O’Connor 1996).
The large energy expenditure and water loss required to maintain heat balance
creates a potential for substantial savings by selecting favorable microsites.
Estimates of energy and water saved by selecting specific microclimates under
hot conditions are few, and those that have been made are usually based on interpolations of measurements of metabolism and water loss from the laboratory. By
roosting in dense vegetation during winter in the Sonoran desert, Phainopelas
increased Tes by ~9.5 °C, a 20% decrease in resting energy expenditure
(Walsberg 1986). The increase in Tes in these roost sites was largely due to wind
shielding (8.0 °C) and to a smaller extent to changes in the radiative environment (1.5 °C) (Walsberg 1986). During summer Phainopeplas occur inland in
regions of western North America where daily maximum temperatures average
39.7 °C. Walsberg (1993) estimated that selection of the coolest microsites reduced evaporative water loss to less than 5% of that predicted for the hottest
available microhabitat. During winter at Tas of 15 °C, Verdins in the Sonoran
desert can reduce resting metabolic rates by 50% by moving to a sunny site protected from wind (Wolf and Walsberg 1996a). At midday in summer, Verdins
and Black-tailed Gnatcatchers selected small shady depressions in the bark of
Paloverde trees, which reduced their Te by approximately 15 °C and, as a consequence, their evaporative water loss by 75-80% (Wolf et al. 1996; Wolf and
BIRDS
Thermoregulatory benefits of microsite selection
55
Walsberg 1996a). Hoopoe Larks in the Arabian desert reduce their evaporative
water loss by 66% when they move out of the sun (3.99 g H2O h-1) into a shady
spot (1.35 g H2O h-1) during the heat of the day (Williams et al. 1999). By retreating underground to the shade of lizard burrows, Hoopoe Larks decreased
TEWL by an additional 65%, compared to their TEWL in above-ground shade.
If they press their ventral apteria against the burrow substrate, TEWL is reduced
to 0.25 g H2O h-1. In total, the TEWL of Hoopoe Larks that lie on the floor of
lizard burrows is potentially 94% lower than that of individuals exposed to direct
solar radiation (Williams et al. 1999).
Mobility
Some species evade desert extremes by flying to regions in which food is plentiful, typically after rainfall (Davies 1984; Schulz and Seddon 1996). How these
nomadic birds locate these favorable areas is unresolved. Other species periodically visit the desert each year in times of mild environmental conditions and
sufficient food supply and migrate elsewhere prior to the onset of summer
(Walsberg 1977; Walsberg 1993). Birds that fly long distances to migrate or to
follow pulses of rain may lose significant amounts of water and use substantial
amounts of energy while moving from one site to another. Comparisons of the
costs and benefits of migratory, nomadic, and resident strategies are needed to
understand how considerations of water, energy balance, and thermoregulatory
capabilities are involved in the movements of desert birds.
Nomadism is a common phenomenon among birds from arid environments,
especially in the southern hemisphere (Keast 1959; Maclean 1996), but unifying
explanations that might account for this behavior have not emerged (Davies
1982). At least 26% of Australian bird species are nomadic (Keast 1959). Most
nomads eat seeds and apparently utilize sources of drinking water regularly
(Maclean 1970a; Willoughby 1971; Davies 1982).
Migratory species that visit deserts in times of mild environmental conditions are
common in most deserts. However, few studies have examined the advantages of
such movements. For species that annually emigrate from the desert during the
hottest portions of the summer, it would be of interest to compare thermoregulatory costs in their summer habitats with costs that they would accrue if they
had remained in the desert. Walsberg (1993) quantified the thermal consequences of microsite selection of male Phainopeplas in three habitats during breeding.
These small (24 g) primarily frugivorous birds range from the southern portion
of the Mexican Plateau into the southwestern United States and occupy the
Sonoran and Colorado deserts during fall, winter, and spring, when mistletoe
berries (Phoradendron californicum) are abundant and environmental temperatures are moderate (Walsberg 1977). They breed during March and April (Sonoran
desert) when insects, important food for their young, become abundant. Prior to
56
DESERT
OF
BEHAVIOR
AND
ECOLOGY
PHYSIOLOGICAL
O p t i m i z a t i o n p ro c e s s e s
For heuristic purposes our conceptual model compartmentalizes aspects of energy expenditure, water balance, and thermoregulation that are potentially important for the survival of desert birds (Figure 1). We end this paper with the
thought that, in reality, each of these compartments is inextricably linked to
the others. For resident birds that do not drink, foods that they choose must
contain adequate water, energy, and other nutrients to satisfy their requirements (MacMillen 1990). The dietary items selected by birds, such as insects,
seeds, or other vegetable material, have consequences for both energy and
water balance. A diet of seeds alone (< 10% H2O) may be able to satisfy energy requirements, but may fall short of fulfilling water needs. This explains why
granivorous birds typically drink during hot periods in the desert. Insects contain ample water (~ 65% H2O) and energy, but may not be abundant enough
to meet all nutrient requirements. Opportunism and omnivory would seem to be
the best strategy of diet selection among desert birds, especially in hyperarid
deserts. Choice of dietary items can be viewed as an optimization process governed
by availability of foods and current needs. As environments become less harsh,
e.g., in more semi-arid areas, and as primary production increases, criteria for diet
selection should change.
Episodes of high Ta, common during summers in some deserts, pose a serious
challenge to the physiological capacities of birds. Elevated heat loads require
evaporative water loss by means of increased cutaneous and respiratory water
loss. The evolution of reduced rates of metabolism can lead to lower rates of
water loss. In addition, evaporative water loss can be minimized by seeking
patches of shade, and sometimes these spots are large enough to permit foraging.
However, at extreme Tas when thermoregulatory costs are highest, seeking deep
shade and pressing the body against cooler substrates limit foraging. Hence,
when evaporative demands are potentially the highest, water intake is lowest.
BIRDS
the onset of summer, they emigrate to oak and riparian woodlands in California,
Arizona, and New Mexico and breed a second time. Walsberg (1993) estimated
Tes in three study sites: the Sonoran desert (spring), semi-arid woodlands along
the coast of California (summer), and semi-arid woodlands in Arizona (summer).
Although the interior woodland (Arizona) was markedly hotter than the other
two sites, Phainopeplas adjusted their daily time-budgets such that the Tes that
they encountered were similar in all three areas, suggesting that migration is a
form of behavioral thermoregulation. Because he lacked information on rates of
water loss at various Tes, Walsberg could not estimate their rates of water loss in
the respective environments. It would have been informative to estimate the
potential costs to Phainopeplas of remaining in the Sonoran during summer.
57
Birds may allow their Tb to rise in these situations, reducing evaporative water
loss that otherwise would be necessary to regulate Tb at lower levels, but they can
not afford to allow Tb to rise much higher than 45 °C. The costs associated with
elevated Tb have not been determined but may take the form of a compromised
immune function or enzyme function. Although the costs and benefits of behavioral and physiological adjustments to heat and aridity are not sufficiently
understood, it is clear that models of survival in desert environments must combine energy, water, and thermoregulation, rather than consider each as a discreet
unit.
Acknowledgments
Funding for this project has been supplied by the National Science Foundation
(JBW), the Columbus Zoo (JBW), the National Wildlife Research Center, Taif,
Saudi Arabia (JBW and BIT), the Stichting Dr. Catharine van Tussenbroek
(BIT) and the Schuurman Schimmel van Outeren Stichting (BIT). We thank
C. Beuchat, D. Goldstein, and B. Mauck for helpful comments on selected portions of the manuscript and W. Dawson and M. Webster for commenting on the
entire manuscript. We thank V. Nolan for his efforts at editing our work and
Heerko Tieleman for making Figure 1.
58
59
PHYSIOLOGICAL
ECOLOGY
AND
BEHAVIOR
OF
DESERT
BIRDS